SARS-CoV-2 Variants: A Synopsis of In Vitro Efficacy Data of Convalescent Plasma, Currently Marketed Vaccines, and Monoclonal Antibodies
Abstract
:- vaccine-elicited T-cell immunity: while neutralizing antibodies are just one arm of the adaptive immune response to vaccines, very few data are available for protection from T-cell immunity, which would be especially relevant in the ones who do not mount antibody responses. Gallagher et al found detectable but diminished T-cell responses to Spike variants (B.1.1.7, B.1.351, and B.1.1.248) among BNT162b2 or mRNA-1273 vaccinated donors [19]. BNT162b2 or mRNA-1273-elicited spike-specific T cells responded similarly to stimulation by Spike epitopes from the ancestral, B.1.1.7 and B.1.351 variant strains, both in terms of cell numbers and phenotypes. In infection-naive individuals, the second dose boosted the quantity but not quality of the T cell response, while in convalescents the second dose helped neither. Spike-specific T cells from convalescent vaccinees differed strikingly from those of infection-naive vaccinees, with phenotypic features suggesting superior long-term persistence and ability to home to the respiratory tract including the nasopharynx [20].
- duration of protection: according to a mathematical model by Luo et al, after mRNA-1273 vaccination, pseudovirus neutralization test against B.1.351 is expected to fall below the lower limit of detection of 20 geometric mean titers on day 100; variant P.1 on day 202, variant B.1.429 on day 258; and variant B.1.1.7 on day 309 [21]. Real-world data instead suggested that binding and functional antibodies against B.1.1.7, B.1.351, P.1, B.1.429, and B.1.526 variants persisted in most subjects, albeit at low levels, for 6 months after the primary series of mRNA-1273 [22].
- postponing second doses has been widely implemented in order to optimize vaccine delivery under manufacturing bottlenecks. In nonconvalescent elderlies higher than age 80 who received the second dose of BNT162b2 after 12 weeks instead of 3, the peak antibody response was 3.5-fold higher, but cellular immune responses were 3.6-fold lower [23].
- heterologous boosting: heterologous immunization strategy combining inactivated and mRNA vaccines can generate robust vaccine responses and therefore provide a rational and effective vaccination regimen [24]. ChAdOx/BNT162b2 booster vaccination was largely comparable to homologous BNT162b2/BNT162b2 vaccination and overall well-tolerated. No major differences were observed in the frequency or severity of local reactions after either of the vaccinations. In contrast, notable differences between the regimens were observed for systemic reactions, which were most frequent after prime immunization with ChAdOx (86%) and less frequent after homologous BNT162b2/BNT162b2 (65%), or heterologous ChAdOx/BNT162b2 boosters (48%) [25]. Neutralizing activity against the prevalent strain B.1.1.7 was 3.9-fold higher than in individuals receiving homologous BNT162b2 vaccination, only 2-fold reduced for variant of concern B.1.351, and similar for variant B.1.617 [26]. Whilst both ChAdOx and BNT162b2 boosted prime-induced immunity, BNT induced significantly higher frequencies of Spike-specific CD4 and CD8 T cells and, in particular, high titers of neutralizing antibodies against the B.1.1.7, B.1.351 and the P.1 VOCs [27].
Variants of Concern (VOC) | Variants of Interest (VOI) | Other | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Therapeutic\Variant | PANGOLIN name | B.1.1.7 | B.1.351 | P.1 | B.1.617.2 | P.2 | B.1.427 B.1.429 | P.3 | B.1.525 | B.1.526 with E484K or S477N | B.1.617.1 | B.1.258D | B.1.1.298 | |
NextStrain name | 20I/S:501Y.V1 | 20H/S:501Y.V2 | 20J/S:501Y.V3 | 21A/S:478K | 20B/S.484K | 20C/S.452R | 20B/S:265C | 20A/S484K | 20C/S.484K | 21A/S:154K | - | - | ||
PHE name | VOC-20DEC-01 | VOC-20DEC-02 | VOC-21JAN-02 | VUI-21APR02 | VUI-21JAN-01 | - | - | VUI-21FEB-03 | - | - | - | - | ||
WHO name | alpha | beta | gamma | delta | zeta | epsilon | theta | eta | iota | kappa | - | - | ||
GISAID name | GRY (formerly GR/501Y.V1) | GH/501Y.V2 | GR/501Y.V3 | G/452R.V3 | GR | GH/452R.V1 | GR | G/484K.V3 | GH | G/452R.V3 | - | - | ||
local name | VUI/VOC 202012/01, UK variant | 501Y.V2 VOC 202012/02 | B.1.1.28.1 B.1.1.248 VOC 202101/02 | Indian variant | B.1.1.28.2 B.1.1.28(E484K) | CAL.20C/L452R, West Coast variant | - | Nigerian variant | - | Indian variant | - | Cluster V | ||
country of first detection | South-East England, UK | South Africa | Amazonas, Brazil | India | Rio de Janeiro, Brazil | Southern California, USA | Brazil | Nigeria | New York, USA | India | Czech Republic, Slovakia | Denmark | ||
convalescent plasma (sera) from previous waves | ↓ [28,29,30,31,32,33,34,35] | ↓↓↓ [29,31,33,34,36,37,38,39,40,41] | ↓↓↓ [42] | = [43] ↓[44,45,46] ↓↓ [41] | = [47] ↓↓↓ [48] (hamsters) | ↓↓ [49] | ? | ? | ↓↓ [50,51] | ? | ↓ [52] | ? | ||
hyperimmune serum (polyvalent immunoglobulins) | = [53] | ↓↓↓ [53] | ↓↓↓ [53] | ? | ? | = [53] | ? | ? | ? | ? | ? | ? | ||
estimated reinfection rate | 0.7% [54] | ? | 6.4% [55] | ? | ? | ? | ? | ? | ? | ? | ? | ? | ||
proven reinfection | 1 case [56] | 1 case [57] | 1 case [58] | ? | 2 cases [59,60] | ? | ? | ? | ? | ? | ? | ? | ||
mAbs- | Eli Lilly (AbCellera/Junshi) | etesevimab (LyCoV016, CB6 or JS016/LY3832479) | ↓↓↓ [29,61] | = [29] | ↓↓↓ [42,61] | ? | ? | ↓↓ [49] | ? | ? | = [51] | ? | ? | ? |
bamlanivimab (LY-CoV555/LY3819253) | ↓↓↓ [29,37,62,63] | = [29,63] | ↓↓↓ [37,42,62] | ↓↓↓ [44,45,46,64] | ↓↓↓ [63] | ↓↓↓ [49,65] | ? | ? | ↓↓↓ [50,51] | ? | ? | ? | ||
LY-CoV1404 | = [66] | = [66] | = [66] | ? | ? | = [66] | ? | ? | = [66] | ? | ? | ? | ||
Regeneron/Roche REGN-CoV2 | imdevimab (REGN10987) | = [29] | = [29] | = [42,61] | ? | ? | = [49] | ? | ? | = [50,51] | ? | ↓↓↓ [52] | ? | |
casirivimab (REGN10933) | ↓↓↓ [61] | ↓↓ [29] | ↓↓↓ [37,42,61] | ? | ? | = [49] | ? | ? | ↓↓↓ [50,51] | ? | ? | ? | ||
Celltrion | regdanvimab (CT-P59) | ↓↓ [67] | ? | ? | ? | ? | ↓↓ [49] | ? | ? | ? | ? | ? | ? | |
A-straZeneca AZD7442 long-acting antibody (LAAB) | AZD8895/COV2-2196 | ↓↓↓ [29] | ↓↓↓ [29] | = [42] | ? | ? | ? | ? | ? | ? | ? | ? | ? | |
AZD1061/COV2-2130 | = [29] | = [29] | = [42] | ? | ? | ? | ? | ? | ? | ? | ? | ? | ||
BMS | C135 | = [29] | = [29] | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? | |
C144 | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? | ||
Vir Biotechnology | VIR-7831/GSK-4182136 (sotrovimab) and VIR-7832/GSK-4182137 (both derived from S309) | = [29,68] | = [29,68] | = [42,68] | ? | ? | ? | ? | ? | ? | ? | ? | ? | |
vaccine | BioNtech/Pfizer | BNT162b2/tozinameran (Comirnaty®) | = [69] ↓ [15,29,31,33,35,37,63,70,71,72,73,74,75] RBD ↓↓↓ [76,77,78] COVID19 75% [79] | =/↓ [29,31,32,33,35,63,70,71,72,73,74,75,80,81,82] RBD [78] COVID19 90% [79,83]-93% [84] | ↓↓ [35,42,75,76,85] | ↓↓↓ [44,45,46,86,87] COVID19 88% [84] | ↓ [63] | =/↓↓ [49,75] RBD [78] | ? | ↓ [88] | ↓↓ [50,51] | ? | ? | = [75] |
Moderna | mRNA-1273 | ↓ [15,29,38,74,75,89] ↓ NHP COVID19 [90] | = [29,30,89] ↓ [74,75,91,92] | =/↓ [42,75] | ↓↓ [44,87] | ? | =/↓↓ [49,75] | ? | ? | ↓↓ [50,51] | ? | ? | = [75] | |
AstraZeneca | AZD1222/ChAdOx1 (Vaxzevria®, Covishield®) | ↓↓↓ [93] = hamster COVID19 [94] COVID19 22% | ? COVID19 90% [83]-66% [84] = hamster COVID19 [94] | ↓↓ [85] | ↓ [45,95] COVID19 % [84] | ? | ? | ? | ? | ? | ? | ? | ? | |
Gamaleya | Sputnik V/Gam-Covid-Vac | ↓↓↓ [96] | = [96] | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? | |
Novovax | NVX-CoV2373 (Covovax®) | ? COVID19: 51% [97] | ↓ [92] | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? | |
Bharat Biotech | BBV152/Covaxin | ? | = [98] ↓ [41] | ? | = [43] ↓ [41] | ↓ [47] | ? | ? | ? | ? | ? | ? | ? | |
SinoVac | CoronaVac | ↓↓↓ [99] | = [99] | ↓↓ [99] | ? | ? | = [99] | ? | ? | ↓↓ [99] | ? | ? | ? | |
J&J/Janssen | JNJ-78436735/Ad26.COV2.S | ? | ↓↓↓ [100] | ? | ? | ? | ? | ? | ? | ? | ? | ? | ? |
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
Abbreviations
nAb | neutralizing antibodies |
CCP | COVID19 convalescent plasma |
RBD | receptor-binding domain |
RBM | receptor-binding motif |
References
- WHO. COVID-19 Weekly Epidemiological Update 25 February 2021. Special Edition: Proposed Working Definitions of SARS-CoV-2 Variants of Interest and Variants of Concern. 2021. Available online: https://www.who.int/publications/m/item/covid-19-weekly-epidemiological-update (accessed on 17 June 2021).
- Focosi, D.; Mazzetti, P.; Pistello, M.M. Viral infection neutralization tests: A focus on SARS-CoV-2 with implications for convalescent plasma therapy. Rev. Med. Virol. 2020, 31, e2170. [Google Scholar] [PubMed]
- Focosi, D.; Novazzi, F.; Genoni, A.; Dentali, F.; Dalla Gasperina, D.; Baj, A.; Maggi, F. Emergence of SARS-CoV-2 Spike Escape Mutation Q493R After Bamlanivimab/Etesevimab Treatment for COVID-19. Res. Sq. 2021. [Google Scholar] [CrossRef]
- Chen, J.; Gao, K.; Wang, R.; Wei, G.-W. Revealing the threat of emerging SARS-CoV-2 mutations to antibody therapies. bioRxiv 2021. [Google Scholar] [CrossRef]
- Chen, X.; Chen, Z.; Azman, A.S.; Sun, R.; Lu, W.; Zheng, N.; Zhou, J.; Wu, Q.; Deng, X.; Zhao, Z.; et al. Comprehensive mapping of neutralizing antibodies against SARS-CoV-2 variants induced by natural infection or vaccination. medRxiv 2021. [Google Scholar] [CrossRef]
- Horspool, A.M.; Ye, C.; Wong, T.Y.; Russ, B.P.; Lee, K.S.; Winters, M.T.; Bevere, J.R.; Kieffer, T.; Martinez, I.; Sourimant, J.; et al. SARS-CoV-2 B.1.1.7 and B.1.351 variants of concern induce lethal disease in K18-hACE2 transgenic mice despite convalescent plasma therapy. bioRxiv 2021. [Google Scholar] [CrossRef]
- Khoury, D.S.; Cromer, D.; Reynaldi, A.; Schlub, T.E.; Wheatley, A.K.; Juno, J.A.; Subbarao, K.; Kent, S.J.; Triccas, J.A.; Davenport, M.P. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat. Med. 2021, 1–7. [Google Scholar] [CrossRef]
- Kustin, T.; Harel, N.; Finkel, U.; Perchik, S.; Harari, S.; Tahor, M.; Caspi, I.; Levy, R.; Leshchinsky, M.; Ken Dror, S.; et al. Evidence for increased breakthrough rates of SARS-CoV-2 variants of concern in BNT162b2 mRNA vaccinated individuals. Nat. Med. 2021. [Google Scholar] [CrossRef]
- Greaney, A.J.; Loes, A.N.; Gentles, L.E.; Crawford, K.H.D.; Starr, T.N.; Malone, K.D.; Chu, H.Y.; Bloom, J.D. The SARS-CoV-2 mRNA-1273 vaccine elicits more RBD-focused neutralization, but with broader antibody binding within the RBD. bioRxiv 2021. [Google Scholar] [CrossRef]
- Klingler, J.; Gregory, S.; Itri, V.; Liu, S.; Bandres, J.C.; Enyindah-Asonye, G.; Liu, X.; Oguntuyo, K.Y.; Amanat, F.; Lee, B. SARS-CoV-2 mRNA vaccines induce a greater array of spike-specific antibody isotypes with more potent complement binding capacity than natural infection. medRxiv 2021. [Google Scholar] [CrossRef]
- Abu Jabal, K.; Ben Amram, H.; Beiruti, K.; Brimat, I.; Abu Saaa, A.; Batish, Y.; Sussan, C.; Zarka, S.; Edelstein, M. SARS-CoV-2 Immunogenicity in individuals infected before and after COVID-19 vaccination: Israel, January-March 2021: Implications for vaccination policy. medRxiv 2021. [Google Scholar] [CrossRef]
- Ranzani, O.T.; Hitchings, M.; Dorion Neto, M.; Lang D’Agostini, T.; Cardoso de Paulha, R.; Ferreira Pereira de Paula, O.; de Moura Villela, F.; Scaramuzzini Torres, M.S.; Barbosa de Oliveira, M.; Schulz, W.; et al. Effectiveness of the CoronaVac vaccine in the elderly population during a P.1 variant-associated epidemic of COVID-19 in Brazil: A test-negative case-control study. medRxiv 2021. [Google Scholar] [CrossRef]
- Nadesalingam, A.; Cantoni, D.; Wells, D.A.; Aguinam, E.T.; Ferrari, M.; Smith, P.; Chan, A.; Carnell, G.; Ohlendorf, L.; Einhauser, S.; et al. Breadth of neutralising antibody responses to SARS-CoV-2 variants of concern is augmented by vaccination following prior infection: Studies in UK healthcare workers and immunodeficient patients. medrXiv 2021. [Google Scholar] [CrossRef]
- Shapiro, J.; Dean, N.E.; Madewell, Z.J.; Yang, Y.; Halloran, M.E.; Longini, I.M. Efficacy Estimates for Various COVID-19 Vaccines: What we Know from the Literature and Reports. medRxiv 2021. [Google Scholar] [CrossRef]
- Stamatatos, L.; Czartoski, J.; Wan, Y.-H.; Homad, L.J.; Rubin, V.; Glantz, H.; Nerdilek, M.; Seydoux, E.; Jennewein, M.F.; MacCamy, A.J.; et al. mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection. Science 2021, eabg9175. [Google Scholar] [CrossRef]
- Trinite, B.; Pradenas, E.; Marfil, S.; Rovirosa, C.; Urrea, V.; Tarres-Freixas, F.; Ortiz, R.; Rodon, J.; Veragara-Alert, J.; Segales, J.; et al. Previous SARS-CoV-2 infection increases B.1.1.7 cross-neutralization by vaccinated individuals. Viruses 2021, 13, 1135. [Google Scholar] [CrossRef]
- Leier, H.C.; Bates, T.A.; Lyski, Z.L.; McBride, S.K.; Lee, D.X.; Coulter, F.J.; Goodman, J.R.; Lu, Z.; Curlin, M.E.; Messer, W.B.; et al. Previously infected vaccinees broadly neutralize SARS-CoV-2 variants. medRxiv 2021. [Google Scholar] [CrossRef]
- Focosi, D.; Baj, A.; Maggi, F. Is a single COVID-19 vaccine dose enough in convalescents? Hum. Vaccines Immunother. 2021, 1–3. [Google Scholar] [CrossRef]
- Gallagher, K.M.E.; Leick, M.B.; Larson, R.C.; Berger, T.R.; Katsis, K.; Yam, J.Y.; Brini, G.; Grauwet, K. MGH COVID-19 Collection & Processing Team; Maus, M.V. SARS -CoV-2 T-cell immunity to variants of concern following vaccination. bioRxiv 2021. [Google Scholar] [CrossRef]
- Neidleman, J.; Luo, X.; McGregor, M.; Xie, G.; Murray, V.; Greene, W.C.; Lee, S.A.; Roan, N.R. mRNA vaccine-induced SARS-CoV-2-specific T cells recognize B.1.1.7 and B.1.351 variants but differ in longevity and homing properties depending on prior infection status. bioRxiv 2021. [Google Scholar] [CrossRef]
- Luo, G.; Hu, Z.; Letterio, J. Modeling and Predicting Antibody Durability for mRNA-1273 Vaccine for SARS-CoV-2 Variants. medRxiv 2021. [Google Scholar] [CrossRef]
- Pegu, A.; O’Connell, S.E.; Schmidt, S.D.; O’Dell, S.; Talana, C.A.; Lai, L.; Albert, J.; Anderson, E.; Bennett, H.; Corbett, K.; et al. Durability of mRNA-1273-induced antibodies against SARS-CoV-2 variants. bioRxiv 2021. [Google Scholar] [CrossRef]
- Parry, H.M.; Bruton, R.; Stephens, C.; Brown, K.; Amirthalingam, G.; Hallis, B.; Otter, A.; Zuo, J.; Moss, P. Extended interval BNT162b2 vaccination enhances peak antibody generation in older people. medRxiv 2021. [Google Scholar] [CrossRef]
- Lin, A.; Liu, J.; Ma, X.; Zhao, F.; Yu, B.; He, J.; Shen, M.; Huang, L.; Tang, H.; Jiang, E.; et al. Heterologous vaccination strategy for containing COVID-19 pandemic. medRxiv 2021. [Google Scholar] [CrossRef]
- Hillus, D.; Tober-Lau, P.; Hastor, H.; Helbig, E.T.; Lippert, L.J.; Thibeault, C.; Solarek, A.; Kalle, C.V.; Corman, V.M.; Kopankiewicz, P.; et al. Reactogenicity of homologous and heterologous prime-boost immunization with BNT162b2 and ChAdOx1-nCoV19: A prospective cohort study. medRxiv 2021. [Google Scholar] [CrossRef]
- Gross, R.; Zanoni, M.; Seidel, A.; Conzelmann, C.; Gilg, A.; Krnavek, D.; Erdemci-evin, S.; Mayer, B.; Hoffmann, M.; Poehlmann, S.; et al. Heterologous ChAdOx1 nCoV-19 and BNT162b2 prime-boost vaccination elicits potent neutralizing antibody responses and T cell reactivity. medrXiv 2021. [Google Scholar] [CrossRef]
- Barros-Martins, J.; Hammerschmidt, S.; Cossmann, A.; Odak, I.; Stankov, M.V.; Morillas Ramos, G.; Jablonka, A.; Heidemann, A.; Ritter, C.; Friedrichsen, M.; et al. Humoral and cellular immune response against SARS-CoV-2 variants following heterologous and homologous ChAdOx1 nCoV-19/BNT162b2 vaccination. medrXiv 2021. [Google Scholar] [CrossRef]
- Rees-Spear, C.; Muir, L.; Griffith, S.A.; Heaney, J.; Aldon, Y.; Snitselaar, J.; Thomas, P.; Graham, C.; Seow, J.; Lee, N.; et al. The impact of Spike mutations on SARS-CoV-2 neutralization. Cell Rep. 2021, 34, 108890. [Google Scholar] [CrossRef] [PubMed]
- Wang, P.; Nair, M.S.; Lihong, L.; Iketani, S.; Luo, Y.; Guo, Y.; Wang, M.; Yu, J.; Zhang, B.; Kwong, P.D.; et al. Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7. Nature 2021, 593, 130–135. [Google Scholar] [CrossRef] [PubMed]
- Edara, V.V.; Floyd, K.; Lai, L.; Gardner, M.; Hudson, W.; Piantadosi, A.; Waggoner, J.; Babiker, A.; Ahmed, R.; Xie, X.; et al. Infection and mRNA-1273 vaccine antibodies neutralize SARS-CoV-2 UK variant. medRxiv 2021. [Google Scholar] [CrossRef]
- Planas, D.; Bruel, T.; Grzelak, L.; Guivel-Benhassine, F.; Staropoli, I.; Porrot, F.; Planchais, C.; Buchrieser, J.; Rajah, M.M.; Bishop, E.; et al. Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies. Nat. Med. 2021, 27, 917–924. [Google Scholar] [CrossRef] [PubMed]
- Brown, J.C.; Goldhill, D.H.; Zhou, J.; Peacock, T.P.; Frise, R.; Goonawardane, N.; Baillon, L.; Kugathasan, R.; Pinto, A.; McKay, P.F.; et al. Increased transmission of SARS-CoV-2 lineage B.1.1.7 (VOC 2020212/01) is not accounted for by a replicative advantage in primary airway cells or antibody escape. BioRxiv 2021. [Google Scholar] [CrossRef]
- Bates, T.A.; Leier, H.C.; Lyski, Z.L.; McBride, S.K.; Coulter, F.J.; Weinstein, J.B.; Goodman, J.R.; Lu, Z.; Siegel, S.A.R.; Sullivan, P.; et al. Neutralization of SARS-CoV-2 variants by convalescent and vaccinated serum. medRxiv 2021. [Google Scholar] [CrossRef]
- Fenwick, C.; Turelli, P.; Pellaton, C.; Farina, A.; Campos, J.; Raclot, C.; Pojer, F.; Cagno, V.; Pantaleo, G.; Trono, D. A multiplexed high-throughput neutralization assay reveals a lack of activity against multiple variants after SARS-CoV-2 infection. medRxiv 2021. [Google Scholar] [CrossRef]
- Caniels, T.G.; Bontjer, I.; van der Straten, K.; Poniman, M.; Burger, J.A.; Appelman, B.; Lavell, A.H.A.; Oomen, M.; Godeke, G.-J.; Valle, C.; et al. Emerging SARS-CoV-2 variants of concern evade humoral immune responses from infection and vaccination. medrXiv 2021. [Google Scholar] [CrossRef]
- Wibmer, C.K.; Ayres, F.; Hermanus, T.; Madzivhandila, M.; Kgagudi, P.; Lambson, B.E.; Vermeulen, M.; van den Berg, K.; Rossouw, T.; Boswell, M.; et al. SARS-CoV-2 501Y.V2 escapes neutralization by South African COVID-19 donor plasma. Nat. Med. 2021. [Google Scholar] [CrossRef]
- Hoffmann, M.; Arora, P.; Gross, R.; Seidel, A.; Hoernich, B.; Hahn, A.; Krueger, N.; Graichen, L.; Hofmann-Winkler, H.; Kempf, A.; et al. SARS-CoV-2 variants B.1.351 and B.1.1.248: Escape from therapeutic antibodies and antibodies induced by infection and vaccination. medRxiv 2021. [Google Scholar] [CrossRef]
- Edara, V.V.; Norwood, C.; Floyd, K.; Lai, L.; Davis-Gardner, M.E.; Hudson, W.H.; Mantus, G.; Nyhoff, L.E.; Adelman, M.W.; Fineman, R.; et al. Reduced binding and neutralization of infection- and vaccine-induced antibodies to the B.1.351 (South African) SARS-CoV-2 variant. bioRxiv 2021. [Google Scholar] [CrossRef]
- Cele, S.; Gazy, I.; Jackson, L.; Hwa, S.-H.; Tegally, H.; Lustig, G.; Giandhari, J.; Pillay, S.; Wilkinson, E.; Naidoo, Y.; et al. Escape of SARS-CoV-2 501Y.V2 variants from neutralization by convalescent plasma. Nature 2021, 593, 142–146. [Google Scholar] [CrossRef]
- Riou, C.; Keeton, R.; Moyo-Gwete, T.; Hermanus, T.; Kgagudi, P.; Baguma, R.; Tegally, H.; Doolabh, D.; Iranzadeh, A.; Tyers, L.; et al. Loss of recognition of SARS-CoV-2 B.1.351 variant spike epitopes but overall preservation of T cell immunity. medrXiv 2021. [Google Scholar] [CrossRef]
- Yadav, P.D.; Sapkal, G.; Ella, R.; Sahay, R.R.; Nyayanit, D.A.; Patil, D.Y.; Deshpande, G.; Shete, A.M.; Gupta, N.; Mohan, V.K.; et al. Neutralization against B.1.351 and B.1.617.2 with sera of COVID-19 recovered cases and vaccinees of BBV152. medrXiv 2021. [Google Scholar] [CrossRef]
- Wang, P.; Wang, M.; Yu, J.; Cerutti, G.; Nair, M.S.; Huang, Y.; Kwong, P.D.; Shapiro, L.; Ho, D.D. Increased Resistance of SARS-CoV-2 Variant P.1 to Antibody Neutralization. Cell Host Microbe 2021, 29, 747–751. [Google Scholar] [CrossRef] [PubMed]
- Yadav, P.; Sapkal, G.N.; Abraham, P.; Ella, R.; Deshpande, G.; Patil, D.Y.; Nyayanit, D.; Gupta, N.; Sahay, R.R.; Shete, A.M.; et al. Neutralization of variant under investigation B.1.617 with sera of BBV152 vaccinees. Clin. Infect. Dis. 2021, ciab411. [Google Scholar] [CrossRef] [PubMed]
- Tada, T.; Zhou, H.; Dcosta, B.M.; Samanovic, M.I.; Mulligan, M.J.; Landau, N.R. The Spike Proteins of SARS-CoV-2 B.1.617 and B.1.618 Variants Identified in India Provide Partial Resistance to Vaccine-elicited and Therapeutic Monoclonal Antibodies. medRxiv 2021. [Google Scholar] [CrossRef]
- Planas, D.; Veyer, D.; Baidaliuk, A.; Staropoli, I.; Guivel-Benhassine, F.; Rajah, M.; Planchais, C.; Porrot, F.; Robillard, N.; Puech, J.; et al. Reduced sensitivity of infectious SARS-CoV-2 variant B.1.617.2 to monoclonal antibodies and sera from convalescent and vaccinated individuals. medRxiv 2021. [Google Scholar] [CrossRef]
- Hoffmann, M.; Hofmann-Winkler, H.; Krueger, N.; Kempf, A.; Nehlmeier, I.; Graichen, L.; Sidarovich, A.; Moldenhauer, A.-S.; Winkler, M.S.; Schulz, S.; et al. SARS-CoV-2 variant B.1.617 is resistant to Bamlanivimab and evades antibodies induced by infection and vaccination. medRxiv 2021. [Google Scholar] [CrossRef]
- Sapkal, G.; Yadav, P.D.; Ella, R.; Abraham, P.; Patil, D.Y.; Gupta, N.; Panda, S.; Mohan, V.K.; Bhargava, B. Neutralization of B.1.1.28 P2 variant with sera of natural SARS-CoV-2 infection and recipients of inactivated COVID-19 vaccine Covaxin. J. Travel Med. 2021, taab077. [Google Scholar] [CrossRef]
- Yadav, P.; Mohandas, S.; Sarkale, P.; Nyayanit, D.; Shete, A.; Sahay, R.; Potdar, V.; Baradkar, S.; Gupta, N.; Sapkal, G.; et al. Isolation of SARS-CoV-2 B.1.1.28.2 P2 variant and pathogenicity comparison with D614G variant in hamster model. medrXiv 2021. [Google Scholar] [CrossRef]
- McCallum, M.; Bassi, J.; De Marco, A.; Chen, A.; Walls, A.C.; Di Iulio, J.; Tortorici, M.A.; Navarro, M.-J.; Silacci-Fregni, C.; Saliba, C.; et al. SARS-CoV-2 immune evasion by variant B.1.427/B.1.429. biorXiv 2021. [Google Scholar] [CrossRef]
- Zhou, H.; Dcosta, B.M.; Samanovic, M.I.; Mulligan, M.J.; Landau, N.R.; Tada, T.B. 1.526 SARS-CoV-2 variants identified in New York City are neutralized by vaccine-elicited and therapeutic monoclonal antibodies. biorXiv 2021. [Google Scholar] [CrossRef]
- Annavajhala, M.K.; Mohri, H.; Zucker, J.E.; Sheng, Z.; Wang, P.; Gomez-Simmonds, A.; Ho, D.D.; Uhlemann, A.-C. A Novel SARS-CoV-2 Variant of Concern, B.1.526, Identified in New York. medrXiv 2021. [Google Scholar] [CrossRef]
- Thomson, E.C.; Rosen, L.E.; Shepherd, J.G.; Spreafico, R.; da Silva Filipe, A.; Wojcechowskyj, J.A.; Davis, C.; Piccoli, L.; Pascall, D.J.; Dillen, J.; et al. The circulating SARS-CoV-2 spike variant N439K maintains fitness while evading antibody-mediated immunity. Cell 2021, 184, 1171–1187. [Google Scholar] [CrossRef]
- Tang, J.; Lee, Y.; Ravichandran, S.; Grubbs, G.; Huang, C.; Stauft, C.; Wang, T.; Golding, B.; Golding, H.; Khurana, S. Reduced neutralization of SARS-CoV-2 variants by convalescent plasma and hyperimmune intravenous immunoglobulins for treatment of COVID-19. medrXiv 2021. [Google Scholar] [CrossRef]
- Graham, M.S.; Sudre, C.H.; May, A.; Antonelli, M.; Murray, B.; Varsavsky, T.; Klaser, K.; Canas, L.D.S.; Molteni, E.; Modat, M.; et al. Changes in symptomatology, reinfection, and transmissibility associated with the SARS-CoV-2 variant B.1.1.7: An ecological study. Lancet Public Health 2021, 6, e335–e345. [Google Scholar] [CrossRef]
- Coutinho, R.M.; Marquitti, F.M.D.; Ferreira, L.S.; Borges, M.E.; Silva, R.L.P.d.; Canton, O.; Portella, T.P.; Lyra, S.P.; Franco, C.; Silva, A.D.; et al. Model-based evaluation of transmissibility and reinfection for the P.1 variant of the SARS-CoV-2. medrXiv 2021. [Google Scholar] [CrossRef]
- Harrington, D.; Kele, B.; Pereira, S.; Couto-Parada, X.; Riddell, A.; Forbes, S.; Dobbie, H.; Cutino-Moguel, T. Confirmed Reinfection with SARS-CoV-2 Variant VOC-202012/01. Clin. Infect. Dis. 2021, ciab0. [Google Scholar] [CrossRef]
- Zucman, N.; Uhel, F.; Descamps, D.; Roux, D.; Ricard, J.D. Severe reinfection with South African SARS-CoV-2 variant 501Y.V2: A case report. Clin. Infect. Dis. 2021, ciab129. [Google Scholar] [CrossRef]
- Naveca, F.; da Costa, C.; Nascimento, V.; Souza, V.; Corado, A.; Nascimento, F.; Costa, A.; Duarte, D.; Silva, G.; Mejía, M.; et al. SARS-CoV-2 Reinfection by the New Variant of Concern (VOC) P.1 in Amazonas, Brazil. Available online: https://virological.org/t/sars-cov-2-reinfection-by-the-new-variant-of-concern-voc-p-1-in-amazonas-brazil/596 (accessed on 27 January 2021).
- Resende, P.; Bezerra, J.; de Vasconcelos, R.; Arantes, I.; Appolinario, L.; Mendonça, A.; Paixao, A.; Duarte Rodrigues, A.; Silva, T.; Rocha, A.; et al. Spike E484K mutation in the first SARS-CoV-2 reinfection case confirmed in Brazil. 2020. Available online: https://virological.org/t/spike-e484k-mutation-in-the-first-sars-cov-2-reinfection-case-confirmed-in-brazil-2020/584 (accessed on 17 June 2021).
- Nonaka, C.; Miranda Franco, M.; Gräf, T.; Mendes, A.V.A.; de Aguiar, R.S.; Giovanetti, M.; Solano de Freitas Souza, B. Genomic Evidence of a Sars-Cov-2 Reinfection Case with E484K Spike Mutation in Brazil. Emerg. Infect. Dis. 2021, 27. [Google Scholar] [CrossRef]
- Wang, R.; Zhang, Q.; Ge, J.; Ren, W.; Zhang, R.; Lan, J.; Ju, B.; Su, B.; Yu, F.; Chen, P.; et al. Spike mutations in SARS-CoV-2 variants confer resistance to antibody neutralization. biorXiv 2021. [Google Scholar] [CrossRef]
- Liu, H.; Wei, P.; Zhang, Q.; Chen, Z.; Aviszus, K.; Downing, W.; Peterson, S.; Reynoso, L.; Downey, G.; Frankel, S.; et al. 501Y.V2 and 501Y.V3 variants of SARS-CoV-2 lose binding to Bamlanivimab in vitro. MAbs 2021, 13, 1919285. [Google Scholar] [CrossRef]
- Widera, M.; Wilhelm, A.; Hoehl, S.; Pallas, C.; Kohmer, N.; Wolf, T.; Rabenau, H.F.; Corman, V.M.; Drosten, C.; Vehreschild, M.J. Bamlanivimab does not neutralize two SARS-CoV-2 variants carrying E484K in vitro. medrXiv 2021. [Google Scholar] [CrossRef]
- Zhang, L.; Huynh, T.; Luan, B. In silico Assessment of Antibody Drug Resistance to Bamlanivimab of SARS-CoV-2 Variant B.1.617. medrXiv 2021. [Google Scholar] [CrossRef]
- Starr, T.N.; Greaney, A.J.; Dingens, A.S.; Bloom, J.D. 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, 100255. [Google Scholar] [CrossRef] [PubMed]
- Westendorf, K.; Žentelis, S.; Foster, D.; Vaillancourt, P.; Wiggin, M.; Lovett, E.; Hendle, J.; Pustilnik, A.; Sauder, J.M.; Kraft, L.; et al. LY-CoV1404 potently neutralizes SARS-CoV-2 variants. biorXiv 2021. [Google Scholar] [CrossRef]
- Lee, S.-Y.; Ryu, D.-K.; Choi, Y.K.; Moore, P.; Baalen, C.A.V.; Song, R.; Tijsma, A.S.; Gwete-Moyo, T.; Kim, M.; Kim, Y.-I.; et al. Therapeutic effect of CT-P59 against SARS-CoV-2 South African variant. medrXiv 2021. [Google Scholar] [CrossRef]
- Cathcart, A.L.; Havenar-Daughton, C.; Lempp, F.A.; Ma, D.; Schmid, M.; Agostini, M.L.; Guarino, B.; Di iulio, J.; Rosen, L.; Tucker, H.; et al. The dual function monoclonal antibodies VIR-7831 and VIR-7832 demonstrate potent in vitro and in vivo activity against SARS-CoV-2. medrXiv 2021. [Google Scholar] [CrossRef]
- Becker, M.; Dulovic, A.; Junker, D.; Ruetalo, N.; Kaiser, P.; Pinilla, Y.; Heinzel, C.; Haering, J.; Traenkle, B.; Wagner, T.; et al. Immune response to SARS-CoV-2 variants of concern in vaccinated individuals. Nat. Commun. 2021, 12, 3109. [Google Scholar] [CrossRef]
- Xie, X.; Liu, Y.; Liu, J.; Zhang, X.; Zou, J.; Fontes-Garfias, C.R.; Xia, H.; Swanson, K.A.; Cutler, M.; Cooper, D. Neutralization of spike 69/70 deletion, E484K, and N501Y SARS-CoV-2 by BNT162b2 vaccine-elicited sera. Nat. Med. 2021, 27, 620–621. [Google Scholar] [CrossRef]
- Tada, T.; Dcosta, B.M.; Samanovic-Golden, M.; Herati, R.S.; Cornelius, A.; Mulligan, M.J.; Landau, N.R. Neutralization of viruses with European, South African, and United States SARS-CoV-2 variant spike proteins by convalescent sera and BNT162b2 mRNA vaccine-elicited antibodies. biorXiv 2021. [Google Scholar] [CrossRef]
- Kuzmina, A.; Khalaila, Y.; Voloshin, O.; Keren-Naus, A.; Bohehm, L.; Raviv, Y.; Shemer-Avni, Y.; Rosenberg, E.; Taube, R. SARS CoV-2 escape variants exhibit differential infectivity and neutralization sensitivity to convalescent or post-vaccination sera. Cell Host Microbe 2021, 29, 522–528. [Google Scholar] [CrossRef]
- Gonzalez, C.; Saade, C.; Bal, A.; Valette, M.; Saker, K.; Lina, B.; Josset, L.; Trabaud, M.-A.; Thiery, G.; Botelho-Nevers, E.; et al. Live virus neutralization testing in convalescent and vaccinated subjects against 19A, 20B, 20I/501Y.V1 and 20H/501.V2 isolates of SARS-CoV-2. medrXiv 2021. [Google Scholar] [CrossRef]
- Liu, J.; Bodnar, B.H.; Wang, X.; Wang, P.; Meng, F.; Khan, A.I.; Saribas, A.S.; Padhiar, N.H.; McCluskey, E.; Shah, S.; et al. Correlation of vaccine-elicited antibody levels and neutralizing activities against SARS-CoV-2 and its variants. biorXiv 2021. [Google Scholar] [CrossRef]
- Garcia-Beltran, W.F.; Lam, E.C.; Denis, K.S.; Nitido, A.D.; Garcia, Z.H.; Hauser, B.M.; Feldman, J.; Pavlovic, M.N.; Gregory, D.J.; Poznansky, M.C.; et al. Multiple SARS-CoV-2 variants escape neutralization by vaccine-induced humoral immunity. Cell 2021, 184, 2372–2383. [Google Scholar] [CrossRef]
- Mohsen, M.; Bachmann, M.F.; Vogel, M.; Augusto, G.S.; Liu, X.; Chang, X. BNT162b2 mRNA COVID-19 vaccine induces antibodies of broader cross-reactivity than natural infection but recognition of mutant viruses is up to 10-fold reduced. Allergy 2021. [Google Scholar] [CrossRef]
- Stankov, M.; Cossmann, A.; Bonifacius, A.; Jablonka, A.; Morillas Ramos, G.; Goedecke, N.; Zychlinsky Scharff, A.; Happle, C.; Boeck, A.-L.; Tran, A.T.; et al. Humoral and cellular immune responses against SARS-CoV-2 variants and human coronaviruses after single BNT162b2 vaccination. medrXiv 2021. [Google Scholar] [CrossRef]
- Strengert, M.; Becker, M.; Ramos, G.M.; Dulovic, A.; Gruber, J.; Juengling, J.; Lürken, K.; Beigel, A.; Wrenger, E.; Lonnemann, G.; et al. Cellular and humoral immunogenicity of a SARS-CoV-2 mRNA vaccine in patients on hemodialysis. medrXiv 2021. [Google Scholar] [CrossRef]
- Abu-Raddad, L.J.; Chemaitelly, H.; Butt, A.A. Effectiveness of the BNT162b2 Covid-19 Vaccine against the B.1.1.7 and B.1.351 Variants. N. Engl. J. Med. 2021. [Google Scholar] [CrossRef]
- Xie, X.; Zou, J.; Fontes-Garfias, C.R.; Xia, H.; Swanson, K.A.; Cutler, M.; Cooper, D.; Menachery, V.D.; Weaver, S.D.; Dormitzer, P.R.; et al. Neutralization of N501Y mutant SARS-CoV-2 by BNT162b2 vaccine-elicited sera. biorXiv 2021. [Google Scholar] [CrossRef]
- Collier, D.; Meng, B.; Ferreira, I.; Datir, R.; Temperton, N.J.; Elmer, A.; Graves, B.; Kingston, N.; McCoy, L.; Smith, K.; et al. Impact of SARS-CoV-2 B.1.1.7 Spike variant on neutralisation potency of sera from individuals vaccinated with Pfizer vaccine BNT162b2. medrXiv 2021. [Google Scholar] [CrossRef]
- Muik, A.; Wallisch, A.-K.; Saenger, B.; Swanson, K.A.; Muehl, J.; Chen, W.; Cai, H.; Sarkar, R.; Tuereci, O.; Dormitzer, P.R.; et al. Neutralization of SARS-CoV-2 lineage B.1.1.7 pseudovirus by BNT162b2 vaccine-elicited human sera. Science 2021, 371, 1152–1153. [Google Scholar] [CrossRef]
- Lumley, S.F.; Rodger, G.; Constantinides, B.; Sanderson, N.; Chau, K.K.; Street, T.L.; O’Donnell, D.; Howarth, A.; Hatch, S.B.; Marsden, B.D.; et al. An observational cohort study on the incidence of SARS-CoV-2 infection and B.1.1.7 variant infection in healthcare workers by antibody and vaccination status. medrXiv 2021. [Google Scholar] [CrossRef]
- Lopez Bernal, J.; Andrews, N.; Gower, C.; Gallagher, E.; Simmons, R.; Thelwall, S.; Tessier, E.; Groves, N.; Dabrera, G.; Myers, R.; et al. Effectiveness of COVID-19 vaccines against the B.1.617.2 variant. medRxiv 2021. [Google Scholar] [CrossRef]
- Dejnirattisai, W.; Zhou, D.; Supasa, P.; Liu, C.; Mentzer, A.J.; Ginn, H.; Zhao, Y.; Duyvesteyn, H.M.E.; Tuekprakhon, A.; Nutalai, R.; et al. Antibody evasion by the Brazilian P.1 strain of SARS-CoV-2. medrXiv 2021. [Google Scholar] [CrossRef]
- Ferreira, I.; Datir, R.; Papa, G.; Kemp, S.; Meng, B.; Rakshit, P.; Singh, S.; Pandey, R.; Ponnusamy, K.; Radhakrishnan, V.S.; et al. SARS-CoV-2 B.1.617 emergence and sensitivity to vaccine-elicited antibodies. medrXiv 2021. [Google Scholar] [CrossRef]
- Edara, V.-V.; Lai, L.; Sahoo, M.; Floyd, K.; Sibai, M.; Solis, D.; Flowers, M.W.; Hussaini, L.; Ciric, C.R.; Bechnack, S.; et al. Infection and vaccine-induced neutralizing antibody responses to the SARS-CoV-2 B.1.617.1 variant. biorXiv 2021. [Google Scholar] [CrossRef]
- Shi, P.-Y.; Liu, J.; Liu, Y.; Xia, H.; Zou, J.; Weaver, S.; Swanson, K.; Cai, H.; Cutler, M.; Cooper, D.; et al. Neutralization of SARS-CoV-2 variants B.1.617.1 and B.1.525 by BNT162b2-elicited sera. Res. Sq. 2021. [Google Scholar] [CrossRef]
- Wu, K.; Werner, A.P.; Moliva, J.I.; Koch, M.; Choi, A.; Narayanan, E.; Stewart-Jones, G.B.E.; Colpitts, T.; Bennett, H.; Boyoglu-Barnum, S.; et al. Serum Neutralizing Activity Elicited by mRNA-1273 Vaccine. N. Engl. J. Med. 2021, 384, 1468–1470. [Google Scholar] [CrossRef]
- Corbett, K.S.; Werner, A.; O’Connell, S.; Gagne, M.; Lai, L.; Moliva, J.I.; Flynn, B.; Choi, A.; Koch, M.; Foulds, K.E.; et al. Evaluation of mRNA-1273 against SARS-CoV-2 B.1.351 Infection in Nonhuman Primates. biorXiv 2021. [Google Scholar] [CrossRef]
- Edara, V.V.; Hudson, W.H.; Xie, X.; Ahmed, R.; Suthar, M.S. Neutralizing Antibodies Against SARS-CoV-2 Variants After Infection and Vaccination. JAMA 2021, 325, 1896–1898. [Google Scholar] [CrossRef]
- Shen, X.; Tang, H.; McDana, C.; Wagh, K.; Fischer, W.; Theiler, J.; Yoon, H.; Li, D.; Haynes, B.F.; Sanders, K.O.; et al. SARS-CoV-2 variant B.1.1.7 is susceptible to neutralizing antibodies elicited by ancestral Spike vaccines. Cell Host Microbe 2021, 29, 529–539. [Google Scholar] [CrossRef]
- Madhi, S.A.; Baillie, V.; Cutland, C.L.; Voysey, M.; Koen, A.L.; Fairlie, L.; Padayachee, S.D.; Dheda, K.; Barnabas, S.L.; Bhorat, Q.E.; et al. Efficacy of the ChAdOx1 nCoV-19 Covid-19 Vaccine against the B.1.351 Variant. N. Engl. J. Med. 2021. [Google Scholar] [CrossRef]
- Fischer, R.; van Doremalen, N.; Adney, D.; Yinda, C.K.; Port, J.R.; Holbrook, M.G.; Schulz, J.E.; Williamson, B.N.; Thomas, T.; Barbian, K.; et al. ChAdOx1 nCoV-19 (AZD1222) protects against SARS-CoV-2 B.1.351 and B.1.1.7. biorXiv 2021. [Google Scholar] [CrossRef]
- Yadav, P.; Sapkal, G.N.; Abraham, P.; Deshpande, G.; Nyayanit, D.A.; Patil, D.Y.; Gupta, N.; Sahay, R.R.; Shete, A.M.; Kumar, S.; et al. Neutralization potential of Covishield vaccinated individuals against B.1.617.1. Clin. Infect. Dis. 2021, ciab483. [Google Scholar] [CrossRef]
- Ikegame, S.; Siddiquey, M.N.A.; Hung, C.-T.; Haas, G.; Brambilla, L.; Oguntunyo, K.Y.; Kowdle, S.; Vilardo, A.E.; Edelstein, A.; Perandones, C.; et al. Qualitatively distinct modes of Sputnik V vaccine-neutralization escape by SARS-CoV-2 Spike variants. medrXiv 2021. [Google Scholar] [CrossRef]
- Shinde, V.; Bhikha, S.; Hossain, Z.; Archary, M.; Bhorat, Q.; Fairlie, L.; Lalloo, U.; Masilela, M.S.L.; Moodley, D.; Hanley, S.; et al. Efficacy of NVX-CoV2373 Covid-19 Vaccine against the B.1.351 Variant. N. Engl. J. Med. 2021, 384, 1899–1909. [Google Scholar] [CrossRef]
- Sapkal, G.N.; Yadav, P.; Ella, R.; Deshpande, G.R.; Sahay, R.R.; Gupta, N.; Mohan, V.K.; Abraham, P.; Panda, S.; Bhargava, B. Neutralization of UK-variant VUI-202012/01 with COVAXIN vaccinated human serum. medrXiv 2021. [Google Scholar] [CrossRef]
- Chen, Y.; Shen, H.; Huang, R.; Tong, X.; Wu, C. Serum neutralising activity against SARS-CoV-2 variants elicited by CoronaVac. Lancet Infect. Dis. 2021. [Google Scholar] [CrossRef]
- Moore, P.; Moyo, T.; Hermanus, T.; Kgagudi, P.; Ayres, F.; Makhado, Z.; Sadoff, J.; Le Gars, M.; van Roey, G.; Crowther, C.; et al. Neutralizing antibodies elicited by the Ad26.COV2.S COVID-19 vaccine show reduced activity against 501Y.V2 (B.1.351), despite protection against severe disease by this variant. biorXiv 2021. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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
Focosi, D.; Tuccori, M.; Baj, A.; Maggi, F. SARS-CoV-2 Variants: A Synopsis of In Vitro Efficacy Data of Convalescent Plasma, Currently Marketed Vaccines, and Monoclonal Antibodies. Viruses 2021, 13, 1211. https://doi.org/10.3390/v13071211
Focosi D, Tuccori M, Baj A, Maggi F. SARS-CoV-2 Variants: A Synopsis of In Vitro Efficacy Data of Convalescent Plasma, Currently Marketed Vaccines, and Monoclonal Antibodies. Viruses. 2021; 13(7):1211. https://doi.org/10.3390/v13071211
Chicago/Turabian StyleFocosi, Daniele, Marco Tuccori, Andreina Baj, and Fabrizio Maggi. 2021. "SARS-CoV-2 Variants: A Synopsis of In Vitro Efficacy Data of Convalescent Plasma, Currently Marketed Vaccines, and Monoclonal Antibodies" Viruses 13, no. 7: 1211. https://doi.org/10.3390/v13071211
APA StyleFocosi, D., Tuccori, M., Baj, A., & Maggi, F. (2021). SARS-CoV-2 Variants: A Synopsis of In Vitro Efficacy Data of Convalescent Plasma, Currently Marketed Vaccines, and Monoclonal Antibodies. Viruses, 13(7), 1211. https://doi.org/10.3390/v13071211