The DOI matches its Crossref record; 48 of the 48 references it cites were found in a registry or an index.
Responses to acute infection with SARS-CoV-2 in the lungs of rhesus macaques, baboons and marmosets
Open accessPublished version of a preprint
Abstract
Non-human primate models will expedite therapeutics and vaccines for coronavirus disease 2019 (COVID-19) to clinical trials. Here, we compare acute severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in young and old rhesus macaques, baboons and old marmosets. Macaques had clinical signs of viral infection, mild to moderate pneumonitis and extra-pulmonary pathologies, and both age groups recovered in two weeks. Baboons had prolonged viral RNA shedding and substantially more lung inflammation compared with macaques. Inflammation in bronchoalveolar lavage was increased in old versus young baboons. Using techniques including computed tomography imaging, immunophenotyping, and alveolar/peripheral cytokine response and immunohistochemical analyses, we delineated cellular immune responses to SARS-CoV-2 infection in macaque and baboon lungs, including innate and adaptive immune cells and a prominent type-I interferon response. Macaques developed T-cell memory phenotypes/responses and bystander cytokine production. Old macaques had lower titres of SARS-CoV-2-specific IgG antibody levels compared with young macaques. Acute respiratory distress in macaques and baboons recapitulates the progression of COVID-19 in humans, making them suitable as models to test vaccines and therapies.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Consistently, the levels of viral spike-protein-specific IgG during early time-points of acute SARS-CoV-2 infection in rhesus macaques are reduced in older macaques compared to young ones, consistent with age crippling the formation of class-switched antibody titers needed to clear the viral infection155.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [155]
Experimental — accuracy not yet measuredIn the citing paper
“Consistently, the levels of viral spike-protein-specific IgG during early time-points of acute SARS-CoV-2 infection in rhesus macaques are reduced in older macaques compared to young ones, consistent with age crippling the formation of class-switched antibody titers needed to clear the viral infection155.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [155]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
1 retracted
Isoniazid and Rifapentine Treatment Eradicates Persistent Mycobacterium tuberculosis in Macaques
Foreman, T. W., Bucşan, A. N., Mehra, S., Peloquin, C. A., Doyle, L. A., Russell‐Lodrigue, K., Gandhi, N. R., Altman, J. D., Day, C. L., Ernst, J., et al. (2019) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201903-0646oc · Cited by 15
Self-citationRetractedHoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T. S., Herrler, G., Wu, N.-H., Nitsche, A., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.052 · Cited by 20,286
Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR
Corman, V. M., Landt, O., Kaiser, M., Molenkamp, R., Meijer, A., Chu, D. K. W., Bleicker, T., Brünink, S., Schneider, J. A., Schmidt, M. L., et al. (2020) · Eurosurveillance · doi:10.2807/1560-7917.es.2020.25.3.2000045 · Cited by 7,266
Virological assessment of hospitalized patients with COVID-2019
Wölfel, R., Corman, V. M., Guggemos, W., Seilmaier, M., Zange, S., Müller, M. A., Niemeyer, D., Jones, T. C., Vollmar, P., Rothe, C., et al. (2020) · Nature · doi:10.1038/s41586-020-2196-x · Cited by 6,661
Restoring function in exhausted CD8 T cells during chronic viral infection
Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., & Ahmed, R. (2005) · Nature · doi:10.1038/nature04444 · Cited by 4,057
Veazey, R. S., DeMaria, M. A., Chalifoux, L. V., Shvetz, D. E., Pauley, D. R., Knight, H., Rosenzweig, M., Johnson, R. P., Desrosiers, R. C., & Lackner, A. A. (1998) · Science · doi:10.1126/science.280.5362.427 · Cited by 1,404
Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells
Matsuyama, S., Nao, N., Shirato, K., Kawase, M., Saito, S., Takayama, I., Nagata, N., Sekizuka, T., Katoh, H., Kato, F., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002589117 · Cited by 1,381
DNA vaccine protection against SARS-CoV-2 in rhesus macaques
Yu, J., Tostanoski, L. H., Peter, L., Mercado, N. B., McMahan, K., Mahrokhian, S. H., Nkolola, J. P., Liu, J., Li, Z., Chandrashekar, A., et al. (2020) · Science · doi:10.1126/science.abc6284 · Cited by 997
Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model
Rockx, B., Kuiken, T., Herfst, S., Bestebroer, T., Lamers, M. M., Oude Munnink, B. B., de Meulder, D., van Amerongen, G., van den Brand, J., Okba, N. M. A., et al. (2020) · Science · doi:10.1126/science.abb7314 · Cited by 901
SARS-CoV-2 infection protects against rechallenge in rhesus macaques
Chandrashekar, A., Liu, J., Martinot, A. J., McMahan, K., Mercado, N. B., Peter, L., Tostanoski, L. H., Yu, J., Maliga, Z., Nekorchuk, M., et al. (2020) · Science · doi:10.1126/science.abc4776 · Cited by 816
Research works printed but not linked: 2
- Munster, V. J. et al. Respiratory disease in rhesus macaques inoculated with SARS-CoV-2. Nature 585, 268–272 (2020). · DOI · Paper page
- Chandrashekar, A. et al. SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science 369, 812–817 (2020). · DOI · Paper page
Cited by
Sorted by citations
BNT162b vaccines protect rhesus macaques from SARS-CoV-2
Vogel, A. B., Kanevsky, I., Che, Y., Swanson, K. A., Muik, A., Vormehr, M., Kranz, L. M., Walzer, K. C., Hein, S., Güler, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03275-y · Cited by 694
Self-citationLethality of SARS-CoV-2 infection in K18 human angiotensin-converting enzyme 2 transgenic mice
Oladunni, F. S., Park, J., Pino, P. A., González, O., Akhter, A., Allué‐Guardia, A., Olmo-Fontánez, A. M., Gautam, S., Garcia‐Vilanova, A., Ye, C., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19891-7 · Cited by 398
Self-citationSARS-CoV-2, COVID-19 and the aging immune system
Bartleson, J. M., Radenkovic, D., Covarrubias, A. J., Furman, D., Winer, D. A., & Verdin, E. (2021) · Nature Aging · doi:10.1038/s43587-021-00114-7 · Cited by 359
Lessons learned 1 year after SARS-CoV-2 emergence leading to COVID-19 pandemic
To, K. K., Sridhar, S., Chiu, K. H., Hung, D. L. L., Li, X., Hung, I. F., Tam, A. R., Chung, T. W., Chan, J. F., Zhang, J., et al. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.1898291 · Cited by 359
Innate immune and inflammatory responses to SARS-CoV-2: Implications for COVID-19
Lowery, S. A., Sariol, A., & Perlman, S. M. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.05.004 · Cited by 303
Comparison of rhesus and cynomolgus macaques as an infection model for COVID-19
Salguero, F. J., White, A., Slack, G. S., Fotheringham, S. A., Bewley, K. R., Gooch, K. E., Longet, S., Humphries, H. E., Watson, R. J., Hunter, L. E., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21389-9 · Cited by 163
Vogel, A. B., Kanevsky, I., Che, Y., Swanson, K. A., Muik, A., Vormehr, M., Kranz, L. M., Walzer, K. C., Hein, S., Güler, A., et al. (2020) · doi:10.1101/2020.09.08.280818 · Cited by 126
Self-citationBlair, R. V., Vaccari, M., Doyle‐Meyers, L. A., Roy, C. J., Russell‐Lodrigue, K., Fahlberg, M. D., Monjure, C. J., Beddingfield, B. J., Plante, K. S., Plante, J. A., et al. (2020) · American Journal Of Pathology · doi:10.1016/j.ajpath.2020.10.016 · Cited by 132
Measuring immunity to SARS-CoV-2 infection: comparing assays and animal models
Khoury, D. S., Wheatley, A. K., Ramuta, M. D., Reynaldi, A., Cromer, D., Subbarao, K., O’Connor, D. H., Kent, S. J., & Davenport, M. P. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-00471-1 · Cited by 115
Esparza, T. J., Martin, N. P., Anderson, G. P., Goldman, E. R., & Brody, D. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-79036-0 · Cited by 118
Rosa, B. A., Ahmed, M., Singh, D. K., Choreño-Parra, J. A., Cole, J., Jiménez-Álvarez, L. A., Rodríguez-Reyna, T. S., Singh, B., Gonzalez, O., Carrion, R., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01829-4 · Cited by 106
Self-citationAnimal models for COVID-19: advances, gaps and perspectives
Fan, C., Wu, Y., Xiong, R., Yang, Y., Ling, C., Liu, S., Liu, S., & Wang, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01087-8 · Cited by 110
Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals
Meekins, D. A., Gaudreault, N. N., & Richt, J. A. (2021) · Viruses · doi:10.3390/v13101993 · Cited by 105
Cool, K. R., Gaudreault, N. N., Morozov, I., Trujillo, J. D., Meekins, D. A., McDowell, C. D., Carossino, M., Bold, D., Mitzel, D., Kwon, T., et al. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.2012528 · Cited by 103
Brain Inflammation and Intracellular α-Synuclein Aggregates in Macaques after SARS-CoV-2 Infection
Philippens, I. H. C. H. M., Böszörményi, K. P., Wubben, J. A. M., Fagrouch, Z. C., van Driel, N., Mayenburg, A. Q., Lozovagia, D., Roos, E., Schurink, B., Bugiani, M., et al. (2022) · Viruses · doi:10.3390/v14040776 · Cited by 102
Wang, S., Li, W., Wang, Z., Yang, W., Li, E., Xia, X., Yan, F., & Chiu, S. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01917-x · Cited by 124
Chan, C. E. Z., Seah, S. G. K., Chye, D. H., Massey, S., Torres, M., Lim, A. P. C., Wong, S. K. K., Neo, J. J. Y., Wong, P. S., Lim, J. H., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0253487 · Cited by 90
Routhu, N. K., Cheedarla, N., Bollimpelli, V. S., Gangadhara, S., Edara, V. V., Lai, L., Sahoo, A., Shiferaw, A., Styles, T. M., Floyd, K. A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23942-y · Cited by 88
Fahlberg, M. D., Blair, R. V., Doyle‐Meyers, L. A., Midkiff, C. C., Zenere, G., Russell‐Lodrigue, K., Monjure, C. J., Haupt, E., Penney, T., Lehmicke, G., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19967-4 · Cited by 85
SARS-CoV-2 induces robust germinal center CD4 T follicular helper cell responses in rhesus macaques
Lakshmanappa, Y. S., Elizaldi, S. R., Roh, J. W., Schmidt, B., Carroll, T. D., Weaver, K. D., Smith, J. C., Verma, A., Deere, J. D., Dutra, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20642-x · Cited by 92
Wu, M., Liu, F., Sun, J., Li, X., He, X.-Y., Zheng, H., Pei, R., Sun, H., Zhou, Y.-H., Yan, Q., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00849-0 · Cited by 86
Neutrophils and COVID-19: Active Participants and Rational Therapeutic Targets
Hazeldine, J., & Lord, J. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.680134 · Cited by 86
Advances and gaps in SARS-CoV-2 infection models
Muñoz‐Fontela, C., Widerspick, L., Albrecht, R. A., Beer, M., Carroll, M. W., de Wit, E., Diamond, M., Dowling, W. E., Funnell, S. G. P., García‐Sastre, A., et al. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010161 · Cited by 76
Type I interferons and SARS-CoV-2: from cells to organisms
Bastard, P., Zhang, Q., Zhang, S., Jouanguy, E., & Casanova, J. (2022) · Current Opinion in Immunology · doi:10.1016/j.coi.2022.01.003 · Cited by 73
Nonhuman Primates in Translational Research
Tarantal, A. F., Noctor, S. C., & Hartigan-O’Connor, D. J. (2022) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-021419-083813 · Cited by 81
SARS-CoV-2 Reverse Zoonoses to Pumas and Lions, South Africa
Koeppel, K. N., Mendes, A., Strydom, A., Rotherham, L. S., Mulumba, M., & Venter, M. (2022) · Viruses · doi:10.3390/v14010120 · Cited by 70
Immunosenescence and inflamm-ageing in COVID-19
Zinatizadeh, M. R., Zarandi, P. K., Ghiasi, M., Kooshki, H., Mohammadi, M., Amani, J., & Rezaei, N. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101818 · Cited by 69
Zoonotic and Reverse Zoonotic Transmissibility of SARS-CoV-2
Goraichuk, I. V., Arefiev, V. L., Stegniy, B. Т., & Gerilovych, A. (2021) · Virus Research · doi:10.1016/j.virusres.2021.198473 · Cited by 66
Cell-Type Apoptosis in Lung during SARS-CoV-2 Infection
Liu, Y., Garron, T. M., Chang, Q., Su, Z., Zhou, C., Qiu, Y., Gong, E. C., Zheng, J., Yin, Y. W., Ksiazek, T. G., et al. (2021) · Pathogens · doi:10.3390/pathogens10050509 · Cited by 61
Welfare, N.-F. E. P. O. A. H. A., Nielsen, S. S., Álvarez, J., Bicout, D., Calistri, P., Canali, E., Drewe, J. A., Garin‐Bastuji, B., Gonzáles, J. L., Gortázar, C., et al. (2023) · EFSA Journal · doi:10.2903/j.efsa.2023.7822 · Cited by 60
Analysis of SARS-CoV-2 infection dynamic in vivo using reporter-expressing viruses
Ye, C., Chiem, K., Park, J., Silvas, J. A., Vasquez, D. M., Sourimant, J., Lin, M. J., Greninger, A. L., Plemper, R. K., Torrelles, J. B., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2111593118 · Cited by 52
Self-citationBöszörményi, K. P., Stammes, M. A., Fagrouch, Z. C., Kiemenyi-Kayere, G., Niphuis, H., Mortier, D., van Driel, N., Nieuwenhuis, I. G., Vervenne, R. A. W., Haaksma, T., et al. (2021) · Viruses · doi:10.3390/v13081673 · Cited by 52
Myeloid cell interferon responses correlate with clearance of SARS-CoV-2
Singh, D. K., Aladyeva, E., Das, S., Singh, B., Esaulova, E., Swain, A., Ahmed, M., Cole, J., Moodley, C., Mehra, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28315-7 · Cited by 47
Self-citationACTIVating Resources for the COVID-19 Pandemic: In Vivo Models for Vaccines and Therapeutics
Hewitt, J., Lutz, C. M., Florence, W. C., Pitt, M. L. M., Rao, S., Rappaport, J., & Haigwood, N. L. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.09.016 · Cited by 47
SARS-CoV-2 vaccines elicit durable immune responses in infant rhesus macaques
Garrido, C., Curtis, A. D., Dennis, M. L., Pathak, S., Gao, H., Montefiori, D. C., Tomai, M. A., Fox, C. B., Kozlowski, P. A., Scobey, T., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abj3684 · Cited by 46
Experimental Models of COVID-19
Caldera-Crespo, L. A., Paidas, M. J., Roy, S., Schulman, C. I., Kenyon, N. S., Daunert, S., & Jayakumar, A. R. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.792584 · Cited by 47
Non-human primate models of human respiratory infections
Lemaître, J., Naninck, T., Delache, B., Creppy, J., Huber, P., Holzapfel, M., Bouillier, C., Contreras, V., Martinon, F., Kahlaoui, N., et al. (2021) · Molecular Immunology · doi:10.1016/j.molimm.2021.04.010 · Cited by 48
SARS-CoV-2 in animals: From potential hosts to animal models
Michelitsch, A., Wernike, K., Ulrich, L., Mettenleiter, T. C., & Beer, M. (2021) · Advances in virus research · doi:10.1016/bs.aivir.2021.03.004 · Cited by 47
Ferrets are valuable models for SARS-CoV-2 research
Ciurkiewicz, M., Armando, F., Schreiner, T., de Buhr, N., Pilchová, V., Krupp-Buzimikic, V., Gabriel, G., von Köckritz‐Blickwede, M., Baumgärtner, W., Schulz, C., et al. (2022) · Veterinary Pathology · doi:10.1177/03009858211071012 · Cited by 43
Kane, Y., Wong, G., & Gao, G. F. (2023) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020420-025011 · Cited by 43
Hasenkrug, K. J., Feldmann, F., Myers, L. M., Santiago, M. L., Guo, K., Barrett, B. S., Mickens, K. L., Carmody, A., Okumura, A., Rao, D., et al. (2021) · mBio · doi:10.1128/mbio.01503-21 · Cited by 40
SARS-CoV-2 variants: biology, pathogenicity, immunity and control
Uraki, R., Korber, B., Diamond, M., & Kawaoka, Y. (2025) · Nature Reviews Microbiology · doi:10.1038/s41579-025-01255-x · Cited by 50
Human endogenous retrovirus K in the respiratory tract is associated with COVID-19 physiopathology
Temerozo, J. R., Rodrigues, N. F., dos Santos, M. C., Hottz, E. D., Sacramento, C. Q., da Silva, A. D. P. D., Mandacaru, S. C., Moraes, E. C. D. S., Trugilho, M. R. O., Gesto, J. S. M., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01260-9 · Cited by 45
Zarkoob, H., Allué‐Guardia, A., Chen, Y., Garcia‐Vilanova, A., Jung, O., Coon, S. L., Song, M. J., Park, J., Oladunni, F. S., Miller, J., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03753-7 · Cited by 37
Self-citationSARS-CoV-2 immunity in animal models
Chen, Z., Yuan, Y., Hu, Q., Zhu, A., Chen, F., Li, S., Guan, X., Lv, C., Tang, T., He, Y., et al. (2024) · Cellular and Molecular Immunology · doi:10.1038/s41423-023-01122-w · Cited by 39
Animal models of SARS-CoV-2 transmission
de Vries, R. D., Rockx, B., Haagmans, B. L., Herfst, S., Koopmans, M., & de Swart, R. L. (2021) · Current Opinion in Virology · doi:10.1016/j.coviro.2021.06.007 · Cited by 37
Singh, B., Moodley, C., Singh, D. K., Escobedo, R. A., Sharan, R., Arora, G., Ganatra, S., Shivanna, V., González, O., Hall-Ursone, S., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.163101 · Cited by 34
Self-citationHarris, P. E., Brasel, T., Massey, C., Herst, C. V., Burkholz, S., Lloyd, P. M., Blankenberg, T., Bey, T. M., Carback, R. T., Hodge, T. W., et al. (2021) · Vaccines · doi:10.3390/vaccines9050520 · Cited by 33
Islam, A., Ferdous, J., Islam, S., Sayeed, M. A., Rahman, M. K., Saha, O., Hassan, M. M., & Shirin, T. (2021) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14356 · Cited by 37
Nelson, C. E., Namasivayam, S., Foreman, T. W., Kauffman, K. D., Sakai, S., Dorosky, D. E., Lora, N. E., Program, N. T. I., Brooks, K., Potter, E. L., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abo0535 · Cited by 36
Upadhyay, A. A., Viox, E. G., Hoang, T. N., Boddapati, A. K., Pino, M., Lee, M. Y.-H., Corry, J., Strongin, Z., Cowan, D. A., Beagle, E. N., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37425-9 · Cited by 38
Jiang, W., Shi, L., Cai, L., Wang, X., Li, J., Li, H., Liang, J., Gu, Q., Ji, G., Li, J., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110112 · Cited by 33
The Common Marmoset—Biomedical Research Animal Model Applications and Common Spontaneous Diseases
Han, H., Powers, S. J., & Gabrielson, K. L. (2022) · Toxicologic Pathology · doi:10.1177/01926233221095449 · Cited by 36
Animal models for SARS‐CoV‐2 infection and pathology
Bi, Z., Hong, W., Yang, H. J., Lu, S., & Peng, X. (2021) · MedComm · doi:10.1002/mco2.98 · Cited by 35
Pahari, S., Arnett, E., Simper, J., Azad, A., Guerrero‐Arguero, I., Ye, C., Zhang, H., Cai, H., Wang, Y., Lai, Z., et al. (2023) · mBio · doi:10.1128/mbio.00834-23 · Cited by 33
Self-citationKenney, D., O’Connell, A. K., Turcinovic, J., Montanaro, P., Hekman, R. M., Tamura, T., Berneshawi, A. R., Cafiero, T. R., Abdullatif, S. A., Blum, B. C., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110714 · Cited by 35
Pereira, A. H. B., Vasconcelos, A. L. C. D., Silva, V. L., Nogueira, B. S., Silva, A. C., Pacheco, R. D. C., Souza, M. D. A., Colodel, É. M., Ubiali, D. G., Biondo, A. W., et al. (2022) · Journal of Comparative Pathology · doi:10.1016/j.jcpa.2022.03.005 · Cited by 32
Age-related differences in immune dynamics during SARS-CoV-2 infection in rhesus macaques
Speranza, E. E., Purushotham, J. N., Port, J. R., Schwarz, B. H., Flagg, M., Williamson, B. N., Feldmann, F., Singh, M., Pérez-Pérez, L., Sturdevant, G. L., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202101314 · Cited by 29
Viox, E. G., Hoang, T. N., Upadhyay, A. A., Nchioua, R., Hirschenberger, M., Strongin, Z., Tharp, G. K., Pino, M., Nguyen, K., Harper, J. L., et al. (2023) · Science Immunology · doi:10.1126/sciimmunol.adg0033 · Cited by 33
Ahsan, N., Rao, R. S. P., Wilson, R. S., Punyamurtula, U., Salvato, F., Petersen, M., Ahmed, M. K., Abid, M. R., Verburgt, J. C., Kihara, D., et al. (2021) · PROTEOMICS · doi:10.1002/pmic.202000279 · Cited by 30
Self-citationCOVID-19 and Pregnancy: Vertical Transmission and Inflammation Impact on Newborns
Joma, M., Fovet, C.-M., Seddiki, N., Gressèns, P., & Laforge, M. (2021) · Vaccines · doi:10.3390/vaccines9040391 · Cited by 32
Modelling behaviors relevant to brain disorders in the nonhuman primate: Are we there yet?
Scott, J. T., & Bourne, J. A. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102183 · Cited by 31
Mooij, P., García‐Arriaza, J., Pérez, P., Lázaro-Frías, A., Verstrepen, B. E., Böszörményi, K. P., Mortier, D., Fagrouch, Z. C., Kiemenyi-Kayere, G., Niphuis, H., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.845887 · Cited by 29
Use of convalescent serum reduces severity of COVID-19 in nonhuman primates
Cross, R. W., Prasad, A. N., Borisevich, V., Woolsey, C. B., Agans, K. N., Deer, D. J., Dobias, N. S., Geisbert, J. B., Fenton, K. A., & Geisbert, T. W. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108837 · Cited by 26
COVID-19 Research: Lessons from Non-Human Primate Models
Albrecht, L., Bishop, E., Jay, B., Lafoux, B., Minoves, M., & Passaes, C. (2021) · Vaccines · doi:10.3390/vaccines9080886 · Cited by 30
Rosenke, K., Feldmann, F., Okumura, A., Hansen, F., Tang-Huau, T.-L., Meade-White, K. D., Kaza, B., Callison, J. A., Lewis, M. C., Smith, B. J., et al. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.1997074 · Cited by 25
Myeloid-Derived Suppressor Cells Mediate T Cell Dysfunction in Nonhuman Primate TB Granulomas
Singh, B., Singh, D. K., Ganatra, S., Escobedo, R. A., Khader, S. A., Schlesinger, L. S., Kaushal, D., & Mehra, S. (2021) · mBio · doi:10.1128/mbio.03189-21 · Cited by 28
Self-citationNelson, C. E., Foreman, T. W., Fukutani, E. R., Kauffman, K. D., Sakai, S., Fleegle, J. D., Gomez, F., Program, N. T. I., Gould, S. T., Nouën, C. L., et al. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1012339 · Cited by 28
Nonhuman primate models for SARS-CoV-2 research: Consider alternatives to macaques
Chang, M., Hild, S. A., & Grieder, F. B. (2021) · Lab Animal · doi:10.1038/s41684-021-00755-6 · Cited by 26
Overview of Nonhuman Primate Models of SARS-CoV-2 Infection
Trichel, A. M. (2021) · Comparative Medicine · doi:10.30802/aalas-cm-20-000119 · Cited by 28
Mitchell, A. S., Hartig, R., Basso, M. A., Jarrett, W., Kästner, S., & Poirier, C. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2020.117700 · Cited by 28
Pacheco, J. A., Molena, K. F., Martins, C. R. O. G., Corona, S. A. M., & Borsatto, M. C. (2022) · Bulletin of the National Research Centre/Bulletin of the National Research Center · doi:10.1186/s42269-022-00830-z · Cited by 25
Bridging animal and clinical research during SARS-CoV-2 pandemic: A new-old challenge
Winkler, M. S., Skirecki, T., Brunkhorst, F. M., Cajander, S., Cavaillon, J., Ferrer, R., Flohé, S. B., García‐Salido, A., Giamarellos‐Bourboulis, E. J., Girardis, M., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103291 · Cited by 26
SARS-CoV-2: Pathogenesis, Molecular Targets and Experimental Models
Kanimozhi, G., Bharathiraja, P., Pawar, C. S., Khan, H. A., Alrokayan, S., & Prasad, N. R. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.638334 · Cited by 24
Modeling SARS-CoV-2: Comparative Pathology in Rhesus Macaque and Golden Syrian Hamster Models
Choudhary, S., Kanevsky, I., Yıldız, S., Sellers, R., Swanson, K., Franks, T., Rathnasinghe, R., Muñoz-Moreno, R., Jangra, S., Gonzalez, O., et al. (2022) · Toxicologic pathology (Print) · doi:10.1177/01926233211072767 · Cited by 24
Self-citationImmune interventions in COVID-19: a matter of time?
Plaçais, L., Richier, Q., Noël, N., Lacombe, K., Mariette, X., & Hermine, O. (2021) · Mucosal Immunology · doi:10.1038/s41385-021-00464-w · Cited by 22
Medical imaging of pulmonary disease in SARS-CoV-2-exposed non-human primates
Stammes, M., Lee, J., Meijer, L., Naninck, T., Doyle-Meyers, L., White, A. G., Borish, H., Hartman, A., Alvarez, X., Ganatra, S. R., et al. (2021) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.12.001 · Cited by 20
Self-citationCell and Animal Models for SARS-CoV-2 Research
Bestion, E., Halfon, P., Mezouar, S., & Mège, J. (2022) · Viruses · doi:10.3390/v14071507 · Cited by 24
Farheen, S., Agrawal, S., Zubair, S., Agrawal, A., Jamal, F., Altaf, I., Anwar, A. K., Umair, S. M., & Owais, M. (2021) · Frontiers in Aging · doi:10.3389/fragi.2021.748591 · Cited by 23
Organoid Models of SARS-CoV-2 Infection: What Have We Learned about COVID-19?
Tran, B. M., Deliyannis, G., Hachani, A., Earnest, L., Torresi, J., & Vincan, E. (2022) · Organoids · doi:10.3390/organoids1010002 · Cited by 21
Bucşan, A. N., Veatch, A. V., Singh, D. K., Akter, S., Golden, N., Kirkpatrick, M. G., Threeton, B., Moodley, C., Ahmed, M., Doyle, L. A., et al. (2022) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202112-2747oc · Cited by 21
Self-citationSharan, R., Ganatra, S., Singh, D. K., Cole, J., Foreman, T. W., Thippeshappa, R., Peloquin, C. A., Shivanna, V., González, O., Day, C. L., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci161564 · Cited by 21
Self-citationExperimental Animal Models of Coronavirus Infections: Strengths and Limitations
Casel, M. A. B., Rollon, R., & Choi, Y. K. (2021) · Immune Network · doi:10.4110/in.2021.21.e12 · Cited by 21
Rompay, K. K. A. V., Olstad, K. J., Sammak, R. L., Dutra, J., Watanabe, J., Usachenko, J. L., Immareddy, R., Verma, A., Lakshmanappa, Y. S., Schmidt, B., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009688 · Cited by 19
Self-citationRitter, J. M., Wilson, T. M., Gary, J. M., Seixas, J. N., Martines, R. B., Bhatnagar, J., Bollweg, B. C., Lee, E. H., Estetter, L. B. C., Silva-Flannery, L. M., et al. (2022) · Veterinary Pathology · doi:10.1177/03009858221079665 · Cited by 20
Singh, D. K., Ahmed, M., Akter, S., Shivanna, V., Bucşan, A. N., Mishra, A., Golden, N., Didier, P. J., Doyle‐Meyers, L. A., Hall-Ursone, S., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57090-4 · Cited by 20
Self-citationAnimal models for COVID-19 and tuberculosis
Corleis, B., Bastian, M., Hoffmann, D., Beer, M., & Dorhoi, A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1223260 · Cited by 21
Melton, A., Doyle‐Meyers, L. A., Blair, R. V., Midkiff, C. C., Melton, H. J., Russell‐Lodrigue, K., Aye, P. P., Schiro, F. R., Fahlberg, M. D., Szeltner, D. M., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010162 · Cited by 19
Sampad, M. J. N., Saiduzzaman, S. M., Walker, Z., Wells, T. N., Wayment, J. X., Ong, E. M., Mdaki, S. D., Tamhankar, M. A., Yuzvinsky, T. D., Patterson, J. L., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2400203121 · Cited by 18
Self-citationBNT162b vaccines are immunogenic and protect non-human primates against SARS-CoV-2Preprint
Vogel, A. B., Kanevsky, I., Che, Y., Swanson, K. A., Muik, A., Vormehr, M., Kranz, L. M., Walzer, K. C., Hein, S., Güler, A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.11.421008 · Cited by 18
Self-citationColeman, C., Doyle‐Meyers, L. A., Russell‐Lodrigue, K., Golden, N., Threeton, B., Song, K., Pierre, G., Baribault, C., Bohm, R. P., Maness, N. J., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.754642 · Cited by 17
Monoclonal Antibodies Protect Aged Rhesus Macaques From SARS-CoV2 Induced Immune Activation
Verma, A., Hawes, C. E., Lakshmanappa, Y. S., Roh, J. W., Schmidt, B., Dutra, J., Louie, W., Liu, H., Ma, Z.-M., Watanabe, J., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109942 · Cited by 17
Hamdy, M. E., El‐Deeb, A. H., Hagag, N. M., Shahein, M. A., Alaidi, O., & Hussein, H. A. (2023) · International Journal of Veterinary Science and Medicine · doi:10.1080/23144599.2023.2222981 · Cited by 17
Immunosenescence and Inflammaging in COVID-19
Asghari, F., Asghary, A., Zolbanin, N. M., Faraji, F., & Jafari, R. (2023) · Viral Immunology · doi:10.1089/vim.2023.0045 · Cited by 17
Carvajal, M., Sáenz, C., Fuentes, N., Guevara, R., Muñoz, E. B., Prado-Vivar, B., Díaz, E. A., Alfonso-Cortes, F., Coloma, J., Grunauer, M., et al. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.02741-23 · Cited by 16
Characteristics of animal models for COVID‐19
Qi, F., & Qin, C. (2022) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12278 · Cited by 14
SARS-CoV-2 antibodies in dogs and cats in a highly infected area of Brazil during the pandemic
Jarrah, S. A., Kmetiuk, L. B., Valleriani, F., Bonfini, B., Lorusso, A., Vasinioti, V. I., Decaro, N., dos Santos, M. T., Spohr, K. A. H., Pratelli, A., et al. (2023) · Frontiers in Veterinary Science · doi:10.3389/fvets.2023.1111728 · Cited by 14
Sacchetto, L., Chaves, B. A., Costa, E. R., Medeiros, A. S. D. M., Gordo, M., Araújo, D. B., Oliveira, D. B. L., da Silva, A. P. B., Negri, A. F., Durigon, E. L., et al. (2021) · Viruses · doi:10.3390/v13101933 · Cited by 15
SARS-CoV-2 at the human-animal interface: A review
Farag, E., Islam, M. M., Enan, K. A., Elhussein, A. M., Bansal, D., & Haroun, M. A. (2021) · Heliyon · doi:10.1016/j.heliyon.2021.e08496 · Cited by 16
Blair, R. V., Vaccari, M., Doyle‐Meyers, L. A., Roy, C. J., Russell‐Lodrigue, K., Fahlberg, M. D., Monjure, C. J., Beddingfield, B. J., Plante, K. S., Plante, J. A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.18.157933 · Cited by 15
Metadata
- Authors
- Singh, D. K., Singh, B., Ganatra, S. R., Gazi, M., Cole, J., Thippeshappa, R., Alfson, K. J., Clemmons, E., Gonzalez, O., Escobedo, R., Lee, T.-H., Chatterjee, A., Goez-Gazi, Y., Sharan, R., Gough, M., Alvarez, C., Blakley, A., Ferdin, J., Bartley, C., Staples, H., Parodi, L., Callery, J., Mannino, A., Klaffke, B., Escareno, P., Platt, R. N., Hodara, V., Scordo, J., Gautam, S., Vilanova, A. G., Olmo-Fontanez, A., Schami, A., Oyejide, A., Ajithdoss, D. K., Copin, R., Baum, A., Kyratsous, C., Alvarez, X., Ahmed, M., Rosa, B., Goodroe, A., Dutton, J., Hall-Ursone, S., Frost, P. A., Voges, A. K., Ross, C. N., Sayers, K., Chen, C., Hallam, C., Khader, S. A., Mitreva, M., Anderson, T. J. C., Martinez-Sobrido, L., Patterson, J. L., Turner, J., Torrelles, J. B., Dick, E. J., Brasky, K., Schlesinger, L. S., Giavedoni, L. D., Carrion, R., & Kaushal, D.
- Affiliations
- Texas Biomedical Research Institute (US)
- Regeneron (United States) (US)
- Washington University in St. Louis (US)
- Corresponding author
- Giavedoni, Luis D.
- Carrion, Ricardo
- Kaushal, Deepak
- ORCID
- Singh, Dhiraj Kumar
- Singh, Bindu
- Ganatra, Shashank R.
- Thippeshappa, Rajesh
- Alfson, Kendra J.
- Clemmons, Elizabeth
- Escobedo, Ruby
- Lee, Tae-Hyung
- Chatterjee, Ayan
- Sharan, Riti
- Bartley, Carmen
- Staples, Hilary
- Mannino, Amanda
- Platt, Roy N.
- Hodara, Vida
- Scordo, Julia
- Gautam, Shalini
- Vilanova, Andreu G.
- Schami, Alyssa
- Oyejide, Adelekan
- Ajithdoss, Dharani K.
- Copin, Richard
- Baum, Alina
- Kyratsous, Christos
- Alvarez, Xavier
- Ahmed, Mushtaq
- Rosa, Bruce
- Goodroe, Anna
- Dutton, John
- Hall-Ursone, Shannan
- Voges, Andra K.
- Ross, Corinna N.
- Sayers, Ken
- Chen, Christopher
- Hallam, Cory
- Khader, Shabaana A.
- Mitreva, Makedonka
- Anderson, Timothy J. C.
- Patterson, Jean L.
- Turner, Joanne
- Torrelles, Jordi B.
- Dick, Edward J.
- Schlesinger, Larry S.
- Giavedoni, Luis D.
- Carrion, Ricardo
- Kaushal, Deepak
- Venue
- Nature Microbiology
- Published
- 2020-12-18
- Volume
- 6
- Issue
- 1
- Pages
- 73-86
- ISSN
- 2058-5276 (ISSN-L)
- PMC
- PMC7890948
- OpenAlex
- W3116593921
- Cited by
- 209
- References
- 45
- Citations by year
- 2026: 9 · 2025: 16 · 2024: 22 · 2023: 29 · 2022: 51 · 2021: 71 · 2020: 11
- FWCI
- 5.37
- Type
- journal article
- Language
- en
- Update notices
- correction (2021-01-18)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Microbiology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (R01AI134236)
- U.S. Department of Health & Human Services | NIH | NIH Office of the Director (P51OD011133)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- SARS-CoV-2, COVID-19 pandemic, nonhuman primate model, rhesus monkeys, baboons, marmoset, age-related immune response, pneumonitis, lung inflammation, viral RNA shedding, type I interferon response, T cell memory, IgG antibody response, cell-mediated immunity
- MeSH terms
- COVID-19, SARS-CoV-2, Animals, Antibodies, Viral, Bronchoalveolar Lavage Fluid, Callithrix, Female, Humans, Immunoglobulin G, Immunity, Cellular, Inflammation, Lung, Macaca mulatta, Male, Monkey Diseases, Papio, Virus Shedding, Bronchoalveolar Lavage, Viral Load, Myeloid Cells, Adaptive Immunity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review