Characterization of SARS-CoV-2 Variants in Military and Civilian Personnel of an Air Force Airport during Three Pandemic Waves in Italy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethical Statement
2.2. Study Design
2.3. Diagnostic Reverse Transcription (RT) Real-Time PCR
2.4. SARS-CoV-2 NGS Sequencing
2.5. SARS-CoV-2 Sanger Sequencing
2.6. Classification and Mutational Analysis
2.7. Phylogenetic Analysis
3. Results
3.1. Demographic Characteristics of the Cohort
3.2. Classification and Timing of Detected Variants
3.3. Whole Genome Analysis
3.3.1. PLpro Protein
3.3.2. 3CLpro Protein
3.3.3. RdRp Protein
3.3.4. Spike Protein
3.3.5. Nucleocapsid Protein
3.4. Phylogenetic and Clustering Analyses
3.5. Sanger Sequencing of Partial Spike Coding Region
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fabiani, M.; Ramigni, M.; Gobbetto, V.; Mateo-Urdiales, A.; Pezzotti, P.; Piovesan, C. Effectiveness of the Comirnaty (BNT162b2, BioNTech/Pfizer) vaccine in preventing SARS-CoV-2 infection among healthcare workers, Treviso province, Veneto region, Italy, 27 December 2020 to 24 March 2021. Euro Surveill. 2021, 26, 2100420. [Google Scholar] [CrossRef]
- Oliani, F.; Savoia, A.; Gallo, G.; Tiwana, N.; Letzgus, M.; Gentiloni, F.; Piatti, A.; Chiappa, L.; Bisesti, A.; Laquintana, D.; et al. Italy’s rollout of COVID-19 vaccinations: The crucial contribution of the first experimental mass vaccination site in Lombardy. Vaccine 2022, 40, 1397–1403. [Google Scholar] [CrossRef] [PubMed]
- Dhanasooraj, D.; Viswanathan, P.; Saphia, S.; Jose, B.P.; Parambath, F.C.; Sivadas, S.; Akash, N.P.; Vimisha, T.V.; Nair, P.R.; Mohan, A.; et al. Genomic surveillance of SARS-CoV-2 by sequencing the RBD region using Sanger sequencing from North Kerala. Front. Public Health 2022, 10, 974667. [Google Scholar] [CrossRef]
- Guthrie, J.L.; Teatero, S.; Zittermann, S.; Chen, Y.; Sullivan, A.; Rilkoff, H.; Joshi, E.; Sivaraman, K.; de Borja, R.; Sundaravadanam, Y.; et al. Detection of the novel SARS-CoV-2 European lineage B.1.177 in Ontario, Canada. J. Clin. Virol. Plus 2021, 1, 100010. [Google Scholar] [CrossRef] [PubMed]
- European Centre for Disease Prevention and Control ECDC. Available online: https://www.ecdc.europa.eu/en (accessed on 11 September 2023).
- World Health Organization Tracking SARS-CoV-2 Variants. Available online: https://www.who.int/activities/tracking-SARS-CoV-2-variants (accessed on 11 September 2023).
- De Marco, C.; Veneziano, C.; Massacci, A.; Pallocca, M.; Marascio, N.; Quirino, A.; Barreca, G.S.; Giancotti, A.; Gallo, L.; Lamberti, A.G.; et al. Dynamics of Viral Infection and Evolution of SARS-CoV-2 Variants in the Calabria Area of Southern Italy. Front. Microbiol. 2022, 13, 934993. [Google Scholar] [CrossRef] [PubMed]
- Chrysostomou, A.C.; Vrancken, B.; Haralambous, C.; Alexandrou, M.; Aristokleous, A.; Christodoulou, C.; Gregoriou, I.; Ioannides, M.; Kalakouta, O.; Karagiannis, C.; et al. Genomic Epidemiology of the SARS-CoV-2 Epidemic in Cyprus from November 2020 to October 2021: The Passage of Waves of Alpha and Delta Variants of Concern. Viruses 2023, 15, 108. [Google Scholar] [CrossRef]
- Hoteit, R.; Yassine, H.M. Biological Properties of SARS-CoV-2 Variants: Epidemiological Impact and Clinical Consequences. Vaccines 2022, 10, 919. [Google Scholar] [CrossRef] [PubMed]
- Zhao, H.; Nguyen, A.; Wu, D.; Li, Y.; Hassan, S.A.; Chen, J.; Shroff, H.; Piszczek, G.; Schuck, P. Plasticity in structure and assembly of SARS-CoV-2 nucleocapsid protein. PNAS Nexus 2022, 1, pgac049. [Google Scholar] [CrossRef]
- Alkhatib, M.; Bellocchi, M.C.; Marchegiani, G.; Grelli, S.; Micheli, V.; Stella, D.; Zerillo, B.; Carioti, L.; Svicher, V.; Rogliani, P.; et al. First Case of a COVID-19 Patient Infected by Delta AY.4 with a Rare Deletion Leading to a N Gene Target Failure by a Specific Real Time PCR Assay: Novel Omicron VOC Might Be Doing Similar Scenario? Microorganisms 2022, 10, 268. [Google Scholar] [CrossRef]
- Stefanelli, P.; Trentini, F.; Guzzetta, G.; Marziano, V.; Mammone, A.; Sane Schepisi, M.; Poletti, P.; Molina Grané, C.; Manica, M.; Del Manso, M.; et al. Co-circulation of SARS-CoV-2 Alpha and Gamma variants in Italy, February and March 2021. Euro Surveill. 2022, 27, 2100429. [Google Scholar] [CrossRef]
- Monitoraggio delle Varianti del Virus SARS-CoV-2 di Interesse in Sanità Pubblica in Italia. Available online: https://www.epicentro.iss.it/coronavirus/sars-cov-2-monitoraggio-varianti-rapporti-periodici (accessed on 11 September 2023).
- Luo, C.H.; Morris, C.P.; Sachithanandham, J.; Amadi, A.; Gaston, D.C.; Li, M.; Swanson, N.J.; Schwartz, M.; Klein, E.Y.; Pekosz, A.; et al. Infection with the Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Delta Variant Is Associated with Higher Recovery of Infectious Virus Compared to the Alpha Variant in Both Unvaccinated and Vaccinated Individuals. Clin. Infect. Dis. 2022, 75, e715–e725. [Google Scholar] [CrossRef] [PubMed]
- La Rosa, G.; Iaconelli, M.; Veneri, C.; Mancini, P.; Bonanno Ferraro, G.; Brandtner, D.; Lucentini, L.; Bonadonna, L.; Rossi, M.; Grigioni, M.; et al. The rapid spread of SARS-COV-2 Omicron variant in Italy reflected early through wastewater surveillance. Sci. Total Environ. 2022, 837, 155767. [Google Scholar] [CrossRef] [PubMed]
- Harris, E. CDC Assesses Risk From BA.2.86, Highly Mutated COVID-19 Variant. JAMA, 2023; epub ahead of print. [Google Scholar] [CrossRef]
- Mohapatra, R.K.; Mishra, S.; Kandi, V.; Branda, F.; Ansari, A.; Rabaan, A.A.; Kudrat-E-Zahan, M. Analyzing the emerging patterns of SARS-CoV-2 Omicron subvariants for the development of next-gen vaccine: An observational study. Health Sci. Rep. 2023, 6, e1596. [Google Scholar] [CrossRef] [PubMed]
- Stanford Coronavirus Resistance Database CoV-RDB. Available online: https://covdb.stanford.edu (accessed on 20 June 2023).
- Bloom, J.D.; Neher, R.A. Fitness effects of mutations to SARS-CoV-2 proteins. Virus Evol. 2023, 9, vead055. [Google Scholar] [CrossRef]
- Sun, C.; Xie, C.; Bu, G.L.; Zhong, L.Y.; Zeng, M.S. Molecular characteristics, immune evasion, and impact of SARS-CoV-2 variants. Signal Transduct. Target. Ther. 2022, 7, 202. [Google Scholar] [CrossRef]
- Ip, J.D.; Wing-Ho Chu, A.; Chan, W.M.; Cheuk-Ying Leung, R.; Umer Abdullah, S.M.; Sun, Y.; Kai-Wang To, K. Global prevalence of SARS-CoV-2 3CL protease mutations associated with nirmatrelvir or ensitrelvir resistance. EBioMedicine 2023, 91, 104559. [Google Scholar] [CrossRef]
- Andrews, H.S.; Herman, J.D.; Gandhi, R.T. Treatments for COVID-19. Annu. Rev. Med. 2023, 75, 25. [Google Scholar] [CrossRef]
- de Oliveira, V.M.; Ibrahim, M.F.; Sun, X.; Hilgenfeld, R.; Shen, J. H172Y mutation perturbs the S1 pocket and nirmatrelvir binding of SARS- CoV-2 main protease through a non native hydrogen bond. bioRxiv 2022. [Google Scholar] [CrossRef]
- Scaglione, V.; Rotundo, S.; Marascio, N.; De Marco, C.; Lionello, R.; Veneziano, C.; Berardelli, L.; Quirino, A.; Olivadese, V.; Serapide, F.; et al. Lessons learned and implications of early therapies for coronavirus disease in a territorial service centre in the Calabria region: A retrospective study. BMC Infect. Dis. 2022, 22, 793. [Google Scholar] [CrossRef]
- Malagón Rojas, J.N.; Mercado, M.; Gómez Rendón, C.P. SARS-CoV-2 and work-related transmission: Results of a prospective cohort of airport workers, 2020. Rev. Bras. Med. Trab. 2020, 18, 371–380. [Google Scholar] [CrossRef] [PubMed]
- De Marco, C.; Marascio, N.; Veneziano, C.; Biamonte, F.; Trecarichi, E.M.; Santamaria, G.; Leviyang, S.; Liberto, M.C.; Mazzitelli, M.; Quirino, A.; et al. Whole-genome analysis of SARS-CoV-2 in a 2020 infection cluster in a nursing home of Southern Italy. Infect. Genet. Evol. 2022, 99, 105253. [Google Scholar] [CrossRef] [PubMed]
- Verde, P.; Marcantonio, C.; Costantino, A.; Martina, A.; Simeoni, M.; Taffon, S.; Tritarelli, E.; Campanella, C.; Cresta, R.; Bruni, R.; et al. Diagnostic accuracy of a SARS-CoV-2 rapid antigen test among military and civilian personnel of an Air Force airport in central Italy. PLoS ONE 2022, 17, e0277904. [Google Scholar] [CrossRef]
- European Regulation (UE) 2016/679. Available online: https://eur-lex.europa.eu/eli/reg/2016/679/oj (accessed on 2 May 2022).
- Italian Decree n. 196 of 2003. Available online: https://web.camera.it/parlam/leggi/deleghe/Testi/03196dl.htm (accessed on 2 May 2022).
- Italian Decree n. 101 of 2018. Available online: https://www.gazzettaufficiale.it/eli/id/2018/09/04/18G00129/sg (accessed on 2 May 2022).
- Ministry of Health Note n. 31400 of 29 September 2020. Available online: https://www.trovanorme.salute.gov.it/norme/renderNormsanPdf?anno=2020&codLeg=76433&parte=1%20&serie=null (accessed on 2 May 2022).
- Ministry of Health Note n. 35324 of 30 October 2020. Available online: https://www.trovanorme.salute.gov.it/norme/renderNormsanPdf?anno=2020&codLeg=76939&parte=1%20&serie=null (accessed on 2 May 2022).
- Ministry of Health Note n. 705 of 8 January 2021. Available online: https://www.trovanorme.salute.gov.it/norme/renderNormsanPdf?anno=2021&codLeg=78155&parte=1%20&serie=null (accessed on 2 May 2022).
- ARTIC Network. Real-Time Molecular Epidemiology for Outbreak Response. Available online: https://artic.network/ncov-2019 (accessed on 2 April 2022).
- Carpenter, R.E.; Tamrakar, V.K.; Almas, S.; Sharma, A.; Sharma, R. SARS-CoV-2 Next Generation Sequencing (NGS) data from clinical isolates from the East Texas Region of the United States. Data Brief 2023, 49, 109312. [Google Scholar] [CrossRef]
- Pangolin COVID-19 Lineage Assigner. Available online: https://pangolin.cog-uk.io (accessed on 5 June 2023).
- Nextclade v2.12.0. Available online: https://clades.nextstrain.org/ (accessed on 6 June 2023).
- La Rosa, G.; Mancini, P.; Bonanno Ferraro, G.; Veneri, C.; Iaconelli, M.; Lucentini, L.; Bonadonna, L.; Brusaferro, S.; Brandtner, D.; Fasanella, A.; et al. Rapid screening for SARS-CoV-2 variants of concern in clinical and environmental samples using nested RT-PCR assays targeting key mutations of the spike protein. Water Res. 2021, 197, 11714. [Google Scholar] [CrossRef]
- La Rosa, G.; Brandtner, D.; Mancini, P.; Veneri, C.; Bonanno Ferraro, G.; Bonadonna, L.; Lucentini, L.; Suffredini, E. Key SARS-CoV-2 Mutations of Alpha, Gamma, and Eta Variants Detected in Urban Wastewaters in Italy by Long-Read Amplicon Sequencing Based on Nanopore Technology. Water 2021, 13, 2503. [Google Scholar] [CrossRef]
- La Rosa, G.; Brandtner, D.; Bonanno Ferraro, G.; Veneri, C.; Mancini, P.; Iaconelli, M.; Lucentini, L.; Del Giudice, C.; Orlandi, L.; SARI Network; et al. Wastewater surveillance of SARS-CoV-2 variants in October-November 2022 in Italy: Detection of XBB.1, BA.2.75 and rapid spread of the BQ.1 lineage. Sci. Total Environ. 2023, 873, 162339. [Google Scholar] [CrossRef] [PubMed]
- MEGA Software. Available online: https://www.megasoftware.net/ (accessed on 14 June 2023).
- Tamura, K.; Stecher, G.; Kumar, S. MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef]
- GISAID-CoVsurver Mutations App. Available online: https://www.gisaid.org/epiflu-applications/covsurver-mutations-app/ (accessed on 15 June 2023).
- Benson, D.A.; Clark, K.; Karsch-Mizrachi, I.; Lipman, D.J.; Ostell, J.; Sayers, E.W. GenBank. Nucleic Acids Res. 2014, 42, 32–37. [Google Scholar] [CrossRef] [PubMed]
- Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673–4680. [Google Scholar] [CrossRef] [PubMed]
- Hall, T.A. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41, 95–98. [Google Scholar]
- Marascio, N.; Cilburunoglu, M.; Torun, E.G.; Centofanti, F.; Mataj, E.; Equestre, M.; Bruni, R.; Quirino, A.; Matera, G.; Ciccaglione, A.R.; et al. Molecular Characterization and Cluster Analysis of SARS-CoV-2 Viral Isolates in Kahramanmaraş City, Turkey: The Delta VOC Wave within One Month. Viruses 2023, 15, 802. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization (WHO). Available online: https://www.who.int/ (accessed on 6 September 2023).
- Bellocchi, M.C.; Scutari, R.; Carioti, L.; Iannetta, M.; Marchegiani, G.; Piermatteo, L.; Coppola, L.; Tedde, S.; Duca, L.; Malagnino, V.; et al. Frequency of Atypical Mutations in the Spike Glycoprotein in SARS-CoV-2 Circulating from July 2020 to July 2022 in Central Italy: A Refined Analysis by Next Generation Sequencing. Viruses 2023, 15, 1711. [Google Scholar] [CrossRef]
- Dolci, M.; Signorini, L.; Cason, C.; Campisciano, G.; Kunderfranco, P.; Pariani, E.; Galli, C.; Petix, V.; Ferrante, P.; Delbue, S.; et al. Circulation of SARS-CoV-2 Variants among Children from November 2020 to January 2022 in Trieste (Italy). Microorganisms 2022, 10, 612. [Google Scholar] [CrossRef] [PubMed]
- Martínez González, B.; Soria, M.E.; Vázquez Sirvent, L.; Ferrer Orta, C.; Lobo Vega, R.; Mínguez, P.; de la Fuente, L.; Llorens, C.; Soriano, B.; Ramos, R.; et al. SARS-CoV-2 Point Mutation and Deletion Spectra and Their Association with Different Disease Outcomes. Microbiol. Spectr. 2022, 10, e0022122. [Google Scholar] [CrossRef] [PubMed]
- Mazhari, S.; Alavifard, H.; Rahimian, K.; Karimi, Z.; Mahmanzar, M.; Sisakht, M.M.; Bitaraf, M.; Arefian, E. SARS-CoV-2 NSP-12 mutations survey during the pandemic in the world. Res. Sq. 2021; preprint. [Google Scholar] [CrossRef]
- Pitts, J.; Li, J.; Perry, J.K.; Du Pont, V.; Riola, N.; Rodriguez, L.; Lu, X.; Kurhade, C.; Xie, X.; Camus, G.; et al. Remdesivir and GS-441524 Retain Antiviral Activity against Delta, Omicron, and Other Emergent SARS-CoV-2 Variants. Antimicrob. Agents Chemother. 2022, 66, e0022222. [Google Scholar] [CrossRef]
- Harvey, W.T.; Carabelli, A.M.; Jackson, B.; Gupta, R.K.; Thomson, E.C.; Harrison, E.M.; Ludden, C.; Reeve, R.; Rambaut, A.; COVID-19 Genomics UK (COG-UK) Consortium; et al. SARS-CoV-2 variants, spike mutations and immune escape. Nat. Rev. Microbiol. 2021, 19, 409–424. [Google Scholar] [CrossRef] [PubMed]
- Kemp, S.A.; Harvey, W.T.; Datir, R.P.; Collier, D.A.; Ferreira, I.A.; Carabelli, A.M.; Gupta, R.K.; Meng, B. Recurrent emergence and transmission of a SARS-CoV-2 spike deletion ΔH69/V70. bioRxiv 2020, preprint. [Google Scholar] [CrossRef]
- Mlcochova, P.; Kemp, S.A.; Dhar, M.S.; Papa, G.; Meng, B.; Ferreira, I.A.T.M.; Datir, R.; Collier, D.A.; Albecka, A.; Singh, S.; et al. SARS-CoV-2 B.1.617.2 Delta variant replication and immune evasion. Nature 2021, 599, 114–119. [Google Scholar] [CrossRef]
- Molina Mora, J.A.; Cordero Laurent, E.; Godinez, A.; Calderon Osorno, M.; Brenes, H.; Soto Garita, C.; Perez Corrales, C.; COINGESA-CR Consorcio Interinstitucional de Estudios Genomicos del SARS-CoV-2 Costa Rica; Drexler, J.F.; Moreira Soto, A.; et al. SARS-CoV-2 Genomic Surveillance in Costa Rica: Evidence of a Divergent Population and an Increased Detection of a Spike T1117I Mutation. Infect. Genet. Evol. 2021; 92, 104872. [Google Scholar] [CrossRef]
- Molina Mora, J.A. Insights into the mutation T1117I in the spike and the lineage B.1.1.389 of SARS-CoV-2 circulating in Costa Rica. Gene Rep. 2022, 27, 101554. [Google Scholar] [CrossRef]
- Zhang, L.; Li, Q.; Nie, J.; Ding, R.; Wang, H.; Wu, J.; Li, X.; Yang, X.; Huang, W.; Wang, Y. Cellular tropism and antigenicity of mink-derived SARS-CoV-2 variants. Signal Transduct. Target. Ther. 2021, 6, 196. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wang, B.; Zhao, Z.; Xu, J.; Zhang, Z.; Zhang, J.; Chen, Y.; Song, X.; Zheng, W.; Hou, L.; et al. Effects of SARS-CoV-2 Omicron BA.1 Spike Mutations on T-Cell Epitopes in Mice. Viruses 2023, 15, 763. [Google Scholar] [CrossRef]
- Dolton, G.; Rius, C.; Hasan, M.S.; Wall, A.; Szomolay, B.; Behiry, E.; Whalley, T.; Southgate, J.; Fuller, A.; COVID-19 Genomics UK (COG-UK) consortium; et al. Emergence of immune escape at dominant SARS-CoV-2 killer T cell epitope. Cell 2022, 185, 2936–2951.e19. [Google Scholar] [CrossRef]
- Guo, E.; Guo, H. CD8 T cell epitope generation toward the continually mutating SARS-CoV-2 spike protein in genetically diverse human population: Implications for disease control and prevention. PLoS ONE 2020, 15, e0239566. [Google Scholar] [CrossRef] [PubMed]
- Martins, Y.; Silva, R. The impact of non-lineage defining mutations in the structural stability for variants of concern of SARS-CoV-2. bioRxiv, 2023; preprint. [Google Scholar] [CrossRef]
- Veneziano, C.; Marascio, N.; De Marco, C.; Quaresima, B.; Biamonte, F.; Trecarichi, E.M.; Santamaria, G.; Quirino, A.; Torella, D.; Quattrone, A.; et al. The Spread of SARS-CoV-2 Omicron Variant in CALABRIA: A Spatio-Temporal Report of Viral Genome Evolution. Viruses 2023, 15, 408. [Google Scholar] [CrossRef]
- Grabowski, F.; Preibisch, G.; Giziński, S.; Kochańczyk, M.; Lipniacki, T. SARS-CoV-2 Variant of Concern 202012/01 Has about Twofold Replicative Advantage and Acquires Concerning Mutations. Viruses 2021, 13, 392. [Google Scholar] [CrossRef]
- Yamamoto, M.; Tomita, K.; Hirayama, Y.; Inoue, J.; Kawaguchi, Y.; Gohda, J. SARS-CoV-2 Omicron spike H655Y mutation is responsible for enhancement of the endosomal entry pathway and reduction of cell surface entry pathways. biorxiv, 2022; preprint. [Google Scholar] [CrossRef]
- Yang, X.J. δ1 variant of SARS-COV-2 acquires spike V1176F and yields a highly mutated subvariant in Europe. biorxiv, 2021; preprint. [Google Scholar] [CrossRef]
- Chakraborty, C.; Bhattacharya, M.; Sharma, A.R. Present variants of concern and variants of interest of severe acute respiratory syndrome coronavirus 2: Their significant mutations in S-glycoprotein, infectivity, re-infectivity, immune escape and vaccines activity. Rev. Med. Virol. 2022, 32, e2270. [Google Scholar] [CrossRef]
- Jangra, S.; Ye, C.; Rathnasinghe, R.; Stadlbauer, D.; Krammer, F.; Simon, V.; Martinez-Sobrido, L.; Garcia-Sastre, A.; Schotsaert, M. The E484K mutation in the SARS-CoV-2 spike protein reduces but does not abolish neutralizing activity of human convalescent and post-vaccination sera. medRxiv, 2021; preprint. [Google Scholar] [CrossRef]
- Liu, Y.; Liu, J.; Plante, K.S.; Plante, J.A.; Xie, X.; Zhang, X.; Ku, Z.; An, Z.; Scharton, D.; Schindewolf, C.; et al. The N501Y spike substitution enhances SARS-CoV-2 transmission. bioRxiv, 2021; preprint. [Google Scholar] [CrossRef]
- Alkhatib, M.; Svicher, V.; Salpini, R.; Ambrosio, F.A.; Bellocchi, M.C.; Carioti, L.; Piermatteo, L.; Scutari, R.; Costa, G.; Artese, A.; et al. SARS-CoV-2 Variants and Their Relevant Mutational Profiles: Update Summer 2021. Microbiol. Spectr. 2021, 9, e0109621. [Google Scholar] [CrossRef] [PubMed]
- Eslami, S.; Glassy, M.C.; Ghafouri Fard, S. A comprehensive overview of identified mutations in SARS CoV-2 spike glycoprotein among Iranian patients. Gene 2022, 813, 146113. [Google Scholar] [CrossRef] [PubMed]
- Shen, L.; Triche, T.J.; Bard, J.D.; Biegel, J.A.; Judkins, A.R.; Gai, X. Spike protein NTD mutation G142D in SARS-CoV-2 Delta VOC lineages is associated with frequent back mutations, increased viral loads, and immune evasion. medRxiv, 2021; preprint. [Google Scholar] [CrossRef]
- Asif, A.; Ilyas, I.; Abdullah, M.; Sarfraz, S.; Mustafa, M.; Mahmood, A. The Comparison of Mutational Progression in SARS-CoV-2: A Short Updated Overview. J. Mol. Pathol. 2022, 3, 201–218. [Google Scholar] [CrossRef]
- Mahmood, T.B.; Hossan, M.I.; Mahmud, S.; Shimu, M.S.S.; Alam, M.J.; Bhuyan, M.M.R.; Emran, T.B. Missense mutations in spike protein of SARS-CoV-2 delta variant contribute to the alteration in viral structure and interaction with hACE2 receptor. Immunity Inflamm. Dis. 2022, 10, e683. [Google Scholar] [CrossRef]
- Mishra, T.; Dalavi, R.; Joshi, G.; Kumar, A.; Pandey, P.; Shukla, S.; Mishra, R.K.; Chande, A. SARS-CoV-2 spike E156G/Δ157-158 mutations contribute to increased infectivity and immune escape. Life Sci. Alliance 2022, 5, e202201415. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Liu, J.; Johnson, B.A.; Xia, H.; Ku, Z.; Schindewolf, C.; Widen, S.G.; An, Z.; Weaver, S.C.; Menachery, V.D.; et al. Delta spike P681R mutation enhances SARS-CoV-2 fitness over Alpha variant. Cell Rep. 2022, 39, 110829. [Google Scholar] [CrossRef] [PubMed]
- Furusawa, Y.; Kiso, M.; Iida, S.; Uraki, R.; Hirata, Y.; Imai, M.; Suzuki, T.; Yamayoshi, S.; Kawaoka, Y. In SARS-CoV-2 delta variants, Spike-P681R and D950N promote membrane fusion, Spike-P681R enhances spike cleavage, but neither substitution affects pathogenicity in hamsters. EBioMedicine 2023, 91, 104561. [Google Scholar] [CrossRef] [PubMed]
- Saunders, N.; Planas, D.; Bolland, W.H.; Rodriguez, C.; Fourati, S.; Buchrieser, J.; Planchais, C.; Prot, M.; Staropoli, I.; Guivel-Benhassine, F.; et al. Fusogenicity and neutralization sensitivity of the SARS-CoV-2 Delta sublineage AY.4.2. EBioMedicine 2022, 77, 103934. [Google Scholar] [CrossRef] [PubMed]
- Pater, A.A.; Bosmeny, M.S.; Barkau, C.L.; Ovington, K.N.; Chilamkurthy, R.; Parasrampuria, M.; Eddington, S.B.; Yinusa, A.O.; White, A.A.; Metz, P.E.; et al. Emergence and Evolution of a Prevalent New SARS-CoV-2 Variant in the United States. bioRxiv, 2021; preprint. [Google Scholar] [CrossRef]
- Saifi, S.; Ravi, V.; Sharma, S.; Swaminathan, A.; Chauhan, N.S.; Pandey, R. SARS-CoV-2 VOCs, Mutational diversity and clinical outcome: Are they modulating drug efficacy by altered binding strength? Genomics 2022, 114, 110466. [Google Scholar] [CrossRef]
- Xia, S.; Wang, L.; Zhu, Y.; Lu, L.; Jiang, S. Origin, virological features, immune evasion and intervention of SARS-CoV-2 Omicron sublineages. Signal Transduct. Target. Ther. 2022, 7, 241. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Wei, G.W. Omicron BA.2 (B.1.1.529.2): High potential to becoming the next dominating variant. arXiv, 2022; preprint. [Google Scholar]
- Muttineni, R.; Binitha, R.N.; Putty, K.; Marapakala, K.; Sandra, K.P.; Panyam, J.; Vemula, A.; Singh, S.M.; Balachandran, S.; Viroji Rao, S.T.; et al. SARS-CoV-2 variants and spike mutations involved in second wave of COVID-19 pandemic in India. Transbound. Emerg. Dis. 2022, 69, e1721–e1733. [Google Scholar] [CrossRef]
- Pastorio, C.; Zech, F.; Noettger, S.; Jung, C.; Jacob, T.; Sanderson, T.; Sparrer, K.M.J.; Kirchhoff, F. Determinants of Spike infectivity, processing, and neutralization in SARS-CoV-2 Omicron subvariants BA.1 and BA.2. Cell Host Microbe 2022, 30, 1255–1268.e5. [Google Scholar] [CrossRef]
- Bugatti, A.; Filippini, F.; Messali, S.; Giovanetti, M.; Ravelli, C.; Zani, A.; Ciccozzi, M.; Caruso, A.; Caccuri, F. The D405N Mutation in the Spike Protein of SARS-CoV-2 Omicron BA.5 Inhibits Spike/Integrins Interaction and Viral Infection of Human Lung Microvascular Endothelial Cells. Viruses 2023, 15, 332. [Google Scholar] [CrossRef]
- Alam, A.S.M.R.U.; Islam, O.K.; Hasan, M.S.; Islam, M.R.; Mahmud, S.; Al-Emran, H.M.; Jahid, I.K.; Crandall, K.A.; Hossain, M.A. Dominant clade-featured SARS-CoV-2 co-occurring mutations reveal plausible epistasis: An in silico based hypothetical model. J. Med. Virol. 2022, 94, 1035–1049. [Google Scholar] [CrossRef] [PubMed]
- Azad, G.K. The molecular assessment of SARS-CoV-2 Nucleocapsid Phosphoprotein variants among Indian isolates. Heliyon 2021, 7, e06167. [Google Scholar] [CrossRef] [PubMed]
- Wu, H.; Xing, N.; Meng, K.; Fu, B.; Xue, W.; Dong, P.; Tang, W.; Xiao, Y.; Liu, G.; Luo, H.; et al. Nucleocapsid mutations R203K/G204R increase the infectivity, fitness, and virulence of SARS-CoV-2. Cell Host Microbe 2021, 29, 1788–1801.e6. [Google Scholar] [CrossRef]
- Mohammad, T.; Choudhury, A.; Habib, I.; Asrani, P.; Mathur, Y.; Umair, M.; Anjum, F.; Shafie, A.; Yadav, D.K.; Hassan, M.I. Genomic Variations in the Structural Proteins of SARS-CoV-2 and Their Deleterious Impact on Pathogenesis: A Comparative Genomics Approach. Front. Cell. Infect. Microbiol. 2021, 11, 765039. [Google Scholar] [CrossRef] [PubMed]
- Díaz, Y.; Ortiz, A.; Weeden, A.; Castillo, D.; González, C.; Moreno, B.; Martínez-Montero, M.; Castillo, M.; Vasquez, G.; Sáenz, L.; et al. SARS-CoV-2 reinfection with a virus harboring mutation in the Spike and the Nucleocapsid proteins in Panama. Int. J. Infect. Dis. 2021, 108, 588–591. [Google Scholar] [CrossRef] [PubMed]
- Hossain, A.; Akter, S.; Rashid, A.A.; Khair, S.; Alam, A.S.M.R.U. Unique mutations in SARS-CoV-2 Omicron subvariants’ non-spike proteins: Potential impacts on viral pathogenesis and host immune evasion. Microb. Pathog. 2022, 170, 105699. [Google Scholar] [CrossRef] [PubMed]
- Lo Presti, A.; Di Martino, A.; Ambrosio, L.; De Sabato, L.; Knijn, A.; Vaccari, G.; Di Bartolo, I.; Morabito, S.; Terregino, C.; Fusaro, A.; et al. Tracking the Selective Pressure Profile and Gene Flow of SARS-CoV-2 Delta Variant in Italy from April to October 2021 and Frequencies of Key Mutations from Three Representative Italian Regions. Microorganisms 2023, 11, 2644. [Google Scholar] [CrossRef]
- Forchette, L.; Sebastian, W.; Liu, T. A comprehensive review of COVID-19 virology, vaccines, variants, and therapeutics. Curr. Med. Sci. 2021, 41, 1037–1051. [Google Scholar] [CrossRef] [PubMed]
- Asgari, S.; Pousaz, L.A. Human genetic variants identified that affect COVID susceptibility and severity. Nature 2021, 600, 390–391. [Google Scholar] [CrossRef]
SARS-CoV-2 Variant | Non-Omicron | Omicron and Sub-Lineages | ||||
---|---|---|---|---|---|---|
Total Cases (n) | 30 | 37 | ||||
Gender | Male | Female | Male (%) | Male | Female | Male (%) |
22 | 7 | 75.9 | 23 | 14 | 62.2 | |
Age (years old) | ||||||
10–19 | 2 | 2 | 50.0 | 0 | 3 | 0.0 |
20–29 | 3 | 0 | 100.0 | 4 | 2 | 66.7 |
30–39 | 2 | 2 | 50.0 | 2 | 1 | 66.7 |
40–49 | 8 | 3 | 72.7 | 5 | 4 | 55.6 |
50–59 | 6 | 0 | 100.0 | 11 | 3 | 78.6 |
60–69 | 0 | 0 | - | 0 | 1 | 0.0 |
≥70 | 0 | 0 | - | 1 | 0 | 100.0 |
not available | 1 | |||||
Clinical manifestations | ||||||
Non-specific symptoms of infection | 7 | 3 | 70.0 | 17 | 12 | 58.6 |
COVID-19 symptoms | 12 | 5 | 70.6 | 18 | 13 | 58.1 |
Previous COVID-19 diagnosis | 6 | 0 | 100.0 | 4 | 7 | 36.4 |
Previous SARS-CoV-2 positive swab | 5 | 1 | 83.3 | 4 | 7 | 36.4 |
Chronic diseases | 3 | 0 | 100.0 | 7 | 8 | 46.7 |
Contact tracing | ||||||
Contact with COVID-19 sick people in the previous 14 days | 9 | 4 | 69.2 | 13 | 12 | 52.0 |
Contact with positive people to the SARS-CoV-2 swab in the previous 14 days | 11 | 4 | 73.3 | 14 | 13 | 51.9 |
not available | 1 |
Sampling Period | ID Sample | Variant/Clade | |
---|---|---|---|
2020 | 3 December | AM-70 | 20E (EU1) |
2021 | 22 January | AM-607 | 20A |
26 January | AM-660 | 20E (EU1) | |
02 February | AM-771 | 20E (EU1) | |
05 February | AM-424 | 20E (EU1) | |
09 February | AM-882 | 20E (EU1) | |
16 February | AM-1059 | 20A | |
16 February | AM-1060 | 20A | |
18 February | AM-1095 | 20E (EU1) | |
24 February | AM-1148 | 20I (Alpha, V1) | |
26 February | AM-1184 | 20E (EU1) | |
05 March | AM-1309 | 20I (Alpha, V1) | |
16 March | AM-272 | 20J (Gamma, V3) | |
19 March | AM-1397 | 20I (Alpha, V1) | |
23 March | AM-299 | 20J (Gamma, V3) | |
30 March | AM-433 | 20I (Alpha, V1) | |
30 March | AM-1281 | 20I (Alpha, V1) | |
22 April | AM-1601 | 20I (Alpha, V1) | |
22 April | AM-1602 | 20I (Alpha, V1) | |
13 December | AM-B | 21J (Delta) | |
2022 | 10 January | AM-2037 | Omicron BA.1.1 |
10 January | AM-2038 | Omicron BA.1.1 | |
10 January | AM-2039 | Omicron BA.1.1 | |
10 January | AM-2040 | Omicron BA.1.1 | |
10 January | AM-2045 | Omicron BA.1.1 | |
10 January | AM-2046 | Omicron BA.1.1 | |
10 January | AM-2050 | Omicron BA.1 | |
17 January | AM-1739 | Omicron BA.1 | |
17 January | AM-1741 | Omicron BA.1 | |
17 January | AM-2058 | Omicron BA.1 | |
17 January | AM-2059 | Omicron BA.1 | |
17 January | AM-2060 | Omicron BA.1 | |
17 January | AM-2071 | Omicron BA.1.1 | |
17 January | AM-2072 | Omicron BA.1 | |
20 January | AM-2092 | Omicron | |
20 January | AM-2094 | Omicron | |
24 January | AM-2096 | Omicron | |
24 January | AM-2097 | Omicron | |
27 January | AM-1273 | Omicron | |
27 January | AM-1281 | Omicron | |
10 February | AM-2074 | Omicron | |
10 February | AM-2109 | Omicron | |
10 February | AM-2110 | Omicron | |
10 February | AM-2111 | Omicron | |
10 February | AM-2116 | Omicron | |
10 February | AM-2117 | Omicron | |
10 February | AM-2118 | Omicron | |
10 February | AM-2119 | Omicron | |
10 February | AM-2120 | Omicron | |
24 February | AM-1438 | Omicron | |
14 March | AM-0236 | Omicron | |
14 March | AM-0299/B | Omicron | |
14 March | AM-0302 | Omicron | |
14 March | AM-0660 | Omicron | |
14 March | AM-2122 | Omicron | |
14 March | AM-2123 | Omicron | |
14 March | AM-2124 | Omicron |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Equestre, M.; Marcantonio, C.; Marascio, N.; Centofanti, F.; Martina, A.; Simeoni, M.; Suffredini, E.; La Rosa, G.; Bonanno Ferraro, G.; Mancini, P.; et al. Characterization of SARS-CoV-2 Variants in Military and Civilian Personnel of an Air Force Airport during Three Pandemic Waves in Italy. Microorganisms 2023, 11, 2711. https://doi.org/10.3390/microorganisms11112711
Equestre M, Marcantonio C, Marascio N, Centofanti F, Martina A, Simeoni M, Suffredini E, La Rosa G, Bonanno Ferraro G, Mancini P, et al. Characterization of SARS-CoV-2 Variants in Military and Civilian Personnel of an Air Force Airport during Three Pandemic Waves in Italy. Microorganisms. 2023; 11(11):2711. https://doi.org/10.3390/microorganisms11112711
Chicago/Turabian StyleEquestre, Michele, Cinzia Marcantonio, Nadia Marascio, Federica Centofanti, Antonio Martina, Matteo Simeoni, Elisabetta Suffredini, Giuseppina La Rosa, Giusy Bonanno Ferraro, Pamela Mancini, and et al. 2023. "Characterization of SARS-CoV-2 Variants in Military and Civilian Personnel of an Air Force Airport during Three Pandemic Waves in Italy" Microorganisms 11, no. 11: 2711. https://doi.org/10.3390/microorganisms11112711