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Clinical and Imaging Characteristics of SARS-CoV-2 Breakthrough Infection in Hospitalized Immunocompromised Patients

  • Jong Eun Lee (Department of Radiology, Chonnam National University Hospital) ;
  • Jinwoo Kim (Department of Radiology, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Pusan National University School of Medicine) ;
  • Minhee Hwang (Department of Radiology, Pusan National University Hospital, Pusan National University School of Medicine and Biomedical Research Institute) ;
  • Yun-Hyeon Kim (Department of Radiology and Biomedical Engineering, Chonnam National University Medical School, Chonnam National University Hospital) ;
  • Myung Jin Chung (Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Won Gi Jeong (Department of Radiology, Chonnam National University Hwasun Hospital and Chonnam National University Medical School) ;
  • Yeon Joo Jeong (Department of Radiology, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Pusan National University School of Medicine)
  • Received : 2023.08.13
  • Accepted : 2024.01.31
  • Published : 2024.05.01

Abstract

Objective: To evaluate the clinical and imaging characteristics of SARS-CoV-2 breakthrough infection in hospitalized immunocompromised patients in comparison with immunocompetent patients. Materials and Methods: This retrospective study analyzed consecutive adult patients hospitalized for COVID-19 who received at least one dose of the SARS-CoV-2 vaccine at two academic medical centers between June 2021 and December 2022. Immunocompromised patients (with active solid organ cancer, active hematologic cancer, active immune-mediated inflammatory disease, status post solid organ transplantation, or acquired immune deficiency syndrome) were compared with immunocompetent patients. Multivariable logistic regression analysis was performed to evaluate the effect of immune status on severe clinical outcomes (in-hospital death, mechanical ventilation, or intensive care unit admission), severe radiologic pneumonia (≥ 25% of lung involvement), and typical CT pneumonia. Results: Of 2218 patients (mean age, 69.5 ± 16.1 years), 274 (12.4%), and 1944 (87.6%) were immunocompromised an immunocompetent, respectively. Patients with active solid organ cancer and patients status post solid organ transplantation had significantly higher risks for severe clinical outcomes (adjusted odds ratio = 1.58 [95% confidence interval {CI}, 1.01-2.47], P = 0.042; and 3.12 [95% CI, 1.47-6.60], P = 0.003, respectively). Patient status post solid organ transplantation and patients with active hematologic cancer were associated with increased risks for severe pneumonia based on chest radiographs (2.96 [95% CI, 1.54-5.67], P = 0.001; and 2.87 [95% CI, 1.50-5.49], P = 0.001, respectively) and for typical CT pneumonia (9.03 [95% CI, 2.49-32.66], P < 0.001; and 4.18 [95% CI, 1.70-10.25], P = 0.002, respectively). Conclusion: Immunocompromised patients with COVID-19 breakthrough infection showed an increased risk of severe clinical outcome, severe pneumonia based on chest radiographs, and typical CT pneumonia. In particular, patients status post solid organ transplantation was specifically found to be associated with a higher risk of all three outcomes than hospitalized immunocompetent patients.

Keywords

References

  1. Jakharia N, Subramanian AK, Shapiro AE. COVID-19 in the immunocompromised host, including people with human immunodeficiency virus. Infect Dis Clin North Am 2022;36:397-421 https://doi.org/10.1016/j.idc.2022.01.006
  2. Siddiqi HK, Mehra MR. COVID-19 illness in native and immunosuppressed states: a clinical-therapeutic staging proposal. J Heart Lung Transplant 2020;39:405-407 https://doi.org/10.1016/j.healun.2020.03.012
  3. Jeong YJ, Wi YM, Park H, Lee JE, Kim SH, Lee KS. Current and emerging knowledge in COVID-19. Radiology 2023;306:e222462
  4. Lee ARYB, Wong SY, Chai LYA, Lee SC, Lee MX, Muthiah MD, et al. Efficacy of covid-19 vaccines in immunocompromised patients: systematic review and meta-analysis. BMJ 2022;376:e068632
  5. Lee JE, Hwang M, Kim YH, Chung MJ, Sim BH, Chae KJ, et al. Imaging and clinical features of COVID-19 breakthrough infections: a multicenter study. Radiology 2022;303:682-692 https://doi.org/10.1148/radiol.213072
  6. Lee JE, Hwang M, Kim YH, Chung MJ, Sim BH, Jeong WG, et al. SARS-CoV-2 variants infection in relationship to imaging-based pneumonia and clinical outcomes. Radiology 2023;306:e221795
  7. Singson JRC, Kirley PD, Pham H, Rothrock G, Armistead I, Meek J, et al. Factors associated with severe outcomes among immunocompromised adults hospitalized for COVID-19 - COVID-NET, 10 states, March 2020-February 2022. MMWR Morb Mortal Wkly Rep 2022;71:878-884 https://doi.org/10.15585/mmwr.mm7127a3
  8. Vijenthira A, Gong IY, Fox TA, Booth S, Cook G, Fattizzo B, et al. Outcomes of patients with hematologic malignancies and COVID-19: a systematic review and meta-analysis of 3377 patients. Blood 2020;136:2881-2892 https://doi.org/10.1182/blood.2020008824
  9. Conway R, Grimshaw AA, Konig MF, Putman M, Duarte-Garcia A, Tseng LY, et al. SARS-CoV-2 infection and COVID-19 outcomes in rheumatic diseases: a systematic literature review and metaanalysis. Arthritis Rheumatol 2022;74:766-775 https://doi.org/10.1002/art.42030
  10. Song Q, Bates B, Shao YR, Hsu FC, Liu F, Madhira V, et al. Risk and outcome of breakthrough COVID-19 infections in vaccinated patients with cancer: real-world evidence from the national COVID cohort collaborative. J Clin Oncol 2022;40:1414-1427 https://doi.org/10.1200/JCO.21.02419
  11. Ao G, Wang Y, Qi X, Nasr B, Bao M, Gao M, et al. The association between severe or death COVID-19 and solid organ transplantation: a systematic review and meta-analysis. Transplant Rev (Orlando) 2021;35:100628
  12. Wang Y, Feng R, Xu J, Shi L, Feng H, Yang H. An updated meta-analysis on the association between HIV infection and COVID-19 mortality. AIDS 2021;35:1875-1878 https://doi.org/10.1097/QAD.0000000000002968
  13. MacKenna B, Kennedy NA, Mehrkar A, Rowan A, Galloway J, Matthewman J, et al. Risk of severe COVID-19 outcomes associated with immune-mediated inflammatory diseases and immune-modifying therapies: a nationwide cohort study in the OpenSAFELY platform. Lancet Rheumatol 2022;4:e490-e506 https://doi.org/10.1016/S2665-9913(22)00098-4
  14. Yoon SH, Ham SY, Nam BD, Chae KJ, Lee D, Yoo JY, et al. Establishment of a nationwide Korean imaging cohort of coronavirus disease 2019. J Korean Med Sci 2020;35:e413
  15. Global Initiative on Sharing All Influenza Data (GISAID). Tracking of hCoV-19 variants [accessed on June 30, 2023]. Available at: https://gisaid.org/hcov19-variants/
  16. Lambrou AS, Shirk P, Steele MK, Paul P, Paden CR, Cadwell B, et al. Genomic surveillance for SARS-CoV-2 variants: predominance of the Delta (B.1.617.2) and Omicron (B.1.1.529) variants - United States, June 2021-January 2022. MMWR Morb Mortal Wkly Rep 2022;71:206-211 https://doi.org/10.15585/mmwr.mm7106a4
  17. Bertuzzi AF, Ciccarelli M, Marrari A, Gennaro N, Dipasquale A, Giordano L, et al. Impact of active cancer on COVID-19 survival: a matched-analysis on 557 consecutive patients at an Academic Hospital in Lombardy, Italy. Br J Cancer 2021;125:358-365 https://doi.org/10.1038/s41416-021-01396-9
  18. Kuderer NM, Choueiri TK, Shah DP, Shyr Y, Rubinstein SM, Rivera DR, et al. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet 2020;395:1907-1918 https://doi.org/10.1016/S0140-6736(20)31187-9
  19. Lee LY, Cazier JB, Angelis V, Arnold R, Bisht V, Campton NA, et al. COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study. Lancet 2020;395:1919-1926 https://doi.org/10.1016/S0140-6736(20)31173-9
  20. Gupta A, Desai N, Sanjeev, Chauhan P, Nityanand S, Hashim Z, et al. Clinical profile and outcome of COVID-19 in haematological malignancies: experience from tertiary care centre in India. Ann Hematol 2022;101:69-79 https://doi.org/10.1007/s00277-021-04644-3
  21. McInnes IB, Gravallese EM. Immune-mediated inflammatory disease therapeutics: past, present and future. Nat Rev Immunol 2021;21:680-686
  22. Sun J, Zheng Q, Madhira V, Olex AL, Anzalone AJ, Vinson A, et al. Association between immune dysfunction and COVID-19 breakthrough infection after SARS-CoV-2 vaccination in the US. JAMA Intern Med 2022;182:153-162 https://doi.org/10.1001/jamainternmed.2021.7024
  23. Link-Gelles R, Levy ME, Natarajan K, Reese SE, Naleway AL, Grannis SJ, et al. Estimation of COVID-19 mRNA vaccine effectiveness and COVID-19 illness and severity by vaccination status during Omicron BA.4 and BA.5 sublineage periods. JAMA Netw Open 2023;6:e232598
  24. Au-Yong I, Higashi Y, Giannotti E, Fogarty A, Morling JR, Grainge M, et al. Chest radiograph scoring alone or combined with other risk scores for predicting outcomes in COVID-19. Radiology 2022;302:460-469 https://doi.org/10.1148/radiol.2021210986
  25. Simpson S, Kay FU, Abbara S, Bhalla S, Chung JH, Chung M, et al. Radiological Society of North America expert consensus document on reporting chest CT findings related to COVID-19: endorsed by the Society of Thoracic Radiology, the American College of Radiology, and RSNA. Radiol Cardiothorac Imaging 2020;2:e200152
  26. Bahremand T, Yao JA, Mill C, Piszczek J, Grant JM, Smolina K. COVID-19 hospitalisations in immunocompromised individuals in the Omicron era: a population-based observational study using surveillance data in British Columbia, Canada. Lancet Reg Health Am 2023;20:100461
  27. Mehrabi Nejad MM, Moosaie F, Dehghanbanadaki H, Haji Ghadery A, Shabani M, Tabary M, et al. Immunogenicity of COVID-19 mRNA vaccines in immunocompromised patients: a systematic review and meta-analysis. Eur J Med Res 2022;27:23
  28. Meshram HS, Kute V, Rane H, Dave R, Banerjee S, Mishra V, et al. Humoral and cellular response of COVID-19 vaccine among solid organ transplant recipients: a systematic review and meta-analysis. Transpl Infect Dis 2022;24:e13926
  29. Uaprasert N, Pitakkitnukun P, Tangcheewinsirikul N, Chiasakul T, Rojnuckarin P. Immunogenicity and risks associated with impaired immune responses following SARS-CoV-2 vaccination and booster in hematologic malignancy patients: an updated meta-analysis. Blood Cancer J 2022;12:173
  30. Bange EM, Han NA, Wileyto P, Kim JY, Gouma S, Robinson J, et al. CD8 T cells compensate for impaired humoral immunity in COVID-19 patients with hematologic cancer. Research Square [Preprint]. 2021 [accessed on October 10, 2023]. Available at: https://doi.org/10.21203/rs.3.rs-162289/v1