Animal Reservoirs and Hosts for Emerging Alphacoronaviruses and Betacoronaviruses

The ongoing global pandemic caused by coronavirus disease has once again demonstrated the role of the family Coronaviridae in causing human disease outbreaks. Because severe acute respiratory syndrome coronavirus 2 was first detected in December 2019, information on its tropism, host range, and clinical manifestations in animals is limited. Given the limited information, data from other coronaviruses might be useful for informing scientific inquiry, risk assessment, and decision-making. We reviewed endemic and emerging infections of alphacoronaviruses and betacoronaviruses in wildlife, livestock, and companion animals and provide information on the receptor use, known hosts, and clinical signs associated with each host for 15 coronaviruses detected in humans and animals. This information can be used to guide implementation of a One Health approach that involves human health, animal health, environmental, and other relevant partners in developing strategies for preparedness, response, and control to current and future coronavirus disease threats.

[1]  Hualan Chen,et al.  Replication, pathogenicity, and transmission of SARS-CoV-2 in minks , 2020, National science review.

[2]  Jeffrey S. Hall,et al.  Experimental challenge of a North American bat species, big brown bat (Eptesicus fuscus), with SARS-CoV-2. , 2020, Transboundary and emerging diseases.

[3]  D. Suarez,et al.  Lack of Susceptibility to SARS-CoV-2 and MERS-CoV in Poultry , 2020, Emerging infectious diseases.

[4]  M. Koopmans,et al.  Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans , 2020, Science.

[5]  S. Vandewoude,et al.  Experimental infection of domestic dogs and cats with SARS-CoV-2: Pathogenesis, transmission, and response to reexposure in cats , 2020, Proceedings of the National Academy of Sciences.

[6]  A. Gruber,et al.  SARS‐CoV‐2 infection of Chinese hamsters (Cricetulus griseus) reproduces COVID‐19 pneumonia in a well‐established small animal model , 2020, Transboundary and emerging diseases.

[7]  M. Koopmans,et al.  Susceptibility of rabbits to SARS-CoV-2 , 2020, bioRxiv.

[8]  M. Beer,et al.  Experimental Infection of Cattle with SARS-CoV-2 , 2020, bioRxiv.

[9]  M. Beer,et al.  Susceptibility of Raccoon Dogs for Experimental SARS-CoV-2 Infection , 2020, bioRxiv.

[10]  Xiaozhong Peng,et al.  Comparison of nonhuman primates identified the suitable model for COVID-19 , 2020, Signal Transduction and Targeted Therapy.

[11]  T. Geisbert,et al.  Intranasal exposure of African green monkeys to SARS-CoV-2 results in acute phase pneumonia with shedding and lung injury still present in the early convalescence phase , 2020, Virology Journal.

[12]  Yong-tang Zheng,et al.  COVID-19-like symptoms observed in Chinese tree shrews infected with SARS-CoV-2 , 2020, Zoological research.

[13]  M. Beer,et al.  SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study , 2020, The Lancet Microbe.

[14]  S. Moroff,et al.  First Reported Cases of SARS-CoV-2 Infection in Companion Animals — New York, March–April 2020 , 2020, MMWR. Morbidity and mortality weekly report.

[15]  M. Koopmans,et al.  SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[16]  D. Chu,et al.  Infection of dogs with SARS-CoV-2 , 2020, Nature.

[17]  Y. Kawaoka,et al.  Transmission of SARS-CoV-2 in Domestic Cats. , 2020, The New England journal of medicine.

[18]  E. Fischer,et al.  Respiratory disease in rhesus macaques inoculated with SARS-CoV-2 , 2020, Nature.

[19]  P. Calistri,et al.  A “One-Health” approach for diagnosis and molecular characterization of SARS-CoV-2 in Italy , 2020, One Health.

[20]  M. Koopmans,et al.  SARS-CoV-2 is transmitted via contact and via the air between ferrets , 2020, bioRxiv.

[21]  T. Kuiken,et al.  Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model , 2020, Science.

[22]  Baoying Huang,et al.  Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS–coronavirus 2 , 2020, Science.

[23]  Eun-Ha Kim,et al.  Infection and Rapid Transmission of SARS-CoV-2 in Ferrets , 2020, Cell Host & Microbe.

[24]  K. To,et al.  Simulation of the clinical and pathological manifestations of Coronavirus Disease 2019 (COVID-19) in golden Syrian hamster model: implications for disease pathogenesis and transmissibility , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[25]  Wenling Wang,et al.  The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice , 2020, Nature.

[26]  G. M. Rosa,et al.  Unveiling patterns of viral pathogen infection in free-ranging carnivores of northern Portugal using a complementary methodological approach , 2020, Comparative Immunology, Microbiology and Infectious Diseases.

[27]  Kai Zhao,et al.  A pneumonia outbreak associated with a new coronavirus of probable bat origin , 2020, Nature.

[28]  Yifei Xu Genetic diversity and potential recombination between ferret coronaviruses from European and American lineages , 2020, Journal of Infection.

[29]  G. Gao,et al.  A Novel Coronavirus from Patients with Pneumonia in China, 2019 , 2020, The New England journal of medicine.

[30]  Y. Hu,et al.  Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China , 2020, The Lancet.

[31]  R. Plowright,et al.  Novel Insights Into Immune Systems of Bats , 2020, Frontiers in Immunology.

[32]  Jiyong Zhou,et al.  Broad Cross-Species Infection of Cultured Cells by Bat HKU2-Related Swine Acute Diarrhea Syndrome Coronavirus and Identification of Its Replication in Murine Dendritic Cells In Vivo Highlight Its Potential for Diverse Interspecies Transmission , 2019, Journal of Virology.

[33]  Md. Mazharul Islam,et al.  Qatar experience on One Health approach for middle-east respiratory syndrome coronavirus, 2012–2017: A viewpoint , 2019, One Health.

[34]  K. Pyrć,et al.  Canine Respiratory Coronavirus, Bovine Coronavirus, and Human Coronavirus OC43: Receptors and Attachment Factors , 2019, Viruses.

[35]  A. Vlasova,et al.  Emerging and re-emerging coronaviruses in pigs , 2019, Current Opinion in Virology.

[36]  V. Misra,et al.  Bats and Coronaviruses , 2019, Viruses.

[37]  B. Meyer,et al.  Development of a Whole-Virus ELISA for Serological Evaluation of Domestic Livestock as Possible Hosts of Human Coronavirus NL63 , 2019, Viruses.

[38]  H. Amer Bovine-like coronaviruses in domestic and wild ruminants , 2018, Animal Health Research Reviews.

[39]  Christian Drosten,et al.  Human coronavirus OC43 outbreak in wild chimpanzees, Côte d´Ivoire, 2016 , 2018, Emerging Microbes & Infections.

[40]  P. Daszak,et al.  Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin , 2018, Nature.

[41]  V. Corman,et al.  Hosts and Sources of Endemic Human Coronaviruses , 2018, Advances in Virus Research.

[42]  T. Goldberg,et al.  Lethal Respiratory Disease Associated with Human Rhinovirus C in Wild Chimpanzees, Uganda, 2013 , 2018, Emerging infectious diseases.

[43]  Vineet D. Menachery,et al.  Further Evidence for Bats as the Evolutionary Source of Middle East Respiratory Syndrome Coronavirus , 2017, mBio.

[44]  J. Segalés,et al.  Livestock Susceptibility to Infection with Middle East Respiratory Syndrome Coronavirus , 2017, Emerging infectious diseases.

[45]  M. Shi,et al.  Surveillance of Bat Coronaviruses in Kenya Identifies Relatives of Human Coronaviruses NL63 and 229E and Their Recombination History , 2017, Journal of Virology.

[46]  P. Daszak,et al.  Global patterns in coronavirus diversity , 2017, Virus evolution.

[47]  F. Taguchi,et al.  Porcine aminopeptidase N is not a cellular receptor of porcine epidemic diarrhea virus, but promotes its infectivity via aminopeptidase activity. , 2016, The Journal of general virology.

[48]  Z. Memish,et al.  Link of a ubiquitous human coronavirus to dromedary camels , 2016, Proceedings of the National Academy of Sciences.

[49]  H. Feldmann,et al.  A Comparative Review of Animal Models of Middle East Respiratory Syndrome Coronavirus Infection , 2016, Veterinary pathology.

[50]  M. Koopmans,et al.  Cross host transmission in the emergence of MERS coronavirus , 2016, Current Opinion in Virology.

[51]  H. Bielefeldt-Ohmann,et al.  Infection, Replication, and Transmission of Middle East Respiratory Syndrome Coronavirus in Alpacas , 2016, Emerging infectious diseases.

[52]  Changhee Lee Porcine epidemic diarrhea virus: An emerging and re-emerging epizootic swine virus , 2015, Virology Journal.

[53]  Ben Hu,et al.  Bat origin of human coronaviruses , 2015, Virology Journal.

[54]  Heather J. Baldwin,et al.  Evidence for an Ancestral Association of Human Coronavirus 229E with Bats , 2015, Journal of Virology.

[55]  Joshua C. Johnson,et al.  Intratracheal exposure of common marmosets to MERS-CoV Jordan-n3/2012 or MERS-CoV EMC/2012 isolates does not result in lethal disease , 2015, Virology.

[56]  H. Moon,et al.  Porcine epidemic diarrhea: a review of current epidemiology and available vaccines , 2015, Clinical and Experimental Vaccine Research.

[57]  J. Weese,et al.  Reducing the risk of pet-associated zoonotic infections , 2015, Canadian Medical Association Journal.

[58]  J. Dushoff,et al.  Estimating the Global Burden of Endemic Canine Rabies , 2015, PLoS neglected tropical diseases.

[59]  T. Kuiken,et al.  Asymptomatic Middle East Respiratory Syndrome Coronavirus Infection in Rabbits , 2015, Journal of Virology.

[60]  Shibo Jiang,et al.  Receptor Usage and Cell Entry of Porcine Epidemic Diarrhea Coronavirus , 2015, Journal of Virology.

[61]  D. Squarre,et al.  Positive Immunolabelling for Feline Infectious Peritonitis in an African Lion (Panthera leo) with Bilateral Panuveitis , 2015, Journal of Comparative Pathology.

[62]  M. Shi,et al.  Discovery, diversity and evolution of novel coronaviruses sampled from rodents in China , 2014, Virology.

[63]  P. Woo,et al.  Discovery of a Novel Coronavirus, China Rattus Coronavirus HKU24, from Norway Rats Supports the Murine Origin of Betacoronavirus 1 and Has Implications for the Ancestor of Betacoronavirus Lineage A , 2014, Journal of Virology.

[64]  Xinxia Peng,et al.  Infection with MERS-CoV Causes Lethal Pneumonia in the Common Marmoset , 2014, PLoS pathogens.

[65]  G. Whittaker,et al.  Canine Enteric Coronaviruses: Emerging Viral Pathogens with Distinct Recombinant Spike Proteins , 2014, Viruses.

[66]  Niels C Pedersen,et al.  An update on feline infectious peritonitis: Diagnostics and therapeutics , 2014, The Veterinary Journal.

[67]  R. Baric,et al.  Mouse Dipeptidyl Peptidase 4 Is Not a Functional Receptor for Middle East Respiratory Syndrome Coronavirus Infection , 2014, Journal of Virology.

[68]  Honglin Chen,et al.  An Animal Model of MERS Produced by Infection of Rhesus Macaques With MERS Coronavirus , 2013, The Journal of infectious diseases.

[69]  Christian Drosten,et al.  Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS , 2013, Antiviral Research.

[70]  B. Bosch,et al.  Adenosine Deaminase Acts as a Natural Antagonist for Dipeptidyl Peptidase 4-Mediated Entry of the Middle East Respiratory Syndrome Coronavirus , 2013, Journal of Virology.

[71]  M. Kasso,et al.  Ecological and Economic Importance of Bats (Order Chiroptera) , 2013 .

[72]  J. Epstein,et al.  Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor , 2013, Nature.

[73]  J. Foley,et al.  RISK FACTORS FOR EXPOSURE TO FELINE PATHOGENS IN CALIFORNIA MOUNTAIN LIONS (PUMA CONCOLOR) , 2013, Journal of wildlife diseases.

[74]  Michael G. Katze,et al.  Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques , 2013, Proceedings of the National Academy of Sciences.

[75]  H. Feldmann,et al.  The Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Does Not Replicate in Syrian Hamsters , 2013, PloS one.

[76]  C. Webb,et al.  A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? , 2013, Proceedings of the Royal Society B: Biological Sciences.

[77]  S. Hietala,et al.  Identification and Characterization of a Novel Alpaca Respiratory Coronavirus Most Closely Related to the Human Coronavirus 229E , 2012, Viruses.

[78]  A. Osterhaus,et al.  Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. , 2012, The New England journal of medicine.

[79]  P. Woo,et al.  Recent Transmission of a Novel Alphacoronavirus, Bat Coronavirus HKU10, from Leschenault's Rousettes to Pomona Leaf-Nosed Bats: First Evidence of Interspecies Transmission of Coronavirus between Bats of Different Suborders , 2012, Journal of Virology.

[80]  C. Boesch,et al.  Noninvasive Monitoring of Respiratory Viruses in Wild Chimpanzees , 2010, EcoHealth.

[81]  Jerry Murray,et al.  Ferret Coronavirus-Associated Diseases , 2010, Veterinary Clinics of North America: Exotic Animal Practice.

[82]  B. Fielding,et al.  Understanding Human Coronavirus HCoV-NL63 , 2010, The open virology journal.

[83]  B. Crossley,et al.  Identification of a Novel Coronavirus Possibly Associated with Acute Respiratory Syndrome in Alpacas (Vicugna Pacos) in California, 2007 , 2010, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[84]  P. Woo,et al.  Coronavirus Diversity, Phylogeny and Interspecies Jumping , 2009, Experimental biology and medicine.

[85]  M. Müller,et al.  Distant Relatives of Severe Acute Respiratory Syndrome Coronavirus and Close Relatives of Human Coronavirus 229E in Bats, Ghana , 2009, Emerging infectious diseases.

[86]  P. Woo,et al.  Identification of Major Histocompatibility Complex Class I C Molecule as an Attachment Factor That Facilitates Coronavirus HKU1 Spike-Mediated Infection , 2008, Journal of Virology.

[87]  K. Erles,et al.  Canine Respiratory Coronavirus: An Emerging Pathogen in the Canine Infectious Respiratory Disease Complex , 2008, Veterinary Clinics of North America: Small Animal Practice.

[88]  J. Teifke,et al.  Clinicopathologic Features of a Systemic Coronavirus-Associated Disease Resembling Feline Infectious Peritonitis in the Domestic Ferret (Mustela putorius) , 2008, Veterinary pathology.

[89]  K. Erles,et al.  Isolation and sequence analysis of canine respiratory coronavirus , 2006, Virus Research.

[90]  Lin-Fa Wang,et al.  Review of Bats and SARS , 2006, Emerging infectious diseases.

[91]  P. Woo,et al.  Comparative Analysis of Twelve Genomes of Three Novel Group 2c and Group 2d Coronaviruses Reveals Unique Group and Subgroup Features , 2006, Journal of Virology.

[92]  Y. Guan,et al.  Prevalence and Genetic Diversity of Coronaviruses in Bats from China , 2006, Journal of Virology.

[93]  P. Lemey,et al.  Evolutionary History of the Closely Related Group 2 Coronaviruses: Porcine Hemagglutinating Encephalomyelitis Virus, Bovine Coronavirus, and Human Coronavirus OC43 , 2006, Journal of Virology.

[94]  J. Kahn,et al.  Coronavirus HKU1 Infection in the United States , 2006, Emerging infectious diseases.

[95]  A. Pratelli Genetic evolution of canine coronavirus and recent advances in prophylaxis. , 2006, Veterinary research.

[96]  V. Martella,et al.  Canine Coronavirus Highly Pathogenic for Dogs , 2006, Emerging infectious diseases.

[97]  M. Kiupel,et al.  Molecular characterization of a novel coronavirus associated with epizootic catarrhal enteritis (ECE) in ferrets , 2006, Virology.

[98]  Chengping Lu,et al.  Detection of canine coronaviruses genotype I and II in raised Canidae animals in China. , 2006, Berliner und Munchener tierarztliche Wochenschrift.

[99]  Y. Guan,et al.  SARS-CoV Infection in a Restaurant from Palm Civet , 2005, Emerging infectious diseases.

[100]  Jonathan H. Epstein,et al.  Bats Are Natural Reservoirs of SARS-Like Coronaviruses , 2005, Science.

[101]  Kwok-Hung Chan,et al.  Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[102]  Ben Berkhout,et al.  Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[103]  W. Marasco,et al.  An animal model of SARS produced by infection of Macaca mulatta with SARS coronavirus , 2005, The Journal of pathology.

[104]  K. Subbarao,et al.  Aged BALB/c Mice as a Model for Increased Severity of Severe Acute Respiratory Syndrome in Elderly Humans , 2005, Journal of Virology.

[105]  Huanming Yang,et al.  SARS-associated Coronavirus Transmitted from Human to Pig , 2005, Emerging infectious diseases.

[106]  Guo-Ping Zhao,et al.  Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Yonggang Liu,et al.  Civets Are Equally Susceptible to Experimental Infection by Two Different Severe Acute Respiratory Syndrome Coronavirus Isolates , 2005, Journal of Virology.

[108]  P. Lemey,et al.  Complete Genomic Sequence of Human Coronavirus OC43: Molecular Clock Analysis Suggests a Relatively Recent Zoonotic Coronavirus Transmission Event , 2005, Journal of Virology.

[109]  Samson S. Y. Wong,et al.  Characterization and Complete Genome Sequence of a Novel Coronavirus, Coronavirus HKU1, from Patients with Pneumonia , 2005, Journal of Virology.

[110]  B. Murphy,et al.  Severe Acute Respiratory Syndrome Coronavirus Infection of Golden Syrian Hamsters , 2005, Journal of Virology.

[111]  S. O’Brien,et al.  Biological and pathological consequences of feline infectious peritonitis virus infection in the cheetah , 1988, Archives of Virology.

[112]  Outbreak of multidrug-resistant Salmonella typhimurium associated with rodents purchased at retail pet stores--United States, December 2003-October 2004. , 2005, MMWR. Morbidity and mortality weekly report.

[113]  H. Field,et al.  Epidemiologic Clues to SARS Origin in China , 2004, Emerging infectious diseases.

[114]  Theo M Bestebroer,et al.  A previously undescribed coronavirus associated with respiratory disease in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[115]  B. Berkhout,et al.  Identification of a new human coronavirus , 2004, Nature Medicine.

[116]  M. Drebot,et al.  Susceptibility of Pigs and Chickens to SARS Coronavirus , 2004, Emerging infectious diseases.

[117]  John L. Sullivan,et al.  Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus , 2003, Nature.

[118]  Albert D. M. E. Osterhaus,et al.  SARS virus infection of cats and ferrets , 2003, Nature.

[119]  X. L. Liu,et al.  Isolation and Characterization of Viruses Related to the SARS Coronavirus from Animals in Southern China , 2003, Science.

[120]  P. Talbot,et al.  Vacuolating encephalitis in mice infected by human coronavirus OC43 , 2003, Virology.

[121]  S H Lee,et al.  The SARS epidemic in Hong Kong , 2003, Journal of epidemiology and community health.

[122]  Malik Peiris,et al.  Aetiology: Koch's postulates fulfilled for SARS virus , 2003, Nature.

[123]  K. Erles,et al.  Detection of a group 2 coronavirus in dogs with canine infectious respiratory disease , 2003, Virology.

[124]  J. V. Ver Hoef,et al.  SEROLOGIC SURVEY FOR CANINE CORONAVIRUS IN WOLVES FROM ALASKA , 2001, Journal of wildlife diseases.

[125]  L. Saif,et al.  Experimental bovine coronavirus in turkey poults and young chickens. , 2001, Avian diseases.

[126]  S. K. Wong,et al.  Healthy pets, healthy people. , 1999, Journal of the American Veterinary Medical Association.

[127]  Y. Izumiya,et al.  Differences in virus receptor for type I and type II feline infectious peritonitis virus , 2014, Archives of Virology.

[128]  Harry Vennema,et al.  Feline Infectious Peritonitis Viruses Arise by Mutation from Endemic Feline Enteric Coronaviruses , 1998, Virology.

[129]  N. Pedersen,et al.  Two related strains of feline infectious peritonitis virus isolated from immunocompromised cats infected with a feline enteric coronavirus , 1996, Journal of clinical microbiology.

[130]  G. Anderson,et al.  Coronavirus isolation from nasal swab samples in cattle with signs of respiratory tract disease after shipping. , 1996, Journal of the American Veterinary Medical Association.

[131]  A. R. Collins HLA class I antigen serves as a receptor for human coronavirus OC43. , 1993, Immunological investigations.

[132]  F. McArdle,et al.  Induction and enhancement of feline infectious peritonitis by canine coronavirus. , 1992, American journal of veterinary research.

[133]  A. Look,et al.  Human aminopeptidase N is a receptor for human coronavirus 229E , 1992, Nature.

[134]  R. H. Jacobson,et al.  Experimental inoculation of cats with human coronavirus 229E and subsequent challenge with feline infectious peritonitis virus. , 1985, Canadian journal of comparative medicine : Revue canadienne de medecine comparee.

[135]  A. Osterhaus,et al.  Feline infectious peritonitis (FIP) virus. III. Studies on the multiplication of FIP virus in the suckling mouse. , 2010, Zentralblatt fur Veterinarmedizin. Reihe B. Journal of veterinary medicine. Series B.

[136]  L. Binn,et al.  Recovery and characterization of a coronavirus from military dogs with diarrhea. , 1974, Proceedings, annual meeting of the United States Animal Health Association.

[137]  R. Chanock,et al.  Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[138]  D. Hamre,et al.  A New Virus Isolated from the Human Respiratory Tract.∗ , 1966, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.