Biologic Disease-modifying Antirheumatic Drug (bDMARD)-induced Neutropenia: A Registry from a Retrospective Cohort of Patients with Rheumatic Diseases Treated with 3 Classes of Intravenous bDMARD

Francisco Espinoza; Pierre Le Blay; Bernard Combe

doi:10.3899/jrheum.150457

REFERENCES

1.↵
1. Bessissow T,
2. Renard M,
3. Hoffman I,
4. Vermeire S,
5. Rutgeerts P,
6. Van Assche G
. Review article: non-malignant haematological complications of anti-tumour necrosis factor alpha therapy. Aliment Pharmacol Ther 2012;36:312–23.
OpenUrl CrossRef PubMed
2.↵
1. Vidal F,
2. Fontova R,
3. Richart C
. Severe neutropenia and thrombocytopenia associated with infliximab. Ann Intern Med 2003;139:W–W63.
OpenUrl PubMed
3.↵
1. US National Cancer Institute
. Common toxicity criteria manual, version 2.0. Bethesda: NCI; 1999.
4.↵
1. Hastings R,
2. Ding T,
3. Butt S,
4. Gadsby K,
5. Zhang W,
6. Moots RJ,
7. et al.
Neutropenia in patients receiving anti-tumor necrosis factor therapy. Arthritis Care Res 2010;62:764–9.
OpenUrl CrossRef
5.↵
1. Genovese MC,
2. Becker JC,
3. Schiff M,
4. Luggen M,
5. Sherrer Y,
6. Kremer J,
7. et al.
Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 2005;353:1114–23.
OpenUrl CrossRef PubMed
6.↵
1. Schiff M,
2. Keiserman M,
3. Codding C,
4. Songcharoen S,
5. Berman A,
6. Nayiager S,
7. et al.
Efficacy and safety of abatacept or infliximab vs placebo in ATTEST: a phase III, multi-centre, randomised, double-blind, placebo-controlled study in patients with rheumatoid arthritis and an inadequate response to methotrexate. Ann Rheum Dis 2008;67:1096–103.
OpenUrl Abstract/FREE Full Text
7.↵
1. Schiff M,
2. Pritchard C,
3. Huffstutter JE,
4. Rodriguez-Valverde V,
5. Durez P,
6. Zhou X,
7. et al.
The 6-month safety and efficacy of abatacept in patients with rheumatoid arthritis who underwent a washout after anti-tumour necrosis factor therapy or were directly switched to abatacept: the ARRIVE trial. Ann Rheum Dis 2009;68:1708–14.
OpenUrl Abstract/FREE Full Text
8.↵
1. Kremer JM,
2. Russell AS,
3. Emery P,
4. Abud-Mendoza C,
5. Szechinski J,
6. Westhovens R,
7. et al.
Long-term safety, efficacy and inhibition of radiographic progression with abatacept treatment in patients with rheumatoid arthritis and an inadequate response to methotrexate: 3-year results from the AIM trial. Ann Rheum Dis 2011;70:1826–30.
OpenUrl Abstract/FREE Full Text
9.↵
1. Furst DE,
2. Schiff MH,
3. Fleischmann RM,
4. Strand V,
5. Birbara CA,
6. Compagnone D,
7. et al.
Adalimumab, a fully human anti tumor necrosis factor-alpha monoclonal antibody, and concomitant standard antirheumatic therapy for the treatment of rheumatoid arthritis: results of STAR (Safety Trial of Adalimumab in Rheumatoid Arthritis). J Rheumatol 2003;30:2563–71.
OpenUrl Abstract/FREE Full Text
10.↵
1. Fleischmann R,
2. Iqbal I,
3. Nandeshwar P,
4. Quiceno A
. Safety and efficacy of disease-modifying anti-rheumatic agents: focus on the benefits and risks of etanercept. Drug Saf 2002;25:173–97.
OpenUrl CrossRef PubMed
11.↵
1. Montané E,
2. Sallés M,
3. Barriocanal A,
4. Riera E,
5. Costa J,
6. Tena X
. Antitumor necrosis factor-induced neutropenia: a case report with double positive rechallenges. Clin Rheumatol 2007;26:1527–9.
OpenUrl CrossRef PubMed
12.↵
1. Wenham C,
2. Gadsby K,
3. Deighton C
. Three significant cases of neutropenia with etanercept [letter]. Rheumatology 2008;47:376–7.
OpenUrl FREE Full Text
13.↵
1. Rajakulendran S,
2. Gadsby K,
3. Allen D,
4. O’Reilly S,
5. Deighton C
. Neutropenia while receiving anti-tumour necrosis factor treatment for rheumatoid arthritis [letter]. Ann Rheum Dis 2006;65:1678–9.
OpenUrl FREE Full Text
14.↵
1. Pappas DA,
2. Shaw JW,
3. Chang H,
4. Cifaldi MA,
5. Reed GW,
6. Garg V,
7. et al.
Laboratory safety of adalimumab and other tumor necrosis factor inhibitors in the treatment of rheumatoid arthritis [abstract]. Ann Rheum Dis 2014;73 Suppl 2:931.
OpenUrl
15.↵
1. Kremer JM,
2. Blanco R,
3. Brzosko M,
4. Burgos-Vargas R,
5. Halland AM,
6. Vernon E,
7. et al.
Tocilizumab inhibits structural joint damage in rheumatoid arthritis patients with inadequate responses to methotrexate: results from the double-blind treatment phase of a randomized placebo-controlled trial of tocilizumab safety and prevention of structural joint damage at one year. Arthritis Rheum 2011;63:609–21.
OpenUrl CrossRef PubMed
16.↵
1. De Benedetti F,
2. Rubio-Pérez N,
3. Salazar CD,
4. Goodman S,
5. Job-Deslandre C,
6. Joos R,
7. et al.
A45: neutropenia with tocilizumab treatment is not associated with increased infection risk in patients with polyarticular-course juvenile idiopathic arthritis [abstract]. Arthritis Rheumatol 2014;66 Suppl 3:S67–8.
OpenUrl
17.↵
1. Genovese MC,
2. McKay JD,
3. Nasonov EL,
4. Mysler EF,
5. da Silva NA,
6. Alecock E,
7. et al.
Interleukin-6 receptor inhibition with tocilizumab reduces disease activity in rheumatoid arthritis with inadequate response to disease-modifying antirheumatic drugs: the tocilizumab in combination with traditional disease-modifying antirheumatic drug therapy study. Arthritis Rheum 2008;58:2968–80.
OpenUrl CrossRef PubMed
18.↵
1. Emery P,
2. Keystone E,
3. Tony HP,
4. Cantagrel A,
5. van Vollenhoven R,
6. Sanchez A,
7. et al.
IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial. Ann Rheum Dis 2008;67:1516–23.
OpenUrl Abstract/FREE Full Text
19.↵
1. Jones G,
2. Sebba A,
3. Gu J,
4. Lowenstein MB,
5. Calvo A,
6. Gomez-Reino JJ,
7. et al.
Comparison of tocilizumab monotherapy versus methotrexate monotherapy in patients with moderate to severe rheumatoid arthritis: the AMBITION study. Ann Rheum Dis 2010;69:88–96.
OpenUrl Abstract/FREE Full Text
20.↵
1. Burmester GR,
2. Rubbert-Roth A,
3. Cantagrel A,
4. Hall S,
5. Leszczynski P,
6. Feldman D,
7. et al.
A randomised, double-blind, parallel-group study of the safety and efficacy of subcutaneous tocilizumab versus intravenous tocilizumab in combination with traditional disease-modifying antirheumatic drugs in patients with moderate to severe rheumatoid arthritis (SUMMACTA study). Ann Rheum Dis 2014;73:69–74.
OpenUrl Abstract/FREE Full Text
21.↵
1. Smolen JS,
2. Beaulieu A,
3. Rubbert-Roth A,
4. Ramos-Remus C,
5. Rovensky J,
6. Alecock E,
7. et al.
Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomised trial. Lancet 2008;371:987–97.
OpenUrl CrossRef PubMed
22.↵
1. Wright HL,
2. Cross AL,
3. Edwards SW,
4. Moots RJ
. Effects of IL-6 and IL-6 blockade on neutrophil function in vitro and in vivo. Rheumatology 2014;53:1321–31.
OpenUrl Abstract/FREE Full Text

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Cited By...

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Keywords

[1] 1.↵
Bessissow T,
Renard M,
Hoffman I,
Vermeire S,
Rutgeerts P,
Van Assche G
. Review article: non-malignant haematological complications of anti-tumour necrosis factor alpha therapy. Aliment Pharmacol Ther 2012;36:312–23.
OpenUrl CrossRef PubMed

[2] Bessissow T,

[3] Renard M,

[4] Hoffman I,

[5] Vermeire S,

[6] Rutgeerts P,

[7] Van Assche G

[8] 2.↵
Vidal F,
Fontova R,
Richart C
. Severe neutropenia and thrombocytopenia associated with infliximab. Ann Intern Med 2003;139:W–W63.
OpenUrl PubMed

[9] Vidal F,

[10] Fontova R,

[11] Richart C

[12] 3.↵
US National Cancer Institute
. Common toxicity criteria manual, version 2.0. Bethesda: NCI; 1999.

[13] US National Cancer Institute

[14] 4.↵
Hastings R,
Ding T,
Butt S,
Gadsby K,
Zhang W,
Moots RJ,
et al.
Neutropenia in patients receiving anti-tumor necrosis factor therapy. Arthritis Care Res 2010;62:764–9.
OpenUrl CrossRef

[15] Hastings R,

[16] Ding T,

[17] Butt S,

[18] Gadsby K,

[19] Zhang W,

[20] Moots RJ,

[21] et al.

[22] 5.↵
Genovese MC,
Becker JC,
Schiff M,
Luggen M,
Sherrer Y,
Kremer J,
et al.
Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 2005;353:1114–23.
OpenUrl CrossRef PubMed

[23] Genovese MC,

[24] Becker JC,

[25] Schiff M,

[26] Luggen M,

[27] Sherrer Y,

[28] Kremer J,

[29] et al.

[30] 6.↵
Schiff M,
Keiserman M,
Codding C,
Songcharoen S,
Berman A,
Nayiager S,
et al.
Efficacy and safety of abatacept or infliximab vs placebo in ATTEST: a phase III, multi-centre, randomised, double-blind, placebo-controlled study in patients with rheumatoid arthritis and an inadequate response to methotrexate. Ann Rheum Dis 2008;67:1096–103.
OpenUrl Abstract/FREE Full Text

[31] Schiff M,

[32] Keiserman M,

[33] Codding C,

[34] Songcharoen S,

[35] Berman A,

[36] Nayiager S,

[37] et al.

[38] 7.↵
Schiff M,
Pritchard C,
Huffstutter JE,
Rodriguez-Valverde V,
Durez P,
Zhou X,
et al.
The 6-month safety and efficacy of abatacept in patients with rheumatoid arthritis who underwent a washout after anti-tumour necrosis factor therapy or were directly switched to abatacept: the ARRIVE trial. Ann Rheum Dis 2009;68:1708–14.
OpenUrl Abstract/FREE Full Text

[39] Schiff M,

[40] Pritchard C,

[41] Huffstutter JE,

[42] Rodriguez-Valverde V,

[43] Durez P,

[44] Zhou X,

[45] et al.

[46] 8.↵
Kremer JM,
Russell AS,
Emery P,
Abud-Mendoza C,
Szechinski J,
Westhovens R,
et al.
Long-term safety, efficacy and inhibition of radiographic progression with abatacept treatment in patients with rheumatoid arthritis and an inadequate response to methotrexate: 3-year results from the AIM trial. Ann Rheum Dis 2011;70:1826–30.
OpenUrl Abstract/FREE Full Text

[47] Kremer JM,

[48] Russell AS,

[49] Emery P,

[50] Abud-Mendoza C,

[51] Szechinski J,

[52] Westhovens R,

[53] et al.

[54] 9.↵
Furst DE,
Schiff MH,
Fleischmann RM,
Strand V,
Birbara CA,
Compagnone D,
et al.
Adalimumab, a fully human anti tumor necrosis factor-alpha monoclonal antibody, and concomitant standard antirheumatic therapy for the treatment of rheumatoid arthritis: results of STAR (Safety Trial of Adalimumab in Rheumatoid Arthritis). J Rheumatol 2003;30:2563–71.
OpenUrl Abstract/FREE Full Text

[55] Furst DE,

[56] Schiff MH,

[57] Fleischmann RM,

[58] Strand V,

[59] Birbara CA,

[60] Compagnone D,

[61] et al.

[62] 10.↵
Fleischmann R,
Iqbal I,
Nandeshwar P,
Quiceno A
. Safety and efficacy of disease-modifying anti-rheumatic agents: focus on the benefits and risks of etanercept. Drug Saf 2002;25:173–97.
OpenUrl CrossRef PubMed

[63] Fleischmann R,

[64] Iqbal I,

[65] Nandeshwar P,

[66] Quiceno A

[67] 11.↵
Montané E,
Sallés M,
Barriocanal A,
Riera E,
Costa J,
Tena X
. Antitumor necrosis factor-induced neutropenia: a case report with double positive rechallenges. Clin Rheumatol 2007;26:1527–9.
OpenUrl CrossRef PubMed

[68] Montané E,

[69] Sallés M,

[70] Barriocanal A,

[71] Riera E,

[72] Costa J,

[73] Tena X

[74] 12.↵
Wenham C,
Gadsby K,
Deighton C
. Three significant cases of neutropenia with etanercept [letter]. Rheumatology 2008;47:376–7.
OpenUrl FREE Full Text

[75] Wenham C,

[76] Gadsby K,

[77] Deighton C

[78] 13.↵
Rajakulendran S,
Gadsby K,
Allen D,
O’Reilly S,
Deighton C
. Neutropenia while receiving anti-tumour necrosis factor treatment for rheumatoid arthritis [letter]. Ann Rheum Dis 2006;65:1678–9.
OpenUrl FREE Full Text

[79] Rajakulendran S,

[80] Gadsby K,

[81] Allen D,

[82] O’Reilly S,

[83] Deighton C

[84] 14.↵
Pappas DA,
Shaw JW,
Chang H,
Cifaldi MA,
Reed GW,
Garg V,
et al.
Laboratory safety of adalimumab and other tumor necrosis factor inhibitors in the treatment of rheumatoid arthritis [abstract]. Ann Rheum Dis 2014;73 Suppl 2:931.
OpenUrl

[85] Pappas DA,

[86] Shaw JW,

[87] Chang H,

[88] Cifaldi MA,

[89] Reed GW,

[90] Garg V,

[91] et al.

[92] 15.↵
Kremer JM,
Blanco R,
Brzosko M,
Burgos-Vargas R,
Halland AM,
Vernon E,
et al.
Tocilizumab inhibits structural joint damage in rheumatoid arthritis patients with inadequate responses to methotrexate: results from the double-blind treatment phase of a randomized placebo-controlled trial of tocilizumab safety and prevention of structural joint damage at one year. Arthritis Rheum 2011;63:609–21.
OpenUrl CrossRef PubMed

[93] Kremer JM,

[94] Blanco R,

[95] Brzosko M,

[96] Burgos-Vargas R,

[97] Halland AM,

[98] Vernon E,

[99] et al.

[100] 16.↵
De Benedetti F,
Rubio-Pérez N,
Salazar CD,
Goodman S,
Job-Deslandre C,
Joos R,
et al.
A45: neutropenia with tocilizumab treatment is not associated with increased infection risk in patients with polyarticular-course juvenile idiopathic arthritis [abstract]. Arthritis Rheumatol 2014;66 Suppl 3:S67–8.
OpenUrl

[101] De Benedetti F,

[102] Rubio-Pérez N,

[103] Salazar CD,

[104] Goodman S,

[105] Job-Deslandre C,

[106] Joos R,

[107] et al.

[108] 17.↵
Genovese MC,
McKay JD,
Nasonov EL,
Mysler EF,
da Silva NA,
Alecock E,
et al.
Interleukin-6 receptor inhibition with tocilizumab reduces disease activity in rheumatoid arthritis with inadequate response to disease-modifying antirheumatic drugs: the tocilizumab in combination with traditional disease-modifying antirheumatic drug therapy study. Arthritis Rheum 2008;58:2968–80.
OpenUrl CrossRef PubMed

[109] Genovese MC,

[110] McKay JD,

[111] Nasonov EL,

[112] Mysler EF,

[113] da Silva NA,

[114] Alecock E,

[115] et al.

[116] 18.↵
Emery P,
Keystone E,
Tony HP,
Cantagrel A,
van Vollenhoven R,
Sanchez A,
et al.
IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial. Ann Rheum Dis 2008;67:1516–23.
OpenUrl Abstract/FREE Full Text

[117] Emery P,

[118] Keystone E,

[119] Tony HP,

[120] Cantagrel A,

[121] van Vollenhoven R,

[122] Sanchez A,

[123] et al.

[124] 19.↵
Jones G,
Sebba A,
Gu J,
Lowenstein MB,
Calvo A,
Gomez-Reino JJ,
et al.
Comparison of tocilizumab monotherapy versus methotrexate monotherapy in patients with moderate to severe rheumatoid arthritis: the AMBITION study. Ann Rheum Dis 2010;69:88–96.
OpenUrl Abstract/FREE Full Text

[125] Jones G,

[126] Sebba A,

[127] Gu J,

[128] Lowenstein MB,

[129] Calvo A,

[130] Gomez-Reino JJ,

[131] et al.

[132] 20.↵
Burmester GR,
Rubbert-Roth A,
Cantagrel A,
Hall S,
Leszczynski P,
Feldman D,
et al.
A randomised, double-blind, parallel-group study of the safety and efficacy of subcutaneous tocilizumab versus intravenous tocilizumab in combination with traditional disease-modifying antirheumatic drugs in patients with moderate to severe rheumatoid arthritis (SUMMACTA study). Ann Rheum Dis 2014;73:69–74.
OpenUrl Abstract/FREE Full Text

[133] Burmester GR,

[134] Rubbert-Roth A,

[135] Cantagrel A,

[136] Hall S,

[137] Leszczynski P,

[138] Feldman D,

[139] et al.

[140] 21.↵
Smolen JS,
Beaulieu A,
Rubbert-Roth A,
Ramos-Remus C,
Rovensky J,
Alecock E,
et al.
Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomised trial. Lancet 2008;371:987–97.
OpenUrl CrossRef PubMed

[141] Smolen JS,

[142] Beaulieu A,

[143] Rubbert-Roth A,

[144] Ramos-Remus C,

[145] Rovensky J,

[146] Alecock E,

[147] et al.

[148] 22.↵
Wright HL,
Cross AL,
Edwards SW,
Moots RJ
. Effects of IL-6 and IL-6 blockade on neutrophil function in vitro and in vivo. Rheumatology 2014;53:1321–31.
OpenUrl Abstract/FREE Full Text

[149] Wright HL,

[150] Cross AL,

[151] Edwards SW,

[152] Moots RJ

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Biologic Disease-modifying Antirheumatic Drug (bDMARD)-induced Neutropenia: A Registry from a Retrospective Cohort of Patients with Rheumatic Diseases Treated with 3 Classes of Intravenous bDMARD

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Biologic Disease-modifying Antirheumatic Drug (bDMARD)-induced Neutropenia: A Registry from a Retrospective Cohort of Patients with Rheumatic Diseases Treated with 3 Classes of Intravenous bDMARD

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