Advertisement
Review| Volume 61, ISSUE 4, 103433, August 2022

Role of therapeutic plasma exchange in the management of COVID-19-induced cytokine storm syndrome

Open AccessPublished:March 22, 2022DOI:https://doi.org/10.1016/j.transci.2022.103433
Role of therapeutic plasma exchange in the management of COVID-19-induced cytokine storm syndrome
Previous ArticleThe impact of immediate adverse donation reactions on the return of volunteers undergoing platelet apheresis

      Abstract

      The risk of mortality in patients with coronavirus disease 2019 (COVID-19) is largely related to an excessive immune response, resulting in a hyperinflammatory and hypercoagulable condition collectively referred to as cytokine storm syndrome (CSS). Management of critically ill patients with COVID-19 has included attempts to abate this process, prevent disease progression, and reduce mortality. In this context, therapeutic plasma exchange (TPE) offers an approach to eliminate inflammatory factors and cytokines, offset the pathologic coagulopathy, and reduce the CSS effects. The aim of this review is to analyze available data on the use of TPE for the treatment of CSS in patients with COVID-19. Systematic searches of PubMed, Scopus and COVID-19 Research were conducted to identify articles published between March 1, 2020 and May 26, 2021 reporting the use of TPE for the treatment of COVID-19-induced CSS. A total of 34 peer-reviewed articles (1 randomized controlled trial, 4 matched case-control series, 15 single-group case series, and 14 case reports), including 267 patients, were selected. Despite the low evidence level of the available data, TPE appeared to be a safe intervention for critically ill patients with COVID-19-induced CSS. Although inconsistencies exist between studies, they showed a general trend for decreased interleukin-6, C-reactive protein, ferritin, D-dimer, and fibrinogen levels and increased lymphocyte counts following TPE, supporting the immunomodulatory effect of this treatment. Moreover, TPE was associated with improvements in clinical outcomes in critically ill patients with COVID-19. While TPE may offer a valuable option to treat patients with COVID-19-induced CSS, high-quality randomized controlled clinical trials are needed to confirm its potential clinical benefits, feasibility, and safety. Moreover, clear criteria should be established to identify patients with CSS who might benefit from TPE.

      Graphical Abstract

      ga1
      Graphical Abstract

      Abbreviations:

      ADAMTS-13 (a disintegrin and metalloproteinase with a thrombospondin type 1 motif, member 13), ARDS (acute respiratory syndrome), ASFA (American Society for Apheresis), CCP (COVID-19 convalescent plasma), COVID-19 (coronavirus disease 2019), CRP (C-reactive protein), CSS (cytokine storm syndrome), FFP (fresh frozen plasma), ICU (intensive care unit), IFN (interferon), IL (interleukin), LOS (length of stay), MAS (macrophage activation syndrome), MODS (multiple organ dysfunction syndrome), PaO2:FiO2 (pressure of arterial oxygen to fractional inspired oxygen concentration), RCT (randomized controlled trial), SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), sHLH (secondary hemophagocytic lymphohistiocytosis), SOFA (Sequential Organ Failure Assessment), TAMOF (thrombocytopenia-associated multiple organ failure), TNF (tumor necrosis factor), TPE (therapeutic plasma exchange)

      Keywords

      1. Background

      The coronavirus disease 2019 (COVID-19) caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is responsible for the pandemic declared by the World Health Organization on March 11, 2020 [
      • Cucinotta D.
      • Vanelli M.
      WHO Declares COVID-19 a Pandemic.
      Acta Biomed. 2020; 91: 157-160
      ]. Up to June 22, 2021, COVID-19 has caused > 177 million infections and > 3.85 million deaths [

      World Health Organization. Weekly Epidemiological Update. Available at: 〈https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports/〉 [Accessed on March 23, 2021].

      ]. Patients with COVID-19 show a variety of symptoms, ranging from mild, flu-like symptoms (81% of cases) to severe (14%) and critical (5%) manifestations [
      • Wu Z.
      • McGoogan J.M.
      Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: Summary of a report of 72 314 cases from the Chinese center for disease control and prevention.
      JAMA. 2020; 323: 1239-1242
      ]. The risk of mortality in critically ill patients is attributed mainly to an excessive immune response rather than to the viral infection itself. Most patients with severe COVID-19 in the intensive care unit (ICU) have significant increases in cytokines and other inflammatory biomarkers, such as interleukins (ILs), interferons (IFNs), tumor necrosis factors (TNFs), colony-stimulating factors, growth factors, ferritin, C-reactive proteins (CRPs), and D-dimers [
      • Song P.
      • Li W.
      • Xie J.
      • Hou Y.
      • You C.
      Cytokine storm induced by SARS-CoV-2.
      Clin Chim Acta. 2020; 509: 280-287
      ,
      • Nagant C.
      • Ponthieux F.
      • Smet J.
      • Dauby N.
      • Doyen V.
      • Besse-Hammer T.
      • et al.
      A score combining early detection of cytokines accurately predicts COVID-19 severity and intensive care unit transfer.
      Int J Infect Dis. 2020; 101: 342-345
      ,
      • Kermali M.
      • Khalsa R.K.
      • Pillai K.
      • Ismail Z.
      • Harky A.
      The role of biomarkers in diagnosis of COVID-19 - A systematic review.
      Life Sci. 2020; 254117788
      ,
      • Xu L.
      • Mao Y.
      • Chen G.
      Risk factors for 2019 novel coronavirus disease (COVID-19) patients progressing to critical illness: a systematic review and meta-analysis.
      Aging (Albany N Y). 2020; 12: 12410-12421
      ,
      • Moore J.B.
      • June C.H.
      Cytokine release syndrome in severe COVID-19.
      Science. 2020; 368: 473-474
      ]. This excessive and prolonged cytokine response can induce the recruitment of other immune cells (e.g., lymphocytes, monocytes/macrophages, dendritic cells), causing an exponential inflammatory growth [
      • Song P.
      • Li W.
      • Xie J.
      • Hou Y.
      • You C.
      Cytokine storm induced by SARS-CoV-2.
      Clin Chim Acta. 2020; 509: 280-287
      ,
      • Shimabukuro-Vornhagen A.
      • Gödel P.
      • Subklewe M.
      • Stemmler H.J.
      • Schlößer H.A.
      • Schlaak M.
      • et al.
      Cytokine release syndrome.
      J Immunother Cancer. 2018; 6: 56
      ,
      • Lippi G.
      • Plebani M.
      Cytokine “storm”, cytokine “breeze”, or both in COVID-19?.
      Clin Chem Lab Med. 2021; 59: 637-639
      ]. This hyperinflammatory condition, often called cytokine storm syndrome (CSS) or cytokine release syndrome, causes complement activation, endothelial damage, pathologic activation of the coagulation system, and increased vascular permeability. Clinically, CSS may result in lung damage, acute respiratory distress syndrome (ARDS), multiple organ dysfunction syndrome (MODS), and sepsis [
      • Song P.
      • Li W.
      • Xie J.
      • Hou Y.
      • You C.
      Cytokine storm induced by SARS-CoV-2.
      Clin Chim Acta. 2020; 509: 280-287
      ,
      • Huang C.
      • Wang Y.
      • Li X.
      • Ren L.
      • Zhao J.
      • Hu Y.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      Lancet. 2020; 395: 497-506
      ,
      • Liu Y.
      • Yang Y.
      • Zhang C.
      • Huang F.
      • Wang F.
      • Yuan J.
      • et al.
      Clinical and biochemical indexes from 2019-nCoV infected patients linked to viral loads and lung injury.
      Sci China Life Sci. 2020; 63: 364-374
      ,
      • Huang Y.
      • Tu M.
      • Wang S.
      • Chen S.
      • Zhou W.
      • Chen D.
      • et al.
      Clinical characteristics of laboratory confirmed positive cases of SARS-CoV-2 infection in Wuhan, China: A retrospective single center analysis.
      Travel Med Infect Dis. 2020; 36101606
      ,
      • Yuki K.
      • Fujiogi M.
      • Koutsogiannaki S.
      COVID-19 pathophysiology: A review.
      Clin Immunol. 2020; 215108427
      ,
      • Ye Q.
      • Wang B.
      • Mao J.
      The pathogenesis and treatment of the `Cytokine Storm' in COVID-19.
      J Infect. 2020; 80: 607-613
      ].
      Currently, there is no approved specific treatment for COVID-19, but various therapeutic agents (e.g., tocilizumab, steroids) showed some level of effectiveness [
      • Bokharee N.
      • Khan Y.H.
      • Khokhar A.
      • Mallhi T.H.
      • Alotaibi N.H.
      • Rasheed M.
      Pharmacological interventions for COVID-19: a systematic review of observational studies and clinical trials.
      Expert Rev Anti Infect Ther. 2021; https://doi.org/10.1080/14787210.2021.1902805
      ]. Besides supportive/standard care, management of patients with COVID-19 might also include timely control of the CSS to prevent disease aggravation and reduce mortality [
      • Song P.
      • Li W.
      • Xie J.
      • Hou Y.
      • You C.
      Cytokine storm induced by SARS-CoV-2.
      Clin Chim Acta. 2020; 509: 280-287
      ,
      • Ye Q.
      • Wang B.
      • Mao J.
      The pathogenesis and treatment of the `Cytokine Storm' in COVID-19.
      J Infect. 2020; 80: 607-613
      ]. In this context, potentially effective treatment approaches include administration of immunomodulators, cytokine antagonists, monoclonal antibodies, and anti-inflammatory drugs [
      • Song P.
      • Li W.
      • Xie J.
      • Hou Y.
      • You C.
      Cytokine storm induced by SARS-CoV-2.
      Clin Chim Acta. 2020; 509: 280-287
      ,
      • Ye Q.
      • Wang B.
      • Mao J.
      The pathogenesis and treatment of the `Cytokine Storm' in COVID-19.
      J Infect. 2020; 80: 607-613
      ,
      • Tharmarajah E.
      • Buazon A.
      • Patel V.
      • Hannah J.R.
      • Adas M.
      • Allen V.B.
      • et al.
      IL-6 inhibition in the treatment of COVID-19: a meta-analysis and meta-regression.
      J Infect. 2021; 82: 178-185
      ,
      • Cron R.Q.
      COVID-19 cytokine storm: targeting the appropriate cytokine.
      Lancet Rheumatol. 2021; 3: e236-e237
      ]. Therapeutic plasma exchange (TPE) may also be a valuable option to control CSS by removing inflammatory markers and cytokines [
      • Song P.
      • Li W.
      • Xie J.
      • Hou Y.
      • You C.
      Cytokine storm induced by SARS-CoV-2.
      Clin Chim Acta. 2020; 509: 280-287
      ,
      • Ye Q.
      • Wang B.
      • Mao J.
      The pathogenesis and treatment of the `Cytokine Storm' in COVID-19.
      J Infect. 2020; 80: 607-613
      ,
      • Reeves H.M.
      • Winters J.L.
      The mechanisms of action of plasma exchange.
      Br J Haematol. 2014; 164: 342-351
      ,
      • Tabibi S.
      • Tabibi T.
      • Conic R.R.Z.
      • Banisaeed N.
      • Streiff M.B.
      Therapeutic plasma exchange: A potential management strategy for critically ill COVID-19 patients.
      J Intensive Care Med. 2020; 35: 827-835
      ]. The purpose of this review is to compile and analyze available data on the use of TPE for the treatment of CSS in patients with COVID-19.

      2. Methods

      A systematic literature search was conducted to identify studies using TPE in hospitalized patients with COVID-19. Systematic searches of PubMed, Scopus, and a Dialog database called COVID-19 Research were conducted for articles published between March 1, 2020 and May 26, 2021. The searches were performed with the following terms: ("plasma exchange" OR “plasmapheresis”) AND (“coronavirus” OR “COVID-19″ OR “SARS-CoV-2″ OR “2019-nCoV”). The search was done on April 24, 2020, and weekly updates were provided thereafter.
      Identified articles were screened by one reviewer. Relevant papers were selected if at least one COVID-19 patient received TPE. Articles were excluded if COVID-19 was not the reason for TPE treatment initiation, the technique was unclear, or the article was not written in English. Systematic literature reviews and meta-analyses were excluded, but their reference lists were checked for relevant articles that might have been overlooked. Subsequently, data concerning the characteristics of patients and their disease, TPE procedures and adjunct treatments, outcomes (laboratory parameters and clinical outcomes), and TPE safety were extracted from selected articles.
      Methodologic classification of articles was performed using the Oxford Centre for Evidence-Based Medicine levels by two assessors, with differences resolved by consensus [

      Howick J., Chalmers I., Glasziou P., Greenhalgh T., Heneghan C., Liberati A., et al. The Oxford Levels of Evidence 2. Oxford Centre for Evidence-Based Medicine. Available at: 〈https://www.cebm.ox.ac.uk/resources/levels-of-evidence/ocebm-levels-of-evidence〉; 2011 [Accessed on March 23, 2021].

      ]. The severity of COVID-19-induced CSS in the selected studies was evaluated using the Penn grading scale by two assessors [
      • Porter D.
      • Frey N.
      • Wood P.A.
      • Weng Y.
      • Grupp S.A.
      Grading of cytokine release syndrome associated with the CAR T cell therapy tisagenlecleucel.
      J Hematol Oncol. 2018; 11: 35
      ].

      3. Results

      3.1 General information on search results

      The systematic literature search identified 468 articles (344 after duplicates removal), of which 77 articles were selected for full-text screening (Fig. 1). Of these, 43 articles did not meet selection criteria. In total, 34 peer-reviewed articles were included (1 randomized controlled clinical trial [RCT] [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ], 4 matched case-control series [
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      ,
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ], 15 single-group case series [
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ], and 14 case reports including < 3 patients [
      • Akkoyunlu Y.
      • Cetin G.
      • Bolukcu S.
      • Okay G.
      • Ogun H.
      • Durdu B.
      • et al.
      The successful management of an elderly Covid-19 infected patient by plasmapheresis.
      Transfus Apher Sci. 2020; 59102924
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      ,
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      ,
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      ,
      • Sadeghi A.
      • Dooghaie Moghadam A.
      • Eslami P.
      • Pirsalehi A.
      • Salari S.
      • Roshandel E.
      Vasculopathy-related cutaneous lesions and intrahepatic cholestasis as synchronous manifestations in a COVID-19 patient; a case report.
      Gastroenterol Hepatol Bed Bench. 2020; 13: 400-404
      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ,
      • Tian H.
      • Sui Y.
      • Tian S.
      • Zou X.
      • Xu Z.
      • He H.
      • et al.
      Case report: clinical treatment of the first critical patient with coronavirus disease (COVID-19) in Liaocheng, Shandong Province.
      Front Med ((Lausanne)). 2020; 7: 249
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ]), disclosing outcomes for 267 TPE-treated patients (Table 1).
      Fig. 1
      Fig. 1PRISMA flowchart. COVID-19, coronavirus disease 2019; CSS, cytokine storm syndrome; n, number of records; TPE, therapeutic plasma exchange.
      Table 1Characteristics of included studies and patients.
      First author, country, study groupOxford level of evidenceNumber of patientsDisease severityARDS, MODS and/or septic shockTypes of organ damageMechanical ventilationSOFA scoreCSS Penn grade*Comorbidities
      Randomized controlled clinical trial
      Faqihi, Saudi Arabia
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      TPE group      		343Life-threateningARDS (43), MODS (43), septic shock (43)Pulmonary embolism (13)MV (43)Median (IQR): 10 (8–13)Grade 4 (43)Diabetes (10), hypertension (19), coronary artery disease (1)
      Control group44Life-threateningARDS (43), MODS (43), septic shock (43)Pulmonary embolism (6)MV (44)Median (IQR): 9 (6–12)Grade 4 (44)Diabetes (8), hypertension (16), coronary artery disease (1)
      Matched case-control series
      Arulkumaran, UK
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      TPE group      		47CriticalARDS (7), MODS (NR), septic shock (NR)Bilateral lung infiltrates (7)MV (3), CPAP (4)NRGrade 3 (3), Grade 4 (4)Asthma (3), obesity (2), nil (1), previous deep vein thrombosis (1), none (1)
      Control group7CriticalNRBilateral lung infiltrates (7)NRNRNRNR
      Gucyetmez, Turkey
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      TPE group      		418 (12 after PSM)Patients in ICUNRPneumonia (18), AKI (6)IMV (16), NIMV (1), HFOT (1)Mean ± SD: 6 ± 1Grade 3 (1; 1 after PSM), Grade 4 (17; 11 after PSM)NR
      Control group35 (12 after PSM)Patients in ICUNRPneumonia (18), AKI (19)IMV (30), NIMV (3) HFOT (2)Median (IQR): 7 (3)Grade 3 (2; 0 after PSM), Grade 4 (33; 12 after PSM)NR
      Kamran, Pakistan
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      TPE group      		471 (45 after PSM)Moderate (3), severe (20), critical (22)NRNRIMV (3), CPAP (19)NRGrade 3 (19), Grade 4 (3), unknown (23)Obstructive air way disease (2), ischemic heart disease (6), diabetes (11), hypertension (9), > 3 comorbidities (4), none (21)
      Control group209 (45 after PSM)Moderate (3), severe (20), critical (22)NRNRIMV (3), CPAP (19)NRGrade 3 (19), Grade 4 (3), unknown (23)Obstructive air way disease (2), ischemic heart disease (6), diabetes (11), hypertension (9), > 3 comorbidities (4), none (21)
      Khamis, Oman
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      TPE group      		411CriticalARDS (10); septic shock (9); MODS (1)Severe pneumonia (1)IMV (10)Median (IQR): 6 (3–9)Grade 3 (1), Grade 4 (10)Obesity (1), diabetes (8), hypertension (6), CKD (1)
      Control group20CriticalARDS (10), septic shock (10), MODS (3)Severe pneumonia (10)IMV (11)Median (IQR): 3 (2–6)Grade 3 (9), Grade 4 (11)Obesity (2), diabetes (7), hypertension (6), CKD (3)
      Single-group case series
      Adeli, Iran
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      		48CriticalARDS (8), MODS (1), septic shock (8)Pulmonary involvement (8)MV (3), oxygen mask (5)NRGrade 3 (5), Grade 4 (3)Hypertension (1), diabetes (2), none (5)
      Alharthy, Saudi Arabia
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      		53Life-threatening with associated thromboinflammation and CNS pathologyARDS (3), MODS (NR), septic shock (NR)Brain infarction (3), pulmonary embolism (3)MV (3)8 (1), 9 (2)Grade 4 (3)Hypertension and diabetes (2), none (1)
      Faqihi, Saudi Arabia
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      		410Life-threateningARDS (10), MODS (10), septic shock (10)Pulmonary embolism (2), AKI (1), pneumonia (10)MV (10)Median (IQR): 11 (8.9–11.5)Grade 4 (10)Diabetes (6), hypertension (5), cardiovascular disease (1), none (4)
      Gluck, USA
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      		410CriticalNRNRIMV (6)NRGrade 3 (4), Grade 4 (6)Diabetes (3), hypertension (5), obesity (6)
      Hashemian, Iran
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      		415CriticalARDS (15), MODS (NR), septic shock (NR)NRIMV (4), NIMV (11)Mean ± SD: 9.6 ± 1.5Grade 3 (11); Grade 4 (4)Hypertension (6), diabetes (5), cardiovascular disease (2), none (5)
      Jaiswal, Dubai, United Arab Emirates
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      		414CriticalARDS (14), MODS (NR), septic shock (14)AKI (5)IMV (14)NRGrade 4 (14)Hypertension (9), none (4)
      Keith, USA
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      		48CriticalARDS (8), MODS (8); septic shock (8)NRMV (7), CPAP (1)Mean (range): 6.8 (2–15)Grade 4 (8)Hypertension (4), hyperlipidemia and gastroesophageal reflux disease (1), cerebral palsy (1), diabetes (1), systemic lupus, erythematosus and benign prostatic hypertrophy (1), prostate cancer (1), obesity (2), dementia, pseudotumor cerebri, renal disease and stroke (1), obstructive sleep apnea, CKD, atrial fibrillation and diastolic heart failure (1)
      Morath, Germany
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      		45CriticalARDS (5), MODS (5), circulatory shock or refractory fever (5)AKI (5)NRNRGrade 4 (5)Diabetes (2), hypertension (3), coronary artery disease (1), schizophrenia and depression (1), atrial fibrillation (1), stroke (1), CKD, obesity (1), none (1)
      Wang, China (Wuhan)
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      		53 childrenCriticalNRAKI (3), pleural effusion (3), ascites (2), gastrointestinal involvement (2)MV (3)NRGrade 4 (3)Immunocompromised patient with acute lymphocytic leukemia (1)
      Zhang, China
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      		53SevereARDS (3), MODS (NR), septic shock (NR)NRHFOT (3)NRGrade 3 (3)NR
      De Prost, France
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      		44Life-threatening with auto-antibodies against type I IFNsARDS (4), MODS (NR), septic shock (1)Pneumonia (4)IMV (3), NIMV (1), ECMO (2)7 (3), 8 (1)Grade 3 (1), Grade 4 (3)Obesity (2), pregnancy (1), hypertension and diabetes (1)
      Fernandez, Spain
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      		44CriticalMODS (3)AKI (3), bilateral lung infiltrates (4), cardiac hypomotility (1), myocarditis (1), thrombotic events (1), acute limb ischemia (1), hepatic encephalopathy (1)IMV (3)6, 7, 9, 11Grade 4 (4)Obesity (2), diabetes (3), hypertension (4), liver transplantation (1), CKD (1), alcoholic liver cirrhosis (1)
      Truong, USA
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      		46Critical with hyperviscosityARDS (3), septic shock (4)AKI (5), encephalopathy (3), cardiac arrhythmias (1), ischemia (1), shock liver (1), lower extremity deep venous thrombosis (1)IMV5, 8, 14, 15Grade 4 (6)Hypertension (3), diabetes (2), seizure disorder (1), COPD (2), coronary artery disease (1), cirrhosis (1)
      Matsushita, Japan

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      		45SevereARDS (1)Bilateral consolidation in the lungs (1), ground-glass opacities in the lungs (3)IMV (3)NRGrade 3 (2), Grade 4 (3)End-stage renal disease on dialysis (2), malignancy (4), diabetes (1), hypertension (1), cerebral infarction and subdural hematoma (1)
      Roshandel, Iran
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      		45CriticalARDS (5)Severe pneumonia and/or ground-glass opacity (5)MV (1), oxygen by mask (4)NRGrade 3 (4), Grade 4 (1)Diabetes (2), hypertension (2), anemia (1), asthma (1), hypothyroidism (1), myocardial infarction (1), chronic lymphocytic leukemia (1), secondary hemophagocytic lymphohistiocytosis (1), hypercholesterolemia and coronary artery bypass grafting (1)
      Case reports
      Akkoyunlu, Turkey
      • Akkoyunlu Y.
      • Cetin G.
      • Bolukcu S.
      • Okay G.
      • Ogun H.
      • Durdu B.
      • et al.
      The successful management of an elderly Covid-19 infected patient by plasmapheresis.
      Transfus Apher Sci. 2020; 59102924
      		51CriticalNRBilateral multiple consolidations in the lungsHFOTNRGrade 3Asthma, hypertension, diabetes
      Altmayer, France
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      		51CriticalARDSBilateral interstitial infiltrates in the lungsIMVNRGrade 4Hypertension, diabetes, overweight
      Bagherzade, Iran
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      		51Critical (respiratory arrest and loss of consciousness)NRBilateral ground-glass opacities in the lungsIMVNRGrade 4NR
      Faqihi, Saudi Arabia
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      		51Life-threateningARDS, sepsisPeripheral neuropathy, peripheral bilateral ground-glass opacities in the lungsIMVNRGrade 4None
      Hua, China

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      		51CriticalNRProgressive lung infiltrates and diffuse griddingIMVNRGrade 4COPD, hypertension, diabetes
      Kamit, Turkey
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      		51 childCriticalARDS, MODS, septic shockPneumonia, sinus tachycardia, metabolic acidosis, renal failureIMVNRGrade 4Angelman syndrome and high-risk T cell acute lymphoblastic leukemia
      Keith, USA

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      		51CriticalARDS, MODS, septic shockPneumonia, hypokinesisCPAP7Grade 4Congestive heart failure, paroxysmal atrial fibrillation, obstructive sleep apnea, hypertension, obesity, diabetes
      Lin, Taiwan
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      		51CriticalNRPneumoniaIMVNRGrade 4NR
      Ma, China
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      		51CriticalNRBilateral ground-glass shadows in the lungs, dry gangrene in the finger, multiple cerebral infarctions, antiphospholipid syndromeIMVNRGrade 4None
      Ragab, Egypt
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      		51SevereARDSDiffuse bilateral patches of ground‐glass opacities in the lungsHFOTNRGrade 3Diabetes, hypertension
      Sadeghi, Iran
      • Sadeghi A.
      • Dooghaie Moghadam A.
      • Eslami P.
      • Pirsalehi A.
      • Salari S.
      • Roshandel E.
      Vasculopathy-related cutaneous lesions and intrahepatic cholestasis as synchronous manifestations in a COVID-19 patient; a case report.
      Gastroenterol Hepatol Bed Bench. 2020; 13: 400-404
      		51SevereNRBilateral multifocal peripheral ground-glass opacity, vasculopathy-related cutaneous manifestation and liver cholestasisNRNRGrade 2None
      Shi, China
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      		51CriticalSeptic shockRapidly progressive pulmonary lesionsHFOTNRGrade 4History of thyroid nodule
      Tian, China
      • Tian H.
      • Sui Y.
      • Tian S.
      • Zou X.
      • Xu Z.
      • He H.
      • et al.
      Case report: clinical treatment of the first critical patient with coronavirus disease (COVID-19) in Liaocheng, Shandong Province.
      Front Med ((Lausanne)). 2020; 7: 249
      		51CriticalNRGround-glass opacity with multiple patchy consolidationsHFOTNRGrade 3Diabetes
      Yang, China
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      		51CriticalARDSPneumoniaIMVNRGrade 4None
      AKI, acute kidney injury; ARDS, acute respiratory distress syndrome; CKD, chronic kidney disease; CNS, central nervous system; COPD, chronic obstructive pulmonary disease; CPAP, continuous positive airway pressure; CSS, cytokine storm syndrome; ECMO, extracorporeal membrane oxygenation; HFOT, high-flow oxygen therapy; ICU, intensive care unit; IFN, interferon; IMV, invasive mechanical ventilation; IQR, interquartile range; MODS, multiple organ dysfunction syndrome; MV, mechanical ventilation; NIMV, non-invasive mechanical ventilation; NR, not reported; PSM, propensity score matching; SD, standard deviation; SOFA, Sequential Organ Function Assessment; TPE, therapeutic plasma exchange; UK, United Kingdom; USA, United States of America. * Evaluated by the authors of this review.
      The RCT was categorized as Oxford level 3 (downgraded because of early termination and small sample size) [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ]. The 4 matched case-control series and 12 single-group case series were categorized as Oxford level 4 [
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      ,
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ], and 3 single-group case series (downgraded because only 3 patients were included) and all case reports as Oxford level 5 [
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,
      • Akkoyunlu Y.
      • Cetin G.
      • Bolukcu S.
      • Okay G.
      • Ogun H.
      • Durdu B.
      • et al.
      The successful management of an elderly Covid-19 infected patient by plasmapheresis.
      Transfus Apher Sci. 2020; 59102924
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      ,
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      ,
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      ,
      • Sadeghi A.
      • Dooghaie Moghadam A.
      • Eslami P.
      • Pirsalehi A.
      • Salari S.
      • Roshandel E.
      Vasculopathy-related cutaneous lesions and intrahepatic cholestasis as synchronous manifestations in a COVID-19 patient; a case report.
      Gastroenterol Hepatol Bed Bench. 2020; 13: 400-404
      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ,
      • Tian H.
      • Sui Y.
      • Tian S.
      • Zou X.
      • Xu Z.
      • He H.
      • et al.
      Case report: clinical treatment of the first critical patient with coronavirus disease (COVID-19) in Liaocheng, Shandong Province.
      Front Med ((Lausanne)). 2020; 7: 249
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ].

      3.2 Patients and disease characteristics

      While most TPE-treated patients had critical or life-threatening COVID-19, a few patients with severe or moderate disease were also included in the selected studies (Table 1). Using the Penn grading scale [
      • Porter D.
      • Frey N.
      • Wood P.A.
      • Weng Y.
      • Grupp S.A.
      Grading of cytokine release syndrome associated with the CAR T cell therapy tisagenlecleucel.
      J Hematol Oncol. 2018; 11: 35
      ], we estimated that all TPE-treated patients had grade 3 or 4 CSS (except one patient with grade 2 CSS). Available Sequential Organ Failure Assessment (SOFA) scores, which are based on the degree of organ dysfunction [
      • Vincent J.L.
      • Moreno R.
      • Takala J.
      • Willatts S.
      • De Mendonça A.
      • Bruining H.
      • et al.
      The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the working group on sepsis-related problems of the European society of intensive care medicine.
      Intensive Care Med. 1996; 22: 707-710
      ] and may help to predict outcomes in critically ill patients, ranged between 2 and 15 (median ranging from 3 to 11).
      Many studies included patients with ARDS [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ], MODS [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ], and/or septic shock [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ]. Other damaged organs included kidneys, liver, brain, heart, and gastrointestinal tract. Acute limb ischemia, neuropathies, and cutaneous manifestations were also reported [
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,
      • Sadeghi A.
      • Dooghaie Moghadam A.
      • Eslami P.
      • Pirsalehi A.
      • Salari S.
      • Roshandel E.
      Vasculopathy-related cutaneous lesions and intrahepatic cholestasis as synchronous manifestations in a COVID-19 patient; a case report.
      Gastroenterol Hepatol Bed Bench. 2020; 13: 400-404
      ]. Almost all patients received oxygen support before TPE administration (e.g., mechanical ventilation, continuous positive airway pressure, or high-flow oxygen therapy) (Table 1). Patients often had underlying comorbidities associated with poor clinical outcomes in COVID-19, such as diabetes, hypertension, obesity, cardiovascular disease, and/or chronic kidney disease (Table 1).

      3.3 Treatment characteristics

      The rationale for TPE treatment in patients with COVID-19 varied between studies, but the most frequent reasons were critical disease consisting of either severe ARDS with high and rapidly increasing ferritin or D-dimer levels [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Akkoyunlu Y.
      • Cetin G.
      • Bolukcu S.
      • Okay G.
      • Ogun H.
      • Durdu B.
      • et al.
      The successful management of an elderly Covid-19 infected patient by plasmapheresis.
      Transfus Apher Sci. 2020; 59102924
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      ,
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      ,
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      ,
      • Tian H.
      • Sui Y.
      • Tian S.
      • Zou X.
      • Xu Z.
      • He H.
      • et al.
      Case report: clinical treatment of the first critical patient with coronavirus disease (COVID-19) in Liaocheng, Shandong Province.
      Front Med ((Lausanne)). 2020; 7: 249
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ], and/or sepsis or MODS [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ] (Table 2).
      Table 2Treatment of COVID-19 patients who received TPE.
      First author, country, study groupNumber of patientsRationale for TPEReplacement fluid and TPE systemVolume of replacement fluidNumber of TPE treatmentFrequency of TPE treatmentAdjunct immunoregulatory therapyOther adjunct treatment linked to TPEOther adjunct treatment not linked to TPE
      Randomized controlled clinical trial
      Faqihi, Saudi Arabia
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      TPE group      		43Patients with life-threatening COVID-19 (ARDS and septic shock or MODS, and with ≥ 1 criteria defining CSS)FFP or Octaplas1.5 plasma volume for the first session, then 1 plasma volumeMedian (IQR): 3 (1–5)DailyNoneNorepinephrine (1 patient)Antivirals (ribavirin), antibacterial medications, dexamethasone, anticoagulation
      Control group44Patients with life-threatening COVID-19 (ARDS and septic shock or MODS, and with ≥ 1 criteria defining CSS)NANANANANoneNorepinephrine (1 patient)Antivirals (ribavirin), antibacterial medications, dexamethasone, anticoagulation
      Matched case-control series
      Arulkumaran, UK
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      TPE group      		7Critically ill patients with severe respiratory failure and elevated thrombo-inflammatory markersOctaplas LG; Spectra Optia Apheresis System3 L5–10DailyNoneNoneIntermediate dose LMWH
      Control group7NANANANANANoneNAIntermediate dose LMWH if confirmed thromboembolic event
      Gucyetmez, Turkey
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      TPE group      		18Patients with pneumonia and D-dimer ≥ 2 mg/LNRNR3NRCytokine filters: 2 (16.7%); IL-6 blocker: 7 (58.3%); steroids: 7 (58.3%)NoneTherapeutic anticoagulation (UFH or LMWH), favipiravir, hydroxychloroquine, azithromycin
      Control group35NANANANANACytokine filters: 1 (8.3%); IL-6 blocker: 6 (50%); steroids: 7 (58.3%)NANA
      Kamran, Pakistan
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      TPE group      		45Patients with CSSFFP and normal saline (2:1); COBE Spectra Apheresis System/ continuous flow centrifugation1.5 plasma volumeMedian (IQR): 2.25 (1–5)DailySteroids, methylprednisoloneNoneAnticoagulation
      Control group45NANANANANASteroids, methylprednisoloneNAAnticoagulation
      Khamis, Oman
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      TPE group      		11Patients with confirmed or imminent respiratory failure and ARDS, severe pneumonia, septic shock or MODSFFP; Spectra Optia Apheresis SystemBody weight (kg) × (1/13) × (100-hematocrit)5DailyTocilizumab: 55% of patientsNRNR
      Control group20NANANANANATocilizumab: 30% of patientsNANR
      Single-group case series
      Adeli, Iran
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      		8Patients with septic shock and ARDS with poor response to antiviral treatment, corticosteroid therapy and interferon administration4 units of FFP, 5 vials of albumin and normal saline2 L3–5DailyInterferon β, corticosteroid therapy (dexamethasone)One or two 10–20 mL calcium gluconate (20%)Hydroxychloroquine sulfate, antiviral drugs
      Alharthy, Saudi Arabia
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      		3Patients with life-threatening COVID-19 (ARDS, thromboembolic disease, and low GCS) and with a microangiopathic patternOctaplas; Spectra Optia Apheresis System1.5 plasma volume for the first dose and then 1 plasma volume5DailyHydrocortisone, interferon β-1bIntravenous calcium replacementChlorpheniramine, ribavirin, antibiotics, therapeutic anticoagulation
      Faqihi, Saudi Arabia
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      		10Patients with life-threatening COVID-19 (ARDS and septic shock, and with > 3 risk factors for CSS)Albumin 5% or FFP in patients with coagulopathy; Spectra Optia

      Apheresis System      		1.0–1.5 plasma volumes5–7DailyIntravenous hydrocortisoneNorepinephrine, vasopressinHydroxychloroquine, antibiotics, prophylactic anticoagulation
      Gluck, USA
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      		10Patients with Penn class 3 or 4 CSS complicating COVID-195% albumin (9 patients) or FFP in patients with coagulopathy (1 patient); Spectra Optia Apheresis System1.0 plasma volume5Daily for 2 consecutive days then every other dayNoneNoneHydroxychloroquine (2 patients)
      Hashemian, Iran
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      		15Patients with ARDS5% human albumin solution and 0.9% saline. 4 patients receive CCP; JMS fully automated SDS-20 hemodialysis machine40 mL/kg body weight33 times a weekCCP in 4 patientsNoneAntiviral drugs, meropenem in patients with respiratory tract infection
      Jaiswal, Dubai, United Arab Emirates
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      		14Critically ill patients (ARDS, sepsis and septic shock)FFP30–40 mL/kg bodyweight1NA500 mL of CCP 8 h after TPE; methylprednisoloneNoneEnoxaparin
      Keith, USA
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      		8Critically ill patients (ARDS, sepsis and septic shock)FFP; Spectra Optia Apheresis SystemApproximately 1 plasma volume1–7DailyCCP (4 patients); methylprednisolone (7 patients); tocilizumab (2 patients)Vasopressor (8 patients)Hydroxychloroquine (5 patients), azithromycin (7 patients), ivermectin (1 patient), anticoagulants (8 patients)
      Morath, Germany
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      		5MODS, ARDS, and AKIFFPMedian: 3.39 L1NATocilizumab (1 patient), interferon (1 patient), prednisolone (2 patients), immunoglobulins (1 patient), CCP (2 patients)Vasopressor treatment (4 patients)Antiviral treatment, antibiotics, antimycotics, hydroxychloroquine.
      Wang, China (Wuhan)
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      		3 childrenCritically ill pediatric patients with AKINRNR2–4VariableCorticosteroid therapy, immunoglobulinsNoneAnticoagulation (heparin), antibiotics, antiviral treatment.
      Zhang, China
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      		3Severe COVID-19 patients with ARDSFFP; plasma separator multi-filtration systemAbout 3 L1NAInterferon α-2bNoneAntiviral treatment, including arbidol.
      De Prost, France
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      		4Patients with life-threatening pneumonia (ARDS, high concentrations of neutralizing auto-antibodies against type I IFNs)Albumin 5% and plasma in different proportions; continuous flow centrifugation (3 patients) or plasma filtration (1 patient)Range: 32–57 mL/kg3–4Daily or every other dayDexamethasoneNoneNone
      Fernandez, Spain
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      		4Critically ill adults with COVID-19 pneumonia that failed conventional interventionsHuman albumin (5%)1.2 plasma volumes (range: 3.8–5 L)2–6Every other dayFFP and immunoglobulins (4 patients), dexamethasone (2 patients), methylprednisolone (2 patients), interferon β-1a (2 patients), tocilizumab (1 patient), anakinra and hydrocortisone (1 patient)Norepinephrine (2 patients)Hydroxychloroquine, antiviral drugs, antibiotics, heparin sodium
      Truong, USA
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      		6Critically ill patients with COVID-19-associated hyperviscosityFFP1 plasma volume2–3DailyNRVasopressors (2)Anticoagulants (heparin, argatroban, bivalirudin, enoxaparin)
      Matsushita, Japan

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      		5ARDS and/or labored respiration and/or tracheal intubation.FFP2.5–3 L3–7Daily or every other dayGlucocorticoid (5 patients), methylprednisolone pulse therapy (3 patients), hemodiafiltration (3 patients), hemoperfusion (2 patients)NRAnticoagulants (heparin), antiviral drugs, antibiotics
      Roshandel, Iran
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      		5Patients with ARDSAlbumin 5% + FFP for the 2 first sessions and CCP for the third session0.75 plasma volume3DailySteroidsNRAntiviral, anti-fungal and antibacterial treatments,
      Case reports
      Akkoyunlu, Turkey
      • Akkoyunlu Y.
      • Cetin G.
      • Bolukcu S.
      • Okay G.
      • Ogun H.
      • Durdu B.
      • et al.
      The successful management of an elderly Covid-19 infected patient by plasmapheresis.
      Transfus Apher Sci. 2020; 59102924
      		1Critically ill patient whose clinical status worsened despite antiviral and tocilizumab treatmentsFFP; multifiltrate model10 units1NATocilizumab, prednisoloneNoneHydroxychloroquine, antibiotics, antiviral treatment, anticoagulation (enoxaparine)
      Altmayer, France
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      		1Patient with ARDS and CSSAlbumin 5%; Spectra Optia1.2 plasma volume4Every other dayNRNoneAntibiotics
      Bagherzade, Iran
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      		1COVID-19 patient with respiratory arrest and loss of consciousnessNRNR5DailyCorticosteroid, interferon β-1b, dexamethasoneVasopressors (norepinephrine)Hydroxychloroquine, antiviral treatment, antibiotics, prophylactic anticoagulation
      Faqihi, Saudi Arabia
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      		1Patient with life-threatening COVID-19 characterized by peripheral neuropathy, ARDS, sepsis, and hyperinflammationOctaplas; Spectra Optia Apheresis System1.5 plasma volume for the first dose; then,1 plasma volume3DailyHydrocortisone, interferon β-1bIntravenous vasopressorsAntiviral treatment, antibiotics, prophylactic anticoagulation
      Hua, China

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      		1Critical COVID-19 patient with prolonged IMVFFP; Diapact CRRT system, and a filter membrane-based apparatus3 L3DailyMethylprednisoloneNorepinephrineAntiviral drugs
      Kamit, Turkey
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      		1 childChild with ARDS with hyperferritinemic MODS, and CSSFFP1.5 plasma volume for the 2 first doses; then 1 plasma volume4DailyTocilizumab, hydrocortisone, intravenous immunoglobulinEpinephrine, norepinephrineAntiviral drug, antibiotics, levetiracetam
      Keith, USA

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      		1Patient with pneumonia, septic shock and MOFFFP4.5 L1NANoneNorepinephrine and midodrineAmiodarone with magnesium and potassium replacement, digoxin, home sotalol
      Lin, Taiwan
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      		1Critically ill COVID-19 patient with CSSFFP0.065 × body weight × (1-hematocrit); 1 plasma (body weight × 40 mL); 1.5 plasma (body weight × 60 mL)3DailyNRNRContinuous venovenous hemofiltration
      Ma, China
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      		1Critically ill COVID-19 patient with CSSNRNR3DailyGamma globulinNRAntibiotics, antiviral drugs, LMWH, aspirin
      Ragab, Egypt
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      		1Patient with severe COVID‐19, ARDS and CSSFFP and CCP (400 mL)(0.065 × body weight) × (1 − hematocrit as a fraction)1NACCP, corticosteroids, methylprednisolone, dexamethasone, tocilizumabHydroxychloroquine sulfate, antibiotics, antiviral drugs, anticoagulant (enoxaparin sodium)
      Sadeghi, Iran
      • Sadeghi A.
      • Dooghaie Moghadam A.
      • Eslami P.
      • Pirsalehi A.
      • Salari S.
      • Roshandel E.
      Vasculopathy-related cutaneous lesions and intrahepatic cholestasis as synchronous manifestations in a COVID-19 patient; a case report.
      Gastroenterol Hepatol Bed Bench. 2020; 13: 400-404
      		1COVID-19 with vasculopathy-related cutaneous manifestation and liver cholestasisCCPNR3NROne unit of washed packed cells injection, prednisoloneNRHydroxychloroquine, naltrexone, hydroxyzine, antibiotics
      Shi, China
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      		1Critically ill COVID-19 patient with CSSFFP6 L4DailyHuman granulocyte-colony stimulating factor, thymalfasin, intravenous immunoglobulin, corticosteroids (methylprednisolone)Vasopressors (dopamine, noradrenalin)Antiviral drugs, antibiotics
      Tian, China
      • Tian H.
      • Sui Y.
      • Tian S.
      • Zou X.
      • Xu Z.
      • He H.
      • et al.
      Case report: clinical treatment of the first critical patient with coronavirus disease (COVID-19) in Liaocheng, Shandong Province.
      Front Med ((Lausanne)). 2020; 7: 249
      		1Critically ill COVID-19 patientMultifiltrate bedside blood purifier and plasma separator2 L1NAThymalfasin, immune globulin, methylprednisoloneNRAntiviral drugs, antibiotics, antimycotics, anticoagulant (enoxaparin)
      Yang, China
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      		1Critically ill COVID-19 patient with pneumonia that did not improve with tocilizumab and continuous renal replacement therapyAlbumin solution; double filtration plasmapheresis with a plasma separator and a plasma fractionator3 L3DailyMultiple blood transfusion including 400 mL CCP, methylprednisolone, tocilizumabNorepinephrineNR
      AKI, acute kidney injury; ARDS, acute respiratory distress syndrome; CCP, COVID-19 convalescent plasma; COVID-19, coronavirus disease 2019; CRRT, continuous renal replacement therapy; CSS, cytokine storm syndrome; FFP, fresh frozen plasma; GCS, Glasgow Coma Scale; IFN, interferon; IQR, interquartile range; IL, interleukin; IMV, invasive mechanical ventilation; LMWH, low molecular weight heparin; MODS, multiple organ dysfunction syndrome; MOF, multiple-organ failure; NA, not applicable; NR, not reported; TPE, therapeutic plasma exchange; UFH, unfractionated heparin; UK, United Kingdom; USA, United States of America.
      In general, three to five TPE sessions were performed [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      ,
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      ,
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      ,
      • Sadeghi A.
      • Dooghaie Moghadam A.
      • Eslami P.
      • Pirsalehi A.
      • Salari S.
      • Roshandel E.
      Vasculopathy-related cutaneous lesions and intrahepatic cholestasis as synchronous manifestations in a COVID-19 patient; a case report.
      Gastroenterol Hepatol Bed Bench. 2020; 13: 400-404
      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ], with a daily or every other day frequency [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Bagherzade M.
      • Parham M.
      • Zohali S.
      • Molaei S.
      • Vafaeimanesh J.
      Plasmapheresis with corticosteroids and antiviral: A life-saving treatment for severe cases of Covid 19.
      Caspian J Intern Med. 2020; 11: 572-576
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      ,
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ]. The most common replacement fluids were fresh frozen plasma (FFP) [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Jaiswal V.
      • Nasa P.
      • Raouf M.
      • Gupta M.
      • Dewedar H.
      • Mohammad H.
      • et al.
      Therapeutic plasma exchange followed by convalescent plasma transfusion in critical COVID-19-An exploratory study.
      Int J Infect Dis. 2021; 102: 332-334
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Akkoyunlu Y.
      • Cetin G.
      • Bolukcu S.
      • Okay G.
      • Ogun H.
      • Durdu B.
      • et al.
      The successful management of an elderly Covid-19 infected patient by plasmapheresis.
      Transfus Apher Sci. 2020; 59102924
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Lin J.H.
      • Chen Y.C.
      • Lu C.L.
      • Hsu Y.N.
      • Wang W.J.
      Application of plasma exchange in association with higher dose CVVH in Cytokine storm complicating COVID-19.
      J Formos Med Assoc. 2020; 119: 1116-1118
      ,
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856
      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ] and 5% albumin solutions [
      • de Prost N.
      • Bastard P.
      • Arrestier R.
      • Fourati S.
      • Mahévas M.
      • Burrel S.
      • et al.
      Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia.
      J Clin Immunol. 2021; 41: 536-544
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ] (Table 2). In some studies, FFP was used only for patients with coagulopathies and 5% albumin was used for other patients [
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ]. Different methods were used to determine the volume of replacement fluid, which was frequently expressed in plasma volume (range: 0.75–1.5) [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Kamran S.M.
      • Mirza Z.E.
      • Naseem A.
      • Liaqat J.
      • Fazal I.
      • Alamgir W.
      • et al.
      Therapeutic plasma exchange for coronavirus disease-2019 triggered cytokine release syndrome; a retrospective propensity matched control study.
      PLoS One. 2021; 16e0244853
      ,
      • Alharthy A.
      • Faqihi F.
      • Balhamar A.
      • Memish Z.A.
      • Karakitsos D.
      Life-threatening COVID-19 presenting as stroke with antiphospholipid antibodies and low ADAMTS-13 activity, and the role of therapeutic plasma exchange: A case series.
      SAGE Open Med Case Rep. 2020; 8: 1-7
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Keith P.D.
      • Scott L.K.
      • Weaver K.E.
      • Day M.
      • Choe C.
      • Perkins L.
      • et al.
      Treatment of critically ill coronavirus disease 2019 patients with adjunct therapeutic plasma exchange: A single-center retrospective case series.
      Crit Care Explor. 2021; 2e0223
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Truong A.D.
      • Auld S.C.
      • Barker N.A.
      • Friend S.
      • Wynn A.T.
      • Cobb J.
      • et al.
      Therapeutic plasma exchange for COVID-19-associated hyperviscosity.
      Transfusion. 2021; 61: 1029-1034
      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Altmayer V.
      • Saheb S.
      • Rohaut B.
      • Marois C.
      • Cao A.
      • Gallo A.
      • et al.
      Therapeutic plasma exchange in a critically ill Covid-19 patient.
      J Clin Apher. 2021; 36: 179-182
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ] or in liters (range: 2–6) [
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Adeli S.H.
      • Asghari A.
      • Tabarraii R.
      • Shajari R.
      • Afshari S.
      • Kalhor N.
      • et al.
      Therapeutic plasma exchange as a rescue therapy in patients with coronavirus disease 2019: a case series.
      Pol Arch Intern Med. 2020; 130: 455-458
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,

      Matsushita Y., Kusaoi M., Hiki M., Murayama G., Abe Y., Nozawa K., et al. Combination therapy with plasma exchange and glucocorticoid may be effective for severe COVID-19 infection: A retrospective observational study. Ther Apher Dial. 2021:PMID: 33887110.

      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,

      Keith P., Day M., Choe C., Perkins L., Moyer L., Hays E., et al. The successful use of therapeutic plasma exchange for severe COVID-19 acute respiratory distress syndrome with multiple organ failure. SAGE Open Med Case Rep. 2020;8:2050313×20933473.

      ,
      • Shi H.
      • Zhou C.
      • He P.
      • Huang S.
      • Duan Y.
      • Wang X.
      • et al.
      Successful treatment with plasma exchange followed by intravenous immunoglobulin in a critically ill patient with COVID-19.
      Int J Antimicrob Agents. 2020; 56105974
      ,
      • Tian H.
      • Sui Y.
      • Tian S.
      • Zou X.
      • Xu Z.
      • He H.
      • et al.
      Case report: clinical treatment of the first critical patient with coronavirus disease (COVID-19) in Liaocheng, Shandong Province.
      Front Med ((Lausanne)). 2020; 7: 249
      ,
      • Yang B.
      • Yang J.
      • Zhou L.
      • Xue C.
      • Li H.
      • Hu W.
      • et al.
      Inflammatory cytokine depletion in severe coronavirus disease 2019 infectious pneumonia: A case report.
      Medicine ((Baltimore)). 2020; 99e23449
      ].
      Besides TPE, many patients received adjunct immunoregulatory therapies, such as cytokine filtration, IL-6 blockers, IL-1 receptor antagonists, corticosteroids, IFN-α, IFN-β, COVID-19 convalescent plasma (CCP), immunoglobulins, human granulocyte-colony stimulating factors, thymalfasin, washed packed cells, hemodiafiltrations, hemoperfusions, or blood transfusions (Table 2). Patients often also received other treatments, including systemic anticoagulants, antibiotics, antiviral drugs, antimycotics, anti-inflammatory drugs, vasopressors, and/or renal replacement therapy. Citrate infusions were used as standard anticoagulant during TPE sessions [
      • Lee G.
      • Arepally G.M.
      Anticoagulation techniques in apheresis: From heparin to citrate and beyond.
      J Clin Apher. 2012; 27: 117-125
      ], and some patients received calcium infusions to prevent hypocalcemia and citrate toxicity.

      3.4 Evolution of immune-inflammatory biomarkers

      Since the main objectives of TPE are to decrease pro-inflammatory cytokines levels and correct coagulopathies, dynamic monitoring of these parameters is useful to evaluate the ability of TPE to abate the CSS.
      The levels of IL-6, a pro-inflammatory cytokine playing an important role in CSS and used as cytokinemia marker [
      • Zhang C.
      • Wu Z.
      • Li J.-W.
      • Zhao H.
      • Wang G.-Q.
      Cytokine release syndrome in severe COVID-19: Interleukin-6 receptor antagonist tocilizumab may be the key to reduce mortality.
      Int J Antimicrob Agents. 2020; 55105954
      ,
      • Webb B.J.
      • Peltan I.D.
      • Jensen P.
      • Hoda D.
      • Hunter B.
      • Silver A.
      • et al.
      Clinical criteria for COVID-19-associated hyperinflammatory syndrome: A cohort study.
      Lancet Rheumatol. 2020; 2: e754-e763
      ], decreased in most studies with available results [
      • Faqihi F.
      • Alharthy A.
      • Abdulaziz S.
      • Balhamar A.
      • Alomari A.
      • AlAseri Z.
      • et al.
      Therapeutic plasma exchange in patients with life-threatening COVID-19: A randomized control clinical trial.
      Int J Antimicrob Agents. 2021; 57106334
      ,
      • Arulkumaran N.
      • Thomas M.
      • Brealey D.
      • Alwan F.
      • Singh D.
      • Lunn M.
      • et al.
      Plasma exchange for COVID-19 thrombo-inflammatory disease.
      eJHaem. 2021; 2: 26-32
      ,
      • Gucyetmez B.
      • Atalan H.K.
      • Sertdemir I.
      • Cakir U.
      • Telci L.
      Therapeutic plasma exchange in patients with COVID-19 pneumonia in intensive care unit: A retrospective study.
      Crit Care. 2020; 24: 492
      ,
      • Khamis F.
      • Al-Zakwani I.
      • Al Hashmi S.
      • Al Dowaiki S.
      • Al Bahrani M.
      • Pandak N.
      • et al.
      Therapeutic plasma exchange in adults with severe COVID-19 infection.
      Int J Infect Dis. 2020; 99: 214-218
      ,
      • Faqihi F.
      • Alharthy A.
      • Alodat M.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Therapeutic plasma exchange in adult critically ill patients with life-threatening SARS-CoV-2 disease: A pilot study.
      J Crit Care. 2020; 60: 328-333
      ,
      • Gluck W.L.
      • Callahan S.P.
      • Brevetta R.A.
      • Stenbit A.E.
      • Smith W.M.
      • Martin J.C.
      • et al.
      Efficacy of therapeutic plasma exchange in the treatment of penn class 3 and 4 cytokine release syndrome complicating COVID-19.
      Respir Med. 2020; 175106188
      ,
      • Hashemian S.M.
      • Shafigh N.
      • Afzal G.
      • Jamaati H.
      • Tabarsi P.
      • Marjani M.
      • et al.
      Plasmapheresis reduces cytokine and immune cell levels in COVID-19 patients with acute respiratory distress syndrome (ARDS).
      Pulmonology. 2020; https://doi.org/10.1016/j.pulmoe.2020.10.017
      ,
      • Morath C.
      • Weigand M.A.
      • Zeier M.
      • Speer C.
      • Tiwari-Heckler S.
      • Merle U.
      Plasma exchange in critically ill COVID-19 patients.
      Crit Care. 2020; 24: 481
      ,
      • Wang X.
      • Chen X.
      • Tang F.
      • Luo W.
      • Fang J.
      • Qi C.
      • et al.
      Be aware of acute kidney injury in critically ill children with COVID-19.
      Pediatr Nephrol. 2021; 36: 163-169
      ,
      • Zhang L.
      • Zhai H.
      • Ma S.
      • Chen J.
      • Gao Y.
      Efficacy of therapeutic plasma exchange in severe COVID-19 patients.
      Br J Haematol. 2020; 190: e181-e183
      ,
      • Fernandez J.
      • Gratacos-Ginès J.
      • Olivas P.
      • Costa M.
      • Nieto S.
      • Mateo D.
      • et al.
      Plasma exchange: An effective rescue therapy in critically ill patients with coronavirus disease 2019 infection.
      Crit Care Med. 2020; 48: e1350-e1355
      ,
      • Roshandel E.
      • Sankanian G.
      • Salimi M.
      • Jalili A.
      • Salari S.
      • Sadeghi A.
      • et al.
      Plasma exchange followed by convalescent plasma transfusion in COVID-19 patients.
      Transfus Apher Sci. 2021; 103141
      ,
      • Faqihi F.
      • Alharthy A.
      • Memish Z.A.
      • Kutsogiannis D.J.
      • Brindley P.G.
      • Karakitsos D.
      Peripheral neuropathy in severe COVID-19 resolved with therapeutic plasma exchange.
      Clin Case Rep. 2020; 8: 3234-3239
      ,

      Hua T., Li M., Li X. Therapeutic plasma exchange therapy support for critical COVID-19: A case report. Ther Apher Dial. 2020:http://dx.doi.org/10.1111/744–9987.13586.

      ,
      • Kamit F.
      • Malbora B.
      • Atay A.
      • Bayirli D.T.
      • Bektas M.
      A fatal case of COVID-19 in a child with ALL: A cytokine storm and hyperferritinemic MODS.
      J Child Sci. 2020; 10: e240-e245
      ,
      • Ma J.
      • Xia P.
      • Zhou Y.
      • Liu Z.
      • Zhou X.
      • Wang J.
      • et al.
      Potential effect of blood purification therapy in reducing cytokine storm as a late complication of critically ill COVID-19.
      Clin Immunol. 2020; 214108408
      ,
      • Ragab D.
      • Salah-Eldin H.
      • Afify M.
      • Soliman W.
      • Badr M.H.
      A case of COVID-19, with cytokine storm, treated by consecutive use of therapeutic plasma exchange followed by convalescent plasma transfusion: A case report.
      J Med Virol. 2021; 93: 1854-1856