High pre-Delta and early-Omicron SARS-CoV-2 seroprevalence detected in dried blood samples from Kinshasa (D.R. Congo).

Publisher: Wiley-Liss Country of Publication: United States NLM ID: 7705876 Publication Model: Print Cited Medium: Internet ISSN: 1096-9071 (Electronic) Linking ISSN: 01466615 NLM ISO Abbreviation: J Med Virol Subsets: MEDLINE

Publication: New York Ny : Wiley-Liss
Original Publication: New York, Liss.

SARS-CoV-2* ; COVID-19*/diagnosis ; COVID-19*/epidemiology; Humans ; Female ; Middle Aged ; Male ; Democratic Republic of the Congo/epidemiology ; Pandemics ; Reproducibility of Results ; Seroepidemiologic Studies ; Antibodies, Viral

Studies on the impact of the COVID-19 pandemic in sub-Saharan Africa have yielded varying results, although authors universally agree the real burden surpasses reported cases. The primary objective of this study was to determine SARS-CoV-2 seroprevalence among patients attending Monkole Hospital in Kinshasa (D.R. Congo). The secondary objective was to evaluate the analytic performance of two chemiluminescence platforms: Elecsys® (Roche) and VirClia® (Vircell) on dried blood spot samples (DBS). The study population (N = 373) was recruited in two stages: a mid-2021 blood donor cohort (15.5% women) and a mid-2022 women cohort. Crude global seroprevalence was 61% (53.9%-67.8%) pre-Delta in 2021 and 90.2% (84.7%-94.2%) post-Omicron in 2022. Anti-spike (S) antibody levels significantly increased from 53.1 (31.8-131.3) U/mL in 2021 to 436.5 (219.3-950.5) U/mL in 2022 and were significantly higher above 45 years old in the 2022 population. Both platforms showed good analytic performance on DBS samples: sensitivity was 96.8% for IgG (antiN/S) (93.9%-98.5%) and 96.0% (93.0%-98.0%) for anti-S quantification. These results provide additional support for the notion that exposure to SARS-CoV-2 is more widespread than indicated by case-based surveillance and will be able to guide the pandemic response and strategy moving forward. Likewise, this study contributes evidence to the reliability of DBS as a tool for serological testing and diagnosis in resource-limited settings.
(© 2024 The Authors. Journal of Medical Virology published by Wiley Periodicals LLC.)

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.
ECDC. SARS‐CoV‐2 variants of concern as of 9 June 2022. Published 2022. Accessed April 4, 2023. https://www.ecdc.europa.eu/en/covid-19/variants-concern.
WHO. Coronavirus disease (COVID‐19): Variants of SARS‐COV‐2. Published 2021. Accessed April 4, 2023. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/question-and-answers-hub/q-a-detail/coronavirus-disease-%28covid-19%29-variants-of-sars-cov-2?gclid=Cj0KCQiA_bieBhDSARIsADU4zLdE7HL9gw_ZUerE4SgXBTFBlo_Gg5DneaSMAtUXowlHA-oUJy8vLYAaAnu0EALw_wc.
Otshudiema JO, Folefack GLT, Nsio JM, et al. Epidemiological comparison of four COVID‐19 waves in the democratic republic of the Congo, March 2020–January 2022. J Epidemiol Global Health. 2022;12(3):316‐327. doi:10.1007/S44197-022-00052-6.
Lau H, Khosrawipour T, Kocbach P, Ichii H, Bania J, Khosrawipour V. Evaluating the massive underreporting and undertesting of COVID‐19 cases in multiple global epicenters. Pulmonology. 2021;27(2):110‐115. doi:10.1016/j.pulmoe.2020.05.015.
Li R, Pei S, Chen B, et al. Substantial undocumented infection facilitates the rapid dissemination of novel coronavirus (SARS‐CoV‐2). Science. 2020;368:489‐493.
Suthar AB, Schubert S, Garon J, Couture A, Brown AM, Charania S. Coronavirus disease case definitions, diagnostic testing criteria, and surveillance in 25 countries with highest reported case counts. Emerging Infect Dis. 2022;28(1):148‐156. doi:10.3201/eid2801.211082.
World Health Organization. WHO Coronavirus Disease (COVID‐19) Dashboard With Vaccination Data | WHO Coronavirus (COVID‐19) Dashboard With Vaccination Data. 2022:1‐5.
Barber RM, Sorensen RJD, Pigott DM, et al. Estimating global, regional, and national daily and cumulative infections with SARS‐CoV‐2 through Nov 14, 2021: a statistical analysis. Lancet. 2022;399(10344):2351‐2380. doi:10.1016/S0140-6736(22)00484-6.
Cabore JW, Karamagi HC, Kipruto HK, et al. COVID‐19 in the 47 countries of the WHO African region: a modelling analysis of past trends and future patterns. Lancet Global Health. 2022;10(8):e1099‐e1114. doi:10.1016/S2214-109X(22)00233-9.
Niama FR, Koukouikila‐Koussounda F, Mayengue PI, et al. Prevalence of SARS‐CoV‐2 antibodies in the Republic of Congo in mid‐2021. IJID Regions. 2022;5:121‐123. doi:10.1016/j.ijregi.2022.09.012.
Fawole OI, Bello S, Adebowale AS, et al. COVID‐19 surveillance in democratic Republic of Congo, Nigeria, Senegal and Uganda: strengths, weaknesses and key lessons. BMC Public Health. 2023;23(1):835. doi:10.1186/s12889-023-15708-6.
Mitangala PN, Irenge LM, Musubao ET, et al. Prevalence of anti‐SARS‐CoV‐2 antibodies in people attending the two main Goma markets in the Eastern Democratic Republic of the Congo. Epidemiol Infect. 2023;151:e167. doi:10.1017/S0950268823001498.
Lawal BJ, Gallagher KE, Kitonsa J, et al. Prevalence of immunoglobulin G and M to SARS‐CoV‐2 and other human coronaviruses in the Democratic Republic of Congo, Sierra Leone, and Uganda: a longitudinal study. Int J Infect Dis. 2023;131:183‐192. doi:10.1016/j.ijid.2023.03.049.
Ndziessi G, Niama RF, Aloumba AG, et al. Seroprevalence of SARS‐CoV‐2 antibodies in Republic of Congo, February 2022. Epidemiol Infect. 2023;151:e162. doi:10.1017/S0950268823001425.
Sandie AB, Ngo Sack F, Medi Sike CI, et al. Spread of SARS‐CoV‐2 infection in adult populations in Cameroon: a repeated cross‐sectional study among blood donors in the cities of Yaoundé and Douala. J Epidemiol Global Health. 2023;13(2):266‐278. doi:10.1007/s44197-023-00102-7.
Janha RE, Bah A, Jah H, et al. SARS‐CoV‐2 seroprevalence in pregnant women during the first three COVID‐19 waves in the Gambia. Int J Infect Dis. 2023;135:109‐117. doi:10.1016/j.ijid.2023.08.012.
Hossain MS, Derrow MM, Mohamed SI, et al. Population‐based sero‐epidemiological investigation of SARS‐CoV‐2 infection in Somalia. J Infect Public Health. 2023;16(6):948‐954. doi:10.1016/j.jiph.2023.04.016.
Bloch EM, Kyeyune D, White JL, et al. SARS‐CoV‐2 seroprevalence among blood donors in Uganda: 2019‐2022. Transfusion. 2023;63(7):1354‐1365. doi:10.1111/trf.17449.
Nyawale HA, Moremi N, Mohamed M, et al. High seroprevalence of SARS‐CoV‐2 in mwanza, northwestern Tanzania: a population‐Based survey. Int J Environ Res Public Health. 2022;19(18):11664. doi:10.3390/ijerph191811664.
Ige FA, Ohihoin GA, Osuolale K, et al. Seroprevalence of SARS‐CoV‐2 IgG among healthcare workers in Lagos, Nigeria. PLoS One. 2023;18(10):e0292440. doi:10.1371/journal.pone.0292440.
Akanmu S, Herrera BB, Chaplin B, et al. High SARS‐CoV‐2 seroprevalence in lagos, Nigeria with robust antibody and cellular immune responses. J Clin Virol Plus. 2023;3(3):100156. doi:10.1016/j.jcvp.2023.100156.
Otiende M, Nyaguara A, Bottomley C, et al. Impact of COVID‐19 on mortality in coastal Kenya: a longitudinal open cohort study. Nat Commun. 2023;14(1):6879. doi:10.1038/s41467-023-42615-6.
Fish CS, Owiti P, Begnel ER, et al. Comparison of nucleocapsid and spike antibody ELISAs for determining SARS‐CoV‐2 seropositivity in Kenyan women and infants. J Med Virol. 2023;95(1):e28221. doi:10.1002/jmv.28221.
Awandu SS, Ochieng Ochieng A, Onyango B, et al. High seroprevalence of immunoglobulin G (IgG) and IgM antibodies to SARS‐CoV‐2 in asymptomatic and symptomatic individuals amidst vaccination roll‐out in Western Kenya. PLoS One. 2022;17(12):e0272751. doi:10.1371/journal.pone.0272751. Calderaro A ed.
Rai P, Kumar BK, Deekshit VK, Karunasagar I, Karunasagar I. Detection technologies and recent developments in the diagnosis of COVID‐19 infection. Appl Microbiol Biotechnol. 2021;105(2):441‐455. doi:10.1007/s00253-020-11061-5.
Lee E, Oh JE. Humoral immunity against SARS‐CoV‐2 and the impact on COVID‐19 pathogenesis. Mol Cells. 2021;44(6):392‐400. doi:10.14348/molcells.2021.0075.
Tso FY, Lidenge SJ, Peña PB, et al. High prevalence of pre‐existing serological cross‐reactivity against severe acute respiratory syndrome coronavirus‐2 (SARS‐CoV‐2) in sub‐saharan Africa. Int J Infect Dis. 2021;102:577‐583. doi:10.1016/j.ijid.2020.10.104.
Sookaromdee P, Wiwanitkit V. COVID‐19 and Tropical Infection: Complexity and Concurrence. In: Advances in Experimental Medicine and Biology. 1318. Springer; 2021:333‐341. doi:10.1007/978-3-030-63761-3_19.
Lapidus S, Liu F, Casanovas‐Massana A, et al. Plasmodium infection is associated with cross‐reactive antibodies to carbohydrate epitopes on the SARS‐CoV‐2 Spike protein. Sci Rep. 2022;12(1):22175. doi:10.1038/s41598-022-26709-7.
Vanroye F, Bossche DV, Brosius I, Tack B, Esbroeck MV, Jacobs J. COVID‐19 antibody detecting rapid diagnostic tests show high cross‐reactivity when challenged with Pre‐Pandemic malaria, schistosomiasis and dengue samples. Diagnostics. 2021;11(7):1163. doi:10.3390/diagnostics11071163.
Barquín D, Ndarabu A, Carlos S, et al. HIV‐1 diagnosis using dried blood spots from patients in Kinshasa, DRC: a tool to detect misdiagnosis and achieve World Health Organization 2030 targets. Int J Infect Dis. 2021;111:253‐260. doi:10.1016/j.ijid.2021.08.035.
Carrasco T, Barquín D, Ndarabu A, et al. HCV diagnosis and sequencing using dried blood spots from patients in Kinshasa (DRC): a tool to achieve who 2030 targets. Diagnostics. 2021;11(3):522. doi:10.3390/diagnostics11030522.
Toh ZQ, Higgins RA, Anderson J, et al. The use of dried blood spots for the serological evaluation of SARS‐CoV‐2 antibodies. J Public Health (Bangkok). 2022;44(2):e260‐e263. doi:10.1093/pubmed/fdab011.
Sims MD, Podolsky RH, Childers KL, et al. Dried blood spots are a valid alternative to venipuncture for COVID‐19 antibody testing. J Immunol Methods. 2023;513:113420. doi:10.1016/j.jim.2022.113420.
Zhao H, Wang M, Muthelo P, et al. Detection of SARS‐CoV‐2 antibodies in serum and dried blood spot samples of vaccinated individuals using a sensitive homogeneous proximity extension assay. New Biotechnol. 2022;72:139‐148. doi:10.1016/J.NBT.2022.11.004.
Guttmann S, Bunte S, Eschrig S, et al. Dried blood spot eluates are suitable for testing of SARS‐CoV‐2 IgG antibodies targeting Spike protein 1 and nucleocapsid protein. Biochem Biophys Rep. 2023;34:101479. doi:10.1016/j.bbrep.2023.101479.
Omosule CL, Conklin J, Seck S, et al. Qualitative and quantitative detection of SARS‐CoV‐2 antibodies from dried blood spots. Clin Biochem. 2023;117:16‐22. doi:10.1016/j.clinbiochem.2021.12.012.
Walker GJ, Davis R, Naing Z, et al. Serological detection of SARS‐CoV‐2 IgG using commercially available enzyme immunoassays on dried blood spots collected from patients. Microbiol Spectr. 2021;9(3):e0124521. doi:10.1128/Spectrum.01245-21.
Miesse PK, Collier BB, Grant RP. Monitoring of SARS‐CoV‐2 antibodies using dried blood spot for at‐home collection. Sci Rep. 2022;12(1):5812. doi:10.1038/s41598-022-09699-4.
Racey CS, Booth A, Albert A, et al. Seropositivity of SARS‐CoV‐2 in an unvaccinated cohort in British Columbia, Canada: a cross‐sectional survey with dried blood spot samples. BMJ Open. 2022;12(8):e062567. doi:10.1136/BMJOPEN-2022-062567.
Rodríguez‐Mateos M, Jaso J, Martínez de Aguirre P, et al. Effect of the hematocrit and storage temperature of dried blood samples in the serological study of mumps, measles and rubella. Diagnostics. 2023;13(3):349. doi:10.3390/diagnostics13030349.
Fernández‐Ciriza L, González Á, del Pozo JL, et al. Humoral and cellular immune response over 9 months of mRNA‐1273, BNT162b2 and ChAdOx1 vaccination in a university hospital in Spain. Sci Rep. 2022;12(1):15606. doi:10.1038/s41598-022-19537-2.
Mulenga LB, Hines JZ, Fwoloshi S, et al. Prevalence of SARS‐CoV‐2 in six districts in Zambia in July, 2020: a cross‐sectional cluster sample survey. Lancet Global Health. 2021;9(6):e773‐e781. doi:10.1016/S2214-109X(21)00053-X.
Nkuba AN, Makiala SM, Guichet E, et al. High prevalence of anti‐Severe acute respiratory syndrome coronavirus 2 (Anti‐SARS‐CoV‐2) antibodies after the first wave of coronavirus disease 2019 (COVID‐19) in Kinshasa, democratic republic of the Congo: results of a cross‐sectional household‐based survey. Clin Infect Dis. 2022;74(5):882‐890. doi:10.1093/cid/ciab515.
Audu RA, Stafford KA, Steinhardt L, et al. Seroprevalence of SARS‐CoV‐2 in four states of Nigeria in October 2020: a population‐based household survey. PLOS Global Public Health. 2022;2(6):e0000363. doi:10.1371/journal.pgph.0000363. Nelson MI ed.
Chisale MRO, Ramazanu S, Mwale SE, et al. Seroprevalence of anti‐SARS‐CoV‐2 antibodies in Africa: a systematic review and meta‐analysis. Rev Med Virol. 2022;32(2):e2271. doi:10.1002/rmv.2271.
Munyeku‐Bazitama Y, Folefack GT, Yambayamba MK, et al. High SARS‐CoV‐2 seroprevalence after second COVID‐19 wave (October 2020–April 2021), democratic republic of the Congo. Emerg Infect Dis. 2023;29(1):89‐97. doi:10.3201/eid2901.221009.
Ouedraogo S, Traoré IT, Kania D, et al. The burden of the coronavirus disease 2019 virus infection in Burkina Faso: results from a world health organization UNITY population‐based, age‐stratified sero‐epidemiological investigation. Influenza Other Respir Viruses. 2023;17(11):e13216. doi:10.1111/irv.13216.
Bingham J, Cable R, Coleman C, et al. Estimates of prevalence of anti‐SARS‐CoV‐2 antibodies among blood donors in South Africa in March 2022. Res Sq, 2022:rs.3.rs‐1687679. doi:10.21203/rs.3.rs-1687679/v1.
Sykes W, Mhlanga L, Swanevelder R, et al. Prevalence of anti‐SARS‐CoV‐2 antibodies among blood donors in Northern Cape, KwaZulu‐Natal, Eastern Cape, and free state provinces of South Africa in January 2021. Res Sq. 2021:rs.3.rs‐233375. doi:10.21203/rs.3.rs-233375/v1.
Iroungou BA, Moussavou PB, Elguero E, et al. Trend of expansion of SARS‐CoV‐2 infection and COVID‐19 burden in Gabon (Central Africa) in mid‐2021, based on a serological survey. IJID Regions. 2022;5:13‐17. doi:10.1016/j.ijregi.2022.08.006.
Lewis HC, Ware H, Whelan M, et al. SARS‐CoV‐2 infection in Africa: a systematic review and meta‐analysis of standardised seroprevalence studies, from January 2020 to December 2021. BMJ Glob Health. 2022;7(8):e008793. doi:10.1136/bmjgh-2022-008793.
Briggs J, Takahashi S, Nayebare P, et al. Seroprevalence of antibodies to SARS‐CoV‐2 in rural households in eastern Uganda, 2020‐2022. JAMA Network Open. 2023;6(2):e2255978. doi:10.1001/jamanetworkopen.2022.55978.
Kolawole OM, Tomori O, Agbonlahor D, et al. SARS CoV‐2 seroprevalence in selected states of high and low disease burden in Nigeria. JAMA Network Open. 2022;5(10):e2236053. doi:10.1001/jamanetworkopen.2022.36053.
Ditekemena JD, Nkamba DM, Muhindo HM, et al. Factors associated with adherence to COVID‐19 prevention measures in the democratic republic of the Congo (DRC): results of an online survey. BMJ Open. 2021;11(1):e043356. doi:10.1136/bmjopen-2020-043356.
Mboussou F, Farham B, Nsasiirwe S, et al. COVID‐19 vaccination in the WHO African region: progress made in 2022 and factors associated. Vaccines. 2023;11(5):1010. doi:10.3390/vaccines11051010.
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.
Ma H, Zeng W, He H, et al. Serum IgA, IgM, and IgG responses in COVID‐19. Cell Mol Immunol. 2020;17(7):773‐775. doi:10.1038/s41423-020-0474-z.
Chen X, Chen Z, Azman AS, et al. Serological evidence of human infection with SARS‐CoV‐2: a systematic review and meta‐analysis. Lancet Global Health. 2021;9(5):e598‐e609. doi:10.1016/S2214-109X(21)00026-7.
Graham NR, Whitaker AN, Strother CA, et al. Kinetics and isotype assessment of antibodies targeting the spike protein receptor‐binding domain of severe acute respiratory syndrome‐coronavirus‐2 in COVID‐19 patients as a function of age, biological sex and disease severity. Clin Transl Immunol. 2020;9(10):e1189. doi:10.1002/cti2.1189.
Müller SA, Wood RR, Hanefeld J, El‐Bcheraoui C. Seroprevalence and risk factors of COVID‐19 in healthcare workers from 11 African countries: a scoping review and appraisal of existing evidence. Health Policy Plan. 2022;37(4):505‐513. doi:10.1093/heapol/czab133.
Souris M, Tshilolo L, Parzy D, et al. Pre‐pandemic cross‐reactive immunity against SARS‐CoV‐2 among central and West African populations. Viruses. 2022;14(10):2259. doi:10.3390/v14102259.
Catlett B, Starr M, Machalek DA, et al. Evaluation of serological assays for SARS‐CoV‐2 antibody testing from dried blood spots collected from cohorts with prior SARS‐CoV‐2 infection. J Clin Virol Plus. 2022;2(3):100093. doi:10.1016/j.jcvp.2022.100093.
Anderson EM, Goodwin EC, Verma A, et al. Seasonal human coronavirus antibodies are boosted upon SARS‐CoV‐2 infection but not associated with protection. Cell. 2021;184(7):1858‐1864. doi:10.1016/j.cell.2021.02.010.
Zava TT, Zava DT. Validation of dried blood spot sample modifications to two commercially available COVID‐19 IgG antibody immunoassays. Bioanalysis. 2021;13(1):13‐28. doi:10.4155/bio-2020-0289.
Carlos S, Martínez‐González MÁ, Burgueño E, et al. Misconceptions about HIV infection in Kinshasa (Democratic Republic of Congo): a case–control study on knowledge, attitudes and practices: Table 1. Sex Transm Infect. 2015;91(5):334‐337. doi:10.1136/sextrans-2014-051734.
Coronavirus (COVID‐19) Vaccinations ‐ Our World in Data. Accessed June 16, 2023 https://ourworldindata.org/covid-vaccinations#licence.

PI16/01908 Fondo de Investigación en Salud-FIS; Grant 045-2015 Government of Navarre

Keywords: COVID‐19; DBS; SARS‐CoV‐2; chemiluminescence; seroprevalence; sub‐Saharan Africa

0 (Antibodies, Viral)

Date Created: 20240322 Date Completed: 20240325 Latest Revision: 20240325

20240325

10.1002/jmv.29529

38516764