Breakthrough infections with the SARS-CoV-2 omicron (B.1.1.529) variant in patients with immune-mediated inflammatory diseases

E.W. Stalman; L. Wieske; K.P.J. van Dam; L.Y. Kummer; Z.L.E. van Kempen; J. Killestein; A.G. Volkers; S.W. Tas; L. Boekel; G.J. Wolbink; A.J. Van der Kooi; J. Raaphorst; M. Lowenberg; R.B. Takkenberg; G.R.A.M. D'Haens; P.I. Spuls; M.W. Bekkenk; A.H. Musters; N.F. Post; A.L. Bosma; M.L. Hilhorst; Y. Vegting; F.J. Bemelman; A.E. Voskuyl; B. Broens; A.P. Sanchez; C.A.C.M. van Els; J. De Wit; A. Rutgers; K. de Leeuw; B. Horvath; J.J.G.M. Verschuuren; A.M. Ruiter; L. van Ouwerkerk; D. van der Woude; C.F. Allaart; O.Y.K. Teng; P. van Paassen; M.H. Busch; P.B.P. Jallah; E. Brusse; P.A. van Doorn; A.E. Baars; D.J. Hijnen; C.R.G. Schreurs; W.L. Van der Pol; H.S. Goedee; M. Steenhuis; S. Keijzer; J.B.D. Keijser; T2B! immunity against SARS-CoV-2 study group; Filip Eftimov

doi:10.1136/ard-2022-222904

Breakthrough infections with the SARS-CoV-2 omicron (B.1.1.529) variant in patients with immune-mediated inflammatory diseases

E.W. Stalman, L. Wieske, K.P.J. van Dam, L.Y. Kummer, Z.L.E. van Kempen, J. Killestein, A.G. Volkers, S.W. Tas, L. Boekel, G.J. Wolbink, A.J. Van der Kooi, J. Raaphorst, M. Lowenberg, R.B. Takkenberg, G.R.A.M. D'Haens, P.I. Spuls, M.W. Bekkenk, A.H. Musters, N.F. Post, A.L. BosmaM.L. Hilhorst, Y. Vegting, F.J. Bemelman, A.E. Voskuyl, B. Broens, A.P. Sanchez, C.A.C.M. van Els, J. De Wit, A. Rutgers, K. de Leeuw, B. Horvath, J.J.G.M. Verschuuren, A.M. Ruiter, L. van Ouwerkerk, D. van der Woude, C.F. Allaart, O.Y.K. Teng, P. van Paassen, M.H. Busch, P.B.P. Jallah, E. Brusse, P.A. van Doorn, A.E. Baars, D.J. Hijnen, C.R.G. Schreurs, W.L. Van der Pol, H.S. Goedee, M. Steenhuis, S. Keijzer, J.B.D. Keijser, T2B! immunity against SARS-CoV-2 study group, Filip Eftimov^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Objectives To compare the cumulative incidence and disease severity of reported SARS-CoV-2 omicron breakthrough infections between patients with immune-mediated inflammatory diseases (IMID) on immunosuppressants and controls, and to investigate determinants for breakthrough infections. Methods Data were used from an ongoing national prospective multicentre cohort study on SARS-CoV-2 vaccination responses in patients with IMID in the Netherlands (Target-to-B! (T2B!) study). Patients wih IMID on immunosuppressants and controls (patients with IMID not on immunosuppressants and healthy controls) who completed primary immunisation were included. The observation period was between 1 January 2022 and 1 April 2022, during which the SARS-CoV-2 omicron (BA.1 and BA.2 subvariant) was dominant. A SARS-CoV-2 breakthrough infection was defined as a reported positive PCR and/or antigen test at least 14 days after primary immunisation. A multivariate logistic regression model was used to investigate determinants. Results 1593 patients with IMID on immunosuppressants and 579 controls were included. The cumulative incidence of breakthrough infections was 472/1593 (29.6%; 95% CI 27% to 32%) in patients with IMID on immunosuppressants and 181/579 (31.3%; 95% CI 28% to 35%) in controls (p=0.42). Three (0.5%) participants had severe disease. Seroconversion after primary immunisation (relative risk, RR 0.71; 95% CI 0.52 to 0.96), additional vaccinations (RR 0.61; 95% CI 0.49 to 0.76) and a prior SARS-CoV-2 infection (RR 0.60; 95% CI 0.48 to 0.75) were associated with decreased risk of breakthrough infection. Conclusions The cumulative incidence of reported SARS-CoV-2 omicron breakthrough infections was high, but similar between patients with IMID on immunosuppressants and controls, and disease severity was mostly mild. Additional vaccinations and prior SARS-CoV-2 infections may reduce the incidence of breakthrough infections.

Original language	English
Pages (from-to)	1757-1766
Number of pages	10
Journal	Annals of the Rheumatic Diseases
Volume	81
Issue number	12
Early online date	5 Sept 2022
DOIs	https://doi.org/10.1136/ard-2022-222904
Publication status	Published - Dec 2022

Keywords

Autoimmune Diseases
Covid-19
Autoimmunity
Vaccination

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10.1136/ard-2022-222904

Cite this

Stalman, E. W., Wieske, L., van Dam, K. P. J., Kummer, L. Y., van Kempen, Z. L. E., Killestein, J., Volkers, A. G., Tas, S. W., Boekel, L., Wolbink, G. J., Van der Kooi, A. J., Raaphorst, J., Lowenberg, M., Takkenberg, R. B., D'Haens, G. R. A. M., Spuls, P. I., Bekkenk, M. W., Musters, A. H., Post, N. F., ... Eftimov, F. (2022). Breakthrough infections with the SARS-CoV-2 omicron (B.1.1.529) variant in patients with immune-mediated inflammatory diseases. Annals of the Rheumatic Diseases, 81(12), 1757-1766. https://doi.org/10.1136/ard-2022-222904

@article{b1072ef5a3f64793b3946d9b2992e19c,

title = "Breakthrough infections with the SARS-CoV-2 omicron (B.1.1.529) variant in patients with immune-mediated inflammatory diseases",

abstract = "Objectives To compare the cumulative incidence and disease severity of reported SARS-CoV-2 omicron breakthrough infections between patients with immune-mediated inflammatory diseases (IMID) on immunosuppressants and controls, and to investigate determinants for breakthrough infections. Methods Data were used from an ongoing national prospective multicentre cohort study on SARS-CoV-2 vaccination responses in patients with IMID in the Netherlands (Target-to-B! (T2B!) study). Patients wih IMID on immunosuppressants and controls (patients with IMID not on immunosuppressants and healthy controls) who completed primary immunisation were included. The observation period was between 1 January 2022 and 1 April 2022, during which the SARS-CoV-2 omicron (BA.1 and BA.2 subvariant) was dominant. A SARS-CoV-2 breakthrough infection was defined as a reported positive PCR and/or antigen test at least 14 days after primary immunisation. A multivariate logistic regression model was used to investigate determinants. Results 1593 patients with IMID on immunosuppressants and 579 controls were included. The cumulative incidence of breakthrough infections was 472/1593 (29.6%; 95% CI 27% to 32%) in patients with IMID on immunosuppressants and 181/579 (31.3%; 95% CI 28% to 35%) in controls (p=0.42). Three (0.5%) participants had severe disease. Seroconversion after primary immunisation (relative risk, RR 0.71; 95% CI 0.52 to 0.96), additional vaccinations (RR 0.61; 95% CI 0.49 to 0.76) and a prior SARS-CoV-2 infection (RR 0.60; 95% CI 0.48 to 0.75) were associated with decreased risk of breakthrough infection. Conclusions The cumulative incidence of reported SARS-CoV-2 omicron breakthrough infections was high, but similar between patients with IMID on immunosuppressants and controls, and disease severity was mostly mild. Additional vaccinations and prior SARS-CoV-2 infections may reduce the incidence of breakthrough infections.",

keywords = "Autoimmune Diseases, Covid-19, Autoimmunity, Vaccination",

author = "E.W. Stalman and L. Wieske and {van Dam}, K.P.J. and L.Y. Kummer and {van Kempen}, Z.L.E. and J. Killestein and A.G. Volkers and S.W. Tas and L. Boekel and G.J. Wolbink and {Van der Kooi}, A.J. and J. Raaphorst and M. Lowenberg and R.B. Takkenberg and G.R.A.M. D'Haens and P.I. Spuls and M.W. Bekkenk and A.H. Musters and N.F. Post and A.L. Bosma and M.L. Hilhorst and Y. Vegting and F.J. Bemelman and A.E. Voskuyl and B. Broens and A.P. Sanchez and {van Els}, C.A.C.M. and {De Wit}, J. and A. Rutgers and {de Leeuw}, K. and B. Horvath and J.J.G.M. Verschuuren and A.M. Ruiter and {van Ouwerkerk}, L. and {van der Woude}, D. and C.F. Allaart and O.Y.K. Teng and {van Paassen}, P. and M.H. Busch and P.B.P. Jallah and E. Brusse and {van Doorn}, P.A. and A.E. Baars and D.J. Hijnen and C.R.G. Schreurs and {Van der Pol}, W.L. and H.S. Goedee and M. Steenhuis and S. Keijzer and J.B.D. Keijser and {T2B! immunity against SARS-CoV-2 study group} and Filip Eftimov",

note = "Funding Information: We thank ZonMw (The Netherlands Organization for Health Research and Development, grant 10430072010007) for the funding of the study and the T2B partners, including the patient groups, and Health Holland for the support in this study. This collaboration project is financed by the PPP Allowance made available by Top Sector Life Sciences & Health to Samenwerkende Gezondheidsfondsen (SGF) under project number LSHM18055-SGF to stimulate public–private partnerships and co-financing by health foundations that are part of the SGF. We also thank E P Moll van Charante (Department of Public and Occupational Health and Department of General Practice, Amsterdam UMC, University of Amsterdam; and Amsterdam Public Health Research Institute, Amsterdam, Netherlands), J A Bogaards (Department of Epidemiology and Data Science, Amsterdam UMC), and R A Scholte (Clinical Research Unit, Amsterdam UMC, University of Amsterdam) for their guidance in the data safety monitoring board. Publisher Copyright: {\textcopyright} 2022 BMJ Publishing Group. All rights reserved.",

year = "2022",

month = dec,

doi = "10.1136/ard-2022-222904",

language = "English",

volume = "81",

pages = "1757--1766",

journal = "Annals of the Rheumatic Diseases",

issn = "0003-4967",

publisher = "BMJ Publishing Group",

number = "12",

}

Stalman, EW, Wieske, L, van Dam, KPJ, Kummer, LY, van Kempen, ZLE, Killestein, J, Volkers, AG, Tas, SW, Boekel, L, Wolbink, GJ, Van der Kooi, AJ, Raaphorst, J, Lowenberg, M, Takkenberg, RB, D'Haens, GRAM, Spuls, PI, Bekkenk, MW, Musters, AH, Post, NF, Bosma, AL, Hilhorst, ML, Vegting, Y, Bemelman, FJ, Voskuyl, AE, Broens, B, Sanchez, AP, van Els, CACM, De Wit, J, Rutgers, A, de Leeuw, K, Horvath, B, Verschuuren, JJGM, Ruiter, AM, van Ouwerkerk, L, van der Woude, D, Allaart, CF, Teng, OYK, van Paassen, P, Busch, MH, Jallah, PBP, Brusse, E, van Doorn, PA, Baars, AE, Hijnen, DJ, Schreurs, CRG, Van der Pol, WL, Goedee, HS, Steenhuis, M, Keijzer, S, Keijser, JBD, T2B! immunity against SARS-CoV-2 study group & Eftimov, F 2022, 'Breakthrough infections with the SARS-CoV-2 omicron (B.1.1.529) variant in patients with immune-mediated inflammatory diseases', Annals of the Rheumatic Diseases, vol. 81, no. 12, pp. 1757-1766. https://doi.org/10.1136/ard-2022-222904

TY - JOUR

T1 - Breakthrough infections with the SARS-CoV-2 omicron (B.1.1.529) variant in patients with immune-mediated inflammatory diseases

AU - Stalman, E.W.

AU - Wieske, L.

AU - van Dam, K.P.J.

AU - Kummer, L.Y.

AU - van Kempen, Z.L.E.

AU - Killestein, J.

AU - Volkers, A.G.

AU - Tas, S.W.

AU - Boekel, L.

AU - Wolbink, G.J.

AU - Van der Kooi, A.J.

AU - Raaphorst, J.

AU - Lowenberg, M.

AU - Takkenberg, R.B.

AU - D'Haens, G.R.A.M.

AU - Spuls, P.I.

AU - Bekkenk, M.W.

AU - Musters, A.H.

AU - Post, N.F.

AU - Bosma, A.L.

AU - Hilhorst, M.L.

AU - Vegting, Y.

AU - Bemelman, F.J.

AU - Voskuyl, A.E.

AU - Broens, B.

AU - Sanchez, A.P.

AU - van Els, C.A.C.M.

AU - De Wit, J.

AU - Rutgers, A.

AU - de Leeuw, K.

AU - Horvath, B.

AU - Verschuuren, J.J.G.M.

AU - Ruiter, A.M.

AU - van Ouwerkerk, L.

AU - van der Woude, D.

AU - Allaart, C.F.

AU - Teng, O.Y.K.

AU - van Paassen, P.

AU - Busch, M.H.

AU - Jallah, P.B.P.

AU - Brusse, E.

AU - van Doorn, P.A.

AU - Baars, A.E.

AU - Hijnen, D.J.

AU - Schreurs, C.R.G.

AU - Van der Pol, W.L.

AU - Goedee, H.S.

AU - Steenhuis, M.

AU - Keijzer, S.

AU - Keijser, J.B.D.

AU - T2B! immunity against SARS-CoV-2 study group

AU - Eftimov, Filip

N1 - Funding Information: We thank ZonMw (The Netherlands Organization for Health Research and Development, grant 10430072010007) for the funding of the study and the T2B partners, including the patient groups, and Health Holland for the support in this study. This collaboration project is financed by the PPP Allowance made available by Top Sector Life Sciences & Health to Samenwerkende Gezondheidsfondsen (SGF) under project number LSHM18055-SGF to stimulate public–private partnerships and co-financing by health foundations that are part of the SGF. We also thank E P Moll van Charante (Department of Public and Occupational Health and Department of General Practice, Amsterdam UMC, University of Amsterdam; and Amsterdam Public Health Research Institute, Amsterdam, Netherlands), J A Bogaards (Department of Epidemiology and Data Science, Amsterdam UMC), and R A Scholte (Clinical Research Unit, Amsterdam UMC, University of Amsterdam) for their guidance in the data safety monitoring board. Publisher Copyright: © 2022 BMJ Publishing Group. All rights reserved.

PY - 2022/12

Y1 - 2022/12

N2 - Objectives To compare the cumulative incidence and disease severity of reported SARS-CoV-2 omicron breakthrough infections between patients with immune-mediated inflammatory diseases (IMID) on immunosuppressants and controls, and to investigate determinants for breakthrough infections. Methods Data were used from an ongoing national prospective multicentre cohort study on SARS-CoV-2 vaccination responses in patients with IMID in the Netherlands (Target-to-B! (T2B!) study). Patients wih IMID on immunosuppressants and controls (patients with IMID not on immunosuppressants and healthy controls) who completed primary immunisation were included. The observation period was between 1 January 2022 and 1 April 2022, during which the SARS-CoV-2 omicron (BA.1 and BA.2 subvariant) was dominant. A SARS-CoV-2 breakthrough infection was defined as a reported positive PCR and/or antigen test at least 14 days after primary immunisation. A multivariate logistic regression model was used to investigate determinants. Results 1593 patients with IMID on immunosuppressants and 579 controls were included. The cumulative incidence of breakthrough infections was 472/1593 (29.6%; 95% CI 27% to 32%) in patients with IMID on immunosuppressants and 181/579 (31.3%; 95% CI 28% to 35%) in controls (p=0.42). Three (0.5%) participants had severe disease. Seroconversion after primary immunisation (relative risk, RR 0.71; 95% CI 0.52 to 0.96), additional vaccinations (RR 0.61; 95% CI 0.49 to 0.76) and a prior SARS-CoV-2 infection (RR 0.60; 95% CI 0.48 to 0.75) were associated with decreased risk of breakthrough infection. Conclusions The cumulative incidence of reported SARS-CoV-2 omicron breakthrough infections was high, but similar between patients with IMID on immunosuppressants and controls, and disease severity was mostly mild. Additional vaccinations and prior SARS-CoV-2 infections may reduce the incidence of breakthrough infections.

AB - Objectives To compare the cumulative incidence and disease severity of reported SARS-CoV-2 omicron breakthrough infections between patients with immune-mediated inflammatory diseases (IMID) on immunosuppressants and controls, and to investigate determinants for breakthrough infections. Methods Data were used from an ongoing national prospective multicentre cohort study on SARS-CoV-2 vaccination responses in patients with IMID in the Netherlands (Target-to-B! (T2B!) study). Patients wih IMID on immunosuppressants and controls (patients with IMID not on immunosuppressants and healthy controls) who completed primary immunisation were included. The observation period was between 1 January 2022 and 1 April 2022, during which the SARS-CoV-2 omicron (BA.1 and BA.2 subvariant) was dominant. A SARS-CoV-2 breakthrough infection was defined as a reported positive PCR and/or antigen test at least 14 days after primary immunisation. A multivariate logistic regression model was used to investigate determinants. Results 1593 patients with IMID on immunosuppressants and 579 controls were included. The cumulative incidence of breakthrough infections was 472/1593 (29.6%; 95% CI 27% to 32%) in patients with IMID on immunosuppressants and 181/579 (31.3%; 95% CI 28% to 35%) in controls (p=0.42). Three (0.5%) participants had severe disease. Seroconversion after primary immunisation (relative risk, RR 0.71; 95% CI 0.52 to 0.96), additional vaccinations (RR 0.61; 95% CI 0.49 to 0.76) and a prior SARS-CoV-2 infection (RR 0.60; 95% CI 0.48 to 0.75) were associated with decreased risk of breakthrough infection. Conclusions The cumulative incidence of reported SARS-CoV-2 omicron breakthrough infections was high, but similar between patients with IMID on immunosuppressants and controls, and disease severity was mostly mild. Additional vaccinations and prior SARS-CoV-2 infections may reduce the incidence of breakthrough infections.

KW - Autoimmune Diseases

KW - Covid-19

KW - Autoimmunity

KW - Vaccination

U2 - 10.1136/ard-2022-222904

DO - 10.1136/ard-2022-222904

M3 - Article

C2 - 36357161

SN - 0003-4967

VL - 81

SP - 1757

EP - 1766

JO - Annals of the Rheumatic Diseases

JF - Annals of the Rheumatic Diseases

IS - 12

ER -