Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals
Abstract
:1. Introduction
Species | Dose Ranges | Inoculation Route | Infectious Viral Shedding | Clinical Signs | Histopathological Changes | Infectious Virus in Tissues | Transmission | Neutralizing Antibody Response | Susceptible to Re-Infection | Natural Infection | References (Experimental Infections) | References (Natural Infections) |
---|---|---|---|---|---|---|---|---|---|---|---|---|
Domestic cat (Felis catus) | 105–7 × 105 pfu | Nasal, oral, tracheal, ocular | 1–6 DPC (nasal/oral) | Subclinical in most studies (adult/subadult); behavior changes, diarrhea, weight loss in one study; potential severe clinical signs in juveniles | Mild/moderate respiratory tract lesions (adult/subadult), severe in juveniles | Consistent in nasal turbinate, soft palate, trachea, tonsil; isolated detection in lung and intestine | Yes, via direct contact; indirect (aerosol) transmission less effective. | Yes, by 7 DPC | Resistant or limited re-infection | Yes, natural infection in domestic cats and large cats from zoos | [36,37,38,39,40,41,42] | [43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67] |
Domestic dog (Canis familiaris) | 105 pfu | Nasal | None | Subclinical | Not reported | Not reported | No transmission | Yes, by 14 DPC | Not tested | Yes | [36,37] | [43,49,50,56,57,59,61,62,68,69,70] |
Syrian golden hamster (Mesocricetus auratus) | 100–105 pfu | nasal | 2–5 DPC (nasal) | Weight loss, lethargy, ruffled fur, hunched posture, respiratory signs, fatal disease reported in older hamsters | Moderate-to-severe lesions in respiratory tract; lesions noted in other tissues | Consistent in nasal turbinate, trachea, lung; 1 sample in brain | Yes, via direct and indirect (aerosol) contact; less efficient via fomites | Yes, by 7 DPC | Resistant to re-infection | None reported | [71,72,73,74,75,76,77,78,79] | |
Chinese hamster (Cricetulus griseus) | 105 pfu | Nasal | Not reported (vRNA in oral swabs 2–5 DPC) | Weight loss | Moderate lesions in lungs reported | Detected in lungs at 2–5 DPC | Not tested | Not tested | Not tested | None reported | [80] | |
Djungarian dwarf hamster (Phodopus sungorus) | 105 pfu | Nasal | Not reported (vRNA in oral swabs 2–5 DPC) | Subclinical | Moderate-to-severe lesions in lungs reported | Detected in lungs at 2–5 DPC | Not tested | Not tested | Not tested | None reported | [81] | |
Campbell’s dwarf hamster (Phodopus campbelli) | 105 pfu | Nasal | Not reported (vRNA in oral swabs 2–5 DPC) | Subclinical | Moderate-to-severe lesions in lungs reported | Detected in lungs at 2–5 DPC | Not tested | Not tested | Not tested | None reported | [81] | |
Roborovski dwarf hamster (Phodopus roborovskii) | 5 × 104–105 pfu | Nasal | Not reported (vRNA in oral swabs 2–3 DPC) | Decreased body temperature, severe weight loss, dyspnea, ruffled fur, depressed behavior, required euthanasia between 3–5 DPC | Severe lesions in the lungs reported | Detected in lungs at 2–3 DPC before euthanasia | Not tested | Not tested | Not tested | None reported | [81] | |
New Zealand white rabbit (Oryctolagus cuniculus) | 104–106 pfu | Nasal | 1–7 DPC (nasal); 1 DPC (oral) | Subclinical | Mild-to-moderate lesions in respiratory tract | Not reported | Not tested | Yes, by 21 DPC | Not tested | None reported | [82] | |
Cottontail rabbit (Sylvilagus sp.) | 3 × 104–8 × 104 pfu | Nasal | None | None | None | None | Not tested | None | Not tested | None reported | [83] | |
Domestic ferret (Mustela putorius furo) | 5 × 102–5 × 106 pfu | Nasal | 2–8 DPC (nasal); 1–5 DPC (oral); 2–4 DPC (saliva); 4 DPC (urine/feces) | Most subclinical; isolated increased body temperature, reduced activity, respiratory signs, reduced activity/appetite, ruffled fur | Mild-to-moderate lesions in respiratory tract | Detected 2–8 DPC in nasal turbinate (high), trachea, larynx, esophagus, soft palate, lung, tonsil | Yes, via direct contact; indirect (aerosol) transmission less effective | Yes, by 10–13 DPC | Resistant to reinfection except with low neutralizing antibodies | Yes | [37,76,84,85,86,87,88,89,90] | [43,91,92] |
American mink (Neovison vison) | 5 × 106 pfu | Nasal | 2–8 DPC (nasal) | Weight loss, some nasal discharge (experimental); Many asymptomatic; nasal discharge, respiratory distress, reduced activity/feed intake, mortality (natural) | Mild-to-severe lesions in respiratory tract | Detected 4 DPC in nasal turbinate, soft palate, tonsil, lung | Yes, via indirect (aerosol) transmission | Yes, by 18 DPC | Not tested, unlikely based on natural infection data | Widespread infection in farms; natural infection from mink to humans, cats, and dogs | [93] | [43,94,95,96,97,98,99] |
Raccoon dog (Nyctereutes procyonoides) | 105 TCID50 | Nasal | 2–4 DPC (nasal/oral) | Most subclinical; isolated lethargy observed | Mild lesions in nasal conchae | None detected | Yes, via indirect (aerosol) transmission | Yes, in some animals by 18 DPC | Not tested | None reported | [100] | |
Domestic cattle (Bos taurus) | 105– 3 × 107 TCID50 | Nasal, tracheal, venous | None (limited vRNA in nasal swabs 2–10 DPC) | Most subclinical; some increased temperature and coughing in calves. | None | None (vRNA detected in one lymph node sample on 10 DPC) | No transmission | Low or absent at 21 DPC | Not tested | None reported | [101,102] | |
Domestic pig (Sus scrofa) | 105–2.5 × 107 pfu | Nasal, oral, tracheal, muscular, venous | Not reported (limited vRNA, mostly between 1 and 3 DPC (oral/nasal) | Most subclinical; one study showed isolated ocular nasal discharge, mild depression, cough | None | Detected in only one lymph node 13 DPC | No transmission | Yes, by muscular or venous administration by 22 DPC | Not tested | None reported | [37,84,103,104,105,106] | |
Domestic chicken (Gallus gallus domesticus) | 7 × 104–106 pfu | Nasal, choanal, oral, ocular | None | Subclinical | None | None | No transmission | None | Not tested | None reported | [37,84,107,108] | |
Japanese quail (Coturnix japonica) | 3 × 105 TCID50 | Choanal | None | Subclinical | None | Not tested | Not tested | None | Not tested | None reported | [107] | |
Turkey (Meleagris gallopavo) | 2 × 105–106 pfu | Nasal, choanal, oral, ocular | None | Subclinical | None | None | Not tested | None | Not tested | None reported | [107] | |
Duck (Anas platyrhinchos domesticus) | 105–106 TCID50 | Nasal, choanal | None | Subclinical | None | Not tested | No transmission | None | Not tested | None reported | [37,107] | |
Goose (Anser cygnoides) | 106 TCID50 | Choanal | None | Subclinical | None | Not tested | Not tested | None | Not tested | None reported | [107] | |
Deer mouse (Peromyscus maniculatus) | 2 × 104–106 TCID50 | Nasal | 1–4 DPC (oral); 2–8 DPC (rectal) | Most subclinical; isolated ruffled fur, one study showed weight loss during acute infection | Mild-to-Moderate lesions in respiratory tract, lesions in olfactory epithelium/brain | Detected 2–6 DPC (nasal turbinate, trachea, lung); low in intestine 2–4 DPC | Yes, transmission over two passages | Yes, by 14 DPC | Not tested | None reported | [83,109,110] | |
Bushy-tailed woodrat (Neotoma cinerea). | 3 × 104–8 × 104 TCID50 | Nasal | 1–5 DPC (oral) | Subclinical | Mild lesions in lung | 3 DPC (nasal turbinate, trachea, lung) | Not tested | Yes, by 28 DPC | Not tested | None reported | [83] | |
Wild House mouse (Mus musculus) | 3 × 104–8 × 104 TCID50 | Nasal | None | Subclinical | None | None | Not tested | None | Not tested | None reported | [83] | |
Fox squirrel (Sciurus niger) | 3 × 104–8 × 104 TCID50 | Nasal | None | Subclinical | None | None | Not tested | Not tested | Not tested | None reported | [83] | |
Wyoming ground squirrel (Urocitellus elegans) | 3 × 104–8 × 104 TCID50 | Nasal | None | Subclinical | None | None | Not tested | Not tested | Not tested | None reported | [83] | |
Black-tailed prairie dog (Cynomys ludovicianus) | 3 × 104–8 × 104 TCID50 | Nasal | None | Subclinical | None | None | Not tested | None | Not tested | None reported | [83] | |
Asian small-clawed otter (Aonyx cinereus) | Not applicable | Not tested | Not tested | Respiratory signs, lethargy | Not tested | Not tested | Yes, via direct contact | Not tested | Not tested | Yes | [111,112] | |
Striped skunk (Mephitis mephitis) | 3 × 104–8 × 104 TCID50 | Nasal | 2–7 DPC (nasal); 2–5 DPC (oral) | Subclinical | None | 3 DPC (nasal turbinate) | Not tested | Yes, by 28 DPC | Not tested | None reported | [83] | |
Raccoon (Procylon lotor) | 3 × 104–8 × 104 TCID50 | Nasal | None | Subclinical | None | None | Not tested | None | Not tested | None reported | [83] | |
White-tailed deer (Odocoileus virginianus) | 106–107 TCID50 | Nasal | 1–5 DPC (nasal); 3 DPC (oral); 5 DPC (rectal); 1 DPC (feces) | Most subclinical; elevated body temperature; some ocular/nasal discharge | Mild lesions in respiratory tract | 4 DPC (trachea/bronchi) | Yes, via direction and indirect (aerosol) contact | Yes, by 7 DPC | Not tested | Yes, determined via serology and RT-qPCR | [113,114] | [115,116] |
Northern Tree shrew (Tupaia belangeri) | 106–107 TCID50 | Nasal, oral, ocular | None reported; no vRNA shedding in one study; variable vRNA shedding in one study | Most subclinical; increase in body temperature | Mild-to-moderate lesions in lungs; several histopathological changes reported in non-respiratory tissues | 4–7 DPC (trachea, lung, pancreas) | Not tested | Reportedly yes, unknown DPC | Not tested | None reported | [117,118] | |
Egyptian fruit bat (Rousettus aegyptiacus) | 105 TCID50 | Nasal | 2 DPC (one oral swab); (vRNA 2–12 DPC (oral); 2–4 DPC (feces) | Subclinical | Mild-to-moderate lesions in upper respiratory tract; some mild lesions in lung | 4 DPC (trachea, lung) | Yes, to proportion of bats via direct contact | Yes, weak response by 8 DPC | Not tested | None reported | [84] | |
Big brown bat (Eptesicus fuscus) | 105 TCID5 | Nasal, Oral | None | Subclinical | None | None | None | None | Not tested | None reported | [119] | |
Rhesus macaque (Macaca mulatta) | 104–5 × 106 pfu | Nasal, oral, tracheal, ocular, venous | 1–5 DPC (nasal); 1–6 DPC (oral); 9 DPC (rectal) | Subclinical, or elevated body temperature, decreased activity, appetite, body weight; changes in respiratory pattern | Mild-to-moderate lesions in respiratory tract | 3 DPC (lungs) | Not tested | Yes, by 8 DPC | Resistant to reinfection | None reported | [120,121,122,123,124,125,126,127,128,129,130,131,132] | |
Cynomolgus macaque (Macaca fascicularis) | 106–2 × 107 pfu | Nasal, oral, tracheal, ocular, venous | 1–7 DPC (nasal, oral); 1–3 DPC (conjunctival) | Subclinical, or elevated body temperature, decreased appetite and body weight. | Mild lesions in respiratory tract | 3 DPC (lungs) | Not tested | Yes, by 7 DPC | Not tested | None reported | [122,128,131,133] | |
African green monkey (Chlorocebus aethiops) | 1.5 × 103–2.5 × 106 pfu | Nasal, oral, tracheal, ocular, aerosol | 2–7, 21 DPC (nasal); 2–9, 21 DPC (oral); 2–5, 14 DPC (rectal) | Decreased appetite, anorexia, elevated body temperature, changes in respiratory rate; ARDS in two animals | Mild respiratory lesions; severe in two animals with ARDS | 5 DPC (lungs) | Not tested | Yes, by 5 DPC | Resistant to reinfection | None reported | [132,134,135,136] | |
Baboon (Papio hamadryas) | 106 pfu | Nasal, tracheal, ocular | Not reported; vRNA detected 3–17 DPC (nasal/rectal) | None reported | Moderate respiratory tract lesions | Not reported; vRNA detected in lungs at 14/17 DPC | Not tested | Not reported | Not tested | None reported | [127] | |
Common marmoset (Callithrix jacchus) | 106 pfu | Nasal, tracheal, ocular | Not reported; vRNA detected 2–12 DPC (nasal), 2–10 DPC (oral/rectal), 2–8 DPC (blood), 6–21 DPC (feces). | Most subclinical, increased body temperature. | Mild respiratory tract lesions. | Not reported; vRNA detected in lungs at 3/14 DPC | Not tested | None detected | Not tested | None reported | [122,127] | |
Western lowland gorilla (Gorilla gorilla) | Not applicable | Not tested | Not tested | Respiratory signs | Not tested | Not tested | Yes, via direct contact | Not tested | Not tested | Yes | [137] |
2. Main Text
2.1. Domestic Animals
2.1.1. Cats
2.1.2. Dogs
2.1.3. Hamsters
2.1.4. Rabbits
2.1.5. Ferrets
2.1.6. Mink
2.1.7. Raccoon Dogs
2.1.8. Cattle
2.1.9. Pigs
2.1.10. Poultry
2.2. Wild/Peridomestic Animals
2.2.1. Deer Mice
2.2.2. Bushy-Tailed Woodrats
2.2.3. House Mice, Fox Squirrels, Wyoming Ground Squirrels, and Black-Tailed Prairie Dogs
2.2.4. Otters
2.2.5. Striped Skunks and Raccoons
2.2.6. White-Tailed Deer
2.2.7. Tree Shrews
2.2.8. Megachiroptera Bats
2.2.9. Microchiroptera Bats
2.2.10. Non-Human Primates
2.2.11. Transgenic Laboratory Mice
3. Summary and Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Meekins, D.A.; Gaudreault, N.N.; Richt, J.A. Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals. Viruses 2021, 13, 1993. https://doi.org/10.3390/v13101993
Meekins DA, Gaudreault NN, Richt JA. Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals. Viruses. 2021; 13(10):1993. https://doi.org/10.3390/v13101993
Chicago/Turabian StyleMeekins, David A., Natasha N. Gaudreault, and Juergen A. Richt. 2021. "Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals" Viruses 13, no. 10: 1993. https://doi.org/10.3390/v13101993
APA StyleMeekins, D. A., Gaudreault, N. N., & Richt, J. A. (2021). Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals. Viruses, 13(10), 1993. https://doi.org/10.3390/v13101993