Impact of Timing of Tocilizumab Use in Hospitalized Patients With SARS-CoV-2 Infection

Anup K Singh; Margarita Oks; Gregg Husk; Samuel P Dechario; Bushra Mina; Kanwaljit Singh; Linda Kirschenbaum; Charles M Carpati; Omar Mahmoud; Nader Ishak Gabra; Oki Ishikawa; Erica Altschultz; Varun Shah; Akhilesh Mahajan; Arun Gautam; Brian Birnbaum; Anthony C Antonacci; Suhail Raoof

doi:10.4187/respcare.08779

References

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World Health Organization. 2021. WHO Coronavirus (COVID-19) Dashboard, May 30, 2021, https://covid19.who.int. Accessed May 30, 2021.
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1. Soy M,
2. Keser G,
3. Atagündüz P,
4. Tabak F,
5. Atagündüz I,
6. Kayhan S
. Cytokine storm in COVID-19: pathogenesis and overview of anti-inflammatory agents used in treatment. Clin Rheumatol 2020;39(7):2085-2094.
OpenUrl PubMed
3.↵
1. Tajbakhsh A,
2. Gheibi Hayat SM,
3. Taghizadeh H,
4. Akbari A,
5. Inabadi M,
6. Savardashtaki A,
7. et al
. COVID-19 adn cardiac injury: clinical manifestations biomarkers, mechanisms, diagnosis, treatment, and follow up. Expert Rev Anti Infect Ther 2021;19(3):345-357.
OpenUrl
4.↵
1. Petrilli CM,
2. Jones SA,
3. Yang J,
4. Rajagopalan H,
5. O’Donnell L,
6. Chernyak Y,
7. et al
. Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ 2020;369:m1966.
OpenUrl Abstract/FREE Full Text
5.↵
1. Yang K,
2. Sheng Y,
3. Huang C,
4. Jin Y,
5. Xiong N,
6. Jiang K,
7. et al
. Clinical characteristics, outcomes, and risk factors for mortality in patients with cancer and COVID-19 in Hubei, China: a multicentre, retrospective, cohort study. Lancet Oncol 2020;21(7):904-913.
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6.↵
1. Rottoli M,
2. Bernante P,
3. Belvedere A,
4. Garelli S,
5. Giannella M,
6. et al
. How important is obesity as a risk factor for respiratory failure, intensive care admission and death in hospitalised COVID-19 patients? Results from a single Italian centre. Eur J Endocrinol 2020;183(4):389-397.
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1. Simonnet A,
2. Chetboun M,
3. Poissy J,
4. Raverdy V,
5. Noulette J,
6. Duhamel A,
7. et al
. High prevalence of obesity in severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) requiring invasive mechanical ventilation. Obesity (Silver Spring) 2020;28(7):1195-1199.
OpenUrl
8.↵
1. Palaiodimos L,
2. Kokkinidis DG,
3. Li W,
4. Karamanis D,
5. Ognibene J,
6. Arora S,
7. et al
. Severe obesity, increasing age and male sex are independently associated with worse in-hospital outcomes, and higher in-hospital mortality, in a cohort of patients with COVID-19 in the Bronx, New York. Metabolism 2020;108:154262.
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1. Goyal P,
2. Choi JJ,
3. Pinheiro LC,
4. Schenck EJ,
5. Chen R,
6. Jabri A,
7. et al
. Clinical characteristics of Covid-19 in New York City. N Engl J Med 2020;382(24):2372-2374.
10.↵
1. Price CC,
2. Altice FL,
3. Shyr Y,
4. Koff A,
5. Pischel L,
6. Goshua G,
7. et al
. Tocilizumab treatment for cytokine release syndrome in hospitalized patient with coronavirus disease 2019: survival and clinical outcomes. CHEST 2020;158(4):1397-1408.
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11.↵
1. Sinha P,
2. Mostaghim A,
3. Bielick CG,
4. McLaughlin A,
5. Hamer DH,
6. Wetzler LM,
7. et al
. Early administration of interleukin-6 inhibitors for patients with severe COVID-19 disease is associated with decreased intubation, reduced mortality, and increased discharge. Int J Infect Dis 2020;99:28-33.
OpenUrl CrossRef PubMed
12.↵
1. Gupta S,
2. Wang W,
3. Hayek SS,
4. Chan L,
5. Mathews KS,
6. Melamed ML,
7. et al
. Association between early treatment with tocilizumab and mortality among critically ill patients with COVID-19. JAMA Intern Med 2021;181(1):41-51.
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13.↵
1. Potere N,
2. Di Nisio M,
3. Cibelli D,
4. Scurti R,
5. Frattari A,
6. Porreca E,
7. et al
. Interleukin-6 receptor blockade with subcutaneous tocilizumab in severe COVID-19 pneumonia and hyperinflammation: a case–control study. Ann Rheum Dis 2021;80(2):1-2.
OpenUrl FREE Full Text
14.
1. Canziani LM,
2. Trovati S,
3. Brunetta E,
4. Testa A,
5. De Santis M,
6. Bombardieri E,
7. et al
. Interleukin-6 receptor blocking with intravenous tocilizumab in COVID-19 severe acute respiratory distress syndrome: a retrospective case-control survival analysis of 128 patients. J Autoimmun 2020;114:102511.
OpenUrl CrossRef PubMed
15.↵
1. Campochiaro C,
2. Della-Torre E,
3. Cavalli G, De Luca G, Ripa M, Boffini,
4. et al
. Efficacy and safety of tocilizumab in severe COVID-19 patients: a single-centre retrospective cohort study. Eur J Intern Med 2020;76:43-49.
OpenUrl CrossRef PubMed
16.↵
1. Jiménez-Brítez G,
2. Ruiz P,
3. Soler X
. Tocilizumab plus glucocorticoids in severe and critically COVID-19 patients. A single center experience. Med Clin (Barc) 2020;155(9):409-411.
OpenUrl
17.↵
1. Rosas IO,
2. Brau N,
3. Waters M,
4. Go RC,
5. Hunter BD,
6. Bhagani S,
7. et al
. Tocilizumab in hospitalized patients with COVID-19 pneumonia. N Engl J Med 2021;348(16):1503-1516.
OpenUrl
18.↵
1. Stone JH,
2. Frigault MJ,
3. Serling-Boyd NJ,
4. Fernandes AD,
5. Harvey L,
6. Foulkes AS,
7. et al
. Efficacy of Tocilizumab in patients hospitalized with Covid-19. N Engl J Med 2020;383(24):2333-2344.
OpenUrl CrossRef PubMed
19.↵
1. Salvarani C,
2. Dolci G,
3. Massari M,
4. Merlo DF,
5. Cavuto S,
6. Savoldi L,
7. et al
. Effect of tocilizumab vs standard care on clinical worsening in patients hospitalized with COVID-19 pneumonia: a randomized clinical trial. JAMA Intern Med 2021;181(1):24-31.
OpenUrl
20.↵
1. Hermine O,
2. Mariette X,
3. Tharaux P-L,
4. Resche-Rigon M,
5. Porcher R,
6. Ravaud P
, CORIMUNO-19 Collaborative Group. Effect of tocilizumab vs usual care in adults hospitalized with COVID-19 and moderate or severe pneumonia: a randomized clinical trial. JAMA Intern Med 2021;181(1):32-40.
OpenUrl
21.↵
1. Horby P,
2. Lim WS,
3. Emberson JR,
4. Mafham M,
5. Bell JL,
6. et al
RECOVERY Collaborative Group; Horby P, Lim WS, Emberson JR, Mafham M, Bell JL, et al. Dexamethasone in hospitalized patients with Covid-19. N Engl J Med 2021;384(8):693-704.
OpenUrl CrossRef PubMed
22.↵
1. Sterne JAC,
2. Murthy S,
3. Diaz JV,
4. Slutsky AS,
5. Villar J,
6. et al
WHO Rapid Evidence Appraisal for COVID-19 Therapies (REACT) Working Group; Sterne JAC, Murthy S, Diaz JV, Slutsky AS, Villar J, et al. Association between administration of systemic corticosteroids and mortality among critically ill patients with COVID-19: a meta-analysis. JAMA 2020;324(13):1330-1341.
OpenUrl CrossRef PubMed
23.↵
1. Ramiro S,
2. Mostard RLM,
3. Magro-Checa C,
4. van Dongen CMP,
5. Dormans T,
6. Buijs J,
7. et al
. Historically controlled comparison of glucocorticoids with or without tocilizumab versus supportive care only in patients with COVID-19-associated cytokine storm syndrome: results of the CHIC study. Ann Rheum Dis 2020;79(9):1143-1151.
OpenUrl Abstract/FREE Full Text
24.↵
RECOVERY Collaborative Group. Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): a randomised, controlled, open-label, platform trial. Lancet 2021;397(10285):1637-1645. May 1
OpenUrl PubMed
25.↵
1. Zhang X,
2. Tan Y,
3. Ling Y,
4. Lu G,
5. Liu F,
6. Yi Z,
7. et al
. Viral and host factors related to the clinical outcome of COVID-19. Nature 2020;583(7816):437-440.
OpenUrl CrossRef PubMed
26.↵
1. Su H,
2. Yang M,
3. Wan C,
4. Yi L-X,
5. Tang F,
6. Zhu H-Y,
7. et al
. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int 2020;98(1):219-227.
OpenUrl CrossRef PubMed
27.↵
1. Wang G,
2. Wu C,
3. Zhang Q,
4. Wu F,
5. Yu B,
6. Lv J,
7. et al
. C-reactive protein level may predict the risk of COVID-19 aggravation. Open Forum Infect Dis 2020;7(5):ofaa153.
OpenUrl CrossRef PubMed
28.↵
1. Sahu BR,
2. Kampa RK,
3. Padhi A,
4. Panda AK
. C-reactive protein: a promising biomarker for poor prognosis in COVID-19 infection. Clin Chim Acta 2020;509(509):91-94.
OpenUrl PubMed

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Keywords

[1] 1.↵
World Health Organization. 2021. WHO Coronavirus (COVID-19) Dashboard, May 30, 2021, https://covid19.who.int. Accessed May 30, 2021.

[2] 2.↵
Soy M,
Keser G,
Atagündüz P,
Tabak F,
Atagündüz I,
Kayhan S
. Cytokine storm in COVID-19: pathogenesis and overview of anti-inflammatory agents used in treatment. Clin Rheumatol 2020;39(7):2085-2094.
OpenUrl PubMed

[3] Soy M,

[4] Keser G,

[5] Atagündüz P,

[6] Tabak F,

[7] Atagündüz I,

[8] Kayhan S

[9] 3.↵
Tajbakhsh A,
Gheibi Hayat SM,
Taghizadeh H,
Akbari A,
Inabadi M,
Savardashtaki A,
et al
. COVID-19 adn cardiac injury: clinical manifestations biomarkers, mechanisms, diagnosis, treatment, and follow up. Expert Rev Anti Infect Ther 2021;19(3):345-357.
OpenUrl

[10] Tajbakhsh A,

[11] Gheibi Hayat SM,

[12] Taghizadeh H,

[13] Akbari A,

[14] Inabadi M,

[15] Savardashtaki A,

[16] et al

[17] 4.↵
Petrilli CM,
Jones SA,
Yang J,
Rajagopalan H,
O’Donnell L,
Chernyak Y,
et al
. Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ 2020;369:m1966.
OpenUrl Abstract/FREE Full Text

[18] Petrilli CM,

[19] Jones SA,

[20] Yang J,

[21] Rajagopalan H,

[22] O’Donnell L,

[23] Chernyak Y,

[24] et al

[25] 5.↵
Yang K,
Sheng Y,
Huang C,
Jin Y,
Xiong N,
Jiang K,
et al
. Clinical characteristics, outcomes, and risk factors for mortality in patients with cancer and COVID-19 in Hubei, China: a multicentre, retrospective, cohort study. Lancet Oncol 2020;21(7):904-913.
OpenUrl CrossRef PubMed

[26] Yang K,

[27] Sheng Y,

[28] Huang C,

[29] Jin Y,

[30] Xiong N,

[31] Jiang K,

[32] et al

[33] 6.↵
Rottoli M,
Bernante P,
Belvedere A,
Garelli S,
Giannella M,
et al
. How important is obesity as a risk factor for respiratory failure, intensive care admission and death in hospitalised COVID-19 patients? Results from a single Italian centre. Eur J Endocrinol 2020;183(4):389-397.
OpenUrl PubMed

[34] Rottoli M,

[35] Bernante P,

[36] Belvedere A,

[37] Garelli S,

[38] Giannella M,

[39] et al

[40] 7.
Simonnet A,
Chetboun M,
Poissy J,
Raverdy V,
Noulette J,
Duhamel A,
et al
. High prevalence of obesity in severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) requiring invasive mechanical ventilation. Obesity (Silver Spring) 2020;28(7):1195-1199.
OpenUrl

[41] Simonnet A,

[42] Chetboun M,

[43] Poissy J,

[44] Raverdy V,

[45] Noulette J,

[46] Duhamel A,

[47] et al

[48] 8.↵
Palaiodimos L,
Kokkinidis DG,
Li W,
Karamanis D,
Ognibene J,
Arora S,
et al
. Severe obesity, increasing age and male sex are independently associated with worse in-hospital outcomes, and higher in-hospital mortality, in a cohort of patients with COVID-19 in the Bronx, New York. Metabolism 2020;108:154262.
OpenUrl CrossRef PubMed

[49] Palaiodimos L,

[50] Kokkinidis DG,

[51] Li W,

[52] Karamanis D,

[53] Ognibene J,

[54] Arora S,

[55] et al

[56] 9.↵
Goyal P,
Choi JJ,
Pinheiro LC,
Schenck EJ,
Chen R,
Jabri A,
et al
. Clinical characteristics of Covid-19 in New York City. N Engl J Med 2020;382(24):2372-2374.

[57] Goyal P,

[58] Choi JJ,

[59] Pinheiro LC,

[60] Schenck EJ,

[61] Chen R,

[62] Jabri A,

[63] et al

[64] 10.↵
Price CC,
Altice FL,
Shyr Y,
Koff A,
Pischel L,
Goshua G,
et al
. Tocilizumab treatment for cytokine release syndrome in hospitalized patient with coronavirus disease 2019: survival and clinical outcomes. CHEST 2020;158(4):1397-1408.
OpenUrl

[65] Price CC,

[66] Altice FL,

[67] Shyr Y,

[68] Koff A,

[69] Pischel L,

[70] Goshua G,

[71] et al

[72] 11.↵
Sinha P,
Mostaghim A,
Bielick CG,
McLaughlin A,
Hamer DH,
Wetzler LM,
et al
. Early administration of interleukin-6 inhibitors for patients with severe COVID-19 disease is associated with decreased intubation, reduced mortality, and increased discharge. Int J Infect Dis 2020;99:28-33.
OpenUrl CrossRef PubMed

[73] Sinha P,

[74] Mostaghim A,

[75] Bielick CG,

[76] McLaughlin A,

[77] Hamer DH,

[78] Wetzler LM,

[79] et al

[80] 12.↵
Gupta S,
Wang W,
Hayek SS,
Chan L,
Mathews KS,
Melamed ML,
et al
. Association between early treatment with tocilizumab and mortality among critically ill patients with COVID-19. JAMA Intern Med 2021;181(1):41-51.
OpenUrl

[81] Gupta S,

[82] Wang W,

[83] Hayek SS,

[84] Chan L,

[85] Mathews KS,

[86] Melamed ML,

[87] et al

[88] 13.↵
Potere N,
Di Nisio M,
Cibelli D,
Scurti R,
Frattari A,
Porreca E,
et al
. Interleukin-6 receptor blockade with subcutaneous tocilizumab in severe COVID-19 pneumonia and hyperinflammation: a case–control study. Ann Rheum Dis 2021;80(2):1-2.
OpenUrl FREE Full Text

[89] Potere N,

[90] Di Nisio M,

[91] Cibelli D,

[92] Scurti R,

[93] Frattari A,

[94] Porreca E,

[95] et al

[96] 14.
Canziani LM,
Trovati S,
Brunetta E,
Testa A,
De Santis M,
Bombardieri E,
et al
. Interleukin-6 receptor blocking with intravenous tocilizumab in COVID-19 severe acute respiratory distress syndrome: a retrospective case-control survival analysis of 128 patients. J Autoimmun 2020;114:102511.
OpenUrl CrossRef PubMed

[97] Canziani LM,

[98] Trovati S,

[99] Brunetta E,

[100] Testa A,

[101] De Santis M,

[102] Bombardieri E,

[103] et al

[104] 15.↵
Campochiaro C,
Della-Torre E,
Cavalli G, De Luca G, Ripa M, Boffini,
et al
. Efficacy and safety of tocilizumab in severe COVID-19 patients: a single-centre retrospective cohort study. Eur J Intern Med 2020;76:43-49.
OpenUrl CrossRef PubMed

[105] Campochiaro C,

[106] Della-Torre E,

[107] Cavalli G, De Luca G, Ripa M, Boffini,

[108] et al

[109] 16.↵
Jiménez-Brítez G,
Ruiz P,
Soler X
. Tocilizumab plus glucocorticoids in severe and critically COVID-19 patients. A single center experience. Med Clin (Barc) 2020;155(9):409-411.
OpenUrl

[110] Jiménez-Brítez G,

[111] Ruiz P,

[112] Soler X

[113] 17.↵
Rosas IO,
Brau N,
Waters M,
Go RC,
Hunter BD,
Bhagani S,
et al
. Tocilizumab in hospitalized patients with COVID-19 pneumonia. N Engl J Med 2021;348(16):1503-1516.
OpenUrl

[114] Rosas IO,

[115] Brau N,

[116] Waters M,

[117] Go RC,

[118] Hunter BD,

[119] Bhagani S,

[120] et al

[121] 18.↵
Stone JH,
Frigault MJ,
Serling-Boyd NJ,
Fernandes AD,
Harvey L,
Foulkes AS,
et al
. Efficacy of Tocilizumab in patients hospitalized with Covid-19. N Engl J Med 2020;383(24):2333-2344.
OpenUrl CrossRef PubMed

[122] Stone JH,

[123] Frigault MJ,

[124] Serling-Boyd NJ,

[125] Fernandes AD,

[126] Harvey L,

[127] Foulkes AS,

[128] et al

[129] 19.↵
Salvarani C,
Dolci G,
Massari M,
Merlo DF,
Cavuto S,
Savoldi L,
et al
. Effect of tocilizumab vs standard care on clinical worsening in patients hospitalized with COVID-19 pneumonia: a randomized clinical trial. JAMA Intern Med 2021;181(1):24-31.
OpenUrl

[130] Salvarani C,

[131] Dolci G,

[132] Massari M,

[133] Merlo DF,

[134] Cavuto S,

[135] Savoldi L,

[136] et al

[137] 20.↵
Hermine O,
Mariette X,
Tharaux P-L,
Resche-Rigon M,
Porcher R,
Ravaud P
, CORIMUNO-19 Collaborative Group. Effect of tocilizumab vs usual care in adults hospitalized with COVID-19 and moderate or severe pneumonia: a randomized clinical trial. JAMA Intern Med 2021;181(1):32-40.
OpenUrl

[138] Hermine O,

[139] Mariette X,

[140] Tharaux P-L,

[141] Resche-Rigon M,

[142] Porcher R,

[143] Ravaud P

[144] 21.↵
Horby P,
Lim WS,
Emberson JR,
Mafham M,
Bell JL,
et al
RECOVERY Collaborative Group; Horby P, Lim WS, Emberson JR, Mafham M, Bell JL, et al. Dexamethasone in hospitalized patients with Covid-19. N Engl J Med 2021;384(8):693-704.
OpenUrl CrossRef PubMed

[145] Horby P,

[146] Lim WS,

[147] Emberson JR,

[148] Mafham M,

[149] Bell JL,

[150] et al

[151] 22.↵
Sterne JAC,
Murthy S,
Diaz JV,
Slutsky AS,
Villar J,
et al
WHO Rapid Evidence Appraisal for COVID-19 Therapies (REACT) Working Group; Sterne JAC, Murthy S, Diaz JV, Slutsky AS, Villar J, et al. Association between administration of systemic corticosteroids and mortality among critically ill patients with COVID-19: a meta-analysis. JAMA 2020;324(13):1330-1341.
OpenUrl CrossRef PubMed

[152] Sterne JAC,

[153] Murthy S,

[154] Diaz JV,

[155] Slutsky AS,

[156] Villar J,

[157] et al

[158] 23.↵
Ramiro S,
Mostard RLM,
Magro-Checa C,
van Dongen CMP,
Dormans T,
Buijs J,
et al
. Historically controlled comparison of glucocorticoids with or without tocilizumab versus supportive care only in patients with COVID-19-associated cytokine storm syndrome: results of the CHIC study. Ann Rheum Dis 2020;79(9):1143-1151.
OpenUrl Abstract/FREE Full Text

[159] Ramiro S,

[160] Mostard RLM,

[161] Magro-Checa C,

[162] van Dongen CMP,

[163] Dormans T,

[164] Buijs J,

[165] et al

[166] 24.↵
RECOVERY Collaborative Group. Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): a randomised, controlled, open-label, platform trial. Lancet 2021;397(10285):1637-1645. May 1
OpenUrl PubMed

[167] 25.↵
Zhang X,
Tan Y,
Ling Y,
Lu G,
Liu F,
Yi Z,
et al
. Viral and host factors related to the clinical outcome of COVID-19. Nature 2020;583(7816):437-440.
OpenUrl CrossRef PubMed

[168] Zhang X,

[169] Tan Y,

[170] Ling Y,

[171] Lu G,

[172] Liu F,

[173] Yi Z,

[174] et al

[175] 26.↵
Su H,
Yang M,
Wan C,
Yi L-X,
Tang F,
Zhu H-Y,
et al
. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int 2020;98(1):219-227.
OpenUrl CrossRef PubMed

[176] Su H,

[177] Yang M,

[178] Wan C,

[179] Yi L-X,

[180] Tang F,

[181] Zhu H-Y,

[182] et al

[183] 27.↵
Wang G,
Wu C,
Zhang Q,
Wu F,
Yu B,
Lv J,
et al
. C-reactive protein level may predict the risk of COVID-19 aggravation. Open Forum Infect Dis 2020;7(5):ofaa153.
OpenUrl CrossRef PubMed

[184] Wang G,

[185] Wu C,

[186] Zhang Q,

[187] Wu F,

[188] Yu B,

[189] Lv J,

[190] et al

[191] 28.↵
Sahu BR,
Kampa RK,
Padhi A,
Panda AK
. C-reactive protein: a promising biomarker for poor prognosis in COVID-19 infection. Clin Chim Acta 2020;509(509):91-94.
OpenUrl PubMed

[192] Sahu BR,

[193] Kampa RK,

[194] Padhi A,

[195] Panda AK

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