Capripoxviruses: A Continuing Worldwide Threat to Sheep, Goats and Cattle

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Public Health Microbiology".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 25143

Special Issue Editor


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Guest Editor
National Centre for Foreign Animal Disease, Winnepeg, MB, Canada
Interests: capripoxvirus; rift valley fever; peste des petits ruminants; avian influenza; African swine fever; vaccines

Special Issue Information

Dear Colleagues,

Sheeppox virus, goatpox virus and lumpy skin disease virus are members of the capripoxvirus genus, which cause poxvirus diseases in sheep, goats and cattle, respectively. Collectively, these diseases cause large production losses throughout many regions in Africa and Eurasia. Lumpy skin disease virus is primarily spread by vectors and has expanded its historical geographic range from Africa into new regions in Eurasia. Since lumpy skin disease virus is a new disease, it is testing local veterinary services’ abilities to control the disease, through the education of producers, diagnostic testing and prevention using vaccines. This Special Issue will cover all topics related to capripoxviruses including their biology, epidemiology, diagnostics and vaccines.

Dr. Shawn Babiuk
Guest Editor

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Keywords

  • capripoxvirus
  • sheeppox
  • goatpox
  • lumpy skin disease
  • diagnostics
  • epidemiology
  • vaccines
  • vectors
Dr. Shawn Babiuk
Guest Editor

Published Papers (9 papers)

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Research

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12 pages, 2838 KiB  
Article
Detection of Clinical and Subclinical Lumpy Skin Disease Using Ear Notch Testing and Skin Biopsies
by Laetitia Aerts, Andy Haegeman, Ilse De Leeuw, Wannes Philips, Willem Van Campe, Isabelle Behaeghel, Laurent Mostin and Kris De Clercq
Microorganisms 2021, 9(10), 2171; https://doi.org/10.3390/microorganisms9102171 - 19 Oct 2021
Cited by 10 | Viewed by 2022
Abstract
Lumpy skin disease (LSD) diagnosis is primarily based on clinical surveillance complemented by PCR of lesion crusts or nodule biopsies. Since LSD can be subclinical, the sensitivity of clinical surveillance could be lower than expected. Furthermore, real-time PCR for the detection of LSD [...] Read more.
Lumpy skin disease (LSD) diagnosis is primarily based on clinical surveillance complemented by PCR of lesion crusts or nodule biopsies. Since LSD can be subclinical, the sensitivity of clinical surveillance could be lower than expected. Furthermore, real-time PCR for the detection of LSD viral DNA in blood samples from subclinical animals is only intermittently positive. Therefore, this study aimed to investigate an acceptable, easily applicable and more sensitive testing method for the detection of clinical and subclinical LSD. An animal experiment was conducted to investigate ear notches and biopsies from unaffected skin taken from the neck and dorsal back as alternatives to blood samples. It was concluded that for early LSD confirmation, normal skin biopsies and ear notches are less fit for purpose, as LSDV DNA is only detectable in these samples several days after it is detectable in blood samples. On the other hand, blood samples are less advisable for the detection of subclinical animals, while ear notches and biopsies were positive for LSD viral DNA in all subclinically infected animals by 16 days post infection. In conclusion, ear notches could be used for surveillance to detect subclinical animals after removing the clinical animals from a herd, to regain trade by substantiating the freedom of disease or to support research on LSDV transmission from subclinical animals. Full article
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16 pages, 2772 KiB  
Article
Validation of TaqMan-Based Assays for Specific Detection and Differentiation of Wild-Type and Neethling Vaccine Strains of LSDV
by Dejan Vidanović, Bojana Tešović, Milanko Šekler, Zoran Debeljak, Nikola Vasković, Kazimir Matović, Andrey Koltsov, Kiril Krstevski, Tamaš Petrović, Ilse De Leeuw and Andy Haegeman
Microorganisms 2021, 9(6), 1234; https://doi.org/10.3390/microorganisms9061234 - 06 Jun 2021
Cited by 9 | Viewed by 3303
Abstract
Lumpy skin disease (LSD) is an important animal disease with significant health and economic impacts. It is considered a notifiable disease by the OIE. Attenuated strains of LSDV have been successfully used as vaccines (LAV) but can also produce mild or systemic reactions. [...] Read more.
Lumpy skin disease (LSD) is an important animal disease with significant health and economic impacts. It is considered a notifiable disease by the OIE. Attenuated strains of LSDV have been successfully used as vaccines (LAV) but can also produce mild or systemic reactions. Vaccination campaigns using LAVs are therefore only viable if accompanying DIVA assays are available. Two DIVA qPCR assays able to distinguish Neethling-based LAVs and wild-type LSDV were developed. Upon validation, both assays were shown to have high sensitivity and specificity with a diagnostic performance comparable to other published DIVA assays. This confirmed their potential as reliable tools to confirm infection in animals during vaccination campaigns based on Neethling vaccine strains. Full article
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13 pages, 3494 KiB  
Article
Molecular Analysis of East African Lumpy Skin Disease Viruses Reveals a Mixed Isolate with Features of Both Vaccine and Field Isolates
by Tesfaye Rufael Chibssa, Melaku Sombo, Jacqueline Kasiiti Lichoti, Tajelser Idris Badri Adam, Yang Liu, Yazeed Abd Elraouf, Reingard Grabherr, Tirumala Bharani K. Settypalli, Francisco J. Berguido, Angelika Loitsch, Mesfin Sahle, Giovanni Cattoli, Adama Diallo and Charles Euloge Lamien
Microorganisms 2021, 9(6), 1142; https://doi.org/10.3390/microorganisms9061142 - 26 May 2021
Cited by 14 | Viewed by 2804
Abstract
Lumpy skin disease (LSD), an economically significant disease in cattle caused by lumpy skin disease virus (LSDV), is endemic to nearly all of Africa. Since 2012, LSDV has emerged as a significant epizootic pathogen given its rapid spread into new geographical locations outside [...] Read more.
Lumpy skin disease (LSD), an economically significant disease in cattle caused by lumpy skin disease virus (LSDV), is endemic to nearly all of Africa. Since 2012, LSDV has emerged as a significant epizootic pathogen given its rapid spread into new geographical locations outside Africa, including the Middle East, Eastern Europe, and Asia. To assess the genetic diversity of LSDVs in East Africa, we sequenced and analyzed the RPO30 and GPCR genes of LSDV in twenty-two archive samples collected in Ethiopia, Kenya, and Sudan before the appearance of LSD in the Middle East and its incursion into Europe. We compared them to publicly available sequences of LSDVs from the same region and those collected elsewhere. The results showed that the East African field isolates in this study were remarkably similar to each other and to previously sequenced field isolates of LSDV for the RPO30 and GPCR genes. The only exception was LSDV Embu/B338/2011, a field virus collected in Kenya, which displayed mixed features between the LSDV Neethling vaccine and field isolates. LSDV Embu/B338/2011 had the same 12-nucleotide insertion found in LSDV Neethling and KS-1 vaccines. Further analysis of the partial EEV glycoprotein, B22R, RNA helicase, virion core protein, NTPase, and N1R/p28-like protein genes showed that LSDV Embu/B338/2011 differs from previously described LSDV variants carrying the 12-nucleotide insertion in the GPCR gene. These findings highlight the importance of the constant monitoring of genetic variation among LSDV isolates. Full article
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14 pages, 32589 KiB  
Article
Engineering of Recombinant Sheep Pox Viruses Expressing Foreign Antigens
by Olga Chervyakova, Elmira Tailakova, Nurlan Kozhabergenov, Sandugash Sadikaliyeva, Kulyaisan Sultankulova, Kunsulu Zakarya, Rinat A. Maksyutov, Vitaliy Strochkov and Nurlan Sandybayev
Microorganisms 2021, 9(5), 1005; https://doi.org/10.3390/microorganisms9051005 - 07 May 2021
Cited by 2 | Viewed by 2505
Abstract
Capripoxviruses with a host range limited to ruminants have the great potential to be used as vaccine vectors. The aim of this work was to evaluate attenuated sheep pox virus (SPPV) vaccine strain NISKHI as a vector expressing several genes. Open reading frames [...] Read more.
Capripoxviruses with a host range limited to ruminants have the great potential to be used as vaccine vectors. The aim of this work was to evaluate attenuated sheep pox virus (SPPV) vaccine strain NISKHI as a vector expressing several genes. Open reading frames SPPV020 (ribonucleotide kinase) and SPPV066 (thymidine kinase) were selected as sites for the insertion of foreign genes. Two integration plasmids with expression cassette were designed and constructed. Recombinant SPPVs expressing an enhanced green fluorescent protein (EGFP) (rSPPV(RRΔ)EGFP and rSPPV(TKΔ)EGFP), Foot-and-mouth disease virus capsid protein (VP1), and Brucella spp. outer membrane protein 25 (OMP25) (rSPPV(RRΔ)VP1A-(TKΔ)OMP25) were generated under the transient dominant selection method. The insertion of foreign genes into the SPPV020 and SPPV066 open reading frames did not influence the replication of the recombinant viruses in the cells. Successful foreign gene expression in vitro was assessed by luminescent microscopy (EGFP) and Western blot (VP1 and OMP25). Our results have shown that foreign genes were expressed by rSPPV both in permissive (lamb testicles) and non-permissive (bovine kidney, saiga kidney, porcine kidney) cells. Mice immunized with rSPPV(RRΔ)VP1A-(TKΔ)OMP25 elicited specific antibodies to both SPPV and foreign genes VP1 and OMP25. Thus, SPPV NISKHI may be used as a potential safe immunogenic viral vector for the development of polyvalent vaccines. Full article
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9 pages, 1236 KiB  
Communication
Use of an Alignment-Free Method for the Geographical Discrimination of GTPVs Based on the GPCR Sequences
by Tesfaye Rufael Chibssa, Yang Liu, Melaku Sombo, Jacqueline Kasiiti Lichoti, Janchivdorj Erdenebaatar, Bazartseren Boldbaatar, Reingard Grabherr, Tirumala Bharani K. Settypalli, Francisco J. Berguido, Angelika Loitsch, Delesa Damena, Giovanni Cattoli, Adama Diallo and Charles Euloge Lamien
Microorganisms 2021, 9(4), 855; https://doi.org/10.3390/microorganisms9040855 - 16 Apr 2021
Viewed by 1785
Abstract
Goatpox virus (GTPV) belongs to the genus Capripoxvirus, together with sheeppox virus (SPPV) and lumpy skin disease virus (LSDV). GTPV primarily affects sheep, goats and some wild ruminants. Although GTPV is only present in Africa and Asia, the recent spread of LSDV in [...] Read more.
Goatpox virus (GTPV) belongs to the genus Capripoxvirus, together with sheeppox virus (SPPV) and lumpy skin disease virus (LSDV). GTPV primarily affects sheep, goats and some wild ruminants. Although GTPV is only present in Africa and Asia, the recent spread of LSDV in Europe and Asia shows capripoxviruses could escape their traditional geographical regions to cause severe outbreaks in new areas. Therefore, it is crucial to develop effective source tracing of capripoxvirus infections. Earlier, conventional phylogenetic methods, based on limited samples, identified three different nucleotide sequence profiles in the G-protein-coupled chemokine receptor (GPCR) gene of GTPVs. However, this method did not differentiate GTPV strains by their geographical origins. We have sequenced the GPCR gene of additional GTPVs and analyzed them with publicly available sequences, using conventional alignment-based methods and an alignment-free approach exploiting k-mer frequencies. Using the alignment-free method, we can now classify GTPVs based on their geographical origin: African GTPVs and Asian GTPVs, which further split into Western and Central Asian (WCA) GTPVs and Eastern and Southern Asian (ESA) GTPVs. This approach will help determine the source of introduction in GTPV emergence in disease-free regions and detect the importation of additional strains in disease-endemic areas. Full article
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14 pages, 751 KiB  
Article
Probe-Based Real-Time qPCR Assays for a Reliable Differentiation of Capripox Virus Species
by Janika Wolff, Martin Beer and Bernd Hoffmann
Microorganisms 2021, 9(4), 765; https://doi.org/10.3390/microorganisms9040765 - 06 Apr 2021
Cited by 11 | Viewed by 2372
Abstract
Outbreaks of the three capripox virus species, namely lumpy skin disease virus, sheeppox virus, and goatpox virus, severely affect animal health and both national and international economies. Therefore, the World Organization for Animal Health (OIE) classified them as notifiable diseases. Until now, discrimination [...] Read more.
Outbreaks of the three capripox virus species, namely lumpy skin disease virus, sheeppox virus, and goatpox virus, severely affect animal health and both national and international economies. Therefore, the World Organization for Animal Health (OIE) classified them as notifiable diseases. Until now, discrimination of capripox virus species was possible by using different conventional PCR protocols. However, more sophisticated probe-based real-time qPCR systems addressing this issue are, to our knowledge, still missing. In the present study, we developed several duplex qPCR assays consisting of different types of fluorescence-labelled probes that are highly sensitive and show a high analytical specificity. Finally, our assays were combined with already published diagnostic methods to a diagnostic workflow that enables time-saving, reliable, and robust detection, differentiation, and characterization of capripox virus isolates. Full article
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6 pages, 837 KiB  
Communication
Thermal Inactivation of Different Capripox Virus Isolates
by Janika Wolff, Martin Beer and Bernd Hoffmann
Microorganisms 2020, 8(12), 2053; https://doi.org/10.3390/microorganisms8122053 - 21 Dec 2020
Cited by 3 | Viewed by 2405
Abstract
Capripox viruses (CaPVs) cause a highly contagious poxvirus disease of livestock animals. Working with CaPVs requires laboratories with a high biosecurity level (BSL 3), and reliable inactivation of these viruses is therefore necessary for working in areas or laboratories with a lower biosecurity [...] Read more.
Capripox viruses (CaPVs) cause a highly contagious poxvirus disease of livestock animals. Working with CaPVs requires laboratories with a high biosecurity level (BSL 3), and reliable inactivation of these viruses is therefore necessary for working in areas or laboratories with a lower biosecurity status. Heat treatment provides a simple and well-established tool for the inactivation due to its substantial advantages (e.g., easy to perform, fast, cheap, and robust). In our study, we determined the time–temperature profiles needed for a fail-safe inactivation procedure using four different CaPV isolates in aqueous solution with and without the addition of protective serum. All four tested CaPV isolates were completely inactivated after 30 min at 56 °C or 10 min at 60 °C. Since different thermal stabilities of other CaPV isolates could not be fully excluded, we recommend an inactivation procedure of 1 h at 56 °C for safe shipment or working in laboratories with lower biosecurity levels than BSL 3. Full article
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20 pages, 3948 KiB  
Article
Establishment of a Challenge Model for Sheeppox Virus Infection
by Janika Wolff, Sahar Abd El Rahman, Jacqueline King, Mohamed El-Beskawy, Anne Pohlmann, Martin Beer and Bernd Hoffmann
Microorganisms 2020, 8(12), 2001; https://doi.org/10.3390/microorganisms8122001 - 15 Dec 2020
Cited by 9 | Viewed by 2257
Abstract
Sheeppox virus (SPPV) together with goatpox virus and lumpy skin disease virus form the genus Capripoxvirus of the Poxviridae family. Due to their great economic importance and major impact on livelihood of small-scale farmers, OIE guidelines classify capripox viruses as notifiable diseases. In [...] Read more.
Sheeppox virus (SPPV) together with goatpox virus and lumpy skin disease virus form the genus Capripoxvirus of the Poxviridae family. Due to their great economic importance and major impact on livelihood of small-scale farmers, OIE guidelines classify capripox viruses as notifiable diseases. In the present study, we examined pathogenesis of an Indian SPPV isolate and an Egyptian SPPV isolate in sheep. Three different infection routes were tested: (i) intravenous infection, (ii) intranasal infection and (iii) contact transmission between infected and naïve sheep. Clinical course, viremia and viral shedding as well as seroconversion were analyzed in order to establish a challenge model for SPPV infections that can be used in future vaccine studies. Next to in vivo characterization, both SPPV strains underwent next- and third-generation sequencing to obtain high quality full-length genomes for genetic characterization and comparison to already published SPPV sequences. Full article
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Review

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16 pages, 783 KiB  
Review
Capripoxvirus Infections in Ruminants: A Review
by Jihane Hamdi, Henry Munyanduki, Khalid Omari Tadlaoui, Mehdi El Harrak and Ouafaa Fassi Fihri
Microorganisms 2021, 9(5), 902; https://doi.org/10.3390/microorganisms9050902 - 23 Apr 2021
Cited by 29 | Viewed by 4357
Abstract
Lumpy skin disease, sheeppox, and goatpox are notifiable diseases of cattle, sheep, and goats, respectively, caused by viruses of the Capripoxvirus genus. They are responsible for both direct and indirect financial losses. These losses arise through animal mortality, morbidity cost of vaccinations, and [...] Read more.
Lumpy skin disease, sheeppox, and goatpox are notifiable diseases of cattle, sheep, and goats, respectively, caused by viruses of the Capripoxvirus genus. They are responsible for both direct and indirect financial losses. These losses arise through animal mortality, morbidity cost of vaccinations, and constraints to animals and animal products’ trade. Control and eradication of capripoxviruses depend on early detection of outbreaks, vector control, strict animal movement, and vaccination which remains the most effective means of control. To date, live attenuated vaccines are widely used; however, conferred protection remains controversial. Many vaccines have been associated with adverse reactions and incomplete protection in sheep, goats, and cattle. Many combination- and recombinant-based vaccines have also been developed. Here, we review capripoxvirus infections and the immunity conferred against capripoxviruses by their respective vaccines for each ruminant species. We also review their related cross protection to heterologous infections. Full article
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