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Genomic characterization of reinfection cases in the first wave of the COVID-19 pandemic in Indonesia

  • Erike Anggraini Suwarsono ,
  • Laifa Annisa Hendarmin ,
  • Chris Adhiyanto ,


Link of Video Abstract:


Background: Coronavirus disease 2019 (COVID-19) has become a significant disease causing a pandemic worldwide. Many variants were detected within the globe and may have an important role in transmission capability or reinfection conditions. The ‘unknown’ level of immunity’s protection from previous infection and the more virulent virus could lead to reinfection. Using the whole genome sequence, we can analyze the genomic insight within the first and second infections to help understand the reinfection pattern of COVID-19.

Methods: In this study, we investigated three COVID-19 cases with reinfection for primary and secondary infection each. The SARS-CoV-2 confirmation was conducted using qPCR with multiplex gene targets Orf1ab and E. Confirmation of reinfection was done by genomic analysis. Library preparation and sequencing were done using ARTIC protocol using nanopore technology.

Results: There was a wide variety of mutations between two episodes of infection and different clinical manifestations in each episode.

Conclusions: The result concluded that reinfection happened in worsened clinical symptoms and distinct genomic variation in each episode of infection


  1. Centers for Disease Control and Prevention. Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1) - United States, May-August 2009. MMWR Morb Mortal Wkly Rep. 2009;58(1):1071-1074.
  2. Centers for Disease Control and Prevention. Intensive-care patients with severe novel influenza A (H1N1) virus infection - Michigan, June 2009. MMWR Morb Mortal Wkly Rep. 2009;58(1):749-752.
  3. Centers for Disease Control and Prevention. Hospitalized patients with novel influenza A (H1N1) virus infection - California, April-May, 2009. MMWR Morb Mortal Wkly Rep. 2009;58(1):536-541.
  4. Mauad T, Hajjar LA, Callegari GD, da Silva LF, Schout D, Galas FR, et al. Lung Pathology in Fatal Novel Human Influenza A (H1N1) Infection. Am J Respir Crit Care Med. 2010;181(1):72-79.
  5. Tillett RL, Sevinsky JR, Hartley PD, Kerwin H, Crawford N, Gorzalski A, et al. Genomic evidence for reinfection with SARS-CoV-2: a case study. The Lancet infectious diseases. 2021;21(1):52-58.
  6. Adhiyanto C, Hendarmin LA, Suwarsono EA, Harriyati Z, Puspitaningrum R, Nurjadi D. The Identification of the SARS-CoV-2 Whole Genome: Nine Cases Among Patients in Banten Province, Indonesia. J Pure Appl Microbiol. 2021;15(2):936-948.
  7. Zhang L, Jackson CB, Mou H, Ojha A, Rangarajan ES, Izard T, et al. The D614G mutation in the SARS-CoV-2 spike protein reduces S1 shedding and increases infectivity. BioRxiv. 2020;1(1):1-25.
  8. Shi PY, Plante J, Liu Y, Liu J, Xia H, Johnson B, Weaver S. Spike mutation D614G alters SARS-CoV-2 fitness and neutralization susceptibility. Research square. 2020;1(1):1-23.
  9. Iwasaki A, Yang Y. The potential danger of suboptimal antibody responses in COVID-19. Nat Rev Immunol. 2020;20(6):339-341.
  10. van Dorp L, Acman M, Richard D, Shaw LP, Ford CE, Ormond L, et al. Emergence of genomic diversity and recurrent mutations in SARS-CoV-2. Infect GenetEvol. 2020;83(4):104351.
  11. Long QX, Liu BZ, Deng HJ, Wu GC, Deng K, Chen YK, et al. Antibody responses to SARS-CoV-2 in patients with COVID-19. Nat Med. 2020;26(6):845-848.
  12. Jungreis I, Sealfon R, Kellis M. SARS-CoV-2 gene content and COVID-19 mutation impact by comparing 44 Sarbecovirus genomes. Nat Commun. 2021;12(1):1-20.
  13. To KKW, Hung IFN, Ip JD, Chu AW, Chan WM, Tam A, et al. Coronavirus Disease 2019 (COVID-19) Re- infection by a Phylogenetically Distinct Severe Acute Respiratory Syndrome Coronavirus 2 Strain Confirmed by Whole Genome Sequencing. Clin Infect Dis. 2020;21(1):52-53.
  14. Sanyang B, Kanteh A, Usuf E, Nadjm B, Jarju S, Bah A, et al. COVID-19 reinfections in The Gambia by phylogenetically distinct SARS-CoV-2 variants—first two confirmed events in west Africa. Lancet Glob Heal; 2021;74(21):2020-2022.
  15. Gaebler C, Wang Z, Lorenzi JC, Muecksch F, Finkin S, Tokuyama M. Evolution of antibody immunity to SARS-CoV-2. Nature. 2021;591(7851):639-644.
  16. Prabawa IMY, Silakarma D, Prabawa IPY, Manuaba IBAP. Physical rehabilitation therapy for long covid-19 patient with respiratory sequelae: A systematic review. Open Access Macedonian Journal of Medical Sciences. 2022;10(F):468-474.
  17. Hsieh PP, Kristian H, Permana AJM, Wongsodiharjo M, Nugraheni PA, Charisti P, et al. The clinical pictures of COVID-19 pediatric patients in dr. R. Soedarsono Regional General Hospital, Pasuruan, East Java, Indonesia. Bali Medical Journal. 2022;11(1):460–465.
  18. Khairuni R, Jusuf NK, Putra IB. The relationship of the use of masks with the event of maskne on Universitas Sumatera Utara Hospital healthcare workers during the COVID-19 pandemic. Bali Medical Journal. 2021;12(2):1171–1174.
  19. Safitri YI, Zuwariah N. The effect of knowledge and attitude of family planning acceptances on iud contraception selection during the COVID-19 pandemic. Bali Medical Journal. 2022;11(2):981–984.

How to Cite

Suwarsono, E. A. ., Hendarmin, L. A., & Adhiyanto, C. . (2023). Genomic characterization of reinfection cases in the first wave of the COVID-19 pandemic in Indonesia. Bali Medical Journal, 12(3), 3141–3145.




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Erike Anggraini Suwarsono
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BMJ Journal

Laifa Annisa Hendarmin
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BMJ Journal

Chris Adhiyanto
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BMJ Journal