Research

13 pages, 935 KiB

Open AccessArticle

Sequencing and Analysis of Lumpy Skin Disease Virus Whole Genomes Reveals a New Viral Subgroup in West and Central Africa

by Ismar R. Haga, Barbara B. Shih, Gessica Tore, Noemi Polo, Paolo Ribeca, Delgerzul Gombo-Ochir, Gansukh Shura, Tsagaan Tserenchimed, Bazarragchaa Enkhbold, Dulam Purevtseren, Gerelmaa Ulziibat, Batchuluun Damdinjav, Lama Yimer, Fufa D. Bari, Daniel Gizaw, Adeyinka Jeremy Adedeji, Rebecca Bitiyong Atai, Jolly Amoche Adole, Banenat Bajehson Dogonyaro, Pradeep Lakpriya Kumarawadu, Carrie Batten, Amanda Corla, Graham L. Freimanis, Chandana Tennakoon, Andy Law, Samantha Lycett, Tim Downing and Philippa M. Beard Show full author list Hide full author list

Viruses 2024, 16(4), 557; https://doi.org/10.3390/v16040557 - 03 Apr 2024

Viewed by 1727

Abstract

Lumpy skin disease virus (LSDV) is a member of the capripoxvirus (CPPV) genus of the Poxviridae family. LSDV is a rapidly emerging, high-consequence pathogen of cattle, recently spreading from Africa and the Middle East into Europe and Asia. We have sequenced the whole [...] Read more.

Lumpy skin disease virus (LSDV) is a member of the capripoxvirus (CPPV) genus of the Poxviridae family. LSDV is a rapidly emerging, high-consequence pathogen of cattle, recently spreading from Africa and the Middle East into Europe and Asia. We have sequenced the whole genome of historical LSDV isolates from the Pirbright Institute virus archive, and field isolates from recent disease outbreaks in Sri Lanka, Mongolia, Nigeria and Ethiopia. These genome sequences were compared to published genomes and classified into different subgroups. Two subgroups contained vaccine or vaccine-like samples (“Neethling-like” clade 1.1 and “Kenya-like” subgroup, clade 1.2.2). One subgroup was associated with outbreaks of LSD in the Middle East/Europe (clade 1.2.1) and a previously unreported subgroup originated from cases of LSD in west and central Africa (clade 1.2.3). Isolates were also identified that contained a mix of genes from both wildtype and vaccine samples (vaccine-like recombinants, grouped in clade 2). Whole genome sequencing and analysis of LSDV strains isolated from different regions of Africa, Europe and Asia have provided new knowledge of the drivers of LSDV emergence, and will inform future disease control strategies. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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14 pages, 1447 KiB

Open AccessArticle

Susceptibility of Mediterranean Buffalo (Bubalus bubalis) following Experimental Infection with Lumpy Skin Disease Virus

by Elisabetta Di Felice, Chiara Pinoni, Emanuela Rossi, Giorgia Amatori, Elisa Mancuso, Federica Iapaolo, Angela Taraschi, Giovanni Di Teodoro, Guido Di Donato, Gaetano Federico Ronchi, Maria Teresa Mercante, Mauro Di Ventura, Daniela Morelli and Federica Monaco

Viruses 2024, 16(3), 466; https://doi.org/10.3390/v16030466 - 19 Mar 2024

Viewed by 568

Abstract

Lumpy skin disease (LSD) is a viral disease of cattle and water buffalo characterized by cutaneous nodules, biphasic fever, and lymphadenitis. LSD is endemic in Africa and the Middle East but has spread to different Asian countries in recent years. The disease is [...] Read more.

Lumpy skin disease (LSD) is a viral disease of cattle and water buffalo characterized by cutaneous nodules, biphasic fever, and lymphadenitis. LSD is endemic in Africa and the Middle East but has spread to different Asian countries in recent years. The disease is well characterized in cattle while little is known about the disease in buffaloes in which no experimental studies have been conducted. Six buffaloes and two cattle were inoculated with an Albanian LSD virus (LSDV) field strain and clinically monitored for 42 days. Only two buffaloes showed fever, skin nodules, and lymphadenitis. All samples collected (blood, swabs, biopsies, and organs) were tested in real-time PCR and were negative. Between day 39 and day 42 after inoculation, anti-LSDV antibodies were detected in three buffaloes by ELISA, but all sera were negative by virus neutralization test (VNT). Cattle showed severe clinical signs, viremia, virus shedding proven by positive real-time PCR results, and seroconversion confirmed by both ELISA and VNT. Clinical findings suggest that susceptibility in buffaloes is limited compared to in cattle once experimentally infected with LSDV. Virological results support the hypothesis of buffalo resistance to LSD and its role as an accidental non-adapted host. This study highlights that the sensitivity of ELISA and VNT may differ between animal species and further studies are needed to investigate the epidemiological role of water buffalo. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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12 pages, 2323 KiB

Open AccessArticle

Detection and Genome Sequencing of Lumpy Skin Disease Viruses in Wildlife Game Species in South Africa

by Antoinette van Schalkwyk, Pravesh Kara, Robert D. Last, Marco Romito and David B. Wallace

Viruses 2024, 16(2), 172; https://doi.org/10.3390/v16020172 - 24 Jan 2024

Viewed by 1005

Abstract

Lumpy skin disease virus (LSDV) has recently undergone rapid spread, now being reported from more than 80 countries, affecting predominantly cattle and to a lesser extent, water buffalo. This poxvirus was previously considered to be highly host-range restricted. However, there is an increasing [...] Read more.

Lumpy skin disease virus (LSDV) has recently undergone rapid spread, now being reported from more than 80 countries, affecting predominantly cattle and to a lesser extent, water buffalo. This poxvirus was previously considered to be highly host-range restricted. However, there is an increasing number of published reports on the detection of the virus from different game animal species. The virus has not only been shown to infect a wide range of game species under experimental conditions, but has also been naturally detected in oryx, giraffe, camels and gazelle. In addition, clinical lumpy skin disease has previously been described in springbok (Antidorcas marsupialis), an African antelope species, in South Africa. This report describes the characterization of lumpy skin disease virus belonging to cluster 1.2, from field samples from springbok, impala (Aepyceros melampus) and a giraffe (Giraffa camelopardalis) in South Africa using PCR, Sanger and whole genome sequencing. Most of these samples were submitted from wild animals in nature reserves or game parks, indicating that the disease is not restricted to captive-bred animals on game farms or zoological gardens. The potential role of wildlife species in the transmission and maintenance of LSDV is further discussed and requires continuing investigation, as the virus and disease may pose a serious threat to endangered species. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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16 pages, 6820 KiB

Open AccessArticle

Harnessing Attenuation-Related Mutations of Viral Genomes: Development of a Serological Assay to Differentiate between Capripoxvirus-Infected and -Vaccinated Animals

by Francisco J. Berguido, Tesfaye Rufael Chibssa, Angelika Loitsch, Yang Liu, Kiril Krstevski, Igor Djadjovski, Eeva Tuppurainen, Tamaš Petrović, Dejan Vidanović, Philippe Caufour, Tirumala Bharani K. Settypalli, Clemens Grünwald-Gruber, Reingard Grabherr, Adama Diallo, Giovanni Cattoli and Charles Euloge Lamien

Viruses 2023, 15(12), 2318; https://doi.org/10.3390/v15122318 - 25 Nov 2023

Viewed by 1221

Abstract

Sheeppox, goatpox, and lumpy skin disease caused by the sheeppox virus (SPPV), goatpox virus (GTPV), and lumpy skin disease virus (LSDV), respectively, are diseases that affect millions of ruminants and many low-income households in endemic countries, leading to great economic losses for the [...] Read more.

Sheeppox, goatpox, and lumpy skin disease caused by the sheeppox virus (SPPV), goatpox virus (GTPV), and lumpy skin disease virus (LSDV), respectively, are diseases that affect millions of ruminants and many low-income households in endemic countries, leading to great economic losses for the ruminant industry. The three viruses are members of the Capripoxvirus genus of the Poxviridae family. Live attenuated vaccines remain the only efficient means for controlling capripox diseases. However, serological tools have not been available to differentiate infected from vaccinated animals (DIVA), though crucial for proper disease surveillance, control, and eradication efforts. We analysed the sequences of variola virus B22R homologue gene for SPPV, GTPV, and LSDV and observed significant differences between field and vaccine strains in all three capripoxvirus species, resulting in the truncation and absence of the B22R protein in major vaccines within each of the viral species. We selected and expressed a protein fragment present in wildtype viruses but absent in selected vaccine strains of all three species, taking advantage of these alterations in the B22R gene. An indirect ELISA (iELISA) developed using this protein fragment was evaluated on well-characterized sera from vaccinated, naturally and experimentally infected, and negative cattle and sheep. The developed wildtype-specific capripox DIVA iELISA showed >99% sensitivity and specificity for serum collected from animals infected with the wildtype virus. To the best of our knowledge, this is the first wildtype-specific, DIVA-capable iELISA for poxvirus diseases exploiting changes in nucleotide sequence alterations in vaccine strains. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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17 pages, 6658 KiB

Open AccessArticle

Lumpy Skin Disease Virus Genome Sequence Analysis: Putative Spatio-Temporal Epidemiology, Single Gene versus Whole Genome Phylogeny and Genomic Evolution

by Floris C. Breman, Andy Haegeman, Nina Krešić, Wannes Philips and Nick De Regge

Viruses 2023, 15(7), 1471; https://doi.org/10.3390/v15071471 - 28 Jun 2023

Cited by 6 | Viewed by 1659

Abstract

Lumpy Skin Disease virus is a poxvirus from the genus Capripox that mainly affects bovines and it causes severe economic losses to livestock holders. The Lumpy Skin Disease virus is currently dispersing in Asia, but little is known about detailed phylogenetic relations between [...] Read more.

Lumpy Skin Disease virus is a poxvirus from the genus Capripox that mainly affects bovines and it causes severe economic losses to livestock holders. The Lumpy Skin Disease virus is currently dispersing in Asia, but little is known about detailed phylogenetic relations between the strains and genome evolution. We reconstructed a whole-genome-sequence (WGS)-based phylogeny and compared it with single-gene-based phylogenies. To study population and spatiotemporal patterns in greater detail, we reconstructed networks. We determined that there are strains from multiple clades within the previously defined cluster 1.2 that correspond with recorded outbreaks across Eurasia and South Asia (Indian subcontinent), while strains from cluster 2.5 spread in Southeast Asia. We concluded that using only a single gene (cheap, fast and easy to routinely use) for sequencing lacks phylogenetic and spatiotemporal resolution and we recommend to create at least one WGS whenever possible. We also found that there are three gene regions, highly variable, across the genome of LSDV. These gene regions are located in the 5′ and 3′ flanking regions of the LSDV genome and they encode genes that are involved in immune evasion strategies of the virus. These may provide a starting point to further investigate the evolution of the virus. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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13 pages, 1685 KiB

Open AccessArticle

Evidence of Lumpy Skin Disease Virus Transmission from Subclinically Infected Cattle by Stomoxys calcitrans

by Andy Haegeman, Charlotte Sohier, Laurent Mostin, Ilse De Leeuw, Willem Van Campe, Wannes Philips, Nick De Regge and Kris De Clercq

Viruses 2023, 15(6), 1285; https://doi.org/10.3390/v15061285 - 30 May 2023

Cited by 7 | Viewed by 1762

Abstract

Lumpy skin disease virus (LSDV) is a vector-transmitted capripox virus that causes disease in cattle. Stomoxys calcitrans flies are considered to be important vectors as they are able to transmit viruses from cattle with the typical LSDV skin nodules to naive cattle. No [...] Read more.

Lumpy skin disease virus (LSDV) is a vector-transmitted capripox virus that causes disease in cattle. Stomoxys calcitrans flies are considered to be important vectors as they are able to transmit viruses from cattle with the typical LSDV skin nodules to naive cattle. No conclusive data are, however, available concerning the role of subclinically or preclinically infected cattle in virus transmission. Therefore, an in vivo transmission study with 13 donors, experimentally inoculated with LSDV, and 13 naïve acceptor bulls was performed whereby S. calcitrans flies were fed on either subclinical- or preclinical-infected donor animals. Transmission of LSDV from subclinical donors showing proof of productive virus replication but without formation of skin nodules was demonstrated in two out of five acceptor animals, while no transmission was seen from preclinical donors that developed nodules after Stomoxys calcitrans flies had fed. Interestingly, one of the acceptor animals which became infected developed a subclinical form of the disease. Our results show that subclinical animals can contribute to virus transmission. Therefore, stamping out only clinically diseased LSDV-infected cattle could be insufficient to completely halt the spread and control of the disease. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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16 pages, 6260 KiB

Open AccessArticle

Poxvirus Infections in Dairy Farms and Transhumance Cattle Herds in Nigeria

by David Oludare Omoniwa, Irene Kasindi Meki, Caleb Ayuba Kudi, Anthony Kojo Sackey, Maryam Aminu, Adeyinka Jeremy Adedeji, Clement Adebajo Meseko, Pam Dachung Luka, Olayinka Oluwafemi Asala, Jolly Amoche Adole, Rebecca Bitiyong Atai, Yakubu Joel Atuman, Tirumala Bharani Kumar Settypalli, Giovanni Cattoli and Charles Euloge Lamien

Viruses 2023, 15(5), 1051; https://doi.org/10.3390/v15051051 - 25 Apr 2023

Cited by 1 | Viewed by 1538

Abstract

Lumpy Skin disease (LSD) is an economically important disease in cattle caused by the LSD virus (LSDV) of the genus Capripoxvirus, while pseudocowpox (PCP) is a widely distributed zoonotic cattle disease caused by the PCP virus (PCPV) of the genus Parapoxvirus. [...] Read more.

Lumpy Skin disease (LSD) is an economically important disease in cattle caused by the LSD virus (LSDV) of the genus Capripoxvirus, while pseudocowpox (PCP) is a widely distributed zoonotic cattle disease caused by the PCP virus (PCPV) of the genus Parapoxvirus. Though both viral pox infections are reportedly present in Nigeria, similarities in their clinical presentation and limited access to laboratories often lead to misdiagnosis in the field. This study investigated suspected LSD outbreaks in organized and transhumance cattle herds in Nigeria in 2020. A total of 42 scab/skin biopsy samples were collected from 16 outbreaks of suspected LSD in five northern States of Nigeria. The samples were analyzed using a high-resolution multiplex melting (HRM) assay to differentiate poxviruses belonging to Orthopoxvirus, Capripoxvirus, and Parapoxvirus genera. LSDV was characterized using four gene segments, namely the RNA polymerase 30 kDa subunit (RPO30), G-protein-coupled receptor (GPCR), the extracellular enveloped virus (EEV) glycoprotein and CaPV homolog of the variola virus B22R. Likewise, the partial B2L gene of PCPV was also analyzed. Nineteen samples (45.2%) were positive according to the HRM assay for LSDV, and five (11.9%) were co-infected with LSDV and PCPV. The multiple sequence alignments of the GPCR, EEV, and B22R showed 100% similarity among the Nigerian LSDV samples, unlike the RPO30 phylogeny, which showed two clusters. Some of the Nigerian LSDVs clustered within LSDV SG II were with commonly circulating LSDV field isolates in Africa, the Middle East, and Europe, while the remaining Nigerian LSDVs produced a unique sub-group. The B2L sequences of Nigerian PCPVs were 100% identical and clustered within the PCPV group containing cattle/Reindeer isolates, close to PCPVs from Zambia and Botswana. The results show the diversity of Nigerian LSDV strains. This paper also reports the first documented co-infection of LSDV and PCPV in Nigeria. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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13 pages, 474 KiB

Open AccessArticle

Development and Validation of a New DIVA Real-Time PCR Allowing to Differentiate Wild-Type Lumpy Skin Disease Virus Strains, Including the Asian Recombinant Strains, from Neethling-Based Vaccine Strains

by Andy Haegeman, Ilse De Leeuw, Wannes Philips and Nick De Regge

Viruses 2023, 15(4), 870; https://doi.org/10.3390/v15040870 - 28 Mar 2023

Cited by 7 | Viewed by 2183

Abstract

The current epidemic in Asia, driven by LSDV recombinants, poses difficulties to existing DIVA PCR tests, as these do not differentiate between homologous vaccine strains and the recombinant strains. We, therefore, developed and validated a new duplex real-time PCR capable of differentiating Neethling-based [...] Read more.

The current epidemic in Asia, driven by LSDV recombinants, poses difficulties to existing DIVA PCR tests, as these do not differentiate between homologous vaccine strains and the recombinant strains. We, therefore, developed and validated a new duplex real-time PCR capable of differentiating Neethling-based vaccine strains from classical and recombinant wild-type strains that are currently circulating in Asia. The DIVA potential of this new assay, seen in the in silico evaluation, was confirmed on samples from LSDV infected and vaccinated animals and on isolates of LSDV recombinants (n = 12), vaccine (n = 5), and classic wild-type strains (n = 6). No cross-reactivity or a-specificity with other capripox viruses was observed under field conditions in non-capripox viral stocks and negative animals. The high analytical sensitivity is translated into a high diagnostic specificity as more than 70 samples were all correctly detected with Ct values very similar to those of a published first-line pan capripox real-time PCR. Finally, the low inter- and intra-run variability observed shows that the new DIVA PCR is very robust which facilitates its implementation in the lab. All validation parameters that are mentioned above indicate the potential of the newly developed test as a promising diagnostic tool which could help to control the current LSDV epidemic in Asia. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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Review

Jump to: Research, Other

29 pages, 1178 KiB

Open AccessReview

Global Burden of Lumpy Skin Disease, Outbreaks, and Future Challenges

by Mahfuza Akther, Syeda Hasina Akter, Subir Sarker, Joshua W. Aleri, Henry Annandale, Sam Abraham and Jasim M. Uddin

Viruses 2023, 15(9), 1861; https://doi.org/10.3390/v15091861 - 31 Aug 2023

Cited by 7 | Viewed by 2878

Abstract

Lumpy skin disease (LSD), a current global concern, causes economic devastation in livestock industries, with cattle and water buffalo reported to have higher morbidity and lower mortality rates. LSD is caused by lumpy skin disease virus (LSDV), a member of the Poxviridae family. [...] Read more.

Lumpy skin disease (LSD), a current global concern, causes economic devastation in livestock industries, with cattle and water buffalo reported to have higher morbidity and lower mortality rates. LSD is caused by lumpy skin disease virus (LSDV), a member of the Poxviridae family. It is an enzootic, rapidly explorative and sometimes fatal infection, characterized by multiple raised nodules on the skin of infected animals. It was first reported in Zambia in 1929 and is considered endemic in Africa south of the Sahara desert. It has gradually spread beyond Africa into the Middle East, with periodic occurrences in Asian and East European countries. Recently, it has been spreading in most Asian countries including far East Asia and threatens incursion to LSD-free countries. Rapid and accurate diagnostic capabilities, virus identification, vaccine development, vector control, regional and international collaborations and effective biosecurity policies are important for the control, prevention, and eradication of LSD infections. This review critically evaluates the global burden of LSD, the chronological historical outbreaks of LSD, and future directions for collaborative global actions. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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Other

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9 pages, 1892 KiB

Open AccessBrief Report

Estimating the Transmission Kernel for Lumpy Skin Disease Virus from Data on Outbreaks in Thailand in 2021

by Veerasak Punyapornwithaya, Roderick Salvador, Wittawat Modethed, Orapun Arjkumpa, Chaiwat Jarassaeng, Georgina Limon and Simon Gubbins

Viruses 2023, 15(11), 2196; https://doi.org/10.3390/v15112196 - 31 Oct 2023

Cited by 1 | Viewed by 1540

Abstract

Nationwide outbreaks of lumpy skin disease (LSD) were observed in Thailand in 2021. A better understanding of its disease transmission is crucial. This study utilized a kernel-based approach to characterize the transmission of LSD between cattle herds. Outbreak data from the Khon Kaen [...] Read more.

Nationwide outbreaks of lumpy skin disease (LSD) were observed in Thailand in 2021. A better understanding of its disease transmission is crucial. This study utilized a kernel-based approach to characterize the transmission of LSD between cattle herds. Outbreak data from the Khon Kaen and Lamphun provinces in Thailand were used to estimate transmission kernels for each province. The results showed that the majority of herd-to-herd transmission occurs over short distances. For Khon Kaen, the median transmission distance from the donor herd was estimated to be between 0.3 and 0.8 km, while for Lamphun, it ranged from 0.2 to 0.6 km. The results imply the critical role that insects may play as vectors in the transmission of LSD within the two study areas. This is the first study to estimate transmission kernels from data on LSD outbreaks in Thailand. The findings from this study offer valuable insights into the spatial transmission of this disease, which will be useful in developing prevention and control strategies. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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71 pages, 2367 KiB

Open AccessSystematic Review

Lumpy Skin Disease: A Systematic Review of Mode of Transmission, Risk of Emergence and Risk Entry Pathway

by Juana Bianchini, Xavier Simons, Marie-France Humblet and Claude Saegerman

Viruses 2023, 15(8), 1622; https://doi.org/10.3390/v15081622 - 25 Jul 2023

Cited by 10 | Viewed by 5480

Abstract

The spread of lumpy skin disease (LSD) to free countries over the last 10 years, particularly countries in Europe, Central and South East Asia, has highlighted the threat of emergence in new areas or re-emergence in countries that achieved eradication. This review aimed [...] Read more.

The spread of lumpy skin disease (LSD) to free countries over the last 10 years, particularly countries in Europe, Central and South East Asia, has highlighted the threat of emergence in new areas or re-emergence in countries that achieved eradication. This review aimed to identify studies on LSD epidemiology. A focus was made on hosts, modes of transmission and spread, risks of outbreaks and emergence in new areas. In order to summarize the research progress regarding the epidemiological characteristics of LSD virus over the last 40 years, the Preferred Reporting Items for Systematic reviews and Meta-Analyses statement guidelines were followed, via two databases, i.e., PubMed (biomedical literature) and Scopus (peer-reviewed literature including scientific journals, books, and conference proceedings). A total of 86 scientific articles were considered and classified according to the type of epidemiological study, i.e., experimental versus observational. The main findings and limitations of the retrieved articles were summarized: buffaloes are the main non-cattle hosts, the main transmission mode is mechanical, i.e., via blood-sucking vectors, and stable flies are the most competent vectors. Vectors are mainly responsible for a short-distance spread, while cattle trade spread the virus over long distances. Furthermore, vaccine-recombinant strains have emerged. In conclusion, controlling animal trade and insects in animal transport trucks are the most appropriate measures to limit or prevent LSD (re)emergence. Full article

(This article belongs to the Special Issue Capripox Viruses: A Continuing Transboundary Threat to Animal Health)

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