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Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (15 November 2020) | Viewed by 82251

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Prof. Dr. Jônatas Abrahão

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Department of Microbiology, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte 31270-901, MT, Brazil
Interests: giant viruses; large viruses; evolution; host–virus interactions
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Prof. Dr. Hermann Meyer

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Bundeswehr Institute of Microbiology, Neuherbergstr. 11, 80937 Munich, Germany
Interests: poxviruses; diagnostics; PCR; NGS; bioterrorism; biosafety; biosecurity
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Dear Colleagues,

Forty-two years ago, in 1977, the last known natural case of smallpox was reported in Somalia. Subsequently, in 1980, following a historic global campaign of surveillance and vaccination, the World Health Assembly declared smallpox to be eradicated. This achievement was certainly reached by a well-coordinated campaign, involving brilliant minds from basic poxvirology, vaccinology, epidemiology, and public health organs.

However, after the smallpox eradication, vaccination campaigns gradually ceased. A lack of vaccinations nevertheless creates a growing population of people now susceptible to infection by poxviruses, previously covered by the smallpox vaccine. These include the orthopoxviruses monkeypox, cowpox, and vaccinia virus. Coincidently or not, in the last decades, an increasing number of cases involving these zoonotic OPVs has been described. This has raised concerns, not only with regard to the (re-)emergence of OPVs, but also about the intentional use of, in particular, the variola virus in bioterrorism attacks. Thus, understanding the epidemiology of zoonotic OPVs is in the interest of public health.

In 2017, Viruses published a successful Special Issue on this topic, with 29 papers from many of the most important experts in the field. In 2019–2020, we will reopen this popular Special Issue for new submissions, in which we welcome the poxvirus community to submit research papers or review articles related to all aspects of orthopoxvirus research, from historical reports to the description of new orthopoxvirus strains. Phylogenetic and epidemiological studies are welcome, as well as papers covering topics like bioterrorism, medical countermeasures, and studies of basic and host–virus relationships.

Prof. Dr. Jonatas Abrahao
Prof. Dr. Hermann Meyer
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Viruses is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

poxvirus
smallpox
variola virus
cowpox virus
vaccinia virus
monkeypox virus
bioterrorism
vaccine
antiviral

Related Special Issue

Smallpox and Emerging Zoonotic Orthopoxviruses: What Is Coming Next? in Viruses (29 articles)

Published Papers (11 papers)

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23 pages, 6695 KiB

Open AccessArticle

Comparative Pathogenesis, Genomics and Phylogeography of Mousepox

by Carla Mavian, Alberto López-Bueno, Rocío Martín, Andreas Nitsche and Antonio Alcamí

Viruses 2021, 13(6), 1146; https://doi.org/10.3390/v13061146 - 15 Jun 2021

Cited by 4 | Viewed by 2526

Abstract

Ectromelia virus (ECTV), the causative agent of mousepox, has threatened laboratory mouse colonies worldwide for almost a century. Mousepox has been valuable for the understanding of poxvirus pathogenesis and immune evasion. Here, we have monitored in parallel the pathogenesis of nine ECTVs in BALB/cJ mice and report the full-length genome sequence of eight novel ECTV isolates or strains, including the first ECTV isolated from a field mouse, ECTV-MouKre. This approach allowed us to identify several genes, absent in strains attenuated through serial passages in culture, that may play a role in virulence and a set of putative genes that may be involved in enhancing viral growth in vitro. We identified a putative strong inhibitor of the host inflammatory response in ECTV-MouKre, an isolate that did not cause local foot swelling and developed a moderate virulence. Most of the ECTVs, except ECTV-Hampstead, encode a truncated version of the P4c protein that impairs the recruitment of virions into the A-type inclusion bodies, and our data suggest that P4c may play a role in viral dissemination and transmission. This is the first comprehensive report that sheds light into the phylogenetic and geographic relationship of the worldwide outbreak dynamics for the ECTV species. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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11 pages, 2225 KiB

Open AccessArticle

Laboratory Infection of Novel Akhmeta Virus in CAST/EiJ Mice

by Clint N. Morgan, Audrey M. Matheny, Yoshinori J. Nakazawa, Chantal Kling, Nadia Gallardo-Romero, Laurie Seigler, Galileu Barbosa Costa, Christina Hutson, Giorgi Maghlakelidze, Victoria Olson and Jeffrey B. Doty

Viruses 2020, 12(12), 1416; https://doi.org/10.3390/v12121416 - 09 Dec 2020

Cited by 2 | Viewed by 2504

Abstract

Akhmeta virus is a zoonotic Orthopoxvirus first identified in 2013 in the country of Georgia. Subsequent ecological investigations in Georgia have found evidence that this virus is widespread in its geographic distribution within the country and in its host-range, with rodents likely involved in its circulation in the wild. Yet, little is known about the pathogenicity of this virus in rodents. We conducted the first laboratory infection of Akhmeta virus in CAST/EiJ Mus musculus to further characterize this novel virus. We found a dose-dependent effect on mortality and weight loss (p < 0.05). Anti-orthopoxvirus antibodies were detected in the second- and third-highest dose groups (5 × 10⁴ pfu and 3 × 10² pfu) at euthanasia by day 10, and day 14 post-infection, respectively. Anti-orthopoxvirus antibodies were not detected in the highest dose group (3 × 10⁶ pfu), which were euthanized at day 7 post-infection and had high viral load in tissues, suggesting they succumbed to disease prior to mounting an effective immune response. In order of highest burden, viable virus was detected in the nostril, lung, tail, liver and spleen. All individuals tested in the highest dose groups were DNAemic. Akhmeta virus was highly pathogenic in CAST/EiJ Mus musculus, causing 100% mortality when ≥3 × 10² pfu was administered. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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13 pages, 2110 KiB

Open AccessArticle

Effect of the Route of Administration of the Vaccinia Virus Strain LIVP to Mice on Its Virulence and Immunogenicity

by Sergei N. Shchelkunov, Stanislav N. Yakubitskiy, Alexander A. Sergeev, Alexei S. Kabanov, Tatiana V. Bauer, Leonid E. Bulychev and Stepan A. Pyankov

Viruses 2020, 12(8), 795; https://doi.org/10.3390/v12080795 - 24 Jul 2020

Cited by 9 | Viewed by 2196

Abstract

The mass smallpox vaccination campaign has played a crucial role in smallpox eradication. Various strains of the vaccinia virus (VACV) were used as a live smallpox vaccine in different countries, their origin being unknown in most cases. The VACV strains differ in terms of pathogenicity exhibited upon inoculation of laboratory animals and reactogenicity exhibited upon vaccination of humans. Therefore, each generated strain or clonal variant of VACV needs to be thoroughly studied in in vivo systems. The clonal variant 14 of LIVP strain (LIVP-14) was the study object in this work. A comparative analysis of the virulence and immunogenicity of LIVP-14 inoculated intranasally (i.n.), intradermally (i.d.), or subcutaneously (s.c.) to BALB/c mice at doses of 10⁸, 10⁷, and 10⁶ pfu was carried out. Adult mice exhibited the highest sensitivity to the i.n. administered LIVP-14 strain, although the infection was not lethal. The i.n. inoculated LIVP-14 replicated efficiently in the lungs. Furthermore, this virus was accumulated in the brain at relatively high concentrations. Significantly lower levels of LIVP-14 were detected in the liver, kidneys, and spleen of experimental animals. No clinical manifestations of the disease were observed after i.d. or s.c. injection of LIVP-14 to mice. After s.c. inoculation, the virus was detected only at the injection site, while it could disseminate to the liver and lungs when delivered via i.d. administration. A comparative analysis of the production of virus-specific antibodies by ELISA and PRNT revealed that the highest level of antibodies was induced in i.n. inoculated mice; a lower level of antibodies was observed after i.d. administration of the virus and the lowest level after s.c. injection. Even at the lowest studied dose (10⁶ pfu), i.n. or i.d. administered LIVP-14 completely protected mice against infection with the cowpox virus at the lethal dose. Our findings imply that, according to the ratio between such characteristics as pathogenicity/immunogenicity/protectivity, i.d. injection is the optimal method of inoculation with the VACV LIVP-14 strain to ensure the safe formation of immune defense after vaccination against orthopoxviral infections. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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16 pages, 3612 KiB

Open AccessArticle

Comparison of Multiplexed Immunofluorescence Imaging to Chromogenic Immunohistochemistry of Skin Biomarkers in Response to Monkeypox Virus Infection

by Anup Sood, Yunxia Sui, Elizabeth McDonough, Alberto Santamaría-Pang, Yousef Al-Kofahi, Zhengyu Pang, Peter B. Jahrling, Jens H. Kuhn and Fiona Ginty

Viruses 2020, 12(8), 787; https://doi.org/10.3390/v12080787 - 23 Jul 2020

Cited by 23 | Viewed by 4952

Abstract

Over the last 15 years, advances in immunofluorescence-imaging based cycling methods, antibody conjugation methods, and automated image processing have facilitated the development of a high-resolution, multiplexed tissue immunofluorescence (MxIF) method with single cell-level quantitation termed Cell DIVE^TM. Originally developed for fixed oncology samples, here it was evaluated in highly fixed (up to 30 days), archived monkeypox virus-induced inflammatory skin lesions from a retrospective study in 11 rhesus monkeys to determine whether MxIF was comparable to manual H-scoring of chromogenic stains. Six protein markers related to immune and cellular response (CD68, CD3, Hsp70, Hsp90, ERK1/2, ERK1/2 pT202_pY204) were manually quantified (H-scores) by a pathologist from chromogenic IHC double stains on serial sections and compared to MxIF automated single cell quantification of the same markers that were multiplexed on a single tissue section. Overall, there was directional consistency between the H-score and the MxIF results for all markers except phosphorylated ERK1/2 (ERK1/2 pT202_pY204), which showed a decrease in the lesion compared to the adjacent non-lesioned skin by MxIF vs an increase via H-score. Improvements to automated segmentation using machine learning and adding additional cell markers for cell viability are future options for improvement. This method could be useful in infectious disease research as it conserves tissue, provides marker colocalization data on thousands of cells, allowing further cell level data mining as well as a reduction in user bias. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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14 pages, 2363 KiB

Open AccessArticle

Conserved Oligomeric Golgi (COG) Complex Proteins Facilitate Orthopoxvirus Entry, Fusion and Spread

by Susan Realegeno, Lalita Priyamvada, Amrita Kumar, Jessica B. Blackburn, Claire Hartloge, Andreas S. Puschnik, Suryaprakash Sambhara, Victoria A. Olson, Jan E. Carette, Vladimir Lupashin and Panayampalli Subbian Satheshkumar

Viruses 2020, 12(7), 707; https://doi.org/10.3390/v12070707 - 30 Jun 2020

Cited by 17 | Viewed by 3665

Abstract

Although orthopoxviruses (OPXV) are known to encode a majority of the genes required for replication in host cells, genome-wide genetic screens have revealed that several host pathways are indispensable for OPXV infection. Through a haploid genetic screen, we previously identified several host genes required for monkeypox virus (MPXV) infection, including the individual genes that form the conserved oligomeric Golgi (COG) complex. The COG complex is an eight-protein (COG1–COG8) vesicle tethering complex important for regulating membrane trafficking, glycosylation enzymes, and maintaining Golgi structure. In this study, we investigated the role of the COG complex in OPXV infection using cell lines with individual COG gene knockout (KO) mutations. COG KO cells infected with MPXV and vaccinia virus (VACV) produced small plaques and a lower virus yield compared to wild type (WT) cells. In cells where the KO phenotype was reversed using a rescue plasmid, the size of virus plaques increased demonstrating a direct link between the decrease in viral spread and the KO of COG genes. KO cells infected with VACV displayed lower levels of viral fusion and entry compared to WT suggesting that the COG complex is important for early events in OPXV infection. Additionally, fewer actin tails were observed in VACV-infected KO cells compared to WT. Since COG complex proteins are required for cellular trafficking of glycosylated membrane proteins, the disruption of this process due to lack of individual COG complex proteins may potentially impair the virus-cell interactions required for viral entry and egress. These data validate that the COG complex previously identified in our genetic screens plays a role in OPXV infection. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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19 pages, 1526 KiB

Open AccessArticle

In Vivo Characterization of a Bank Vole-Derived Cowpox Virus Isolate in Natural Hosts and the Rat Model

by Saskia Weber, Kathrin Jeske, Rainer G. Ulrich, Christian Imholt, Jens Jacob, Martin Beer and Donata Hoffmann

Viruses 2020, 12(2), 237; https://doi.org/10.3390/v12020237 - 20 Feb 2020

Cited by 3 | Viewed by 2611

Abstract

Cowpox virus (CPXV) belongs to the genus Orthopoxvirus in the Poxviridae family and is endemic in western Eurasia. Based on seroprevalence studies in different voles from continental Europe and UK, voles are suspected to be the major reservoir host. Recently, a CPXV was isolated from a bank vole (Myodes glareolus) in Germany that showed a high genetic similarity to another isolate originating from a Cotton-top tamarin (Saguinus oedipus). Here we characterize this first bank vole-derived CPXV isolate in comparison to the related tamarin-derived isolate. Both isolates grouped genetically within the provisionally called CPXV-like 3 clade. Previous phylogenetic analysis indicated that CPXV is polyphyletic and CPXV-like 3 clade represents probably a different species if categorized by the rules used for other orthopoxviruses. Experimental infection studies with bank voles, common voles (Microtus arvalis) and Wistar rats showed very clear differences. The bank vole isolate was avirulent in both common voles and Wistar rats with seroconversion seen only in the rats. In contrast, inoculated bank voles exhibited viral shedding and seroconversion for both tested CPXV isolates. In addition, bank voles infected with the tamarin-derived isolate experienced a marked weight loss. Our findings allow for the conclusion that CPXV isolates might differ in their replication capacity in different vole species and rats depending on their original host. Moreover, the results indicate host-specific differences concerning CPXV-specific virulence. Further experiments are needed to identify individual virulence and host factors involved in the susceptibility and outcome of CPXV-infections in the different reservoir hosts. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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12 pages, 587 KiB

Open AccessArticle

Field Trial Vaccination against Cowpox in Two Alpaca Herds

by Almut Prkno, Donata Hoffmann, Matthias Kaiser, Daniela Goerigk, Martin Pfeffer, Karsten Winter, Thomas W. Vahlenkamp, Martin Beer and Alexander Starke

Viruses 2020, 12(2), 234; https://doi.org/10.3390/v12020234 - 20 Feb 2020

Cited by 3 | Viewed by 2845

Abstract

In Europe, cowpox virus (CPXV) infection in South American camelids occurs as a so-called spill-over infection. Although infected animals generally have a mild form of the disease and survive, cases of fatal generalised CPXV infection have also been described. Prevention by prophylactic vaccination is the only way to protect animals from disease. In the present study, modified vaccinia virus Ankara (MVA) vaccine, which has been successfully used in many animal species, was used in a prime-boost vaccination regimen in two alpaca herds with a history of CPXV infection. The focus of the study was the prevention of further clinical cases, and to determine the safety and immunogenicity of the MVA vaccine in alpacas. The MVA vaccine was well tolerated and safe in the 94 animals vaccinated. An indirect immunofluorescence assay (IFA) using MVA as an antigen showed that the seroprevalence of antibody after booster vaccination was 81.3% in herd I and 91.7% in herd II. Detectable antibody titres declined to 15.6% in herd I and 45.8% in herd II over a 12-month period after booster vaccination. Animals could be divided into four groups based on individual antibody titres determined over one year: Group 1 consisted of 19.3% of animals that were seropositive until the end of the trial period; Group 2 consisted of 58.0% of animals that were seropositive after booster vaccination, but seronegative one year later; Group 3 consisted of 14.7% of animals that were not seropositive at any time point; and Group 4 consisted of 7.9% of animals that were seropositive after initial immunisation, seronegative six months later, but seropositive or intermediate in IFA one year after immunisation, likely because of natural exposure. In new-born crias born to MVA-vaccinated mares, specific maternal antibodies were detected in 50.0% of animals up to 14 weeks of age. Our results confirm that MVA vaccination is a feasible tool for the prevention of CPXV disease in alpacas. Long-term studies are needed to verify future vaccination regimen in CPXV affected herds. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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20 pages, 822 KiB

Open AccessReview

Here, There, and Everywhere: The Wide Host Range and Geographic Distribution of Zoonotic Orthopoxviruses

by Natalia Ingrid Oliveira Silva, Jaqueline Silva de Oliveira, Erna Geessien Kroon, Giliane de Souza Trindade and Betânia Paiva Drumond

Viruses 2021, 13(1), 43; https://doi.org/10.3390/v13010043 - 30 Dec 2020

Cited by 97 | Viewed by 9222

Abstract

The global emergence of zoonotic viruses, including poxviruses, poses one of the greatest threats to human and animal health. Forty years after the eradication of smallpox, emerging zoonotic orthopoxviruses, such as monkeypox, cowpox, and vaccinia viruses continue to infect humans as well as wild and domestic animals. Currently, the geographical distribution of poxviruses in a broad range of hosts worldwide raises concerns regarding the possibility of outbreaks or viral dissemination to new geographical regions. Here, we review the global host ranges and current epidemiological understanding of zoonotic orthopoxviruses while focusing on orthopoxviruses with epidemic potential, including monkeypox, cowpox, and vaccinia viruses. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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29 pages, 1630 KiB

Open AccessReview

Monkeypox Virus in Nigeria: Infection Biology, Epidemiology, and Evolution

by Emmanuel Alakunle, Ugo Moens, Godwin Nchinda and Malachy Ifeanyi Okeke

Viruses 2020, 12(11), 1257; https://doi.org/10.3390/v12111257 - 05 Nov 2020

Cited by 418 | Viewed by 35384

Abstract

Monkeypox is a zoonotic disease caused by monkeypox virus (MPXV), which is a member of orthopoxvirus genus. The reemergence of MPXV in 2017 (at Bayelsa state) after 39 years of no reported case in Nigeria, and the export of travelers’ monkeypox (MPX) from Nigeria to other parts of the world, in 2018 and 2019, respectively, have raised concern that MPXV may have emerged to occupy the ecological and immunological niche vacated by smallpox virus. This review X-rays the current state of knowledge pertaining the infection biology, epidemiology, and evolution of MPXV in Nigeria and worldwide, especially with regard to the human, cellular, and viral factors that modulate the virus transmission dynamics, infection, and its maintenance in nature. This paper also elucidates the role of recombination, gene loss and gene gain in MPXV evolution, chronicles the role of signaling in MPXV infection, and reviews the current therapeutic options available for the treatment and prevention of MPX. Additionally, genome-wide phylogenetic analysis was undertaken, and we show that MPXV isolates from recent 2017 outbreak in Nigeria were monophyletic with the isolate exported to Israel from Nigeria but do not share the most recent common ancestor with isolates obtained from earlier outbreaks, in 1971 and 1978, respectively. Finally, the review highlighted gaps in knowledge particularly the non-identification of a definitive reservoir host animal for MPXV and proposed future research endeavors to address the unresolved questions. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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11 pages, 252 KiB

Open AccessReview

Smallpox in the Post-Eradication Era

by Hermann Meyer, Rosina Ehmann and Geoffrey L. Smith

Viruses 2020, 12(2), 138; https://doi.org/10.3390/v12020138 - 24 Jan 2020

Cited by 89 | Viewed by 11959

Abstract

Widespread vaccination programmes led to the global eradication of smallpox, which was certified by the World Health Organisation (WHO), and, since 1978, there has been no case of smallpox anywhere in the world. However, the viable variola virus (VARV), the causative agent of smallpox, is still kept in two maximum security laboratories in Russia and the USA. Despite the eradication of the disease smallpox, clandestine stocks of VARV may exist. In a rapidly changing world, the impact of an intentional VARV release in the human population would nowadays result in a public health emergency of global concern: vaccination programmes were abolished, the percentage of immunosuppressed individuals in the human population is higher, and an increased intercontinental air travel allows for the rapid viral spread of diseases around the world. The WHO has authorised the temporary retention of VARV to enable essential research for public health benefit to take place. This work aims to develop diagnostic tests, antiviral drugs, and safer vaccines. Advances in synthetic biology have made it possible to produce infectious poxvirus particles from chemicals in vitro so that it is now possible to reconstruct VARV. The status of smallpox in the post-eradication era is reviewed. Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

Other

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7 pages, 915 KiB

Open AccessBrief Report

Genome Sequencing of a Camelpox Vaccine Reveals Close Similarity to Modified Vaccinia virus Ankara (MVA)

by Maurilia Marcacci, Abdelmalik I. Khalafalla, Zulaikha M. Al Hammadi, Federica Monaco, Cesare Cammà, Mohammed F. Yusof, Saeed M. Al Yammahi, Iolanda Mangone, Fabrizia Valleriani, Mohamed A. Alhosani, Nicola Decaro, Alessio Lorusso, Salama S. Almuhairi and Giovanni Savini

Viruses 2020, 12(8), 786; https://doi.org/10.3390/v12080786 - 23 Jul 2020

Cited by 3 | Viewed by 2551

Abstract

Camelpox is a viral contagious disease of Old-World camelids sustained by Camelpox virus (CMLV). The disease is characterized by mild, local skin or severe systemic infections and may have a major economic impact due to significant losses in terms of morbidity and mortality, weight loss, and low milk yield. Prevention of camelpox is performed by vaccination. In this study, we investigated the composition of a CMLV-based, live-attenuated commercial vaccine using next-generation sequencing (NGS) technology. The results of this analysis revealed genomic sequences of Modified Vaccinia virus Ankara (MVA). Full article

(This article belongs to the Special Issue Smallpox and Emerging Zoonotic Orthopoxviruses 2.0: What Is Coming Next?)

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