The predictive markers of severity and mortality in hospitalized hemodialysis patients with COVID-19 during Omicron epidemic
Corresponding Author
Masataka Banshodani
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Correspondence
Masataka Banshodani, Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, 3-30, Nakajimacho, Naka-ku, Hiroshima 730-8655, Japan
Email: [email protected]
Search for more papers by this authorHideki Kawanishi
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorTakayuki Hirai
Kidney Disease and Dialysis, Akane-Foundation, Ajina Tsuchiya Hospital, Hatsukaichi, Japan
Search for more papers by this authorYusuke Kawai
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorShinji Hashimoto
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorSadanori Shintaku
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorMisaki Moriishi
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorSeiji Marubayashi
Kidney Disease and Dialysis, Akane-Foundation, Ajina Tsuchiya Hospital, Hatsukaichi, Japan
Search for more papers by this authorShinichiro Tsuchiya
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorCorresponding Author
Masataka Banshodani
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Correspondence
Masataka Banshodani, Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, 3-30, Nakajimacho, Naka-ku, Hiroshima 730-8655, Japan
Email: [email protected]
Search for more papers by this authorHideki Kawanishi
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorTakayuki Hirai
Kidney Disease and Dialysis, Akane-Foundation, Ajina Tsuchiya Hospital, Hatsukaichi, Japan
Search for more papers by this authorYusuke Kawai
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorShinji Hashimoto
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorSadanori Shintaku
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorMisaki Moriishi
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorSeiji Marubayashi
Kidney Disease and Dialysis, Akane-Foundation, Ajina Tsuchiya Hospital, Hatsukaichi, Japan
Search for more papers by this authorShinichiro Tsuchiya
Kidney Disease and Blood Purification Therapy, Akane-Foundation, Tsuchiya General Hospital, Hiroshima, Japan
Search for more papers by this authorAbstract
Introduction
Predictive markers and prognosis remain unclear in hospitalized hemodialysis (HD) patients with coronavirus disease 2019 (COVID-19) during the Omicron epidemic.
Methods
We evaluated characteristics, laboratory parameters, and outcomes in hospitalized HD patients with COVID-19 (n = 102) at two centers between January and April 2022.
Results
The 30-day mortality rate was higher in moderate–critical group (n = 43) than mild group (n = 59) (16.3% vs. 1.7%; p = 0.007), and higher in patients with lower CC chemokine ligand 17 (CCL17) levels (<95.0 pg/mL) compared with normal CCL17 levels (19.0% versus 4.9%; p = 0.03). In multivariate analyses, a low CCL17 level (p = 0.003) was associated with moderate–critical conditions, and moderate–critical conditions (p = 0.04) were associated with 30-day mortality, whereas CCL17 was not associated with 30-day mortality.
Conclusions
COVID-19 remains a fatal complication, and CCL17 was a predictive marker of severity in hospitalized HD patients during the Omicron epidemic.
CONFLICT OF INTEREST
The authors declare no potential conflict of interest.
Supporting Information
Filename | Description |
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tap13970-sup-0001-TableS1.docxWord 2007 document , 64.6 KB | Table S1. Pharmacological treatment, renal replacement therapy, oxygen inhalation, and respiratory treatment in hospitalized hemodialysis patients with COVID-19 (mild versus moderate–critical groups) |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020; 382(8): 727–33.
- 2Zhang J, Cai Y, Lavine CL, Peng H, Zhu H, Anand K, et al. Structural and functional impact by SARS-CoV-2 Omicron spike mutations. Cell Rep. 2022; 39(4):110729.
- 3Yin W, Xu Y, Xu P, Cao X, Wu C, Gu C, et al. Structures of the Omicron spike trimer with ACE2 and an anti-Omicron antibody. Science. 2022; 375(6584): 1048–53.
- 4Takashita E, Kinoshita N, Yamayoshi S, Sakai-Tagawa Y, Fujisaki S, Ito M, et al. Efficacy of antibodies and antiviral drugs against Covid-19 Omicron variant. N Engl J Med. 2022; 386(10): 995–8.
- 5Takashita E, Kinoshita N, Yamayoshi S, Sakai-Tagawa Y, Fujisaki S, Ito M, et al. Efficacy of antiviral agents against the SARS-CoV-2 Omicron subvariant BA.2. N Engl J Med. 2022; 386(15): 1475–7.
- 6Takashita E, Yamayoshi S, Simon V, van Bakel H, Sordillo EM, Pekosz A, et al. Efficacy of antibodies and antiviral drugs against Omicron BA.2.12.1, BA.4, and BA.5 subvariants. N Engl J Med. 2022; 387(5): 468–70.
- 7Chung EYM, Palmer SC, Natale P, Krishnan A, Cooper TE, Saglimbene VM, et al. Incidence and outcomes of COVID-19 in people with CKD: a systematic review and meta-analysis. Am J Kidney Dis. 2021; 78(6): 804–15.
- 8Hilbrands LB, Duivenvoorden R, Vart P, Franssen CFM, Hemmelder MH, Jager KJ, et al. COVID-19-related mortality in kidney transplant and dialysis patients: results of the ERACODA collaboration. Nephrol Dial Transplant. 2020; 35(11): 1973–83.
- 9Carr EJ, Wu M, Harvey R, Billany RE, Wall EC, Kelly G, et al. Omicron neutralising antibodies after COVID-19 vaccination in haemodialysis patients. Lancet. 2022; 399(10327): 800–2.
- 10Cinkilic O, Anft M, Blazquez-Navarro A, Meister TL, Roch T, Stervbo U, et al. Inferior humoral and sustained cellular immunity against wild-type and omicron variant of concern in hemodialysis patients immunized with 3 SARS-CoV-2 vaccine doses compared with 4 doses. Kidney Int. 2022; 101(6): 1287–9.
- 11Chinnadurai R, Wu HHL, Cox E, Moore J, Clough T, Lamerton E, et al. Humoral response in hemodialysis patients following COVID-19 vaccination and breakthrough infections during Delta and Omicron variant predominance. Vaccines (Basel). 2022; 10(4):498.
- 12Imai T, Yoshida T, Baba M, Nishimura M, Kakizaki M, Yoshie O. Molecular cloning of a novel T cell-directed CC chemokine expressed in thymus by signal sequence trap using Epstein-Barr virus vector. J Biol Chem. 1996; 271(35): 21514–21.
- 13Kataoka Y. Thymus and activation-regulated chemokine as a clinical biomarker in atopic dermatitis. J Dermatol. 2014; 41(3): 221–9.
- 14Engle SM, Chang CY, Ulrich BJ, Satterwhite A, Hayes T, Robling K, et al. Predictive biomarker modeling of pediatric atopic dermatitis severity based on longitudinal serum collection. Clin Exp Immunol. 2022; 207(3): 253–62.
- 15Sugiyama M, Kinoshita N, Ide S, Nomoto H, Nakamoto T, Saito S, et al. Serum CCL17 level becomes a predictive marker to distinguish between mild/moderate and severe/critical disease in patients with COVID-19. Gene. 2021; 766:145145.
- 16Ko K, Takahashi K, Nagashima S, Bunthen B, Ouoba S, Takafuta T, et al. Exercising the sanger sequencing strategy for variants screening and full-length genome of SARS-CoV-2 virus during alpha, delta, and omicron outbreaks in Hiroshima. Viruses. 2022; 14(4):720.
- 17Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987; 40(5): 373–83.
- 18Sundararajan V, Henderson T, Perry C, Muggivan A, Quan H, Ghali WA. New ICD-10 version of the Charlson comorbidity index predicted in-hospital mortality. J Clin Epidemiol. 2004; 57(12): 1288–94.
- 19Sugiyama M, Kimura T, Naito S, Mukaide M, Shinauchi T, Ueno M, et al. Development of specific and quantitative real-time detection PCR and immunoassays for lambda3-interferon. Hepatol Res. 2012; 42(11): 1089–99.
- 20Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72314 cases from the Chinese Center for Disease Control and Prevention. Jama. 2020; 323(13): 1239–42.
- 21Yamaoka M, Banshodani M, Muraoka S, Tanaka K, Kimura A, Tani H, et al. COVID-19-associated pulmonary aspergillosis in hemodialysis patients. Clin Kidney J. 2022; 15(5): 985–91.
- 22Banshodani M, Shintaku S, Kawanishi H. Combination therapy for COVID-19 in hemodialysis patients: pharmacological treatments and renal replacement therapy based on the severity. Ther Apher Dial. 2022; 26(2): 475–7.
- 23Krutikov M, Stirrup O, Nacer-Laidi H, Azmi B, Fuller C, Tut G, et al. Outcomes of SARS-CoV-2 omicron infection in residents of long-term care facilities in England (VIVALDI): a prospective, cohort study. Lancet Healthy Longev. 2022; 3(5): e347–e55.
- 24Lauring AS, Tenforde MW, Chappell JD, Gaglani M, Ginde AA, McNeal T, et al. Clinical severity of, and effectiveness of mRNA vaccines against, covid-19 from omicron, delta, and alpha SARS-CoV-2 variants in the United States: prospective observational study. BMJ. 2022; 376:e069761.
- 25Flythe JE, Assimon MM, Tugman MJ, Chang EH, Gupta S, Shah J, et al. Characteristics and outcomes of individuals with pre-existing kidney disease and COVID-19 admitted to intensive care units in the United States. Am J Kidney Dis. 2021; 77(2): 190–203 e1.
- 26Ng JH, Hirsch JS, Wanchoo R, Sachdeva M, Sakhiya V, Hong S, et al. Outcomes of patients with end-stage kidney disease hospitalized with COVID-19. Kidney Int. 2020; 98(6): 1530–9.
- 27Williamson EJ, Walker AJ, Bhaskaran K, Bacon S, Bates C, Morton CE, et al. Factors associated with COVID-19-related death using OpenSAFELY. Nature. 2020; 584(7821): 430–6.
- 28Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020; 395(10229): 1054–62.
- 29Wynants L, Van Calster B, Collins GS, Riley RD, Heinze G, Schuit E, et al. Prediction models for diagnosis and prognosis of covid-19 infection: systematic review and critical appraisal. BMJ. 2020; 369:m1328.
- 30Petrilli CM, Jones SA, Yang J, Rajagopalan H, O'Donnell L, Chernyak Y, et al. Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ. 2020; 369:m1966. https://doi.org/10.1136/bmj.m1966
- 31Guo T, Fan Y, Chen M, Wu X, Zhang L, He T, et al. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020; 5(7): 811–8.
- 32Muik A, Lui BG, Wallisch AK, Bacher M, Muhl J, Reinholz J, et al. Neutralization of SARS-CoV-2 omicron by BNT162b2 mRNA vaccine-elicited human sera. Science. 2022; 375(6581): 678–80.
- 33Hsieh YH, Wang WC, Hung TW, Lee CC, Tsai JP. C-C motif chemokine ligand-17 as a novel biomarker and regulator of epithelial mesenchymal transition in renal fibrogenesis. Cell. 2021; 10(12):3345.
- 34Lebherz-Eichinger D, Klaus DA, Reiter T, Horl WH, Haas M, Ankersmit HJ, et al. Increased chemokine excretion in patients suffering from chronic kidney disease. Transl Res. 2014; 164(6): 433.e1–43.e2.
- 35Nakayama T, Morimoto K, Uchiyama K, Kusahana E, Washida N, Azegami T, et al. Serum thymus and activation-regulated chemokine level is associated with the severity of chronic kidney disease-associated pruritus in patients undergoing peritoneal dialysis. Perit Dial Int. 2022; 42(4): 415–24.
- 36Hasegawa T, Hato T, Okayama T, Ikeo K, Miyamoto Y, Iwanaga N, et al. Th1 cytokine endotype discriminates and predicts severe complications in COVID-19. Eur Cytokine Netw. 2022; 33(2): 1–12.
- 37Alberici F, Delbarba E, Manenti C, Econimo L, Valerio F, Pola A, et al. A report from the Brescia Renal COVID Task Force on the clinical characteristics and short-term outcome of hemodialysis patients with SARS-CoV-2 infection. Kidney Int. 2020; 98(1): 20–6.
- 38Goicoechea M, Sanchez Camara LA, Macias N, Munoz de Morales A, Rojas AG, Bascunana A, et al. COVID-19: clinical course and outcomes of 36 hemodialysis patients in Spain. Kidney Int. 2020; 98(1): 27–34.
- 39Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan. China JAMA. 2020; 323(11): 1061–9.
- 40Shang W, Li Y, Li H, Li W, Li C, Cai Y, et al. Correlation between laboratory parameters on admission and outcome of COVID-19 in maintenance hemodialysis patients. Int Urol Nephrol. 2021; 53(1): 165–9.
- 41Turgutalp K, Ozturk S, Arici M, Eren N, Gorgulu N, Islam M, et al. Determinants of mortality in a large group of hemodialysis patients hospitalized for COVID-19. BMC Nephrol. 2021; 22(1): 29.
- 42Regev-Yochay G, Gonen T, Gilboa M, Mandelboim M, Indenbaum V, Amit S, et al. Efficacy of a fourth dose of Covid-19 mRNA vaccine against omicron. N Engl J Med. 2022; 386(14): 1377–80.