Twelve-month anti-SARS-CoV-2 antibody kinetics in COVID-19 patients from Bejaia, Algeria
The COVID-19 pandemic has highlighted the importance of understanding long-term humoral immunity after SARS-CoV-2 infection. This study evaluated the kinetics and persistence of anti-SARS-CoV-2 immunoglobulin M (IgM) and immunoglobulin G (IgG) antibodies in hospitalized patients who recovered and identified factors associated with antibody responses. A total of 96 patients hospitalized with real-time polymerase chain reaction-confirmed COVID-19 between June and September 2020 were included. Sequential serum samples were collected up to 365 days after symptom onset. Anti-SARS-CoV-2 IgM and IgG antibodies targeting spike (S) and nucleocapsid (N) proteins were evaluated on days 28, 90, 180, and 365 using chemiluminescent immunoassay (MAGLUMI). Clinical, epidemiological, and radiological data were analyzed. All convalescent patients developed detectable IgG antibodies, and 92.7% were IgG seropositive. Antibody titers and seropositivity rates declined over time; however, IgG antibodies remained more stable and persisted throughout the 12-month follow-up, whereas IgM antibodies became undetectable in most cases. Nevertheless, 12.5% of patients still had detectable IgM antibodies one year after symptom onset, whereas IgG seropositivity remained above 70%. Higher IgG titers were significantly associated with age ≥ 50 years, severe COVID-19, and SARS-CoV-2 pneumonia. Patients vaccinated before the final follow-up demonstrated a strong booster response with significantly higher IgG levels than unvaccinated individuals. In conclusion, symptomatic COVID-19 induces a durable humoral immune response that persists for at least 12 months. Hybrid immunity resulting from natural infection combined with vaccination appears to provide the strongest protection against SARS-CoV-2.
- Siddiquea BN, Shetty A, Bhattacharya O, Afroz A, Billah B. Global epidemiology of COVID-19 knowledge, attitude and practice: a systematic review and meta-analysis. BMJ Open. 2021;11(9):e051447. doi: 10.1136/bmjopen-2021-051447
- Isho B, Abe KT, Zuo M, et al. Persistence of serum and saliva antibody responses to sars-Cov-2 spike antigens in covid-19 patients. Sci Immunol. 2020;5(52):eabe5511. doi: 10.1126/sciimmunol.abe5511
- Atyeo C, Fischinger S, Zohar T, et al. Distinct early serological signatures track with SARS-CoV-2 survival. Immunity. 2020;53(3):524–532.e4. doi: 10.1016/j.immuni.2020.07.020
- Gaebler C, Wang Z, Lorenzi JCC, et al. Tokuyama M. Evolution of antibody immunity to SARS-CoV-2. Nature. 2021;591(7851):639–644. doi: 10.1038/s41586-021-03207-w
- Iyer AS, Jones FK, Nodoushani A, et al. Persistence and decay of human antibody responses to the receptor binding domain of SARS-CoV-2 spike protein in COVID-19 patients. Sci Immunol. 2020;5(52). doi: 10.1126/sciimmunol.abe0367
- Chang CK, Hou MH, Chang CF, Hsiao CD, Huang TH. The SARS coronavirus nucleocapsid protein--forms and functions. Antiviral Res. 2014;103:39-50. doi: 10.1016/j.antiviral.2013.12.009.
- Ibarrondo FJ, Fulcher JA, Goodman-Meza D, et al. Rapid decay of anti–SARS-CoV-2 antibodies in persons with mild COVID-19. N Engl J Med. 2020;383(11):1085–1087. doi: 10.1056/NEJMc2025179
- Anand SP, Prevost J, Nayrac M, et al. Longitudinal analysis of humoral immunity against SARS-CoV-2 Spike in convalescent individuals up to eight months post-symptom onset. Cell Rep Med. 2021;2(6):100290. doi: 10.1016/j.xcrm.2021.100290
- Wajnberg A, Amanat F, Firpo A, et al. Robust neutralizing antibodies to SARS-CoV-2 infection persist for months. Science. 2020;370(6521):1227–1230. doi: 10.1126/science.abd7728
- Davies NG, Abbott S, Barnard RC, et al. Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science. 2021:372(6538). doi: 10.1126/science.abg3055
- Hu J, Peng P, Wang K, et al. Emerging SARS-CoV-2 variants reduce neutralization sensitivity to convalescent sera and monoclonal antibodies. Cell Mol Immunol. 2021;18(4):1061– 1063. doi: 10.1038/s41423-021-00648-1
- Sabino EC, Buss LF, Carvalho MPS, et al. Resurgence of COVID-19 in Manaus, Brazil, despite high seroprevalence. Lancet. 2021;397(10273):452–455. doi: 10.1016/S0140-6736(21)00183-5
- Tegally H, Wilkinson E, Giovanetti M, et al. Detection of a SARS-CoV-2 variant of concern in South Africa. Nature. 2021;592(7854):438–443. doi: 10.1038/s41586-021-03402-9
- Dumache R, Enache A, Macasoi I, et al. Sars-Cov-2: An overview of the genetic profile and vaccine effectiveness of the five variants of concern. Pathogens. 2022;11(5):516. doi: 10.3390/pathogens11050516.
- Folegatti PM, Ewer KJ, Aley PK, et al. Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trial. Lancet. 2020;396(10249):467–78. doi: 10.1016/S0140-6736(20)31604-4
- Wang H, Zhang Y, Huang B, et al. Development of an Inactivated Vaccine Candidate, BBIBP-CorV, with Potent Protection against SARS-CoV-2. Cell. 2020;182(3):713–21 e9. Epub 2020/08/12. doi: 10.1016/j.cell.2020.06.008
- Zhu FC, Guan XH, Li YH, et al. Immunogenicity and safety of a recombinant adenovirus type-5-vectored COVID-19 vaccine in healthy adults aged 18 years or older: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet. 2020;396(10249):479–88. doi: 10.1016/S0140-6736(20)31605-6
- Theel ES, Slev P, Wheeler S, et al. The Role of Antibody Testing for SARS-CoV-2: Is There One? J Clin Microbiol. 2020;58(8). doi: 10.1128/JCM.00797-20
- Kissler SM, Tedijanto C, Goldstein E, Grad YH, Lipsitch M, Projecting the transmission dynamics of SARS-CoV-2 through the post-pandemic period. Science. 368(6493), 860–868 (2020). doi: 10.1126/science.abb5793
- Dobaño C, Ramírez-Morros A, Alonso S. et al. Sustained seropositivity up to 20.5 months after COVID-19. BMC Med 20(1), 379 (2022). doi: 10.1186/s12916-022-02570-3
- Gallais F, Gantner P, Bruel T, et al. Evolution of antibody responses up to 13 months after sars-Cov-2 infection and risk of reinfection. EBioMedicine (2021) 71:103561. doi: 10.1016/j.ebiom.2021.103561
- Štěpánek L, Janošíková M, Štěpánek L, Nakládalová M, Boriková A. The kinetics and predictors of anti-SARS-CoV-2 antibodies up to 8 months after symptomatic COVID-19: A Czech cross-sectional study. J Med Virol. 2022 Aug;94(8):3731-3738. doi: 10.1002/jmv.27784
- Van Elslande J, Oyaert M, Lorent N, et al. Lower persistence of anti-nucleocapsid compared to anti-spike antibodies up to one year after SARS-CoV-2 infection. Diagn Microbiol Infect Dis. 2022;103(1):115659. doi: 10.1016/j.diagmicrobio.2022.115659
- Dehgani-Mobaraki P, Zaidi AK, Yadav N, Floridi A, Floridi E. Longitudinal observation of antibody responses for 14 months after SARS-CoV-2 infection. Clin. Immunol. 2021;230:108814. doi: 10.1016/j.clim.2021.108814
- Zhu L, Xu X, Zhu B, et al. Kinetics of SARS-CoV-2 Specific and Neutralizing Antibodies over Seven Months after Symptom Onset in COVID-19 Patients. Microbiol Spectr. 2021;9(2):e0059021. doi: 10.1128/Spectrum.00590-21
- Luo H, Camilleri D, Garitaonandia I, et al. Kinetics of anti-SARS-CoV-2 IgG antibody levels and potential influential factors in subjects with COVID-19: A 11-month follow-up study. Diagn Microbiol Infect Dis. 2021;101(4):115537. doi: 10.1016/j.diagmicrobio.2021.115537
- Chansaenroj J, Yorsaeng R, Puenpa J, et al. Long-term persistence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike protein-specific and neutralizing antibodies in recovered COVID-19 patients. PLoS ONE. 2022;17(4):e0267102. doi: 10.1371/journal.pone.0267102
- Masiá M, Fernández-González M, Telenti G, et al. Durable antibody response one year after hospitalization for COVID-19: A longitudinal cohort study. J Autoimmun. 2021;123:102703. doi: 10.1016/j.jaut.2021.102703
- Rosati M, Terpos E, Ntanasis-Stathopoulos I, et al. Sequential analysis of binding and neutralizing antibody in COVID-19 convalescents patients at 14 Months after SARS-CoV-2 infection. Front. Immunol. 2021;12:793953. doi: 10.3389/fimmu.2021.793953
- Choe PG, Kang CK, Kim KH, et al. Persistence of Neutralizing Antibody Response up to 1 Year After Asymptomatic or Symptomatic SARS-CoV-2 Infection. J Infect Dis. 2021;224(6):1097-1099. doi: 10.1093/infdis/jiab339
- Li C, Yu D, Wu X, et al. Twelve-month specific igg response to sars-Cov-2 receptor-binding domain among covid-19 convalescent plasma donors in wuhan. Nat Commun 2021;12(1):4144. doi: 10.1038/s41467-021-24230-5
- Zuanich C, Garcia Rosolen N, Olmos Vargas P, Arévalo D, Donati P, Balbaryski J. SARS-CoV-2 antibodies kinetics in hospitalized patients. 82(1): 3-12. Accessed May 13, 2023. http://www.scielo.org.ar/scielo.php?script=sci_ arttext&pid=S0025-76802022000100003&lng=es.
- Hansen CH, Michlmayr D, Gubbels SM, Molbak K, Ethelberg S. Assessment of protection against reinfection with SARS-CoV-2 among 4 million PCR-tested individuals in Denmark in 2020: a population-level observational study. Lancet. 2021;397(10280):1204-12. doi: 10.1016/S0140-6736(21)00575-4
- Capetti AF, Borgonovo F, Mileto D, et al. One-year durability of anti-spike IgG to SARS-CoV-2: Preliminary data from the anticrown prospective observational study one year durability of COVID-19 anti-spike IgG. J Infect. 2021;83(2):237-279. doi: 10.1016/j.jinf.2021.05.023
- Li Y, Wang X, Shen XR, et al. A 1-year longitudinal study on COVID-19 convalescents reveals persistence of anti-SARS-CoV-2 humoral and cellular immunity. Emerg Microbes Infect. 2022;11(1):902-913. doi: 10.1080/22221751.2022.2049984
- Alter G, Seder R. The Power of Antibody-Based Surveillance. N Engl J Med. 2020;383(18):1782-1784. doi: 10.1056/NEJMe2028079
- Ponde RAA. Serological markers of acute infection by hepatitis A, B, C, D, E and G viruses revisited. Arch Virol. 2017; 162 (12):3587–3602. doi: 10.1007/s00705-017-3538-3.
- Muecksch F, Wise H, Batchelor B, et al. Longitudinal analysis of clinical serology assay performance and neutralising antibody levels in COVID19 convalescents. medRxiv. 2020. doi: 10.1101/2020.08.05.20169128
- Dan JM, Mateus J, Kato Y, et al. Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection. Science. 2021;371(6529) doi: 10.1126/science.abf4063
- Terpos E, Stellas D, Rosati M, et al. Sars-Cov-2 antibody kinetics eight months from covid-19 onset: Persistence of spike antibodies but loss of neutralizing antibodies in24% of convalescent plasma donors. Eur J Internal Med. 2021;89:87–96. doi: 10.1016/j.ejim.2021.05.010.
- Gudbjartsson DF, Norddahl GL, Melsted P, et al. Humoral Immune Response to SARS-CoV-2 in Iceland. N Engl J Med. 2020;383(18):1724-1734. doi: 10.1056/NEJMoa2026116 42
- Zeng F, Wu M, Wang J, Li J, Hu G, Wang L. Over 1-year duration and age difference of SARS-CoV-2 antibodies in convalescent COVID-19 patients. J Med Virol. 2021;93(12):6506-6511. doi: 10.1002/jmv.27152
- Lu Z, Laing ED, Pena DaMata J, et al. Durability of SARS-CoV-2-specific T cell responses at 12-months post-infection. J Infect Dis. 2021;224(12):2010-2019. doi: 10.1093/infdis/jiab543
- Zhang J, Lin H, Ye B, et al. One-year sustained cellular and humoral immunities of COVID-19 convalescents. Clin Infect Dis. 2021;75(1):e1072-e1081. doi: 10.1093/cid/ciab884
- Xiao K, Yang H, Liu B, et al. Antibodies can last for more than 1 year after SARS-CoV-2 infection: A follow-up study from survivors of COVID-19. Front Med. 2021;8 doi: 10.3389/fmed.2021.684864
- Murray K, Garcia M, Yan C, Gorchakov R. Persistence of Detectable Immunoglobulin M Antibodies Up to 8 Years After Infection with West Nile Virus. Am J Trop Med Hyg. 2013;89(5):996–1000. doi: 10.4269/ajtmh.13-0232
- Seow J, Graham C, Merrick B, et al. Longitudinal observation and decline of neutralizing antibody responses in the three months following sars-Cov-2 infection in humans. Nat Microbiol. 2020;5(12):1598–607. doi: 10.1038/s41564-020-00813-8
- Assaid N, Arich S, Charoute H, et al. Kinetics of SARS-CoV-2 IgM and IgG Antibodies 3 Months after COVID-19 Onset in Moroccan Patients. Am J Trop Med Hyg. 2022;108(1):145-154. doi: 10.4269/ajtmh.22-0448
- Gudbjartsson DF, Norddahl GL, Melsted P, et al. Humoral immune response to SARS-CoV-2 in Iceland. N Engl J Med. 2020;383(18):1724-1734. doi: 10.1056/NEJMoa2026116
- Peng J, Liu ZY, Yu XJ, et al. Antibody response in COVID-19 patients with and without re-positive RT-PCR results during the convalescent phase. Arch Virol. 2021;166(8):2299-2303. doi: 10.1007/s00705-021-05132-9
- Zhan Y, Zhu Y, Wang S, et al. Sars-Cov-2 immunity and functional recovery of covid-19 patients 1-year after infection. Signal Transduct Target Ther. 2021;6(1):368. doi: 10.1038/s41392-021-00777-z
- Zhou ZH, Dharmarajan S, Lehtimaki M, Kirshner SL, Kozlowski S, Subbarao K. Early antibody responses associated with survival in Covid19 patients. PloS Pathog. 2021;17(7):e1009766. doi: 10.1371/journal.ppat.1009766
- Klein SL, Pekosz A, Park HS, et al. Sex, age, and hospitalization drive antibody responses in a covid-19 convalescent plasma donor population. J Clin Invest. 2020;130(11):6141–50. doi: 10.1172/jci142004
- De Silvestro G, Marson P, La Raja M, et al. Outcome of sarscov-2 in patients treated with convalescent plasma: One-year of data from the veneto region (Italy) registry. Eur J Intern Med. 2022;97:42–9. doi: 10.1016/j.ejim.2021.12.023
- Choe PG, Kim KH, Kang CK, et al. Antibody Responses 8 Months after Asymptomatic or Mild SARS-CoV-2 Infection. Emerg Infect Dis. 2021;27(3):928-931. doi: 10.3201/eid2703.204543
- Bal A, Trabaud MA, Fassier JB, et al. Six-month antibody response to SARS-CoV-2 in healthcare workers assessed by virus neutralization and commercial assays. Clin Microbiol Infect. 2021;27(6):933-935. doi: 10.1016/j.cmi.2021.01.003
- Xiang F, Wang X, He X, et al. Antibody Detection and Dynamic Characteristics in Patients With Coronavirus Disease 2019. Clin Infect Dis. 2020;71(8):1930-1934. doi: 10.1093/cid/ciaa461
- Feng C, Shi J, Fan Q, et al. Protective humoral and cellular immune responses to sars-Cov-2 persist up to 1 year after recovery. Nat Commun. 2021;12(1):4984. doi: 10.1038/s41467-021-25312-0
- Chao YX, Rötzschke O, Tan EK. The role of iga in covid-19. Brain Behav Immun. 2020;87:182–3. doi: 10.1016/j.bbi.2020.05.057
- Jiang S, Hillyer C, Du L. Neutralizing antibodies against SARS-CoV-2 and other human coronaviruses. Trends Immunol. 2020;41(5):355–359. doi: 10.1016/j.it.2020.03.007
- Wu LP, Wang NC, Chang YH, et al. Duration of antibody responses after severe acute respiratory syndrome. Emerg Infect Dis. 2007;13(10):1562. doi: 10.3201/eid1310.070576
- Mo H, Zeng G, Ren X, et al. Longitudinal profile of antibodies against SARS-coronavirus in SARS patients and their clinical significance. Respirology. 2006;11(1): 49–53. doi: 10.1111/j.1440-1843.2006.00783.x
- Long QX, Tang XJ, Shi QL, et al. Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections. Nat Med. 2020;26(8):1200–1204. doi: 10.1038/s41591-020-0965-6
- Wang X, Guo X, Xin Q, et al. Neutralizing Antibody Responses to Severe Acute Respiratory Syndrome Coronavirus 2 in Coronavirus Disease 2019 Inpatients and Convalescent Patients. Clin Infect Dis. 2020;71(10):2688-2694. doi: 10.1093/cid/ciaa721
- Liu A, Wang W, Zhao X, et al. Disappearance of antibodies to SARS-CoV-2 in a -COVID-19 patient after recovery. Clin Microbiol Infect. 2020;26(12):1703-1705. doi: 10.1016/j.cmi.2020.07.009
- Achiron A, Gurevich M, Falb R, Dreyer-Alster S, Sonis P, Mandel M. SARS-CoV-2 antibody dynamics and B-cell memory response over time in COVID-19 convalescent subjects. Clin Microbiol Infect. 2021;27(9):1349.e1-1349.e6. doi: 10.1016/j.cmi.2021.05.008
- Korte W, Buljan M, Rösslein M, et al. SARS-CoV-2 IgG and IgA antibody response is gender dependent; and IgG antibodies rapidly decline early on. J Infect. 2021;82(1):e11-e14. doi: 10.1016/j.jinf.2020.08.032
- Nag DS, Chaudhry R, Mishra M, Rai S, Gupta M. A Prospective Study on Rapidly Declining SARS-CoV-2 IgG Antibodies Within One to Three Months of Testing IgG Positive: Can It Lead to Potential Reinfections?. Cureus. 2020;12(12):e11845. doi: 10/7759/cureus.11845
- Long QX, Liu BZ, Deng HJ, et al. Antibody responses to SARS-CoV-2 in patients with COVID-19. NatMed. 2020;26(6):845-848. doi: 10.1038/s41591-020-0897-1
- Van Elslande J, Gruwier L, Godderis L, Vermeersch P. Estimated Half-Life of SARS-CoV-2 Anti-Spike Antibodies More Than Double the Half-Life of Anti-nucleocapsid Antibodies in Healthcare Workers. Clin Infect Dis. 2021;73(12):2366-2368. doi: 10.1093/cid/ciab219
- Ojeda DS, Gonzalez Lopez Ledesma MM, Pallarés HM, et al. Emergency response for evaluating SARS-CoV-2 immune status, seroprevalence and convalescent plasma in Argentina. PLoS Pathog. 2021;17(1):e1009161. doi: 10.1371/journal.ppat.1009161
- Yang HS, Costa V, Racine-Brzostek SE, et al. Association of Age With SARS-CoV-2 Antibody Response. JAMA Netw Open. 2021;4(3):e214302. doi: 10.1001/jamanetworkopen.2021.4302
- Shomron N. Nivel de anticuerpos varía en hombres y mujeres tras covid, según un estudio. [Antibody levels vary between men and women after COVID, according to a study]. Accessed July 13, 2021. https://www.swissinfo.ch/spa/ coronavirus-vacuna_nivel-de-anticuerpos-var%C3%ADa-en-hombres-y-mujeres-tras-covid-seg%C3%BAn-un-estudio/46782892
- Guzmán-Martínez O, Guardado K, Varela-Cardoso M, et al. Generation and persistence of S1 igg and neutralizing antibodies in post-Covid-19 patients. Infection. 2021;50(2):447–56. doi: 10.1007/s15010-021-01705-7
- Markmann AJ, Giallourou N, Bhowmik DR, et al. Sex disparities and neutralizing antibody durability to SARS-CoV-2 infection in convalescent individuals. Immunology. 2021;6(4). doi: 10.1128/msphere.00275-21
- Moradi G, Mohamadi Bolbanabad A, Ahmadi S, et al. Persistence assessment of SARS-CoV-2-specificIgG antibody in recovered COVID-19 individuals and its association with clinical symptoms and disease severity: A prospective longitudinal cohort study. Int Immunopharmacol. 2021;98:107893. doi: 10.1016/j.intimp.2021.107893
- Cameron A, Porterfield CA, Byron LD, et al. A Multiplex Microsphere IgG Assay for SARS-CoV-2 Using ACE2-Mediated Inhibition as a Surrogate for Neutralization. J Clin Microbiol. 2021;59(2):e02489-20. doi: 10.1128/JCM.02489-20
- Graham NR, Whitaker AN, Strother CA, et al. Kinetics and isotype assessment of antibodies targeting the spike protein receptor-binding domain of severe acute respiratorysyndrome-coronavirus-2 in COVID-19 patients as a function of age, biological sex and disease severity. Clin Transl Immunol. 2020;9(10). doi: 10.1002/cti2.1189
- Post N, Eddy D, Huntley C, et al. Antibody response to SARS-CoV-2 infection in humans: A systematic review. PLoS ONE. 2020;15(12):e0244126. doi: 10.1371/journal.pone.0244126
- Fischinger S, Boudreau C.M, Butler A.L, Streeck H, Alter G. Sex differences in vaccine-induced humoral immunity. Semin Immunopathol. 2019;41(2):239–249. doi: 10.1007/s00281-018-0726-5
- Scully EP, Haverfield J, Ursin RL, Tannenbaum C, Klein SL. Considering how biological sex impacts immune responses and COVID-19 outcomes. Nat Rev Immunol. 2020;20(7):442–447. doi: 10.1038/s41577-020-0348-8
- Feng X, Yin J, Zhang J, et al. Longitudinal Profiling of Antibody Response in Patients With COVID-19 in a Tertiary Care Hospital in Beijing, China. Front Immunol. 2021;12:614436. doi: 10.3389/fimmu.2021.614436
- Lee SW, Moon JY, Lee SK, et al. Anti-SARS-CoV-2 Spike Protein RBD Antibody Levels After Receiving a Second Dose of ChAdOx1 nCov-19 (AZD1222) Vaccine in Healthcare Workers: Lack of Association With Age, Sex, Obesity, and Adverse Reactions. Front Immunol. 2021;12:779212. doi: 10.3389/fimmu.2021.779212
- Legros V, Denolly S, Vogrig M, et al. A longitudinal study of SARS-CoV-2-infected patients reveals a high correlation between neutralizing antibodies and COVID-19 severity. Cell Mol Immunol. 2021;18(2):318–327. doi: 10.1038/s41423-020-00588-2
- Grzelak L, Velay A, Madec Y, et al. Sex Differences in the Evolution of Neutralizing Antibodies to Severe Acute Respiratory Syndrome Coronavirus 2. J Infect Dis. 2021;224(6):983-988. doi: 10.1093/infdis/jiab127
- Mehew J, Johnson R, Roberts D, Harvala H. Convalescent plasma for COVID-19: male gender, olderage and hospitalisation associated with high neutralising antibody levels, England, 22 April to 12 May 2020. Euro Surveill. 2020;25(45):2001754. doi: 10.2807/1560-7917.ES.2020.25.45.2001754
- Nayak K, Gottimukkala K, Kumar S, et al. Characterization of neutralizing versus binding antibodies and memory B cells in COVID-19 recovered individuals from India. Virology. 2021;558:13-21. doi: 10.1016/j.virol.2021.02.002
- Bunders MJ, Altfeld M. Implications of Sex Differences in Immunity for SARS-CoV-2 Pathogenesis and Design of Therapeutic Interventions. Immunity. 2020;53(3):487-495. doi: 10.1016/j.immuni.2020.08.003
- Zeng F, Dai C, Cai P, et al. A comparison study of SARS-CoV-2 IgG antibody between male and female COVID-19 patients: A possible reason underlying different outcome between sex. J Med Virol. 2020;92(10):2050-2054. doi: 10.1002/jmv.25989
- Zheng Z, Peng F, Xu B, et al. Risk factors of critical & mortal COVID-19 cases: A systematic literature review and meta-analysis. J Infect. 2020;81(2):e16-e25. doi: 10.1016/j.jinf.2020.04.021
- Fang X, Li S, Yu H, et al. Epidemiological, comorbidity factors with severity and prognosis of COVID-19: a systematic review and meta-analysis. Aging. 2020;12(13):12493-12503. doi: 10.18632/aging.103579
- Ssentongo P, Ssentongo AE, Heilbrunn ES, Ba DM, Chinchilli VM, Hirst JA. Association of cardiovascular disease and 10 other pre-existing comorbidities with COVID-19 mortality: A systematic review and meta-analysis. PLoS ONE. 2020;15(8):e0238215. doi: 10.1371/journal.pone.0238215
- Földi M, Farkas N, Kiss S, et al. Obesity is a risk factor for developing critical condition in COVID-19 patients: A systematic review and meta-analysis. Obes Rev. 2020;21(10):e13095. doi: 10.1111/obr.13095
- Gazzaz ZJ. Diabetes and COVID-19. Open Life Sci. 2021;16(1):297-302. doi: 10.1515/biol-2021-0034
- Wang Y, Xu J, Wang Y, Hou H, Feng H, Yang H. An updated meta-analysis on the relationship between obesity and COVID-19 mortality. Metabolism. 2021;122:154820. doi: 10.1016/j.metabol.2021.154820
- Aghili SMM, Ebrahimpur M, Arjmand B, et al. Obesity in COVID-19 era, implications for mechanisms, comorbidities, and prognosis: a review and meta-analysis. Int J Obes. 2021;45(5):998-1016. doi: 10.1038/s41366-021-00776-8
- Biswas M, Rahaman S, Biswas TK, Haque Z, Ibrahim B. Association of Sex, Age, and Comorbidities with Mortality in COVID-19 Patients: A Systematic Review and Meta-Analysis. Intervirology. 2021;64(1):36-47. doi: 10.1159/000512592
- Gerhards C, Thiaucourt M, Kittel M, et al. Longitudinal assessment of anti-SARS-CoV-2 antibody dynamics and clinical features following convalescence from a COVID-19 infection. Int J Infect Dis. 2021;107:221-227. doi: 10.1016/j.ijid.2021.04.080
- Horton DB, Barrett ES, Roy J, et al. Determinants and Dynamics of SARS-CoV-2 Infection in a Diverse Population: 6-Month Evaluation of a Prospective Cohort Study. J Infect Dis. 2021;224(8):1345-1356. doi: 10.1093/infdis/jiab411
- Huang, M, Lu, QB, Zhao, H. et al. Temporal antibody responses to SARS-CoV-2 in patients of coronavirus disease 2019. Cell Discov. 2020;6(1). doi: 10.1038/s41421-020-00209-2
- Terpos E, Politou M, Sergentanis TN, et al. Anti-SARS-CoV-2 Antibody Responses in Convalescent Plasma Donors Are Increased in Hospitalized Patients; Subanalyses of a Phase 2 Clinical Study. Microorganisms. 2020;8(12):1885. doi: 10.3390/microorganisms8121885
- Nielsen SS, Vibholm LK, Monrad I, et al. Sars-Cov-2 elicits robust adaptive immune responses regardless of disease severity. eBioMedicine. 2021;68:103410. doi: 10.1016/j.ebiom.2021.103410
- Zhang B, Yue D, Wang Y, Wang F, Wu S, Hou H. The dynamics of immune response in covid-19 patients with different illness severity. J Med Virol. 2021;93(2):1070-1077. doi: 10.1002/jmv.26504
- Guo J, Li L, Wu Q, et al. Detection and predictors of anti-SARS-CoV-2 antibody levels in COVID-19patients at 8 months after symptom onset. Future Virol. 2021;16(12):795-804. doi: 10.2217/fvl-2021-0141
- Hansen CB, Jarlhelt I, Pérez-Alós L, et al. SARS-CoV-2 Antibody Responses Are Correlated to Disease Severity in COVID-19 Convalescent Individuals. J Immunol. 2021;206(1):109-117. doi: 10.4049/jimmunol.2000898
- Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi: 10.1016/S0140-6736(20)30183-5
- Anka AU, Tahir MI, Abubakar SD, et al. Coronavirus disease 2019 (COVID-19): An overview of the immunopathology, serological diagnosis and management. Scand J Immunol. 2021;93(4):e12998. doi: 10.1111/sji.12998
- Sun B, Feng Y, Mo X, et al. Kinetics of SARS-CoV-2 specific IgM and IgG responses in COVID-19 patients. Emerg Microbes Infect. 2020;9(1):940-948. doi: 10.1080/22221751.2020.1762515
- Kang CK, Kim M, Hong J, et al. Distinct Immune Response at 1 Year Post-COVID-19 According to Disease Severity. Front. Immunol. 2022;13:830433. doi: 10.3389/fimmu.2022.830433
- Liu Y, Yan LM, Wan L, et al. Viral dynamics in mild and severe cases of COVID-19. Lancet Infect Dis. 2020;20(6):656-657. doi: 10.1016/S1473-3099(20)30232-2
- Kwon JS, Kim JY, Kim MC, et al. Factors of Severity in Patients with COVID-19: Cytokine/Chemokine Concentrations, Viral Load, and Antibody Responses. Am J Trop Med Hyg. 2020;103(6):2412-2418. doi: 10.4269/ajtmh.20-1110
- Kang CK, Kim M, Lee S, et al. Longitudinal Analysis of Human Memory T-Cell Response According to the Severity of Illness up to 8 Months After Severe Acute Respiratory Syndrome Coronavirus 2 Infection. J Infect Dis. 2021;224(1):39-48. doi: 10.1093/infdis/jiab159
- Kang CK, Han GC, Kim M, et al. Aberrant hyperactivation of cytotoxic T-cell as a potential determinant of COVID-19 severity. Int J Infect Dis. 2020;97:313-321. doi: 10.1016/j.ijid.2020.05.106
- Okba NMA, Muller MA, Li W, et al. SARS-COV-2 specific antibody responses in COVID-19 patients. MedRxiv. 2020;1–18, doi: 10.1101/2020.03.18.20038059
- Li K, Huang B, Wu M, et al. Dynamic changes in anti-SARS-CoV-2 antibodies during SARS-CoV-2 infection and recovery from COVID-19. Nat Commun. 2020;11(1):6044. doi: 10.1038/s41467-020-19943-y
- Bläckberg A, Fernström N, Sarbrant E, Rasmussen M, Sunnerhagen T, Zivkovic AR. Antibody kinetics and clinical course of COVID-19 a prospective observational study. PLoS ONE. 2021;16(3):e0248918. doi: 10.1371/journal.pone.0248918
- Tan W, Lu Y, Zhang J, et al. Viral kinetics and antibody responses in patients with COVID-19. MedRxiv. 2020. doi: 10.1101/2020.03.24.20042382
- Huergo MAC, Thanh NTK. Current advances in the detection of COVID-19 and evaluation of the humoral response. Analyst. 2021;146(2):382-402. doi: 10.1039/D0AN01686A
- Pizzi R, Gallego S, Blanco S, et al. Response to the SARS-CoV-2 Pandemic in Córdoba: Detection of Neutralizing Antibodies in Recovered Individuals within the Province. Accessed July 01, 2020. https://repositoriosdigitales.mincyt.gob.ar/vufind/ Record/RDUUNC_dd9da3ee7cb4ec9ab58800dc03cc8b78
- Zhang C, Gu J, Chen Q, et al. Clinical and epidemiological characteristics of pediatric SARS-CoV-2 infections in China: a multicenter case series. PLoS Med. 2020;17(6):e1003130. doi: 10.1371/journal.pmed.1003130
- Zhao J, Yuan Q, Wang H, et al. Antibody responses to sars-Cov-2 in patients with novel coronavirus disease 2019. Clin Infect Dis. 2020;71(16):2027–2034. doi: 10.1093/cid/ciaa344
- Vogelzang EH, Loeff FC, Derksen NIL, et al. Development of a SARS-CoV-2 total antibody assay and the dynamics of antibody response over time in hospitalized and non hospitalized patients with COVID-19. J Immunol. 2020;205(12):3491–3499. doi: 10.4049/jimmunol.2000767
- Hartog G, Schepp RM, Kuijer M, et al. SARS-CoV-2-specificantibody detection for seroepidemiology: a multiplex analysis approach accounting for accurate seroprevalence. J Infect Dis. 2020;222(9):1452–1461. doi: 10.1093/infdis/jiaa479
- To KK, Tsang OT, Leung WS, et al. Temporal profiles of viral load in posterior oropharyngeal saliva samples and serum antibody responses during infection by SARS-CoV-2: an observational cohort study. Lancet Infect Dis. 2020;20(5):565–574. doi: 10.1016/S1473-3099(20)30196-1
- Sakhi H, Dahmane D, Attias P, et al. Kinetics of anti-SARS-CoV-2 IgG antibodies in hemodialysis patients 6 months after infection. J Am Soc Nephrol. 2021;32(5):1033–1036. doi: 10.1681/ASN.2020111618
- Hu WT, Howell JC, Ozturk T, et al. Antibody Profiles Accordingto Mild or Severe SARS-CoV-2 Infection, Atlanta, Georgia, USA, 2020. Emerg Infect Dis. 2020;26(12):2974–2978. doi: 10.3201/eid2612.203334
- Chirathaworn C, Sripramote M, Chalongviriyalert P, et al. SARS-CoV-2 RNA shedding in recovered COVID-19 cases and the presence of antibodies against SARS-CoV-2 in recovered COVID-19 cases and close contacts, Thailand, April-June 2020. PLoS ONE. 2020;15(10):e0236905. doi: 10.1371/journal.pone.0236905
- Lin L, Luo S, Qin R, et al. Long-term infection of SARS-CoV-2 changed the body’s immune status. Clin. Immunol. 2020;218:108524. doi: 10.1016/j.clim.2020.108524
- Ebrahim F, Tabal S, Lamami Y, et al. Anti-SARS-CoV-2 IgG antibodies after recovery from COVID-19 or vaccination in Libyan population: comparison of four vaccines. Vaccines. 2022;10(12):2002. doi: 10.3390/vaccines10122002
- Azak E, Karadenizli A, Uzuner H, Karakaya N, Canturk NZ, Hulagu S, 2021. Comparison of an inactivated Covid19 vaccine-induced antibody response with concurrent natural Covid19 infection. IntJ Infect Dis. 2021;113: 58–64. doi: 10.1016/j.ijid.2021.09.060
- Tretyn A. Szczepanek J, Skorupa M, et al. Differences in the concentration of anti-SARS-CoV-2 IgG antibodies post-COVID-19 recovery or post-vaccination. Cells. 2021;10(8):1952. doi: 10.3390/cells10081952
- Goel RR, Apostolidis SA, Painter MM, et al. Distinct antibody and memory B cell responses in SARS-CoV-2 naïveand recovered individuals after Mrna vaccination. Sci. Immunol. 2021;6(58). doi: 10.1126/sciimmunol.abi6950
- Racine-Brzostek SE, Yee JK, Sukhu A, et al. Rapid, robust, and sustainable antibody responses to mRNA COVID-19 vaccine in convalescent COVID-19 individuals. JCI Insight. 2021;6(20):151477. doi: 10.1172/jci.insight.151477
- Ruetalo N, Flehmig B, Schindler M, et al. Long-Term Humoral Immune Response against SARS-CoV-2 after Natural Infection and Subsequent Vaccination According to WHO International Binding Antibody Units (BAU/mL). Viruses. 2021;13(12):2336. doi: 10.3390/v13122336
- Anichini G, Terrosi C, Gandolfo C, et al. SARS-CoV-2 antibody response in persons with past natural infection. N Engl J Med. 2021;385(1):90-92. doi: 10.1056/NEJMc2103825
