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10.3390/v13081673
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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
1,†,
Marieke A. Stammes
2,†,
Zahra C. Fagrouch
1,
Gwendoline Kiemenyi-Kayere
1,
Henk Niphuis
1,
Daniella Mortier
1,
Nikki van Driel
3,
Ivonne Nieuwenhuis
2,
Richard A. W. Vervenne
2,
Tom Haaksma
3,
Boudewijn Ouwerling
3,
Deborah Adema
3,
Roja Fidel Acar
1,
Ella Zuiderwijk-Sick
4,
Lisette Meijer
2,
Petra Mooij
1,
Ed J. Remarque
1,
Herman Oostermeijer
1,
Gerrit Koopman
1,
Alexis C. R. Hoste
5,
Patricia Sastre
5,
Bart L. Haagmans
6,
Ronald E. Bontrop
7,8,
Jan A. M. Langermans
3,9,
Willy M. Bogers
1,
Ivanela Kondova
3,
Ernst J. Verschoor
1,* and
Babs E. Verstrepen
1add Show full author list remove Hide full author list
1
Biomedical Primate Research Centre (BPRC), Department of Virology, 2288 GJ Rijswijk, The Netherlands
2
Department of Parasitology, BPRC, 2288 GJ Rijswijk, The Netherlands
3
Animal Science Department, BPRC, 2288 GJ Rijswijk, The Netherlands
4
Alternatives Unit, BPRC, 2288 GJ Rijswijk, The Netherlands
5
Eurofins-Inmunología y Genética Aplicada (Eurofins-INGENASA), 28037 Madrid, Spain
6
Department of Viroscience, Erasmus University Medical Center, 3015 GD Rotterdam, The Netherlands
7
Department of Comparative Genetics and Refinement, BPRC, 2288 GJ Rijswijk, The Netherlands
8
Department of Biology, Theoretical Biology and Bioinformatics, Utrecht University, 3584 CH Utrecht, The Netherlands
9
Unit Animals in Science and Society, Department of Population Health Sciences, Veterinary Faculty, Utrecht University, 3584 CL Utrecht, The Netherlands
*
Author to whom correspondence should be addressed.
†
These authors contributed equally.
Viruses 2021, 13(8), 1673; https://doi.org/10.3390/v13081673
Submission received: 23 June 2021 / Revised: 13 August 2021 / Accepted: 18 August 2021 / Published: 23 August 2021
(This article belongs to the Special Issue SARS-CoV-2 and Animal Models)
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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. 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.
Keywords: SARS-CoV-2; COVID-19; non-human primates; animal models; NHPs SARS-CoV-2; COVID-19; non-human primates; animal models; NHPs

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MDPI and ACS Style

Böszörményi, K.P.; Stammes, M.A.; Fagrouch, Z.C.; Kiemenyi-Kayere, G.; Niphuis, H.; Mortier, D.; van Driel, N.; Nieuwenhuis, I.; Vervenne, R.A.W.; Haaksma, T.; et al. 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. Viruses 2021, 13, 1673. https://doi.org/10.3390/v13081673

AMA Style

Böszörményi KP, Stammes MA, Fagrouch ZC, Kiemenyi-Kayere G, Niphuis H, Mortier D, van Driel N, Nieuwenhuis I, Vervenne RAW, Haaksma T, et al. 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. Viruses. 2021; 13(8):1673. https://doi.org/10.3390/v13081673

Chicago/Turabian Style

Böszörményi, Kinga P., Marieke A. Stammes, Zahra C. Fagrouch, Gwendoline Kiemenyi-Kayere, Henk Niphuis, Daniella Mortier, Nikki van Driel, Ivonne Nieuwenhuis, Richard A. W. Vervenne, Tom Haaksma, and et al. 2021. "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" Viruses 13, no. 8: 1673. https://doi.org/10.3390/v13081673

APA Style

Böszörményi, K. P., Stammes, M. A., Fagrouch, Z. C., Kiemenyi-Kayere, G., Niphuis, H., Mortier, D., van Driel, N., Nieuwenhuis, I., Vervenne, R. A. W., Haaksma, T., Ouwerling, B., Adema, D., Acar, R. F., Zuiderwijk-Sick, E., Meijer, L., Mooij, P., Remarque, E. J., Oostermeijer, H., Koopman, G., ... Verstrepen, B. E. (2021). 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. Viruses, 13(8), 1673. https://doi.org/10.3390/v13081673

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