Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Radiologic Abnormalities in Prolonged SARS-CoV-2 Infection: A Systematic Review

  • Kyongmin Sarah Beck (Department of Radiology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Jeong-Hwa Yoon (Institute of Health Policy and Management, Medical Research Center, Seoul National University) ;
  • Soon Ho Yoon (Department of Radiology, Seoul National University Hospital, Seoul National College of Medicine)
  • Received : 2023.09.25
  • Accepted : 2024.02.24
  • Published : 2024.05.01
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Abstract

We systematically reviewed radiological abnormalities in patients with prolonged SARS-CoV-2 infection, defined as persistently positive polymerase chain reaction (PCR) results for SARS-CoV-2 for > 21 days, with either persistent or relapsed symptoms. We extracted data from 24 patients (median age, 54.5 [interquartile range, 44-64 years]) reported in the literature and analyzed their representative CT images based on the timing of the CT scan relative to the initial PCR positivity. Our analysis focused on the patterns and distribution of CT findings, severity scores of lung involvement on a scale of 0-4, and the presence of migration. All patients were immunocompromised, including 62.5% (15/24) with underlying lymphoma and 83.3% (20/24) who had received anti-CD20 therapy within one year. Median duration of infection was 90 days. Most patients exhibited typical CT appearance of coronavirus disease 19 (COVID-19), including ground-glass opacities with or without consolidation, throughout the follow-up period. Notably, CT severity scores were significantly lower during ≤ 21 days than during > 21 days (P < 0.001). Migration was observed on CT in 22.7% (5/22) of patients at ≤ 21 days and in 68.2% (15/22) to 87.5% (14/16) of patients at > 21 days, with rare instances of parenchymal bands in previously affected areas. Prolonged SARS-CoV-2 infection usually presents as migrating typical COVID-19 pneumonia in immunocompromised patients, especially those with impaired B-cell immunity.

Keywords

References

  1. Machkovech HM, Hahn AM, Garonzik Wang J, Grubaugh ND, Halfmann PJ, Johnson MC, et al. Persistent SARS-CoV-2 infection: significance and implications. Lancet Infect Dis 2024 Feb 7 [Epub]. https://doi.org/10.1016/S1473-3099(23)00815-0
  2. Cevik M, Tate M, Lloyd O, Maraolo AE, Schafers J, Ho A. SARSCoV-2, SARS-CoV, and MERS-CoV viral load dynamics, duration of viral shedding, and infectiousness: a systematic review and meta-analysis. Lancet Microbe 2021;2:e13-e22 https://doi.org/10.1016/S2666-5247(20)30172-5
  3. Vena A, Taramasso L, Di Biagio A, Mikulska M, Dentone C, De Maria A, et al. Prevalence and clinical significance of persistent viral shedding in hospitalized adult patients with SARS-CoV-2 infection: a prospective observational study. Infect Dis Ther 2021;10:387-398 https://doi.org/10.1007/s40121-020-00381-8
  4. He X, Lau EHY, Wu P, Deng X, Wang J, Hao X, et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat Med 2020;26:672-675 https://doi.org/10.1038/s41591-020-0869-5
  5. Lee CY, Shah MK, Hoyos D, Solovyov A, Douglas M, Taur Y, et al. Prolonged SARS-CoV-2 infection in patients with lymphoid malignancies. Cancer Discov 2022;12:62-73 https://doi.org/10.1158/2159-8290.CD-21-1033
  6. Hettle D, Hutchings S, Muir P, Moran E. Persistent SARSCoV-2 infection in immunocompromised patients facilitates rapid viral evolution: retrospective cohort study and literature review. Clin Infect Pract 2022;16:100210
  7. Lee J, Lee R, Beck KS, Han DH, Min GJ, Chang S, et al. Migratory pneumonia in prolonged SARS-CoV-2 infection in patients treated with B-cell depletion therapies for B-cell lymphoma. Korean J Radiol 2023;24:362-370 https://doi.org/10.3348/kjr.2022.0844
  8. Nagai H, Saito M, Adachi E, Sakai-Tagawa Y, Yamayoshi S, Kiso M, et al. Casirivimab/imdevimab for active COVID-19 pneumonia which persisted for nine months in a patient with follicular lymphoma during anti-CD20 therapy. Jpn J Infect Dis 2022;75:608-611 https://doi.org/10.7883/yoken.JJID.2022.092
  9. Moutinho-Pereira S, Calisto R, Sabio F, Guerreiro L. High-titre convalescent plasma therapy for an immunocompromised patient with systemic lupus erythematosus with protracted SARS-CoV-2 infection. BMJ Case Rep 2021;14:e244853
  10. Gu J, Yang L, Li T, Liu Y, Zhang J, Ning K, et al. Temporal relationship between serial RT-PCR results and serial chest CT imaging, and serial CT changes in coronavirus 2019 (COVID-19) pneumonia: a descriptive study of 155 cases in China. Eur Radiol 2021;31:1175-1184 https://doi.org/10.1007/s00330-020-07268-9
  11. Revel MP, Boussouar S, de Margerie-Mellon C, Saab I, Lapotre T, Mompoint D, et al. Study of thoracic CT in COVID-19: the STOIC project. Radiology 2021;301:E361-E370 https://doi.org/10.1148/radiol.2021210384
  12. Salehi S, Abedi A, Balakrishnan S, Gholamrezanezhad A. Coronavirus disease 2019 (COVID-19): a systematic review of imaging findings in 919 patients. AJR Am J Roentgenol 2020;215:87-93 https://doi.org/10.2214/AJR.20.23034
  13. Simpson S, Kay FU, Abbara S, Bhalla S, Chung JH, Chung M, et al. Radiological Society of North America expert consensus statement on reporting chest CT findings related to COVID-19. Endorsed by the Society of Thoracic Radiology, the American College of Radiology, and RSNA - secondary publication. J Thorac Imaging 2020;35:219-227 https://doi.org/10.1097/RTI.0000000000000524
  14. Degli Antoni M, Crosato V, Pennati F, Borghesi A, Cristini G, Allegri R, et al. COVID-19 pneumonia with migratory pattern in agammaglobulinemic patients: a report of two cases and review of literature. Tomography 2023;9:894-900
  15. Nakajima Y, Ogai A, Furukawa K, Arai R, Anan R, Nakano Y, et al. Prolonged viral shedding of SARS-CoV-2 in an immunocompromised patient. J Infect Chemother 2021;27:387-389 https://doi.org/10.1016/j.jiac.2020.12.001
  16. Yasuda H, Tsukune Y, Watanabe N, Sugimoto K, Uchimura A, Tateyama M, et al. Persistent COVID-19 pneumonia and failure to develop anti-SARS-CoV-2 antibodies during rituximab maintenance therapy for follicular lymphoma. Clin Lymphoma Myeloma Leuk 2020;20:774-776 https://doi.org/10.1016/j.clml.2020.08.017
  17. Yasuda H, Mori Y, Chiba A, Bai J, Murayama G, Matsushita Y, et al. Resolution of one-year persisting COVID-19 pneumonia and development of immune thrombocytopenia in a follicular lymphoma patient with preceding rituximab maintenance therapy: a follow-up report and literature review of cases with prolonged infections. Clin Lymphoma Myeloma Leuk 2021;21:e810-e816 https://doi.org/10.1016/j.clml.2021.07.004
  18. Kintrilis N, Gkinos CP, Galinos I. Prolonged COVID-19 in a multiple sclerosis patient treated with rituximab. Cureus 2022;14:e32523
  19. Cerezoli MT, Prats JAGG, Medeiros AK, Santana DVG, da Costa FM, Torres US, et al. Clinical and radiological improvement of protracted COVID-19 and good syndrome secondary to advanced thymoma. Pulmonology 2022;28:472-475 https://doi.org/10.1016/j.pulmoe.2022.04.011
  20. Villasenor-Echavarri R, Gomez-Romero L, Martin-Onraet A, Herrera LA, Escobar-Arrazola MA, Ramirez-Vega OA, et al. SARS-CoV-2 genome variations in viral shedding of an immunocompromised patient with non-Hodgkin's lymphoma. Viruses 2023;15:377
  21. Nagasaki Y, Kadowaki M, Nakamura A, Etoh Y, Shimo M, Ishihara S, et al. A case of a malignant lymphoma patient persistently infected with SARS-CoV-2 for more than 6 months. Medicina (Kaunas) 2023;59:108
  22. Trottier CA, Wong B, Kohli R, Boomsma C, Magro F, Kher S, et al. Dual antiviral therapy for persistent coronavirus disease 2019 and associated organizing pneumonia in an immunocompromised host. Clin Infect Dis 2023;76:923-925 https://doi.org/10.1093/cid/ciac847
  23. Ertesvag NU, Sakkestad ST, Zhou F, Hoff I, Kristiansen T, Jonassen TM, et al. Persistent fever and positive PCR 90 days post-SARS-CoV-2 infection in a rituximab-treated patient: a case of late antiviral treatment. Viruses 2022;14:1757
  24. Lyz˙wa E, Sobiecka M, Lewandowska K, Siemion-Szczes'niak I, Baran'ska I, Klatt M, et al. Prolonged SARS-CoV-2 infection and organizing pneumonia in a patient with follicular lymphoma, treated with obinutuzumab-challenging recognition and treatment. Viruses 2023;15:693
  25. Thornton CS, Huntley K, Berenger BM, Bristow M, Evans DH, Fonseca K, et al. Prolonged SARS-CoV-2 infection following rituximab treatment: clinical course and response to therapeutic interventions correlated with quantitative viral cultures and cycle threshold values. Antimicrob Resist Infect Control 2022;11:28
  26. Shoji K, Suzuki A, Okamoto M, Tsinda EK, Sugawara N, Sasaki M, et al. Prolonged shedding of infectious viruses with haplotype switches of SARS-CoV-2 in an immunocompromised patient. J Infect Chemother 2022;28:1001-1004 https://doi.org/10.1016/j.jiac.2022.04.004
  27. Daoussis D, Leonidou L, Kalogeropoulou C, Paliogianni F, Tzouvelekis A. Protracted severe COVID-19 pneumonia following rituximab treatment: caution needed. Rheumatol Int 2021;41:1839-1843 https://doi.org/10.1007/s00296-021-04969-2
  28. Ford ES, Simmons W, Karmarkar EN, Yoke LH, Braimah AB, Orozco JJ, et al. Successful treatment of prolonged, severe coronavirus disease 2019 lower respiratory tract disease in a B cell acute lymphoblastic leukemia patient with an extended course of remdesivir and nirmatrelvir/ritonavir. Clin Infect Dis 2023;76:926-929 https://doi.org/10.1093/cid/ciac868
  29. Nakamura K, Sugiyama M, Ishizuka H, Sasajima T, Minakawa Y, Sato H, et al. Prolonged infective SARS-CoV-2 omicron variant shedding in a patient with diffuse large B cell lymphoma successfully cleared after three courses of remdesivir. J Infect Chemother 2023;29:820-824 https://doi.org/10.1016/j.jiac.2023.05.003
  30. Pan F, Ye T, Sun P, Gui S, Liang B, Li L, et al. Time course of lung changes at chest CT during recovery from coronavirus disease 2019 (COVID-19). Radiology 2020;295:715-721 https://doi.org/10.1148/radiol.2020200370
  31. Wang Y, Dong C, Hu Y, Li C, Ren Q, Zhang X, et al. Temporal changes of CT findings in 90 patients with COVID-19 pneumonia: a longitudinal study. Radiology 2020;296:E55-E64 https://doi.org/10.1148/radiol.2020200843
  32. Kwee TC, Kwee RM. Chest CT in COVID-19: what the radiologist needs to know. Radiographics 2020;40:1848-1865 https://doi.org/10.1148/rg.2020200159
  33. Pal Singh S, Dammeijer F, Hendriks RW. Role of Bruton's tyrosine kinase in B cells and malignancies. Mol Cancer 2018;17:57
  34. Gagelmann N, Passamonti F, Wolschke C, Massoud R, Niederwieser C, Adjalle R, et al. Antibody response after vaccination against SARS-CoV-2 in adults with hematological malignancies: a systematic review and meta-analysis. Haematologica 2022;107:1840-1849 https://doi.org/10.3324/haematol.2021.280163
  35. Infectious Diseases Society of America. What is a cycle threshold value? [accessed on January 5, 2024]. Available at: https://www.idsociety.org/covid-19-real-time-learningnetwork/diagnostics/what-is-a-cycle-threshold-value/#/+/0/publishedDate_na_dt/desc/
  36. Rabaan AA, Tirupathi R, Sule AA, Aldali J, Mutair AA, Alhumaid S, et al. Viral dynamics and real-time RT-PCR Ct values correlation with disease severity in COVID-19. Diagnostics (Basel) 2021;11:1091
  37. Kory P, Kanne JP. SARS-CoV-2 organising pneumonia: 'has there been a widespread failure to identify and treat this prevalent condition in COVID-19?' BMJ Open Respir Res 2020;7:e000724
  38. Chong WH, Saha BK, Chopra A. Does COVID-19 pneumonia signify secondary organizing pneumonia?: a narrative review comparing the similarities between these two distinct entities. Heart Lung 2021;50:667-674 https://doi.org/10.1016/j.hrtlng.2021.04.009