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SARS-CoV-2 and Animal Models
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SARS-CoV-2 and Animal Models

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "SARS-CoV-2 and COVID-19".

Deadline for manuscript submissions: closed (31 March 2023) | Viewed by 83690

Special Issue Editor

Dr. F. Javier Salguero

E-Mail Website
Guest Editor
Public Health England, PHE Porton Down, Salisbury SP4 0JG, UK
Interests: comparative pathology; animal models; infectious diseases; zoonoses; public health; transboundary and emerging diseases; 3Rs

Special Issue Information

Dear Colleagues,

The current COVID-19 pandemic caused by severe acute respiratory syndrome coronavirus (SARS-CoV-2) has resulted in a highly significant public health concern worldwide. Animal models for SARS-CoV-2 infection were established quite rapidly after the initial phases of the pandemic, and they have been crucial to the development of vaccines and therapies against the disease. However, infections and disease models recapitulating the range of the severity of the infection in humans are still missing. Moreover, the emergence of new variants of concern in different regions will need further studies of pathogenicity and transmission, and animal models will play an important role in elucidating the key aspects of these. The development of alternative models in line with the 3Rs is also an important approach to gain further insight into the pathogenesis of this disease.

The aim of this Special Issue is to provide data on the development and application of animal models of SARS-CoV-2 together with new in vitro technologies that will help characterise the infection by this virus and produce effective prophylactic and therapeutic approaches to combat the pandemic.

Dr. F. Javier Salguero
Guest Editor

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Keywords

  • SARS-CoV-2
  • COVID-19
  • animal model
  • infectious disease
  • coronavirus
  • pathology
  • 3Rs
  • immune response
  • in vitro
  • in vivo

Published Papers (21 papers)

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18 pages, 36391 KiB  
Article
Immune Responses and Pathogenesis following Experimental SARS-CoV-2 Infection in Domestic Cats
by Sandra Vreman, Elisabeth M. D. L. van der Heijden, Lars Ravesloot, Irene S. Ludwig, Judith M. A. van den Brand, Frank Harders, Andries A. Kampfraath, Herman F. Egberink, Jose L. Gonzales, Nadia Oreshkova, Femke Broere, Wim H. M. van der Poel and Nora M. Gerhards
Viruses 2023, 15(5), 1052; https://0-doi-org.brum.beds.ac.uk/10.3390/v15051052 - 25 Apr 2023
Viewed by 1783
Abstract
Several reports demonstrated the susceptibility of domestic cats to SARS-CoV-2 infection. Here, we describe a thorough investigation of the immune responses in cats after experimental SARS-CoV-2 inoculation, along with the characterization of infection kinetics and pathological lesions. Specific pathogen-free domestic cats (n [...] Read more.
Several reports demonstrated the susceptibility of domestic cats to SARS-CoV-2 infection. Here, we describe a thorough investigation of the immune responses in cats after experimental SARS-CoV-2 inoculation, along with the characterization of infection kinetics and pathological lesions. Specific pathogen-free domestic cats (n = 12) were intranasally inoculated with SARS-CoV-2 and subsequently sacrificed on DPI (days post-inoculation) 2, 4, 7 and 14. None of the infected cats developed clinical signs. Only mild histopathologic lung changes associated with virus antigen expression were observed mainly on DPI 4 and 7. Viral RNA was present until DPI 7, predominantly in nasal and throat swabs. The infectious virus could be isolated from the nose, trachea and lungs until DPI 7. In the swab samples, no biologically relevant SARS-CoV-2 mutations were observed over time. From DPI 7 onwards, all cats developed a humoral immune response. The cellular immune responses were limited to DPI 7. Cats showed an increase in CD8+ cells, and the subsequent RNA sequence analysis of CD4+ and CD8+ subsets revealed a prominent upregulation of antiviral and inflammatory genes on DPI 2. In conclusion, infected domestic cats developed a strong antiviral response and cleared the virus within the first week after infection without overt clinical signs and relevant virus mutations. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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18 pages, 4234 KiB  
Article
Upper Respiratory Infection Drives Clinical Signs and Inflammatory Responses Following Heterologous Challenge of SARS-CoV-2 Variants of Concern in K18 Mice
by Jacob H. Nichols, Evan P. Williams, Jyothi Parvathareddy, Xueyuan Cao, Ying Kong, Elizabeth Fitzpatrick, Richard J. Webby and Colleen B. Jonsson
Viruses 2023, 15(4), 946; https://0-doi-org.brum.beds.ac.uk/10.3390/v15040946 - 11 Apr 2023
Viewed by 1520
Abstract
The evolution of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has resulted in the emergence of several variants of concern (VOC) with increased immune evasion and transmissibility. This has motivated studies to assess protection conferred by earlier strains following infection or vaccination [...] Read more.
The evolution of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has resulted in the emergence of several variants of concern (VOC) with increased immune evasion and transmissibility. This has motivated studies to assess protection conferred by earlier strains following infection or vaccination to each new VOC. We hypothesized that while NAbs play a major role in protection against infection and disease, a heterologous reinfection or challenge may gain a foothold in the upper respiratory tract (URT) and result in a self-limited viral infection accompanied by an inflammatory response. To test this hypothesis, we infected K18-hACE2 mice with SARS-CoV-2 USA-WA1/2020 (WA1) and, after 24 days, challenged with WA1, Alpha, or Delta. While NAb titers against each virus were similar across all cohorts prior to challenge, the mice challenged with Alpha and Delta showed weight loss and upregulation of proinflammatory cytokines in the URT and lower RT (LRT). Mice challenged with WA1 showed complete protection. We noted increased levels of viral RNA transcripts only in the URT of mice challenged with Alpha and Delta. In conclusion, our results suggested self-limiting breakthrough infections of Alpha or Delta in the URT, which correlated with clinical signs and a significant inflammatory response in mice. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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25 pages, 7250 KiB  
Article
Host Response of Syrian Hamster to SARS-CoV-2 Infection including Differences with Humans and between Sexes
by Martina Castellan, Gianpiero Zamperin, Giulia Franzoni, Greta Foiani, Maira Zorzan, Petra Drzewnioková, Marzia Mancin, Irene Brian, Alessio Bortolami, Matteo Pagliari, Annalisa Oggiano, Marta Vascellari, Valentina Panzarin, Sergio Crovella, Isabella Monne, Calogero Terregino, Paola De Benedictis and Stefania Leopardi
Viruses 2023, 15(2), 428; https://0-doi-org.brum.beds.ac.uk/10.3390/v15020428 - 03 Feb 2023
Cited by 5 | Viewed by 4597
Abstract
The emergence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has highlighted the importance of having proper tools and models to study the pathophysiology of emerging infectious diseases to test therapeutic protocols, assess changes in viral phenotypes, and evaluate the effects of viral [...] Read more.
The emergence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has highlighted the importance of having proper tools and models to study the pathophysiology of emerging infectious diseases to test therapeutic protocols, assess changes in viral phenotypes, and evaluate the effects of viral evolution. This study provided a comprehensive characterization of the Syrian hamster (Mesocricetus auratus) as an animal model for SARS-CoV-2 infection using different approaches (description of clinical signs, viral load, receptor profiling, and host immune response) and targeting four different organs (lungs, intestine, brain, and PBMCs). Our data showed that both male and female hamsters were susceptible to the infection and developed a disease similar to the one observed in patients with COVID-19 that included moderate to severe pulmonary lesions, inflammation, and recruitment of the immune system in the lungs and at the systemic level. However, all animals recovered within 14 days without developing the severe pathology seen in humans, and none of them died. We found faint evidence for intestinal and neurological tropism associated with the absence of lesions and a minimal host response in intestines and brains, which highlighted another crucial difference with the multiorgan impairment of severe COVID-19. When comparing male and female hamsters, we observed that males sustained higher viral RNA shedding and replication in the lungs, suffered from more severe symptoms and histopathological lesions, and triggered higher pulmonary inflammation. Overall, these data confirmed the Syrian hamster as a suitable model for mild to moderate COVID-19 and reflected sex-related differences in the response against the virus observed in humans. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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16 pages, 10278 KiB  
Article
Characterization of Three Variants of SARS-CoV-2 In Vivo Shows Host-Dependent Pathogenicity in Hamsters, While Not in K18-hACE2 Mice
by Gabriela Toomer, Whitney Burns, Liliana Garcia, Gerelyn Henry, Anthony Biancofiori, Albert George, Ciera Duffy, Justin Chu, Morgan Sides, Melissa Muñoz, Kelly Garcia, Anya Nikolai-Yogerst, Xinjian Peng, Landon Westfall and Robert Baker
Viruses 2022, 14(11), 2584; https://0-doi-org.brum.beds.ac.uk/10.3390/v14112584 - 21 Nov 2022
Cited by 5 | Viewed by 2875
Abstract
Animal models are used in preclinical trials to test vaccines, antivirals, monoclonal antibodies, and immunomodulatory drug therapies against SARS-CoV-2. However, these drugs often do not produce equivalent results in human clinical trials. Here, we show how different animal models infected with some of [...] Read more.
Animal models are used in preclinical trials to test vaccines, antivirals, monoclonal antibodies, and immunomodulatory drug therapies against SARS-CoV-2. However, these drugs often do not produce equivalent results in human clinical trials. Here, we show how different animal models infected with some of the most clinically relevant SARS-CoV-2 variants, WA1/2020, B.1.617.2/Delta, B.1.1.529/Omicron, and BA5.2/Omicron, have independent outcomes. We show that in K18-hACE2 mice, B.1.617.2 is more pathogenic, followed by WA1, while B.1.1.529 showed an absence of clinical signs. Only B.1.1.529 was able to infect C57BL/6J mice, which lack the human ACE2 receptor. B.1.1.529-infected C57BL/6J mice had different T cell profiles compared to infected K18-hACE2 mice, while viral shedding profiles and viral titers in lungs were similar between the K18-hACE2 and the C57BL/6J mice. These data suggest B.1.1.529 virus adaptation to a new host and shows that asymptomatic carriers can accumulate and shed virus. Next, we show how B.1.617.2, WA1 and BA5.2/Omicron have similar viral replication kinetics, pathogenicity, and viral shedding profiles in hamsters, demonstrating that the increased pathogenicity of B.1.617.2 observed in mice is host-dependent. Overall, these findings suggest that small animal models are useful to parallel human clinical data, but the experimental design places an important role in interpreting the data. Importance: There is a need to investigate SARS-CoV-2 variant phenotypes in different animal models due to the lack of reproducible outcomes when translating experiments to the human population. Our findings highlight the correlation of clinically relevant SARS-CoV-2 variants in animal models with human infections. Experimental design and understanding of correct animal models are essential to interpreting data to develop antivirals, vaccines, and other therapeutic compounds against COVID-19. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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13 pages, 2746 KiB  
Article
Susceptibility of Domestic Goat (Capra aegagrus hircus) to Experimental Infection with Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) B.1.351/Beta Variant
by Leira Fernández-Bastit, Núria Roca, Miguel Romero-Durana, Jordi Rodon, Guillermo Cantero, Óscar García, Carlos López, Mònica Pérez, Rosa López, Jorge Carrillo, Nuria Izquierdo-Useros, Julià Blanco, Bonaventura Clotet, Joan Pujols, Júlia Vergara-Alert, Joaquim Segalés and Cristina Lorca-Oró
Viruses 2022, 14(9), 2002; https://0-doi-org.brum.beds.ac.uk/10.3390/v14092002 - 09 Sep 2022
Cited by 4 | Viewed by 2489
Abstract
A wide range of animal species are susceptible to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. Natural and/or experimental infections have been reported in pet, zoo, farmed and wild animals. Interestingly, some SARS-CoV-2 variants, such as B.1.1.7/Alpha, B.1.351/Beta, and B.1.1.529/Omicron, were [...] Read more.
A wide range of animal species are susceptible to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. Natural and/or experimental infections have been reported in pet, zoo, farmed and wild animals. Interestingly, some SARS-CoV-2 variants, such as B.1.1.7/Alpha, B.1.351/Beta, and B.1.1.529/Omicron, were demonstrated to infect some animal species not susceptible to classical viral variants. The present study aimed to elucidate if goats (Capra aegagrus hircus) are susceptible to the B.1.351/Beta variant. First, an in silico approach was used to predict the affinity between the receptor-binding domain of the spike protein of SARS-CoV-2 B.1.351/Beta variant and angiotensin-converting enzyme 2 from goats. Moreover, we performed an experimental inoculation with this variant in domestic goat and showed evidence of infection. SARS-CoV-2 was detected in nasal swabs and tissues by RT-qPCR and/or immunohistochemistry, and seroneutralisation was confirmed via ELISA and live virus neutralisation assays. However, the viral amount and tissue distribution suggest a low susceptibility of goats to the B.1.351/Beta variant. Therefore, although monitoring livestock is advisable, it is unlikely that goats play a role as SARS-CoV-2 reservoir species, and they are not useful surrogates to study SARS-CoV-2 infection in farmed animals. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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15 pages, 5639 KiB  
Article
Early Isolates of SARS-CoV-2 Result in Different Pathogenesis in the Transduced Mouse Model of COVID-19
by Sophie J. Smither, Sarah Kempster, Simon L. Priestnall, Alejandro Suárez-Bonnet, Helen Stapleton, Thomas R. Laws, Deborah Ferguson, Neil Almond, Mark S. Lever and E. Diane Williamson
Viruses 2022, 14(8), 1769; https://0-doi-org.brum.beds.ac.uk/10.3390/v14081769 - 13 Aug 2022
Viewed by 1423
Abstract
A transduced mouse model of SARS-CoV-2 infection was established using Balb/c mice. This was achieved through the adenovirus-vectored delivery of the hACE2 gene, to render the mice transiently susceptible to the virus. The model was characterised in terms of the dissemination of hACE2 [...] Read more.
A transduced mouse model of SARS-CoV-2 infection was established using Balb/c mice. This was achieved through the adenovirus-vectored delivery of the hACE2 gene, to render the mice transiently susceptible to the virus. The model was characterised in terms of the dissemination of hACE2 receptor expression, the dissemination of three SARS-CoV-2 virus variants in vivo up to 10 days following challenge, the resulting histopathology and the clinical signs induced in the mice. In transduced mice, the infection was short-term, with a rapid loss in body weight starting at day 2 with maximum weight loss at day 4, followed by subsequent recovery until day 10. The induced expression of the hACE2 receptor was evident in the lungs, but, upon challenge, the SARS-CoV-2 virus disseminated beyond the lungs to spleen, liver and kidney, peaking at day 2 post infection. However, by day 10 post infection, the virus was undetectable. The lung histopathology was characterised by bronchial and alveolar inflammation, which was still present at day 10 post infection. Transduced mice had differential responses to viral variants ranking CVR-Glasgow 1 > Victoria-1 > England-2 isolates in terms of body weight loss. The transduced mouse model provides a consistent and manipulatable model of SARS-CoV-2 infection to screen viral variants for their relative virulence and possible interventions. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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20 pages, 4230 KiB  
Article
Histopathological and Immunological Findings in the Common Marmoset Following Exposure to Aerosolized SARS-CoV-2
by Rachel E. Ireland, Carwyn D. Davies, Emma Keyser, James S. F. Findlay, Lin Eastaugh, Thomas R. Laws, Francisco J. Salguero, Laura Hunter and Michelle Nelson
Viruses 2022, 14(7), 1580; https://0-doi-org.brum.beds.ac.uk/10.3390/v14071580 - 21 Jul 2022
Cited by 2 | Viewed by 1802
Abstract
There is an enduring requirement to develop animal models of COVID-19 to assess the efficacy of vaccines and therapeutics that can be used to treat the disease in humans. In this study, six marmosets were exposed to a small particle aerosol (1–3 µm) [...] Read more.
There is an enduring requirement to develop animal models of COVID-19 to assess the efficacy of vaccines and therapeutics that can be used to treat the disease in humans. In this study, six marmosets were exposed to a small particle aerosol (1–3 µm) of SARS-CoV-2 VIC01 that delivered the virus directly to the lower respiratory tract. Following the challenge, marmosets did not develop clinical signs, although a disruption to the normal diurnal temperature rhythm was observed in three out of six animals. Early weight loss and changes to respiratory pattern and activity were also observed, yet there was limited evidence of viral replication or lung pathology associated with infection. There was a robust innate immunological response to infection, which included an early increase in circulating neutrophils and monocytes and a reduction in the proportion of circulating T-cells. Expression of the ACE2 receptor in respiratory tissues was almost absent, but there was ubiquitous expression of TMPRSS2. The results of this study indicate that exposure of marmosets to high concentrations of aerosolised SARS-CoV-2 did not result in the development of clear, reproducible signs of COVID-19. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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22 pages, 3475 KiB  
Article
Neuroinvasion and Neurotropism by SARS-CoV-2 Variants in the K18-hACE2 Mouse
by Frauke Seehusen, Jordan J. Clark, Parul Sharma, Eleanor G. Bentley, Adam Kirby, Krishanthi Subramaniam, Sabina Wunderlin-Giuliani, Grant L. Hughes, Edward I. Patterson, Benedict D. Michael, Andrew Owen, Julian A. Hiscox, James P. Stewart and Anja Kipar
Viruses 2022, 14(5), 1020; https://0-doi-org.brum.beds.ac.uk/10.3390/v14051020 - 11 May 2022
Cited by 45 | Viewed by 6111
Abstract
Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) not only affects the respiratory tract but also causes neurological symptoms such as loss of smell and taste, headache, fatigue or severe cerebrovascular complications. Using transgenic mice expressing human angiotensin-converting enzyme 2 (hACE2), we investigated the [...] Read more.
Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) not only affects the respiratory tract but also causes neurological symptoms such as loss of smell and taste, headache, fatigue or severe cerebrovascular complications. Using transgenic mice expressing human angiotensin-converting enzyme 2 (hACE2), we investigated the spatiotemporal distribution and pathomorphological features in the CNS following intranasal infection with SARS-CoV-2 variants, as well as after prior influenza A virus infection. Apart from Omicron, we found all variants to frequently spread to and within the CNS. Infection was restricted to neurons and appeared to spread from the olfactory bulb mainly in basally oriented regions in the brain and into the spinal cord, independent of ACE2 expression and without evidence of neuronal cell death, axonal damage or demyelination. However, microglial activation, microgliosis and a mild macrophage and T cell dominated inflammatory response was consistently observed, accompanied by apoptotic death of endothelial, microglial and immune cells, without their apparent infection. Microgliosis and immune cell apoptosis indicate a potential role of microglia for pathogenesis and viral effect in COVID-19 and the possible impairment of neurological functions, especially in long COVID. These data may also be informative for the selection of therapeutic candidates and broadly support the investigation of agents with adequate penetration into relevant regions of the CNS. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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23 pages, 6119 KiB  
Article
Exposure Route Influences Disease Severity in the COVID-19 Cynomolgus Macaque Model
by Sandra L. Bixler, Christopher P. Stefan, Alexandra N. Jay, Franco D. Rossi, Keersten M. Ricks, Charles J. Shoemaker, Alicia M. Moreau, Xiankun Zeng, Jay W. Hooper, David N. Dyer, Ondraya M. Frick, Jeffrey W. Koehler, Brian J. Kearney, Nina DiPinto, Jun Liu, Samantha D. Tostenson, Tamara L. Clements, Jeffrey M. Smith, Joshua A. Johnson, Kerry L. Berrier, Heather L. Esham, Korey L. Delp, Susan R. Coyne, Holly A. Bloomfield, Paul A. Kuehnert, Kristen Akers, Kathleen M. Gibson, Timothy D. Minogue, Aysegul Nalca and Margaret L. M. Pittadd Show full author list remove Hide full author list
Viruses 2022, 14(5), 1013; https://0-doi-org.brum.beds.ac.uk/10.3390/v14051013 - 10 May 2022
Cited by 7 | Viewed by 2011
Abstract
The emergence of SARS-CoV-2 and the subsequent pandemic has highlighted the need for animal models that faithfully replicate the salient features of COVID-19 disease in humans. These models are necessary for the rapid selection, testing, and evaluation of potential medical countermeasures. Here, we [...] Read more.
The emergence of SARS-CoV-2 and the subsequent pandemic has highlighted the need for animal models that faithfully replicate the salient features of COVID-19 disease in humans. These models are necessary for the rapid selection, testing, and evaluation of potential medical countermeasures. Here, we performed a direct comparison of two distinct routes of SARS-CoV-2 exposure—combined intratracheal/intranasal and small particle aerosol—in two nonhuman primate species, rhesus and cynomolgus macaques. While all four experimental groups displayed very few outward clinical signs, evidence of mild to moderate respiratory disease was present on radiographs and at necropsy. Cynomolgus macaques exposed via the aerosol route also developed the most consistent fever responses and had the most severe respiratory disease and pathology. This study demonstrates that while all four models produced suitable representations of mild COVID-like illness, aerosol exposure of cynomolgus macaques to SARS-CoV-2 produced the most severe disease, which may provide additional clinical endpoints for evaluating therapeutics and vaccines. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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14 pages, 2917 KiB  
Article
Activity of a Carbohydrate-Binding Module Therapy, Neumifil, against SARS-CoV-2 Disease in a Hamster Model of Infection
by Rachel Fell, Jane A. Potter, Samantha Yuille, Franscisco J. Salguero, Robert Watson, Didier Ngabo, Karen Gooch, Roger Hewson, David Howat and Stuart Dowall
Viruses 2022, 14(5), 976; https://0-doi-org.brum.beds.ac.uk/10.3390/v14050976 - 06 May 2022
Cited by 4 | Viewed by 1811
Abstract
The rapid global spread of severe acute respiratory coronavirus 2 (SARS-CoV-2) has resulted in an urgent effort to find efficacious therapeutics. Broad-spectrum therapies which could be used for other respiratory pathogens confer advantages, as do those based on targeting host cells that are [...] Read more.
The rapid global spread of severe acute respiratory coronavirus 2 (SARS-CoV-2) has resulted in an urgent effort to find efficacious therapeutics. Broad-spectrum therapies which could be used for other respiratory pathogens confer advantages, as do those based on targeting host cells that are not prone to the development of resistance by the pathogen. We tested an intranasally delivered carbohydrate-binding module (CBM) therapy, termed Neumifil, which is based on a CBM that has previously been shown to offer protection against the influenza virus through the binding of sialic acid receptors. Using the recognised hamster model of SARS-CoV-2 infection, we demonstrate that Neumifil significantly reduces clinical disease severity and pathological changes in the nasal cavity. Furthermore, we demonstrate Neumifil binding to the human angiotensin-converting enzyme 2 (ACE2) receptor and spike protein of SARS-CoV-2. This is the first report describing the testing of this type of broad-spectrum antiviral therapy in vivo and provides evidence for the advancement of Neumifil in further preclinical and clinical studies. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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12 pages, 1102 KiB  
Article
Immunogenicity of an AAV-Based COVID-19 Vaccine in Murine Models of Obesity and Aging
by Dawid Maciorowski, Cheikh Diop, Urja Bhatt, Reynette Estelien, Dan Li, Ruchi Chauhan, Luk H. Vandenberghe and Nerea Zabaleta
Viruses 2022, 14(4), 820; https://0-doi-org.brum.beds.ac.uk/10.3390/v14040820 - 15 Apr 2022
Cited by 1 | Viewed by 2421
Abstract
The SARS-CoV-2 pandemic has had a disastrous impact on global health. Although some vaccine candidates have been effective in combating SARS-CoV-2, logistical, economical, and sociological aspects still limit vaccine access globally. Recently, we reported on two room-temperature stable AAV-based COVID-19 vaccines that induced [...] Read more.
The SARS-CoV-2 pandemic has had a disastrous impact on global health. Although some vaccine candidates have been effective in combating SARS-CoV-2, logistical, economical, and sociological aspects still limit vaccine access globally. Recently, we reported on two room-temperature stable AAV-based COVID-19 vaccines that induced potent and protective immunogenicity following a single injection in murine and primate models. Obesity and old age are associated with increased mortality in COVID-19, as well as reduced immunogenicity and efficacy of vaccines. Here, we investigated the effectiveness of the AAVCOVID vaccine candidates in murine models of obesity and aging. Results demonstrate that obesity did not significantly alter the immunogenicity of either vaccine candidate. In aged mice, vaccine immunogenicity was impaired. These results suggest that AAV-based vaccines may have limitations in older populations and may be equally applicable in obese and non-obese populations. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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15 pages, 3373 KiB  
Article
Brain Inflammation and Intracellular α-Synuclein Aggregates in Macaques after SARS-CoV-2 Infection
by Ingrid H. C. H. M. Philippens, Kinga P. Böszörményi, Jacqueline A. M. Wubben, Zahra C. Fagrouch, Nikki van Driel, Amber Q. Mayenburg, Diana Lozovagia, Eva Roos, Bernadette Schurink, Marianna Bugiani, Ronald E. Bontrop, Jinte Middeldorp, Willy M. Bogers, Lioe-Fee de Geus-Oei, Jan A. M. Langermans, Ernst J. Verschoor, Marieke A. Stammes and Babs E. Verstrepen
Viruses 2022, 14(4), 776; https://0-doi-org.brum.beds.ac.uk/10.3390/v14040776 - 08 Apr 2022
Cited by 24 | Viewed by 11497
Abstract
SARS-CoV-2 causes acute respiratory disease, but many patients also experience neurological complications. Neuropathological changes with pronounced neuroinflammation have been described in individuals after lethal COVID-19, as well as in the CSF of hospitalized patients with neurological complications. To assess whether neuropathological changes can [...] Read more.
SARS-CoV-2 causes acute respiratory disease, but many patients also experience neurological complications. Neuropathological changes with pronounced neuroinflammation have been described in individuals after lethal COVID-19, as well as in the CSF of hospitalized patients with neurological complications. To assess whether neuropathological changes can occur after a SARS-CoV-2 infection, leading to mild-to-moderate disease, we investigated the brains of four rhesus and four cynomolgus macaques after pulmonary disease and without overt clinical symptoms. Postmortem analysis demonstrated the infiltration of T-cells and activated microglia in the parenchyma of all infected animals, even in the absence of viral antigen or RNA. Moreover, intracellular α-synuclein aggregates were found in the brains of both macaque species. The heterogeneity of these manifestations in the brains indicates the virus’ neuropathological potential and should be considered a warning for long-term health risks, following SARS-CoV-2 infection. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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15 pages, 6128 KiB  
Article
Protective Immunity of the Primary SARS-CoV-2 Infection Reduces Disease Severity Post Re-Infection with Delta Variants in Syrian Hamsters
by Sreelekshmy Mohandas, Pragya D. Yadav, Anita Shete, Dimpal Nyayanit, Rajlaxmi Jain, Gajanan Sapkal and Chandrashekhar Mote
Viruses 2022, 14(3), 596; https://0-doi-org.brum.beds.ac.uk/10.3390/v14030596 - 13 Mar 2022
Cited by 5 | Viewed by 2666
Abstract
The Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) Delta variant has evolved to become the dominant SARS-CoV-2 lineage with multiple sub-lineages and there are also reports of re-infections caused by this variant. We studied the disease characteristics induced by the Delta AY.1 variant and [...] Read more.
The Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) Delta variant has evolved to become the dominant SARS-CoV-2 lineage with multiple sub-lineages and there are also reports of re-infections caused by this variant. We studied the disease characteristics induced by the Delta AY.1 variant and compared it with the Delta and B.1 variants in Syrian hamsters. We also assessed the potential of re-infection by these variants in Coronavirus disease 2019 recovered hamsters 3 months after initial infection. The variants produced disease characterized by high viral load in the respiratory tract and interstitial pneumonia. The Delta AY.1 variant produced mild disease in the hamster model and did not show any evidence of neutralization resistance due to the presence of the K417N mutation, as speculated. Re-infection with a high virus dose of the Delta and B.1 variants 3 months after B.1 variant infection resulted in reduced virus shedding, disease severity and increased neutralizing antibody levels in the re-infected hamsters. The reduction in viral load and lung disease after re-infection with the Delta AY.1 variant was not marked. Upper respiratory tract viral RNA loads remained similar after re-infection in all the groups. The present findings show that prior infection could not produce sterilizing immunity but that it can broaden the neutralizing response and reduce disease severity in case of reinfection. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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20 pages, 5563 KiB  
Article
High-Fat High-Sugar Diet-Induced Changes in the Lipid Metabolism Are Associated with Mildly Increased COVID-19 Severity and Delayed Recovery in the Syrian Hamster
by Julia R. Port, Danielle R. Adney, Benjamin Schwarz, Jonathan E. Schulz, Daniel E. Sturdevant, Brian J. Smith, Victoria A. Avanzato, Myndi G. Holbrook, Jyothi N. Purushotham, Kaitlin A. Stromberg, Ian Leighton, Catharine M. Bosio, Carl Shaia and Vincent J. Munster
Viruses 2021, 13(12), 2506; https://0-doi-org.brum.beds.ac.uk/10.3390/v13122506 - 14 Dec 2021
Cited by 16 | Viewed by 3526
Abstract
Pre-existing comorbidities such as obesity or metabolic diseases can adversely affect the clinical outcome of COVID-19. Chronic metabolic disorders are globally on the rise and often a consequence of an unhealthy diet, referred to as a Western Diet. For the first time in [...] Read more.
Pre-existing comorbidities such as obesity or metabolic diseases can adversely affect the clinical outcome of COVID-19. Chronic metabolic disorders are globally on the rise and often a consequence of an unhealthy diet, referred to as a Western Diet. For the first time in the Syrian hamster model, we demonstrate the detrimental impact of a continuous high-fat high-sugar diet on COVID-19 outcome. We observed increased weight loss and lung pathology, such as exudate, vasculitis, hemorrhage, fibrin, and edema, delayed viral clearance and functional lung recovery, and prolonged viral shedding. This was accompanied by an altered, but not significantly different, systemic IL-10 and IL-6 profile, as well as a dysregulated serum lipid response dominated by polyunsaturated fatty acid-containing phosphatidylethanolamine, partially recapitulating cytokine and lipid responses associated with severe human COVID-19. Our data support the hamster model for testing restrictive or targeted diets and immunomodulatory therapies to mediate the adverse effects of metabolic disease on COVID-19. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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12 pages, 3716 KiB  
Article
Development of a Hamster Natural Transmission Model of SARS-CoV-2 Infection
by Stuart Dowall, Francisco J. Salguero, Nathan Wiblin, Susan Fotheringham, Graham Hatch, Simon Parks, Kathryn Gowan, Debbie Harris, Oliver Carnell, Rachel Fell, Robert Watson, Victoria Graham, Karen Gooch, Yper Hall, Simon Mizen and Roger Hewson
Viruses 2021, 13(11), 2251; https://0-doi-org.brum.beds.ac.uk/10.3390/v13112251 - 09 Nov 2021
Cited by 15 | Viewed by 2633
Abstract
The global pandemic of coronavirus disease (COVID-19) caused by infection with severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) has led to an international thrust to study pathogenesis and evaluate interventions. Experimental infection of hamsters and the resulting respiratory disease is one of the preferred [...] Read more.
The global pandemic of coronavirus disease (COVID-19) caused by infection with severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) has led to an international thrust to study pathogenesis and evaluate interventions. Experimental infection of hamsters and the resulting respiratory disease is one of the preferred animal models since clinical signs of disease and virus shedding are similar to more severe cases of human COVID-19. The main route of challenge has been direct inoculation of the virus via the intranasal route. To resemble the natural infection, we designed a bespoke natural transmission cage system to assess whether recipient animals housed in physically separate adjacent cages could become infected from a challenged donor animal in a central cage, with equal airflow across the two side cages. To optimise viral shedding in the donor animals, a low and moderate challenge dose were compared after direct intranasal challenge, but similar viral shedding responses were observed and no discernible difference in kinetics. The results from our natural transmission set-up demonstrate that most recipient hamsters are infected within the system developed, with variation in the kinetics and levels of disease between individual animals. Common clinical outputs used for the assessment in directly-challenged hamsters, such as weight loss, are less obvious in hamsters who become infected from naturally acquiring the infection. The results demonstrate the utility of a natural transmission model for further work on assessing the differences between virus strains and evaluating interventions using a challenge system which more closely resembles human infection. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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10 pages, 2803 KiB  
Article
SARS-CoV-2 Delta Variant Pathogenesis and Host Response in Syrian Hamsters
by Sreelekshmy Mohandas, Pragya Dhruv Yadav, Anita Shete, Dimpal Nyayanit, Gajanan Sapkal, Kavita Lole and Nivedita Gupta
Viruses 2021, 13(9), 1773; https://0-doi-org.brum.beds.ac.uk/10.3390/v13091773 - 05 Sep 2021
Cited by 35 | Viewed by 5557
Abstract
B.1.617 is becoming a dominant Severe Acute Respiratory Syndrome-Coronavirus-2 (SARS-CoV-2) lineage worldwide with many sublineages, of which B.1.617.2 is designated as a variant of concern. The pathogenicity of B.1.617.2 (Delta) and B.1.617.3 lineage of SARS-CoV-2 was evaluated and compared with that of B.1, [...] Read more.
B.1.617 is becoming a dominant Severe Acute Respiratory Syndrome-Coronavirus-2 (SARS-CoV-2) lineage worldwide with many sublineages, of which B.1.617.2 is designated as a variant of concern. The pathogenicity of B.1.617.2 (Delta) and B.1.617.3 lineage of SARS-CoV-2 was evaluated and compared with that of B.1, an early virus isolate with D614G mutation in a Syrian hamster model. Viral load, antibody response, and lung disease were studied. There was no significant difference in the virus shedding pattern among these variants. High levels of SARS-CoV-2 sub genomic RNA were detected in the respiratory tract of hamsters infected with the Delta variant for 14 days, which warrants further transmission studies. The Delta variant induced lung disease of moderate severity in about 40% of infected animals, which supports the attributed disease severity of the variant. Cross neutralizing antibodies were detected in animals infected with B.1, Delta, and B.1.617.3 variant, but neutralizing capacity was significantly lower with B.1.351 (Beta variant). Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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23 pages, 7272 KiB  
Article
The Post-Acute Phase of SARS-CoV-2 Infection in Two Macaque Species Is Associated with Signs of Ongoing Virus Replication and Pathology in Pulmonary and Extrapulmonary Tissues
by Kinga P. Böszörményi, Marieke A. Stammes, Zahra C. Fagrouch, Gwendoline Kiemenyi-Kayere, Henk Niphuis, Daniella Mortier, Nikki van Driel, Ivonne Nieuwenhuis, Richard A. W. Vervenne, Tom Haaksma, Boudewijn Ouwerling, Deborah Adema, Roja Fidel Acar, Ella Zuiderwijk-Sick, Lisette Meijer, Petra Mooij, Ed J. Remarque, Herman Oostermeijer, Gerrit Koopman, Alexis C. R. Hoste, Patricia Sastre, Bart L. Haagmans, Ronald E. Bontrop, Jan A. M. Langermans, Willy M. Bogers, Ivanela Kondova, Ernst J. Verschoor and Babs E. Verstrepenadd Show full author list remove Hide full author list
Viruses 2021, 13(8), 1673; https://0-doi-org.brum.beds.ac.uk/10.3390/v13081673 - 23 Aug 2021
Cited by 22 | Viewed by 7642
Abstract
The post-acute phase of SARS-CoV-2 infection was investigated in rhesus (Macaca mulatta) and cynomolgus macaques (Macaca fascicularis). During the acute phase of infection, SARS-CoV-2 was shed via the nose and throat, and viral RNA was occasionally detected in feces. [...] Read more.
The post-acute phase of SARS-CoV-2 infection was investigated in rhesus (Macaca mulatta) and cynomolgus macaques (Macaca fascicularis). During the acute phase of infection, SARS-CoV-2 was shed via the nose and throat, and viral RNA was occasionally detected in feces. This phase coincided with a transient change in systemic immune activation. Even after the alleged resolution of the infection, computed tomography (CT) and positron emission tomography (PET)-CT revealed pulmonary lesions and activated tracheobronchial lymph nodes in all animals. Post-mortem histological examination of the lung tissue revealed mostly marginal or resolving minimal lesions that were indicative of SARS-CoV-2 infection. Evidence for SARS-CoV-2-induced histopathology was also found in extrapulmonary tissue samples, such as conjunctiva, cervical, and mesenteric lymph nodes. However, 5–6 weeks after SARS-CoV-2 exposure, upon necropsy, viral RNA was still detectable in a wide range of tissue samples in 50% of the macaques and included amongst others the heart, the respiratory tract and surrounding lymph nodes, salivary gland, and conjunctiva. Subgenomic messenger RNA was detected in the lungs and tracheobronchial lymph nodes, indicative of ongoing virus replication during the post-acute phase. These results could be relevant for understanding the long-term consequences of COVID-19 in humans. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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16 pages, 6992 KiB  
Article
Clinical and Histopathologic Features of a Feline SARS-CoV-2 Infection Model Are Analogous to Acute COVID-19 in Humans
by Jennifer M. Rudd, Miruthula Tamil Selvan, Shannon Cowan, Yun-Fan Kao, Cecily C. Midkiff, Sai Narayanan, Akhilesh Ramachandran, Jerry W. Ritchey and Craig A. Miller
Viruses 2021, 13(8), 1550; https://0-doi-org.brum.beds.ac.uk/10.3390/v13081550 - 05 Aug 2021
Cited by 19 | Viewed by 5081
Abstract
The emergence and ensuing dominance of COVID-19 on the world stage has emphasized the urgency of efficient animal models for the development of therapeutics for and assessment of immune responses to SARS-CoV-2 infection. Shortcomings of current animal models for SARS-CoV-2 include limited lower [...] Read more.
The emergence and ensuing dominance of COVID-19 on the world stage has emphasized the urgency of efficient animal models for the development of therapeutics for and assessment of immune responses to SARS-CoV-2 infection. Shortcomings of current animal models for SARS-CoV-2 include limited lower respiratory disease, divergence from clinical COVID-19 disease, and requirements for host genetic modifications to permit infection. In this study, n = 12 specific-pathogen-free domestic cats were infected intratracheally with SARS-CoV-2 to evaluate clinical disease, histopathologic lesions, and viral infection kinetics at 4 and 8 days post-inoculation; n = 6 sham-inoculated cats served as controls. Intratracheal inoculation of SARS-CoV-2 produced a significant degree of clinical disease (lethargy, fever, dyspnea, and dry cough) consistent with that observed in the early exudative phase of COVID-19. Pulmonary lesions such as diffuse alveolar damage, hyaline membrane formation, fibrin deposition, and proteinaceous exudates were also observed with SARS-CoV-2 infection, replicating lesions identified in people hospitalized with ARDS from COVID-19. A significant correlation was observed between the degree of clinical disease identified in infected cats and pulmonary lesions. Viral loads and ACE2 expression were also quantified in nasal turbinates, distal trachea, lungs, and other organs. Results of this study validate a feline model for SARS-CoV-2 infection that results in clinical disease and histopathologic lesions consistent with acute COVID-19 in humans, thus encouraging its use for future translational studies. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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Jump to: Research

28 pages, 2368 KiB  
Systematic Review
The Reassessed Potential of SARS-CoV-2 Attenuation for COVID-19 Vaccine Development—A Systematic Review
by Marcin Goławski, Piotr Lewandowski, Iwona Jabłońska and Marcin Delijewski
Viruses 2022, 14(5), 991; https://0-doi-org.brum.beds.ac.uk/10.3390/v14050991 - 07 May 2022
Cited by 8 | Viewed by 4140
Abstract
Live-attenuated SARS-CoV-2 vaccines received relatively little attention during the COVID-19 pandemic. Despite this, several methods of obtaining attenuated coronaviruses are known. In this systematic review, the strategies of coronavirus attenuation, which may potentially be applied to SARS-CoV-2, were identified. PubMed, Scopus, Web of [...] Read more.
Live-attenuated SARS-CoV-2 vaccines received relatively little attention during the COVID-19 pandemic. Despite this, several methods of obtaining attenuated coronaviruses are known. In this systematic review, the strategies of coronavirus attenuation, which may potentially be applied to SARS-CoV-2, were identified. PubMed, Scopus, Web of Science and Embase databases were searched to identify relevant articles describing attenuating mutations tested in vivo. In case of coronaviruses other than SARS-CoV-2, sequence alignment was used to exclude attenuating mutations that cannot be applied to SARS-CoV-2. Potential immunogenicity, safety and efficacy of the attenuated SARS-CoV-2 vaccine were discussed based on animal studies data. A total of 27 attenuation strategies, used to create 101 different coronaviruses, have been described in 56 eligible articles. The disruption of the furin cleavage site in the SARS-CoV-2 spike protein was identified as the most promising strategy. The replacement of core sequences of transcriptional regulatory signals, which prevents recombination with wild-type viruses, also appears particularly advantageous. Other important attenuating mutations encompassed mostly the prevention of evasion of innate immunity. Sufficiently attenuated coronaviruses typically caused no meaningful disease in susceptible animals and protected them from challenges with virulent virus. This indicates that attenuated COVID-19 vaccines may be considered as a potential strategy to fight the threat posed by SARS-CoV-2. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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Graphical abstract

10 pages, 7007 KiB  
Brief Report
SARS-CoV-2 Variants of Concern Infect the Respiratory Tract and Induce Inflammatory Response in Wild-Type Laboratory Mice
by Shannon Stone, Hussin Alwan Rothan, Janhavi Prasad Natekar, Pratima Kumari, Shaligram Sharma, Heather Pathak, Komal Arora, Tabassum Tasnim Auroni and Mukesh Kumar
Viruses 2022, 14(1), 27; https://0-doi-org.brum.beds.ac.uk/10.3390/v14010027 - 24 Dec 2021
Cited by 20 | Viewed by 5786
Abstract
The emergence of new severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) variants of concern pose a major threat to public health, due to possible enhanced virulence, transmissibility and immune escape. These variants may also adapt to new hosts, in part through mutations in the [...] Read more.
The emergence of new severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) variants of concern pose a major threat to public health, due to possible enhanced virulence, transmissibility and immune escape. These variants may also adapt to new hosts, in part through mutations in the spike protein. In this study, we evaluated the infectivity and pathogenicity of SARS-CoV-2 variants of concern in wild-type C57BL/6 mice. Six-week-old mice were inoculated intranasally with a representative virus from the original B.1 lineage, or the emerging B.1.1.7 and B.1.351 lineages. We also infected a group of mice with a mouse-adapted SARS-CoV-2 (MA10). Viral load and mRNA levels of multiple cytokines and chemokines were analyzed in the lung tissues on day 3 after infection. Our data show that unlike the B.1 virus, the B.1.1.7 and B.1.351 viruses are capable of infecting C57BL/6 mice and replicating at high concentrations in the lungs. The B.1.351 virus replicated to higher titers in the lungs compared with the B.1.1.7 and MA10 viruses. The levels of cytokines (IL-6, TNF-α, IL-1β) and chemokine (CCL2) were upregulated in response to the B.1.1.7 and B.1.351 infection in the lungs. In addition, robust expression of viral nucleocapsid protein and histopathological changes were detected in the lungs of B.1.351-infected mice. Overall, these data indicate a greater potential for infectivity and adaptation to new hosts by emerging SARS-CoV-2 variants. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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8 pages, 706 KiB  
Case Report
First Detection of SARS-CoV-2 Delta (B.1.617.2) Variant of Concern in a Dog with Clinical Signs in Spain
by Leira Fernández-Bastit, Jordi Rodon, Edwards Pradenas, Silvia Marfil, Benjamin Trinité, Mariona Parera, Núria Roca, Anna Pou, Guillermo Cantero, Cristina Lorca-Oró, Jorge Carrillo, Nuria Izquierdo-Useros, Bonaventura Clotet, Marc Noguera-Julián, Julià Blanco, Júlia Vergara-Alert and Joaquim Segalés
Viruses 2021, 13(12), 2526; https://0-doi-org.brum.beds.ac.uk/10.3390/v13122526 - 16 Dec 2021
Cited by 19 | Viewed by 4104
Abstract
Several cases of naturally infected dogs with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have been reported despite the apparently low susceptibility of this species. Here, we document the first reported case of infection caused by the Delta (B.1.617.2) variant of concern (VOC) [...] Read more.
Several cases of naturally infected dogs with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have been reported despite the apparently low susceptibility of this species. Here, we document the first reported case of infection caused by the Delta (B.1.617.2) variant of concern (VOC) in a dog in Spain that lived with several household members suffering from Coronavirus Infectious Disease 2019 (COVID-19). The animal displayed mild digestive and respiratory clinical signs and had a low viral load in the oropharyngeal swab collected at the first sampling. Whole-genome sequencing indicated infection with the Delta variant, coinciding with the predominant variant during the fifth pandemic wave in Spain. The dog seroconverted, as detected 21 days after the first sampling, and developed neutralizing antibodies that cross-neutralized different SARS-CoV-2 variants. This study further emphasizes the importance of studying the susceptibility of animal species to different VOCs and their potential role as reservoirs in the context of COVID-19. Full article
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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