SARS-CoV-2 variants, immune escape, and countermeasures
Yi Zhang1, Haocheng Zhang1, Wenhong Zhang1,2()
1. Department of Infectious Diseases, National Medical Center for Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, Huashan Hospital, Fudan University, Shanghai 200040, China 2. State Key Laboratory of Genetic Engineering and Institute of Biostatistics, School of Life Sciences, Fudan University, Shanghai 200040, China
Coronavirus disease 2019 (COVID-19) has become a global pandemic disease. SARS-CoV-2 variants have aroused great concern and are expected to continue spreading. Although many countries have promoted roll-out vaccination, the immune barrier has not yet been fully established, indicating that populations remain susceptible to infection. In this review, we summarize the literature on variants of concern and focus on the changes in their transmissibility, pathogenicity, and resistance to the immunity constructed by current vaccines. Furthermore, we analyzed relationships between variants and breakthrough infections, as well as the paradigm of new variants in countries with high vaccination rates. Terminating transmission, continuing to strengthen variant surveillance, and combining nonpharmaceutical intervention measures and vaccines are necessary to control these variants.
P Zhou, XL Yang, XG Wang, B Hu, L Zhang, W Zhang, HR Si, Y Zhu, B Li, CL Huang, HD Chen, J Chen, Y Luo, H Guo, RD Jiang, MQ Liu, Y Chen, XR Shen, X Wang, XS Zheng, K Zhao, QJ Chen, F Deng, LL Liu, B Yan, FX Zhan, YY Wang, GF Xiao, ZL Shi. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020; 579(7798): 270–273 https://doi.org/10.1038/s41586-020-2012-7
pmid: 32015507
2
S Su, G Wong, W Shi, J Liu, ACK Lai, J Zhou, W Liu, Y Bi, GF Gao. Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol 2016; 24(6): 490–502 https://doi.org/10.1016/j.tim.2016.03.003
pmid: 27012512
3
F Wu, S Zhao, B Yu, YM Chen, W Wang, ZG Song, Y Hu, ZW Tao, JH Tian, YY Pei, ML Yuan, YL Zhang, FH Dai, Y Liu, QM Wang, JJ Zheng, L Xu, EC Holmes, YZ Zhang. A new coronavirus associated with human respiratory disease in China. Nature 2020; 579(7798): 265–269 https://doi.org/10.1038/s41586-020-2008-3
pmid: 32015508
A Telenti, A Arvin, L Corey, D Corti, MS Diamond, A García-Sastre, RF Garry, EC Holmes, PS Pang, HW Virgin. After the pandemic: perspectives on the future trajectory of COVID-19. Nature 2021; 596(7873): 495–504 https://doi.org/10.1038/s41586-021-03792-w
pmid: 34237771
WT Harvey, AM Carabelli, B Jackson, RK Gupta, EC Thomson, EM Harrison, C Ludden, R Reeve, A Rambaut; COVID-19 Genomics UK (COG-UK) Consortium, SJ Peacock, DL Robertson. SARS-CoV-2 variants, spike mutations and immune escape. Nat Rev Microbiol 2021; 19(7): 409–424 https://doi.org/10.1038/s41579-021-00573-0
pmid: 34075212
8
World Health Organization. Tracking SARS-CoV-2 variants. 2020
9
The New York Times. Tracking coronavirus vaccinations around the world. 2021
10
E Hacisuleyman, C Hale, Y Saito, NE Blachere, M Bergh, EG Conlon, DJ Schaefer-Babajew, J DaSilva, F Muecksch, C Gaebler, R Lifton, MC Nussenzweig, T Hatziioannou, PD Bieniasz, RB Darnell. Vaccine breakthrough infections with SARS-CoV-2 variants. N Engl J Med 2021; 384(23): 2212–2218 https://doi.org/10.1056/NEJMoa2105000
pmid: 33882219
11
ND Grubaugh, WP Hanage, AL Rasmussen. Making sense of mutation: what D614G means for the COVID-19 pandemic remains unclear. Cell 2020; 182(4): 794–795 https://doi.org/10.1016/j.cell.2020.06.040
pmid: 32697970
12
E Volz, V Hill, JT McCrone, A Price, D Jorgensen, Á O'Toole, J Southgate, R Johnson, B Jackson, FF Nascimento, SM Rey, SM Nicholls, RM Colquhoun, A da Silva Filipe, J Shepherd, DJ Pascall, R Shah, N Jesudason, K Li, R Jarrett, N Pacchiarini, M Bull, L Geidelberg, I Siveroni; COG-UK Consortium, I Goodfellow, NJ Loman, OG Pybus, DL Robertson, EC Thomson, A Rambaut, TR Connor. Evaluating the effects of SARS-CoV-2 spike mutation D614G on transmissibility and pathogenicity. Cell 2021; 184(1): 64–75.e11 https://doi.org/10.1016/j.cell.2020.11.020
pmid: 33275900
13
N Al Kaabi, Y Zhang, S Xia, Y Yang, MM Al Qahtani, N Abdulrazzaq, M Al Nusair, M Hassany, JS Jawad, J Abdalla, SE Hussein, SK Al Mazrouei, M Al Karam, X Li, X Yang, W Wang, B Lai, W Chen, S Huang, Q Wang, T Yang, Y Liu, R Ma, ZM Hussain, T Khan, M Saifuddin Fasihuddin, W You, Z Xie, Y Zhao, Z Jiang, G Zhao, Y Zhang, S Mahmoud, I ElTantawy, P Xiao, A Koshy, WA Zaher, H Wang, K Duan, A Pan, X Yang. Effect of 2 inactivated SARS-CoV-2 vaccines on symptomatic COVID-19 infection in adults: a randomized clinical trial. JAMA 2021; 326(1): 35–45 https://doi.org/10.1001/jama.2021.8565
pmid: 34037666
14
L Yurkovetskiy, X Wang, KE Pascal, C Tomkins-Tinch, TP Nyalile, Y Wang, A Baum, WE Diehl, A Dauphin, C Carbone, K Veinotte, SB Egri, SF Schaffner, JE Lemieux, JB Munro, A Rafique, A Barve, PC Sabeti, CA Kyratsous, NV Dudkina, K Shen, J Luban. Structural and functional analysis of the D614G SARS-CoV-2 spike protein variant. Cell 2020; 183(3): 739–751.e8 https://doi.org/10.1016/j.cell.2020.09.032
pmid: 32991842
15
B Meng, SA Kemp, G Papa, R Datir, IATM Ferreira, S Marelli, WT Harvey, S Lytras, A Mohamed, G Gallo, N Thakur, DA Collier, P Mlcochova; COVID-19 Genomics UK (COG-UK) Consortium, LM Duncan, AM Carabelli, JC Kenyon, AM Lever, A De Marco, C Saliba, K Culap, E Cameroni, NJ Matheson, L Piccoli, D Corti, LC James, DL Robertson, D Bailey, RK Gupta. Recurrent emergence of SARS-CoV-2 spike deletion H69/V70 and its role in the Alpha variant B.1.1.7. Cell Rep 2021; 35(13):109292 https://doi.org/10.1016/j.celrep.2021.109292
pmid: 34166617
16
NG Davies, S Abbott, RC Barnard, CI Jarvis, AJ Kucharski, JD Munday, CAB Pearson, TW Russell, DC Tully, AD Washburne, T Wenseleers, A Gimma, W Waites, KLM Wong, K van Zandvoort, JD Silverman; CMMID COVID-19 Working Group; COVID-19 Genomics UK (COG-UK) Consortium, K Diaz-Ordaz, R Keogh, RM Eggo, S Funk, M Jit, KE Atkins, WJ Edmunds. Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science 2021; 372(6538): eabg3055 https://doi.org/10.1126/science.abg3055
pmid: 33658326
17
M Kidd, A Richter, A Best, N Cumley, J Mirza, B Percival, M Mayhew, O Megram, F Ashford, T White, E Moles-Garcia, L Crawford, A Bosworth, SF Atabani, T Plant, A McNally. S-Variant SARS-CoV-2 lineage B1.1.7 is associated with significantly higher viral load in samples tested by TaqPath polymerase chain reaction. J Infect Dis 2021; 223(10): 1666–1670 https://doi.org/10.1093/infdis/jiab082
pmid: 33580259
18
NG Davies, CI Jarvis, WJ Edmunds, NP Jewell, K Diaz-Ordaz, RH Keogh. Increased mortality in community-tested cases of SARS-CoV-2 lineage B.1.1.7. Nature 2021; 593(7858): 270–274 https://doi.org/10.1038/s41586-021-03426-1
19
R Challen, E Brooks-Pollock, JM Read, L Dyson, K Tsaneva-Atanasova, L Danon. Risk of mortality in patients infected with SARS-CoV-2 variant of concern 202012/1: matched cohort study. BMJ 2021; 372: n579 https://doi.org/10.1136/bmj.n579
pmid: 33687922
20
DA Collier, A De Marco, IATM Ferreira, B Meng, RP Datir, AC Walls, SA Kemp, J Bassi, D Pinto, C Silacci-Fregni, S Bianchi, MA Tortorici, J Bowen, K Culap, S Jaconi, E Cameroni, G Snell, MS Pizzuto, AF Pellanda, C Garzoni, A Riva; CITIID-NIHR BioResource COVID-19 Collaboration, A Elmer, N Kingston, B Graves, LE McCoy, KGC Smith, JR Bradley, N Temperton, L Ceron-Gutierrez, G Barcenas-Morales; COVID-19 Genomics UK (COG-UK) Consortium, W Harvey, HW Virgin, A Lanzavecchia, L Piccoli, R Doffinger, M Wills, D Veesler, D Corti, RK Gupta. Sensitivity of SARS-CoV-2 B.1.1.7 to mRNA vaccine-elicited antibodies. Nature 2021; 593(7857): 136–141 https://doi.org/10.1038/s41586-021-03412-7
pmid: 33706364
21
H Tegally, E Wilkinson, M Giovanetti, A Iranzadeh, V Fonseca, J Giandhari, D Doolabh, S Pillay, EJ San, N Msomi, K Mlisana, A von Gottberg, S Walaza, M Allam, A Ismail, T Mohale, AJ Glass, S Engelbrecht, G Van Zyl, W Preiser, F Petruccione, A Sigal, D Hardie, G Marais, NY Hsiao, S Korsman, MA Davies, L Tyers, I Mudau, D York, C Maslo, D Goedhals, S Abrahams, O Laguda-Akingba, A Alisoltani-Dehkordi, A Godzik, CK Wibmer, BT Sewell, J Lourenço, LCJ Alcantara, SL Kosakovsky Pond, S Weaver, D Martin, RJ Lessells, JN Bhiman, C Williamson, T de Oliveira. Detection of a SARS-CoV-2 variant of concern in South Africa. Nature 2021; 592(7854): 438–443 https://doi.org/10.1038/s41586-021-03402-9
pmid: 33690265
22
Q Li, J Nie, J Wu, L Zhang, R Ding, H Wang, Y Zhang, T Li, S Liu, M Zhang, C Zhao, H Liu, L Nie, H Qin, M Wang, Q Lu, X Li, J Liu, H Liang, Y Shi, Y Shen, L Xie, L Zhang, X Qu, W Xu, W Huang, Y Wang. SARS-CoV-2 501Y.V2 variants lack higher infectivity but do have immune escape. Cell 2021; 184(9): 2362–2371.e9 https://doi.org/10.1016/j.cell.2021.02.042
pmid: 33735608
23
NR Faria, TA Mellan, C Whittaker, IM Claro, DDS Candido, S Mishra, MAE Crispim, FC Sales, I Hawryluk, JT McCrone, RJG Hulswit, LAM Franco, MS Ramundo, JG de Jesus, PS Andrade, TM Coletti, GM Ferreira, CAM Silva, ER Manuli, RHM Pereira, PS Peixoto, MU Kraemer, N Jr Gaburo, CDC Camilo, H Hoeltgebaum, WM Souza, EC Rocha, LM de Souza, MC de Pinho, LJT Araujo, FSV Malta, AB de Lima, JDP Silva, DAG Zauli, AC de S Ferreira, RP Schnekenberg, DJ Laydon, PGT Walker, HM Schlüter, ALP Dos Santos, MS Vidal, VS Del Caro, RMF Filho, HM Dos Santos, RS Aguiar, JLP Modena, B Nelson, JA Hay, M Monod, X Miscouridou, H Coupland, R Sonabend, M Vollmer, A Gandy, MA Suchard, TA Bowden, SLK Pond, CH Wu, O Ratmann, NM Ferguson, C Dye, NJ Loman, P Lemey, A Rambaut, NA Fraiji, Carvalho MDPSS, OG Pybus, S Flaxman, S Bhatt, EC Sabino. Genomics and epidemiology of a novel SARS-CoV-2 lineage in Manaus, Brazil. Science 2021; 372(6544): 815–821 https://doi.org/10.1126/science.abh2644
pmid: 33853970
24
Virological. Identification of SARS-CoV-2 P.1-related lineages in Brazil provides new insights about the mechanisms of emergence of Variants of Concern. 2021
25
FG Naveca, V Nascimento, VC de Souza, AL Corado, F Nascimento, G Silva, Á Costa, D Duarte, K Pessoa, M Mejía, MJ Brandão, M Jesus, L Gonçalves, CF da Costa, V Sampaio, D Barros, M Silva, T Mattos, G Pontes, L Abdalla, JH Santos, I Arantes, FZ Dezordi, MM Siqueira, GL Wallau, PC Resende, E Delatorre, T Gräf, G Bello. COVID-19 in Amazonas, Brazil, was driven by the persistence of endemic lineages and P.1 emergence. Nat Med 2021; 27(7): 1230–1238 https://doi.org/10.1038/s41591-021-01378-7
pmid: 34035535
26
Outbreak.info. Mutation Tracker. 2021
27
P Mlcochova, SA Kemp, MS Dhar, G Papa, B Meng, IATM Ferreira, R Datir, DA Collier, A Albecka, S Singh, R Pandey, J Brown, J Zhou, N Goonawardane, S Mishra, C Whittaker, T Mellan, R Marwal, M Datta, S Sengupta, K Ponnusamy, VS Radhakrishnan, A Abdullahi, O Charles, P Chattopadhyay, P Devi, D Caputo, T Peacock, C Wattal, N Goel, A Satwik, R Vaishya, M Agarwal; Indian SARS-CoV-2 Genomics Consortium (INSACOG); Genotype to Phenotype Japan (G2P-Japan) Consortium; CITIID-NIHR BioResource COVID-19 Collaboration, A Mavousian, JH Lee, J Bassi, C Silacci-Fegni, C Saliba, D Pinto, T Irie, I Yoshida, WL Hamilton, K Sato, S Bhatt, S Flaxman, LC James, D Corti, L Piccoli, WS Barclay, P Rakshit, A Agrawal, RK Gupta. SARS-CoV-2 B.1.617.2 Delta variant replication and immune evasion. Nature 2021; 599(7883): 114–119 https://doi.org/10.1038/s41586-021-03944-y
pmid: 34488225
28
R Challen, L Dyson, C Overton, L Guzman-Rincon, E Hill, H Stage, E Brooks-Pollock, L Pellis, F Scarabel, DJ Pascall, P Blomquist, MJ Tildesley, D Williamson, S Siegert, X Xiong, B Youngman, JUNIPER Consortium, JM Read, JR Gog, MJ Keeling, L Danon. Early epidemiological signatures of novel SARS-CoV-2 variants: establishment of B.1.617.2 in England. medRxiv 2021; 2021.06.05.21258365 https://doi.org/10.1101/2021.06.05.21258365
29
C Motozono, M Toyoda, J Zahradnik, A Saito, H Nasser, TS Tan, I Ngare, I Kimura, K Uriu, Y Kosugi, Y Yue, R Shimizu, J Ito, S Torii, A Yonekawa, N Shimono, Y Nagasaki, R Minami, T Toya, N Sekiya, T Fukuhara, Y Matsuura, G Schreiber; Genotype to Phenotype Japan (G2P-Japan) Consortium, T Ikeda, S Nakagawa, T Ueno, K Sato. SARS-CoV-2 spike L452R variant evades cellular immunity and increases infectivity. Cell Host Microbe 2021; 29(7): 1124–1136.e11 https://doi.org/10.1016/j.chom.2021.06.006
pmid: 34171266
30
KA Twohig, T Nyberg, A Zaidi, S Thelwall, MA Sinnathamby, S Aliabadi, SR Seaman, RJ Harris, R Hope, J Lopez-Bernal, E Gallagher, A Charlett, D De Angelis, AM Presanis, G Dabrera; COVID-19 Genomics UK (COG-UK) consortium. Hospital admission and emergency care attendance risk for SARS-CoV-2 delta (B.1.617.2) compared with alpha (B.1.1.7) variants of concern: a cohort study. Lancet Infect Dis 2021; S1473-3099(21)00475-8 https://doi.org/10.1016/S1473-3099(21)00475-8
pmid: 34461056
31
Public Health England. SARS-CoV-2 variants of concern and variants under investigation in England Technical briefing 22. 2021
32
I Kimura, Y Kosugi, J Wu, D Yamasoba, EP Butlertanaka, YL Tanaka, Y Liu, K Shirakawa, Y Kazuma, R Nomura, Y Horisawa, K Tokunaga, A Takaori-Kondo, H Arase, A Saito, S Nakagawa, K Sato. SARS-CoV-2 Lambda variant exhibits higher infectivity and immune resistance. bioRxiv 2021: 2021.07.28.454085 https://doi.org/10.1101/2021.07.28.454085
33
AP Jr West, JO Wertheim, JC Wang, TI Vasylyeva, JL Havens, MA Chowdhury, E Gonzalez, CE Fang, SS Di Lonardo, S Hughes, JL Rakeman, HH Lee, CO Barnes, PNP Gnanapragasam, Z Yang, C Gaebler, M Caskey, MC Nussenzweig, JR Keeffe, PJ Bjorkman. Detection and characterization of the SARS-CoV-2 lineage B.1.526 in New York. Nat Commun 2021; 12(1): 4886 https://doi.org/10.1038/s41467-021-25168-4
pmid: 34373458
34
TN Starr, AJ Greaney, A Addetia, WW Hannon, MC Choudhary, AS Dingens, JZ Li, JD Bloom. Prospective mapping of viral mutations that escape antibodies used to treat COVID-19. Science 2021; 371(6531): 850–854 https://doi.org/10.1126/science.abf9302
pmid: 33495308
35
S Cherian, V Potdar, S Jadhav, P Yadav, N Gupta, M Das, P Rakshit, S Singh, P Abraham, S Panda, N Team. SARS-CoV-2 spike mutations, L452R, T478K, E484Q and P681R, in the second wave of COVID-19 in Maharashtra, India. Microorganisms 2021; 9(7): 1542 https://doi.org/103390/microorganisms9071542
pmid: 34361977
36
X Deng, MA Garcia-Knight, MM Khalid, V Servellita, C Wang, MK Morris, A Sotomayor-González, DR Glasner, KR Reyes, AS Gliwa, NP Reddy, C Sanchez San Martin, S Federman, J Cheng, J Balcerek, J Taylor, JA Streithorst, S Miller, B Sreekumar, PY Chen, U Schulze-Gahmen, TY Taha, JM Hayashi, CR Simoneau, GR Kumar, S McMahon, PV Lidsky, Y Xiao, P Hemarajata, NM Green, A Espinosa, C Kath, M Haw, J Bell, JK Hacker, C Hanson, DA Wadford, C Anaya, D Ferguson, PA Frankino, H Shivram, LF Lareau, SK Wyman, M Ott, R Andino, CY Chiu. Transmission, infectivity, and neutralization of a spike L452R SARS-CoV-2 variant. Cell 2021; 184(13): 3426–3437.e8 https://doi.org/10.1016/j.cell.2021.04.025
pmid: 33991487
37
Y Watanabe, JD Allen, D Wrapp, JS McLellan, M Crispin. Site-specific glycan analysis of the SARS-CoV-2 spike. Science 2020; 369(6501): 330–333 https://doi.org/10.1126/science.abb9983
pmid: 32366695
38
JA Plante, BM Mitchell, KS Plante, K Debbink, SC Weaver, VD Menachery. The variant gambit: COVID-19’s next move. Cell Host Microbe 2021; 29(4): 508–515 https://doi.org/10.1016/j.chom.2021.02.020
pmid: 33789086
39
P Wang, MS Nair, L Liu, S Iketani, Y Luo, Y Guo, M Wang, J Yu, B Zhang, PD Kwong, BS Graham, JR Mascola, JY Chang, MT Yin, M Sobieszczyk, CA Kyratsous, L Shapiro, Z Sheng, Y Huang, DD Ho. Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7. Nature 2021; 593(7857): 130–135 https://doi.org/10.1038/s41586-021-03398-2
pmid: 33684923
40
TN Starr, AJ Greaney, AS Dingens, JD Bloom. Complete map of SARS-CoV-2 RBD mutations that escape the monoclonal antibody LY-CoV555 and its cocktail with LY-CoV016. Cell Rep Med 2021; 2(4): 100255 https://doi.org/10.1016/j.xcrm.2021.100255
pmid: 33842902
R Copin, A Baum, E Wloga, KE Pascal, S Giordano, BO Fulton, A Zhou, N Negron, K Lanza, N Chan, A Coppola, J Chiu, M Ni, Y Wei, GS Atwal, AR Hernandez, K Saotome, Y Zhou, MC Franklin, AT Hooper, S McCarthy, S Hamon, JD Hamilton, HM Staples, K Alfson, R Carrion Jr, S Ali, T Norton, S Somersan-Karakaya, S Sivapalasingam, GA Herman, DM Weinreich, L Lipsich, N Stahl, AJ Murphy, GD Yancopoulos, CA Kyratsous. The monoclonal antibody combination REGEN-COV protects against SARS-CoV-2 mutational escape in preclinical and human studies. Cell 2021; 184(15): 3949–3961.e11 https://doi.org/10.1016/j.cell.2021.06.002
pmid: 34161776
43
KRW Emary, T Golubchik, PK Aley, CV Ariani, B Angus, S Bibi, B Blane, D Bonsall, P Cicconi, S Charlton, EA Clutterbuck, AM Collins, T Cox, TC Darton, C Dold, AD Douglas, CJA Duncan, KJ Ewer, AL Flaxman, SN Faust, DM Ferreira, S Feng, A Finn, PM Folegatti, M Fuskova, E Galiza, AL Goodman, CM Green, CA Green, M Greenland, B Hallis, PT Heath, J Hay, HC Hill, D Jenkin, S Kerridge, R Lazarus, V Libri, PJ Lillie, C Ludden, NG Marchevsky, AM Minassian, AC McGregor, YF Mujadidi, DJ Phillips, E Plested, KM Pollock, H Robinson, A Smith, R Song, MD Snape, RK Sutherland, EC Thomson, M Toshner, DPJ Turner, J Vekemans, TL Villafana, CJ Williams, AVS Hill, T Lambe, SC Gilbert, M Voysey, MN Ramasamy, AJ; COVID-19 Genomics UK consortium; AMPHEUS Project; Oxford COVID-19 Vaccine Trial Group Pollard. Efficacy of ChAdOx1 nCoV-19 (AZD1222) vaccine against SARS-CoV-2 variant of concern 202012/01 (B.1.1.7): an exploratory analysis of a randomised controlled trial. Lancet 2021; 397(10282): 1351–1362 https://doi.org/10.1016/S0140-6736(21)00628-0
pmid: 33798499
44
Novavax. Novavax COVID-19 vaccine demonstrates 89.3% efficacy in UK phase 3 trial. 2021
45
P Supasa, D Zhou, W Dejnirattisai, C Liu, AJ Mentzer, HM Ginn, Y Zhao, HME Duyvesteyn, R Nutalai, A Tuekprakhon, B Wang, GC Paesen, J Slon-Campos, C López-Camacho, B Hallis, N Coombes, KR Bewley, S Charlton, TS Walter, E Barnes, SJ Dunachie, D Skelly, SF Lumley, N Baker, I Shaik, HE Humphries, K Godwin, N Gent, A Sienkiewicz, C Dold, R Levin, T Dong, AJ Pollard, JC Knight, P Klenerman, D Crook, T Lambe, E Clutterbuck, S Bibi, A Flaxman, M Bittaye, S Belij-Rammerstorfer, S Gilbert, DR Hall, MA Williams, NG Paterson, W James, MW Carroll, EE Fry, J Mongkolsapaya, J Ren, DI Stuart, GR Screaton. Reduced neutralization of SARS-CoV-2 B.1.1.7 variant by convalescent and vaccine sera. Cell 2021; 184(8): 2201–2211.e7 https://doi.org/10.1016/j.cell.2021.02.033
pmid: 33743891
46
Y Liu, J Liu, H Xia, X Zhang, CR Fontes-Garfias, KA Swanson, H Cai, R Sarkar, W Chen, M Cutler, D Cooper, SC Weaver, A Muik, U Sahin, KU Jansen, X Xie, PR Dormitzer, PY Shi. Neutralizing activity of BNT162b2-elicited serum. N Engl J Med 2021; 384: 1466–1468 https://doi.org/101056/NEJMc2102017
pmid: 33684280
47
GL Wang, ZY Wang, LJ Duan, QC Meng, MD Jiang, J Cao, L Yao, KL Zhu, WC Cao, MJ Ma. Susceptibility of circulating SARS-CoV-2 variants to neutralization. N Engl J Med 2021; 384(24): 2354–2356 https://doi.org/10.1056/NEJMc2103022
pmid: 33822491
48
WF Garcia-Beltran, EC Lam, K St Denis, AD Nitido, ZH Garcia, BM Hauser, J Feldman, MN Pavlovic, DJ Gregory, MC Poznansky, A Sigal, AG Schmidt, AJ Iafrate, V Naranbhai, AB Balazs. Multiple SARS-CoV-2 variants escape neutralization by vaccine-induced humoral immunity. Cell 2021; 184(9): 2372–2383.e9 https://doi.org/10.1016/j.cell.2021.03.013
49
K Wu, AP Werner, M Koch, A Choi, E Narayanan, GBE Stewart-Jones, T Colpitts, H Bennett, S Boyoglu-Barnum, W Shi, JI Moliva, NJ Sullivan, BS Graham, A Carfi, KS Corbett, RA Seder, DK Edwards. Serum neutralizing activity elicited by mRNA-1273 vaccine. N Engl J Med 2021; 384(15): 1468–1470 https://doi.org/10.1056/NEJMc2102179
pmid: 33730471
50
B Huang, L Dai, H Wang, Z Hu, X Yang, W Tan, F Gao. Neutralization of SARS-CoV-2 VOC 501YV2 by human antisera elicited by both inactivated BBIBP-CorV and recombinant dimeric RBD ZF2001 vaccines. bioRxiv 2021: 20210201429069 https://doi.org/101101/20210201429069
51
D Planas, D Veyer, A Baidaliuk, I Staropoli, F Guivel-Benhassine, MM Rajah, C Planchais, F Porrot, N Robillard, J Puech, M Prot, F Gallais, P Gantner, A Velay, J Le Guen, N Kassis-Chikhani, D Edriss, L Belec, A Seve, L Courtellemont, H Péré, L Hocqueloux, S Fafi-Kremer, T Prazuck, H Mouquet, T Bruel, E Simon-Lorière, FA Rey, O Schwartz. Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization. Nature 2021; 596(7871): 276–280 https://doi.org/10.1038/s41586-021-03777-9
pmid: 34237773
52
Novavax. COVID-19 vaccine demonstrates 90% overall efficacy and 100% protection against moderate and severe disease in PREVENT-19 phase 3 trial. 2021
53
J Lopez Bernal, N Andrews, C Gower, E Gallagher, R Simmons, S Thelwall, J Stowe, E Tessier, N Groves, G Dabrera, R Myers, CNJ Campbell, G Amirthalingam, M Edmunds, M Zambon, KE Brown, S Hopkins, M Chand, M Ramsay. Effectiveness of Covid-19 vaccines against the B.1.617.2 (Delta) variant. N Engl J Med 2021; 385(7): 585–594 https://doi.org/10.1056/NEJMoa2108891
pmid: 34289274
54
N Dagan, N Barda, E Kepten, O Miron, S Perchik, MA Katz, MA Hernán, M Lipsitch, B Reis, RD Balicer. BNT162b2 mRNA Covid-19 vaccine in a nationwide mass vaccination setting. N Engl J Med 2021; 384(15): 1412–1423 https://doi.org/10.1056/NEJMoa2101765
pmid: 33626250
55
LJ Abu-Raddad, H Chemaitelly, AA; National Study Group for COVID-19 Vaccination Butt. Effectiveness of the BNT162b2 Covid-19 vaccine against the B.1.1.7 and B.1.351 variants. N Engl J Med 2021; 385(2): 187–189 https://doi.org/10.1056/NEJMc2104974
pmid: 33951357
56
E Mahase. Covid-19: Novavax vaccine efficacy is 86% against UK variant and 60% against South African variant. BMJ 2021; 372: n296 https://doi.org/10.1136/bmj.n296
pmid: 33526412
57
SA Madhi, V Baillie, CL Cutland, M Voysey, AL Koen, L Fairlie, SD Padayachee, K Dheda, SL Barnabas, QE Bhorat, C Briner, G Kwatra, K Ahmed, P Aley, S Bhikha, JN Bhiman, AE Bhorat, J du Plessis, A Esmail, M Groenewald, E Horne, SH Hwa, A Jose, T Lambe, M Laubscher, M Malahleha, M Masenya, M Masilela, S McKenzie, K Molapo, A Moultrie, S Oelofse, F Patel, S Pillay, S Rhead, H Rodel, L Rossouw, C Taoushanis, H Tegally, A Thombrayil, S van Eck, CK Wibmer, NM Durham, EJ Kelly, TL Villafana, S Gilbert, AJ Pollard, T de Oliveira, PL Moore, A Sigal, A Izu; NGS-SA Group; Wits-VIDA COVID Group. Efficacy of the ChAdOx1 nCoV-19 Covid-19 vaccine against the B.1.351 variant. N Engl J Med 2021; 384(20): 1885–1898 https://doi.org/10.1056/NEJMoa2102214
pmid: 33725432
58
R Palacios, AP Batista, CSN Albuquerque, EG Patiño. Efficacy and safety of a COVID-19 inactivated vaccine in healthcare professionals in Brazil: The PROFISCOV Study. SSRN 2021: 3822780 https://doi.org/10.2139/ssrn.3822780
59
A Jara, EA Undurraga, C González, F Paredes, T Fontecilla, G Jara, A Pizarro, J Acevedo, K Leo, F Leon, C Sans, P Leighton, P Suárez, H García-Escorza, R Araos. Effectiveness of an inactivated SARS-CoV-2 vaccine in Chile. N Engl J Med 2021; 385(10): 875–884 https://doi.org/10.1056/NEJMoa2107715
pmid: 34233097
60
A Sheikh, J McMenamin, B Taylor, C; Public Health Scotland and the EAVE II Collaborators Robertson. SARS-CoV-2 Delta VOC in Scotland: demographics, risk of hospital admission, and vaccine effectiveness. Lancet 2021; 397(10293): 2461–2462 https://doi.org/10.1016/S0140-6736(21)01358-1
pmid: 34139198
61
EC Wall, M Wu, R Harvey, G Kelly, S Warchal, C Sawyer, R Daniels, L Adams, P Hobson, E Hatipoglu, Y Ngai, S Hussain, K Ambrose, S Hindmarsh, R Beale, A Riddell, S Gamblin, M Howell, G Kassiotis, V Libri, B Williams, C Swanton, S Gandhi, DL Bauer. AZD1222-induced neutralising antibody activity against SARS-CoV-2 Delta VOC. Lancet 2021; 398(10296): 207–209 https://doi.org/10.1016/S0140-6736(21)01462-8
pmid: 34197809
62
XN Li, Y Huang, W Wang, QL Jing, CH Zhang, PZ Qin, WJ Guan, L Gan, YL Li, WH Liu, H Dong, YT Miao, SJ Fan, ZB Zhang, DM Zhang, NS Zhong. Effectiveness of inactivated SARS-CoV-2 vaccines against the Delta variant infection in Guangzhou: a test-negative case-control real-world study. Emerg Microbes Infect 2021; 10(1): 1751–1759 https://doi.org/10.1080/22221751.2021.1969291
pmid: 34396940
63
MG Thompson, E Stenehjem, S Grannis, SW Ball, AL Naleway, TC Ong, MB DeSilva, K Natarajan, CH Bozio, N Lewis, K Dascomb, BE Dixon, RJ Birch, SA Irving, S Rao, E Kharbanda, J Han, S Reynolds, K Goddard, N Grisel, WF Fadel, ME Levy, J Ferdinands, B Fireman, J Arndorfer, NR Valvi, EA Rowley, P Patel, O Zerbo, EP Griggs, RM Porter, M Demarco, L Blanton, A Steffens, Y Zhuang, N Olson, M Barron, P Shifflett, SJ Schrag, JR Verani, A Fry, M Gaglani, E Azziz-Baumgartner, NP Klein. Effectiveness of Covid-19 vaccines in ambulatory and inpatient care settings. N Engl J Med 2021; 385(15): 1355–1371 https://doi.org/10.1056/NEJMoa2110362
pmid: 34496194
64
P Bager, J Wohlfahrt, M Rasmussen, M Albertsen, TG Krause. Hospitalisation associated with SARS-CoV-2 delta variant in Denmark. Lancet Infect Dis 2021; 21(10): 1351 https://doi.org/10.1016/S1473-3099(21)00580-6
pmid: 34487704
65
H Rincon-Arevalo, M Choi, AL Stefanski, F Halleck, U Weber, F Szelinski, B Jahrsdörfer, H Schrezenmeier, C Ludwig, A Sattler, K Kotsch, A Potekhin, Y Chen, GR Burmester, KU Eckardt, GM Guerra, P Durek, F Heinrich, M Ferreira-Gomes, A Radbruch, K Budde, AC Lino, MF Mashreghi, E Schrezenmeier, T Dörner. Impaired humoral immunity to SARS-CoV-2 BNT162b2 vaccine in kidney transplant recipients and dialysis patients. Sci Immunol 2021; 6(60): eabj1031 https://doi.org/10.1126/sciimmunol.abj1031
pmid: 34131023
66
M Yuan, D Huang, CD Lee, NC Wu, AM Jackson, X Zhu, H Liu, L Peng, MJ van Gils, RW Sanders, DR Burton, SM Reincke, H Prüss, J Kreye, D Nemazee, AB Ward, IA Wilson. Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants. Science 2021; 373(6556): 818–823 https://doi.org/10.1126/science.abh1139
pmid: 34016740
67
B Agerer, M Koblischke, V Gudipati, LF Montaño-Gutierrez, M Smyth, A Popa, JW Genger, L Endler, DM Florian, V Mühlgrabner, M Graninger, SW Aberle, AM Husa, LE Shaw, A Lercher, P Gattinger, R Torralba-Gombau, D Trapin, T Penz, D Barreca, I Fae, S Wenda, M Traugott, G Walder, WF Pickl, V Thiel, F Allerberger, H Stockinger, E Puchhammer-Stöckl, W Weninger, G Fischer, W Hoepler, E Pawelka, A Zoufaly, R Valenta, C Bock, W Paster, R Geyeregger, M Farlik, F Halbritter, JB Huppa, JH Aberle, A Bergthaler. SARS-CoV-2 mutations in MHC-I-restricted epitopes evade CD8+ T cell responses. Sci Immunol 2021; 6(57): eabg6461 https://doi.org/10.1126/sciimmunol.abg6461
pmid: 33664060
68
CJ Reynolds, C Pade, JM Gibbons, DK Butler, AD Otter, K Menacho, M Fontana, A Smit, JE Sackville-West, T Cutino-Moguel, MK Maini, B Chain, M Noursadeghi; UK COVIDsortium Immune Correlates Network, T Brooks, A Semper, C Manisty, TA Treibel, JC Moon; UK COVIDsortium Investigators, AM Valdes, Á McKnight, DM Altmann, R Boyton. Prior SARS-CoV-2 infection rescues B and T cell responses to variants after first vaccine dose. Science 2021; 372(6549): 1418–1423 https://doi.org/10.1126/science.abh1282
pmid: 33931567
69
J Keehner, LE Horton, NJ Binkin, LC Laurent, D Pride, CA Longhurst, SR Abeles, FJ Torriani. Resurgence of SARS-CoV-2 infection in a highly vaccinated health system workforce. N Engl J Med 2021; 385(14): 1330–1332 https://doi.org/10.1056/NEJMc2112981
pmid: 34469645
70
AE McEwen, S Cohen, C Bryson-Cahn, C Liu, SA Pergam, J Lynch, A Schippers, K Strand, E Whimbey, NS Mani, AJ Zelikoff, VA Makarewicz, ER Brown, SAM Bakhash, NR Baker, J Castor, RJ Livingston, ML Huang, KR Jerome, AL Greninger, P Roychoudhury. Variants of concern are overrepresented among post-vaccination breakthrough infections of SARS-CoV-2 in Washington State. Clin Infect Dis 2021; ciab581 https://doi.org/10.1093/cid/ciab581
pmid: 34166484
71
Centers for Disease Control and Prevention. COVID-19 vaccine breakthrough infections reported to CDC—United States, January 1–April 30, 2021. 2021
72
M Bergwerk, T Gonen, Y Lustig, S Amit, M Lipsitch, C Cohen, M Mandelboim, EG Levin, C Rubin, V Indenbaum, I Tal, M Zavitan, N Zuckerman, A Bar-Chaim, Y Kreiss, G Regev-Yochay. Covid-19 breakthrough infections in vaccinated health care workers. N Engl J Med 2021; 385(16): 1474–1484 https://doi.org/10.1056/NEJMoa2109072
pmid: 34320281
73
T Kustin, N Harel, U Finkel, S Perchik, S Harari, M Tahor, I Caspi, R Levy, M Leshchinsky, S Ken Dror, G Bergerzon, H Gadban, F Gadban, E Eliassian, O Shimron, L Saleh, H Ben-Zvi, E Keren Taraday, D Amichay, A Ben-Dor, D Sagas, M Strauss, Y Shemer Avni, A Huppert, E Kepten, RD Balicer, D Netzer, S Ben-Shachar, A Stern. Evidence for increased breakthrough rates of SARS-CoV-2 variants of concern in BNT162b2-mRNA-vaccinated individuals. Nat Med 2021; 27(8): 1379–1384 https://doi.org/10.1038/s41591-021-01413-7
pmid: 34127854
74
SD Pollett, SA Richard, AC Fries, MP Simons, K Mende, T Lalani, T Lee, S Chi, R Mody, C Madar, A Ganesan, DT Larson, CJ Colombo, R Colombo, EC Samuels, CC Broder, ED Laing, DR Smith, D Tribble, BK Agan, TH Burgess. The SARS-CoV-2 mRNA vaccine breakthrough infection phenotype includes significant symptoms, live virus shedding, and viral genetic diversity. Clin Infect Dis 2021; ciab543 https://doi.org/10.1093/cid/ciab543
pmid: 34117878
75
The New York Times. Coronavirus in the U.S.: latest map and case count. 2021
76
Evening Standard. Delta variant cases up 79% in a week with young people ‘driving the spread’. 2021
77
JM Dan, J Mateus, Y Kato, KM Hastie, ED Yu, CE Faliti, A Grifoni, SI Ramirez, S Haupt, A Frazier, C Nakao, V Rayaprolu, SA Rawlings, B Peters, F Krammer, V Simon, EO Saphire, DM Smith, D Weiskopf, A Sette, S Crotty. Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection. Science 2021; 371(6529): eabf4063 https://doi.org/10.1126/science.abf4063
pmid: 33408181
78
C Gaebler, Z Wang, JCC Lorenzi, F Muecksch, S Finkin, M Tokuyama, A Cho, M Jankovic, D Schaefer-Babajew, TY Oliveira, M Cipolla, C Viant, CO Barnes, Y Bram, G Breton, T Hägglöf, P Mendoza, A Hurley, M Turroja, K Gordon, KG Millard, V Ramos, F Schmidt, Y Weisblum, D Jha, M Tankelevich, G Martinez-Delgado, J Yee, R Patel, J Dizon, C Unson-O’Brien, I Shimeliovich, DF Robbiani, Z Zhao, A Gazumyan, RE Schwartz, T Hatziioannou, PJ Bjorkman, S Mehandru, PD Bieniasz, M Caskey, MC Nussenzweig. Evolution of antibody immunity to SARS-CoV-2. Nature 2021; 591(7851): 639–644 https://doi.org/10.1038/s41586-021-03207-w
pmid: 33461210
79
DS Khoury, D Cromer, A Reynaldi, TE Schlub, AK Wheatley, JA Juno, K Subbarao, SJ Kent, JA Triccas, MP Davenport. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med 2021; 27(7): 1205–1211 https://doi.org/10.1038/s41591-021-01377-8
pmid: 34002089
80
O Milman, I Yelin, N Aharony, R Katz, E Herzel, A Ben-Tov, J Kuint, S Gazit, G Chodick, T Patalon, R Kishony. Community-level evidence for SARS-CoV-2 vaccine protection of unvaccinated individuals. Nat Med 2021; 27(8): 1367–1369 https://doi.org/10.1038/s41591-021-01407-5
pmid: 34113015
81
J Salo, M Hägg, M Kortelainen, T Leino, T Saxell, M Siikanen, L Sääksvuori. The indirect effect of mRNA-based Covid-19 vaccination on unvaccinated household members. medRxiv 2021: 2021.05.27.21257896 https://doi.org/10.1101/2021.05.27.21257896
82
Moderna. COVID-19 vaccine retains neutralizing activity against emerging variants first identified in the U.K. and the Republic of South Africa. 2021
83
Pfizer. BioNTech to seek authorization for COVID booster shot as Delta variant spreads. 2021
84
PR Krause, TR Fleming, IM Longini, R Peto, S Briand, DL Heymann, V Beral, MD Snape, H Rees, AM Ropero, RD Balicer, JP Cramer, C Muñoz-Fontela, M Gruber, R Gaspar, JA Singh, K Subbarao, MD Van Kerkhove, S Swaminathan, MJ Ryan, AM Henao-Restrepo. SARS-CoV-2 variants and vaccines. N Engl J Med 2021; 385(2): 179–186 https://doi.org/10.1056/NEJMsr2105280
pmid: 34161052
85
World Health Organization. Episode #45—Delta variant. 2021
86
J Yang, V Marziano, X Deng, G Guzzetta, J Zhang, F Trentini, J Cai, P Poletti, W Zheng, W Wang, Q Wu, Z Zhao, K Dong, G Zhong, C Viboud, S Merler, M Ajelli, H Yu. Despite vaccination, China needs non-pharmaceutical interventions to prevent widespread outbreaks of COVID-19 in 2021. Nat Hum Behav 2021; 5(8): 1009–1020 https://doi.org/10.1038/s41562-021-01155-z
pmid: 34158650
87
S Moore, EM Hill, MJ Tildesley, L Dyson, MJ Keeling. Vaccination and non-pharmaceutical interventions for COVID-19: a mathematical modelling study. Lancet Infect Dis 2021; 21(6): 793–802 https://doi.org/10.1016/S1473-3099(21)00143-2
pmid: 33743847
