A single intranasal administration of AdCOVID protects against SARS-CoV-2 infection in the upper and lower respiratory tracts

References

• Chan JF, Zhang AJ, Yuan S, Poon VK, Chan CC, Lee AC, Chan WM, Fan Z, Tsoi HW, Wen L, et al. Simulation of the clinical and pathological manifestations of coronavirus disease 2019 (COVID-19) in a golden Syrian Hamster Model: implications for disease pathogenesis and transmissibility. Clin Infect Dis. 2020;71:1–11.
   PubMed Web of Science ®Google Scholar
• Prather KA, Marr LC, Schooley RT, McDiarmid MA, Wilson ME, Milton DK. Airborne transmission of SARS-CoV-2. Science. 2020;370(6514):303–04. doi:10.1126/science.abf0521.
   PubMed Web of Science ®Google Scholar
• Letko M, Marzi A, Munster V. Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses. Nature Microbiol. 2020;5(4):562–69. doi:10.1038/s41564-020-0688-y.
   PubMed Web of Science ®Google Scholar
• Sungnak W, Huang N, Becavin C, Berg M, Queen R, Litvinukova M, Talavera-López C, Maatz H, Reichart D, Sampaziotis F, et al. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med. 2020;26:681–87.
   PubMed Web of Science ®Google Scholar
• Hou YJ, Okuda K, Edwards CE, Martinez DR, Asakura T, Dinnon KH, 3rd, Kato T, Lee RE, Yount BL, Mascenik TM, et al. SARS-CoV-2 reverse genetics reveals a variable infection gradient in the respiratory tract. Cell. 2020;182(2):429–46 e14. doi:10.1016/j.cell.2020.05.042.
   PubMed Web of Science ®Google Scholar
• Kawasuji H, Takegoshi Y, Kaneda M, Ueno A, Miyajima Y, Kawago K, Fukui Y, Yoshida Y, Kimura M, Yamada H, et al. Transmissibility of COVID-19 depends on the viral load around onset in adult and symptomatic patients. PloS One. 2020;15:e0243597.
   PubMed Web of Science ®Google Scholar
• Pujadas E, Chaudhry F, McBride R, Richter F, Zhao S, Wajnberg A, Nadkarni G, Glicksberg BS, Houldsworth J, Cordon-Cardo C. SARS-CoV-2 viral load predicts COVID-19 mortality. Lancet Respir Med. 2020;8(9):e70. doi:10.1016/S2213-2600(20)30354-4.
   PubMed Web of Science ®Google Scholar
• Fajnzylber J, Regan J, Coxen K, Corry H, Wong C, Rosenthal A, Worrall D, Giguel F, Piechocka-Trocha A, Atyeo C, et al. SARS-CoV-2 viral load is associated with increased disease severity and mortality. Nat Commun. 2020;11(1):5493. doi:10.1038/s41467-020-19057-5.
   PubMed Web of Science ®Google Scholar
• Kim JY, Ko JH, Kim Y, Kim YJ, Kim JM, Chung YS, Kim HM, Han MG, Kim SY, Chin BS. Viral load kinetics of SARS-CoV-2 infection in first two patients in Korea. J Korean Med Sci. 2020;35:e86.
   PubMed Web of Science ®Google Scholar
• Zou L, Ruan F, Huang M, Liang L, Huang H, Hong Z, Yu J, Kang M, Song Y, Xia J, et al. SARS-CoV-2 viral load in upper respiratory specimens of infected patients. N Engl J Med. 2020;382(12):1177–79. doi:10.1056/NEJMc2001737.
   PubMed Web of Science ®Google Scholar
• Siddiqi HK, Mehra MR. COVID-19 illness in native and immunosuppressed states: a clinical–therapeutic staging proposal. J Heart Lung Transplant. 2020;39(5):405–07. doi:10.1016/j.healun.2020.03.012.
   PubMed Web of Science ®Google Scholar
• Yap JKY, Moriyama M, Iwasaki A. Inflammasomes and pyroptosis as therapeutic targets for COVID-19. J Immunol. 2020;205(2):307–12. doi:10.4049/jimmunol.2000513.
   PubMed Web of Science ®Google Scholar
• Pons S, Fodil S, Azoulay E, Zafrani L. The vascular endothelium: the cornerstone of organ dysfunction in severe SARS-CoV-2 infection. Crit Care. 2020;24(1):353. doi:10.1186/s13054-020-03062-7.
   PubMed Web of Science ®Google Scholar
• Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Marc GP, Moreira ED, Zerbini C, et al. Safety and Efficacy of the BNT162b2 mRNA Covid-19 Vaccine. N Engl J Med. 2020;383:2603–15.
   PubMed Web of Science ®Google Scholar
• Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB, et al. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N Engl J Med. 2021;384(5):403–16. doi:10.1056/NEJMoa2035389.
   PubMed Web of Science ®Google Scholar
• Sadoff J, Gray G, Vandebosch A, Cardenas V, Shukarev G, Grinsztejn B, Goepfert PA, Truyers C, Fennema H, Spiessens B, et al. Safety and efficacy of single-dose Ad26.COV2.S vaccine against Covid-19. N Engl J Med. 2021;384:2187–201.
   PubMed Web of Science ®Google Scholar
• Administration USFaD. COVID-19 vaccines. U.S. Food and Drug Administration; 2021.
   Google Scholar
• Khan WH, Hashmi Z, Goel A, Ahmad R, Gupta K, Khan N, Alam I, Ahmed F, Ansari MA. COVID-19 pandemic and vaccines update on challenges and resolutions. Front Cell Infect Microbiol. 2021;11:690621. doi:10.3389/fcimb.2021.690621.
   PubMed Web of Science ®Google Scholar
• Chan RWY, Liu S, Cheung JY, Tsun JGS, Chan KC, Chan KYY, Fung GPG, Li AM, Lam HS. The mucosal and serological immune responses to the novel coronavirus (SARS-CoV-2) Vaccines. Front Immunol. 2021;12:744887. doi:10.3389/fimmu.2021.744887.
   PubMed Web of Science ®Google Scholar
• Corbett KS, Flynn B, Foulds KE, Francica JR, Boyoglu-Barnum S, Werner AP, Flach B, O’Connell S, Bock KW, Minai M, et al. Evaluation of the mRNA-1273 Vaccine against SARS-CoV-2 in nonhuman primates. N Engl J Med. 2020;383:1544–55.
   PubMed Web of Science ®Google Scholar
• Taddio A, Ipp M, Thivakaran S, Jamal A, Parikh C, Smart S, Sovran J, Stephens D, Katz J. Survey of the prevalence of immunization non-compliance due to needle fears in children and adults. Vaccine. 2012;30:4807–12. doi:10.1016/j.vaccine.2012.05.011.
   PubMed Web of Science ®Google Scholar
• Croyle MA, Patel A, Tran KN, Gray M, Zhang Y, Strong JE, Feldmann H, Kobinger GP. Nasal delivery of an adenovirus-based vaccine bypasses pre-existing immunity to the vaccine carrier and improves the immune response in mice. PloS One. 2008;3:e3548. doi:10.1371/journal.pone.0003548.
   PubMed Web of Science ®Google Scholar
• Zhang JTE, Feng T, Shi Z, Van Kampen KR, Tang DC. Adenovirus-vectored drug-vaccine duo as a rapid-response tool for conferring seamless protection against influenza. PloS One. 2011;6:e22605.
   PubMed Web of Science ®Google Scholar
• Krishnan V, Andersen BH, Shoemaker C, Sivko GS, Tordoff KP, Stark GV, Zhang J, Feng T, Duchars M, Roberts MS, et al. Efficacy and immunogenicity of single-dose AdVAV intranasal anthrax vaccine compared to anthrax vaccine absorbed in an aerosolized spore rabbit challenge model. Clin Vaccine Immunol. 2015;22:430–39. doi:10.1128/CVI.00690-14.
   PubMed Web of Science ®Google Scholar
• Wold WS, Toth K. Adenovirus vectors for gene therapy, vaccination and cancer gene therapy. Curr Gene Ther. 2013;13:421–33.
   PubMed Web of Science ®Google Scholar
• Zhang C, Zhou D. Adenoviral vector-based strategies against infectious disease and cancer. Hum Vaccin Immunother. 2016;12:2064–74.
   PubMed Web of Science ®Google Scholar
• Hassan AO, Kafai NM, Dmitriev IP, Fox JM, Smith BK, Harvey IB, Chen RE, Winkler ES, Wessel AW, Case JB, et al. A single-dose intranasal ChAd vaccine protects upper and lower respiratory tracts against SARS-CoV-2. Cell. 2020;183:169–84 e13. doi:10.1016/j.cell.2020.08.026.
   PubMed Web of Science ®Google Scholar
• Yusuf H, Kett V. Current prospects and future challenges for nasal vaccine delivery. Hum Vaccin Immunother. 2017;13:34–45.
   PubMed Web of Science ®Google Scholar
• King RG, Silva-Sanchez A, Peel JN, Botta D, Dickson AM, Pinto AK, Meza-Perez S, Allie SR, Schultz MD, Liu M, et al. Single-dose intranasal administration of AdCOVID elicits systemic and mucosal immunity against SARS-CoV-2 and fully protects mice from lethal challenge. Vaccines (Basel). 2021;9. doi:10.3390/vaccines9080881.
   Web of Science ®Google Scholar
• Ma C, Wang L, Tao X, Zhang N, Yang Y, Tseng CK, Li F, Zhou Y, Jiang S, Du L. Searching for an ideal vaccine candidate among different MERS coronavirus receptor-binding fragments—the importance of immunofocusing in subunit vaccine design. Vaccine. 2014;32(46):6170–76. doi:10.1016/j.vaccine.2014.08.086.
   PubMed Web of Science ®Google Scholar
• Piccoli L, Park YJ, Tortorici MA, Czudnochowski N, Walls AC, Beltramello M, Silacci-Fregni C, Pinto D, Rosen LE, Bowen JE, et al. Mapping neutralizing and immunodominant sites on the SARS-CoV-2 spike receptor-binding domain by structure-guided high-resolution serology. Cell. 2020;183:1024–42.
   PubMed Web of Science ®Google Scholar
• Starr TN, Czudnochowski N, Liu Z, Zatta F, Park YJ, Addetia A, Pinto D, Beltramello M, Hernandez P, Greaney AJ, et al. SARS-CoV-2 RBD antibodies that maximize breadth and resistance to escape. Nature. 2021;597:97–102.
   PubMed Web of Science ®Google Scholar
• Greaney AJ, Loes AN, Gentles LE, Crawford KHD, Starr TN, Malone KD, Chu HY, Bloom JD. Antibodies elicited by mRNA-1273 vaccination bind more broadly to the receptor binding domain than do those from SARS-CoV-2 infection. Sci Transl Med. 2021;13:eabi9915.
   PubMed Web of Science ®Google Scholar
• Zost SJ, Gilchuk P, Case JB, Binshtein E, Chen RE, Nkolola JP, Schäfer A, Reidy JX, Trivette A, Nargi RS, et al. Potently neutralizing and protective human antibodies against SARS-CoV-2. Nature. 2020;584:443–49. doi:10.1038/s41586-020-2548-6.
   PubMed Web of Science ®Google Scholar
• Dan JM, Mateus J, Kato Y, Hastie KM, Yu ED, Faliti CE, Grifoni A, Ramirez SI, Haupt S, Frazier A, et al. Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection. Science. 2021;371:eabf4063.
   PubMed Web of Science ®Google Scholar
• Seydoux E, Homad LJ, MacCamy AJ, Parks KR, Hurlburt NK, Jennewein MF, Akins NR, Stuart AB, Wan YH, Feng J, et al. Analysis of a SARS-CoV-2-infected individual reveals development of potent neutralizing antibodies with limited somatic mutation. Immunity. 2020;53:98–105.
   PubMed Web of Science ®Google Scholar
• Tang DC, Zhang J, Toro H, Shi Z, Van Kampen KR. Adenovirus as a carrier for the development of influenza virus-free avian influenza vaccines. Expert Rev Vaccines. 2009;8:469–81.
   PubMed Web of Science ®Google Scholar
• Carroll T, Fox D, van Doremalen N, Ball E, Morris MK, Sotomayor-Gonzalez A, Servellita V, Rustagi A, Yinda CK, Fritts L, et al. The B.1.427/1.429 (epsilon) SARS-CoV-2 variants are more virulent than ancestral B.1 (614G) in Syrian hamsters. PLoS Pathog. 2022;18:e1009914. doi:10.1371/journal.ppat.1009914.
   PubMed Web of Science ®Google Scholar
• Bewley KR, Coombes NS, Gagnon L, McInroy L, Baker N, Shaik I, St-Jean JR, St-Amant N, Buttigieg KR, Humphries HE, et al. Quantification of SARS-CoV-2 neutralizing antibody by wild-type plaque reduction neutralization, microneutralization and pseudotyped virus neutralization assays. Nat Protoc. 2021;16:3114–40. doi:10.1038/s41596-021-00536-y.
   PubMed Web of Science ®Google Scholar
• Gruber AD, Osterrieder N, Bertzbach LD, Vladimirova D, Greuel S, Ihlow J, Horst D, Trimpert J, Dietert K. Standardization of reporting criteria for lung pathology in SARS-CoV-2-infected Hamsters: what matters? Am J Respir Cell Mol Biol. 2020;63:856–59.
   PubMed Web of Science ®Google Scholar
• Li Q, Vijaykumar K, Philips SE, Hussain SS, Huynh VN, Fernandez-Petty CM, Lever JE, Foote JB, Ren J, Campos-Gómez J, et al. Mucociliary transport deficiency and disease progression in Syrian Hamsters with SARS-CoV-2 infection. bioRxiv. 2022.
   Google Scholar
• Kumari P, Rothan HA, Natekar JP, Stone S, Pathak H, Strate PG, Arora K, Brinton MA, Kumar M. Neuroinvasion and encephalitis following intranasal inoculation of SARS-CoV-2 in K18-hACE2 mice. Viruses. 2021;13:132. doi:10.3390/v13010132.
   PubMed Web of Science ®Google Scholar
• Song E, Zhang C, Israelow B, Lu-Culligan A, Prado AV, Skriabine S, Lu P, Weizman O-E, Liu F, Dai Y, et al. Neuroinvasion of SARS-CoV-2 in human and mouse brain. J Exp Med. 2021;218. doi:10.1084/jem.20202135.
   Web of Science ®Google Scholar
• Gould VMW, Francis JN, Anderson KJ, Georges B, Cope AV, Tregoning JS. Nasal IgA provides protection against human influenza challenge in volunteers with low serum influenza antibody titre. Front Microbiol. 2017;8:900.
   PubMed Web of Science ®Google Scholar
• Belshe RB, Gruber WC, Mendelman PM, Mehta HB, Mahmood K, Reisinger K, Treanor J, Zangwill K, Hayden F, Bernstein D, et al. Correlates of immune protection induced by live, attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine. J Infect Dis. 2000;181:1133–37. doi:10.1086/315323.
   PubMed Web of Science ®Google Scholar
• Tasker S, Wight O’Rourke A, Suyundikov A, Jackson Booth P-G, Bart S, Krishnan V, Zhang J, Anderson KJ, Georges B, Roberts MS. Safety and immunogenicity of a novel intranasal influenza vaccine (NasoVAX): a phase 2 randomized, controlled trial. Vaccines. 2021;9:224.
   Web of Science ®Google Scholar
• Kim E, Okada K, Beeler JA, Crim RL, Piedra PA, Gilbert BE, Gambotto A. Development of an adenovirus-based respiratory syncytial virus vaccine: preclinical evaluation of efficacy, immunogenicity, and enhanced disease in a cotton rat model. J Virol. 2014;88:5100–08. doi:10.1128/JVI.03194-13.
   PubMed Web of Science ®Google Scholar
• Li H, Wang Y, Ji M, Pei F, Zhao Q, Zhou Y, Hong Y, Han S, Wang J, Wang Q, et al. Transmission routes analysis of SARS-CoV-2: a systematic review and case report. Front Cell Dev Biol. 2020;8:618. doi:10.3389/fcell.2020.00618.
   PubMed Web of Science ®Google Scholar
• Ahn JH, Kim J, Hong SP, Choi SY, Yang MJ, Ju YS, Kim YT, Kim HM, Rahman MDT, Chung MK, et al. Nasal ciliated cells are primary targets for SARS-CoV-2 replication in the early stage of COVID-19. J Clin Invest. 2021;131:131. doi:10.1172/JCI148517.
   Web of Science ®Google Scholar
• Richard M, van den Brand JMA, Bestebroer TM, Lexmond P, de Meulder D, Fouchier RAM, Lowen AC, Herfst S. Influenza A viruses are transmitted via the air from the nasal respiratory epithelium of ferrets. Nat Commun. 2020;11:766.
   PubMed Web of Science ®Google Scholar
• Mulay A, Konda B, Garcia G, Jr., Yao C, Beil S, Villalba JM, Koziol C, Sen C, Purkayastha A, Kolls JK, et al. SARS-CoV-2 infection of primary human lung epithelium for COVID-19 modeling and drug discovery. Cell Rep. 2021;35:109055. doi:10.1016/j.celrep.2021.109055.
   PubMed Web of Science ®Google Scholar
• Tian S, Xiong Y, Liu H, Niu L, Guo J, Liao M, Xiao S-Y. Pathological study of the 2019 novel coronavirus disease (COVID-19) through postmortem core biopsies. Mod Pathol. 2020;33:1007–14. doi:10.1038/s41379-020-0536-x.
   PubMed Web of Science ®Google Scholar
• Bourgonje AR, Abdulle AE, Timens W, Hillebrands JL, Navis GJ, Gordijn SJ, Bolling MC, Dijkstra G, Voors AA, Osterhaus AD, et al. Angiotensin-Converting enzyme 2 (ACE2), SARS-CoV -2 and the pathophysiology of coronavirus disease 2019 (COVID -19). J Pathol. 2020;251:228–48. doi:10.1002/path.5471.
   PubMed Web of Science ®Google Scholar
• Ku MW, Bourgine M, Authie P, Lopez J, Nemirov K, Moncoq F, Noirat A, Vesin B, Nevo F, Blanc C, et al. Intranasal vaccination with a lentiviral vector protects against SARS-CoV-2 in preclinical animal models. Cell Host Microbe. 2021;29:236–49 e6. doi:10.1016/j.chom.2020.12.010.
   PubMed Web of Science ®Google Scholar
• Lowen AC, Steel J, Mubareka S, Carnero E, Garcia-Sastre A, Palese P. Blocking interhost transmission of influenza virus by vaccination in the guinea pig model. J Virol. 2009;83:2803–18.
   PubMed Web of Science ®Google Scholar
• Price GE, Lo CY, Misplon JA, Epstein SL, García-Sastre A. Mucosal immunization with a candidate universal influenza vaccine reduces virus transmission in a mouse model. J Virol. 2014;88:6019–30. doi:10.1128/JVI.03101-13.
   PubMed Web of Science ®Google Scholar
• An D, Li K, Rowe DK, Diaz MCH, Griffin EF, Beavis AC, Johnson SK, Padykula I, Jones CA, Briggs K, et al. Protection of K18-hACE2 mice and ferrets against SARS-CoV-2 challenge by a single-dose mucosal immunization with a parainfluenza virus 5–based COVID-19 vaccine. Sci Adv. 2021;7. doi:10.1126/sciadv.abi5246.
   Web of Science ®Google Scholar
• van Doremalen N, Lambe T, Spencer A, Belij-Rammerstorfer S, Purushotham JN, Port JR, van Doremalen N, Avanzato VA, Bushmaker T, Flaxman A, et al. ChAdox1 nCov-19 vaccine prevents SARS-CoV-2 pneumonia in rhesus macaques. Nature. 2020;586:578–82. doi:10.1038/s41586-020-2608-y.
   PubMed Web of Science ®Google Scholar
• Wu S, Huang J, Zhang Z, Wu J, Zhang J, Hu H, Zhu T, Zhang J, Luo L, Fan P, et al. Safety, tolerability, and immunogenicity of an aerosolised adenovirus type-5 vector-based COVID-19 vaccine (Ad5-nCov) in adults: preliminary report of an open-label and randomised phase 1 clinical trial. Lancet Infect Dis. 2021;21:1654–64. doi:10.1016/S1473-3099(21)00396-0.
   PubMed Web of Science ®Google Scholar
• Lapuente D, Fuchs J, Willar J, Vieira Antao A, Eberlein V, Uhlig N, Issmail L, Schmidt A, Oltmanns F, Peter AS, et al. Protective mucosal immunity against SARS-CoV-2 after heterologous systemic prime-mucosal boost immunization. Nat Commun. 2021;12:6871. doi:10.1038/s41467-021-27063-4.
   PubMed Web of Science ®Google Scholar
• Bosnjak B, Odak I, Barros-Martins J, Sandrock I, Hammerschmidt SI, Permanyer M, Patzer GE, Greorgiev H, Jauregui RG, Tscherne A, et al. Intranasal delivery of MVA vector vaccine induces effective pulmonary immunity against SARS-CoV-2 in rodents. Front Immunol. 2021;12:772240.
   PubMed Web of Science ®Google Scholar