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Factors associated with adverse COVID-19 outcomes in patients with psoriasis—insights from a global registry–based study - 09/01/21

Doi : 10.1016/j.jaci.2020.10.007 
Satveer K. Mahil, PhD, MRCP a, , Nick Dand, PhD b, c, , Kayleigh J. Mason, PhD d, Zenas Z.N. Yiu, PhD, MRCP d, Teresa Tsakok, MRCP a, Freya Meynell, MSc a, Bola Coker, MSc e, Helen McAteer, BSc f, Lucy Moorhead, MA a, Teena Mackenzie, BSc g, Maria Teresa Rossi, MD h, Raquel Rivera, MD i, Emmanuel Mahe, MD j, k, Andrea Carugno, MD l, Michela Magnano, MD m, Giulia Rech, MD m, Esther A. Balogh, MD n, Steven R. Feldman, MD, PhD n, Claudia De La Cruz, MD o, Siew Eng Choon, MBBS, FRCP p, Luigi Naldi, MD q, Jo Lambert, MD, PhD r, Phyllis Spuls, MD, PhD s, Denis Jullien, MD, PhD k, t, Hervé Bachelez, MD, PhD u, v, Devon E. McMahon, MD w, Esther E. Freeman, MD x, Paolo Gisondi, MD y, Luis Puig, MD PhD z, Richard B. Warren, PhD, FRCP d, Paola Di Meglio, PhD aa, Sinéad M. Langan, PhD, FRCP a, bb, Francesca Capon, PhD b, Christopher E.M. Griffiths, MD, FMedSci d, Jonathan N. Barker, MD, FRCP aa, Catherine H. Smith, MD, FRCP a,
on behalf of the

PsoProtect study group

  For a complete list of PsoProtect study group collaborators, please see the Acknowledgment section at the end of this article.
Aadarsh Shah, MRCP, Alberto Barea, MSc, Alberto Romero-Maté, MD, Alekya Singapore, MD, Alexandra Paolino, MRCP, Alice Mwale, BSc, Ana Maria Morales Callaghan, MD, Ana Martinez, MD, Andrew DeCrescenzo, MD, Andrew E. Pink, MRCP, PhD, Ann Jones, BSc, Ann Sergeant, MD, Annette Essex, RGN, Anthony Bewley, FRCP, Areti Makrygeorgou, MBBS, Astrid van Huizen, MD, Beatriz Pérez-Suárez, MD, PhD, Benhadou Farida, MD, PhD, Birgitta Wilson Claréus, MD, Carla Tubau Prims, MD, Carrie Davis, MD, Catherine Quinlan, MRCPI, Catriona Maybury, MRCP, PhD, Gonzalez A. Cesar, MD, Charlotte Barclay, BSc, Claudio Greco, MD, Danielle Brassard, MD, Deanna Cummings, BSc, Deepti Kolli, MD, Vincent Descamps, MD, PhD, Diana Ruiz Genao, MD, Efrossini Carras, BSc, MRCP, Elena Hawryluk, MD, PhD, Eliseo Martínez-García, MD, PhD, Elzbieta Klujszo, MD, Emily Dwyer, BSc, Emmanuel Toni, BSc, Enikö Sonkoly, MD, PhD, Enrique Loayza, MD, Esteban Daudén, MD, PhD, Fernando Valenzuela, MD, Georgi Popov, MD, PhD, Georgie King, MSc, Girard Celine, MD, Gloria Aparicio, MD, Graham A. Johnston, FRCP, Gustavo Anibal Cardozo, MD, Ian Pearson, MRCP, Ignacio Yanguas, MD, Jamie Weisman, MD, Jennifer E. Carolan, MSc, Jenny Hughes, FRCP, Jose-Maria Ortiz-Salvador, MD, PhD, Jose-Manuel Carrascosa, MD, PhD, Joseph J. Schwartz, MD, Karina Jackson, MSc, Kathryn G. Kerisit, MD, MPH, Keith Wu, MD, Leila Asfour, MRCP, Leontien de Graaf, MD, Cécile Lesort, MD, Lieve Meuleman, MD, Liv Eidsmo, MD, PhD, Lone Skov, MD, PhD, Lorraine Gribben, BSc, Malcolm Rustin, MD, Manel Velasco, MD, Manisha Panchal, MD, Manpreet Lakhan, MRCP, Manuel D. Franco, MD, Marie-Louise Svensson, BSc, Mark Vandaele, MD, Maruska Marovt, MD, PhD, Omid Zargari, MD, Pablo De Caso, MD, Paulo Varela, MD, Peter Jenkin, MD, FAAD, Céline Phan, MD, Philip Hampton, FRCP, PhD, Portia Goldsmith, MD, FRCP, Rachel Bak, MD, Reinhart Speeckaert, MD, PhD, Ricardo Romiti, MD, PhD, Richard Woolf, MRCP, PhD, Rogelio Mercado-Seda, MD, Rohima Khatun, BSc, Romana Ceovic, MD, Rosa Taberner, MD, Russell W. Cohen, MD, FAAD, Simina Stefanescu, MD, Sarah Kirk, BSc, Saskia Reeken, BSc, Shanti Ayob, MRCP, Silvia Pérez-Barrio, MD, Stefano Piaserico, MD, PhD, Susannah Hoey, MD, Tiago Torres, MD, PhD, Toomas Talme, MD, PhD, Trupti V. Desai, MD, Adrienne J. van Geest, MD, Victoria King, BSc, Vito Di Lernia, MD, Zahira Koreja, BSc, Vito Zeeshaan Hasab, MBBS

a St John’s Institute of Dermatology, Guy’s and St Thomas’ NHS Foundation Trust and King's College London, London, United Kingdom 
b Department of Medical and Molecular Genetics, School of Basic and Medical Biosciences, Faculty of Life Sciences and Medicine, King's College London, London, United Kingdom 
c Health Data Research UK, London, United Kingdom 
d Dermatology Centre, Salford Royal NHS Foundation Trust, The University of Manchester, Manchester Academic Health Science Centre, National Institute for Health Research Manchester Biomedical Research Centre, Manchester, United Kingdom 
e National Institute for Health Research Biomedical Research Centre at Guy’s and St Thomas’ NHS Foundation Trust, London, United Kingdom 
f The Psoriasis Association, Northampton, United Kingdom 
g Dermatology Department, Churchill Hospital, Oxford, United Kingdom 
h Dermatology Department, Spedali Civili Hospital, Brescia, Italy 
i Dermatology Department, Hospital Universitario 12 de Octubre, Universidad Complutense de Madrid, Madrid, Spain 
j Department of Dermatology, Hôpital Victor Dupouy, Argenteuil, France 
k Groupe de recherche sur le psoriasis (GrPso) de la Société Française de Dermatologie, Paris, France 
l Dermatology Unit, ASST Papa Giovanni XXIII Hospital, Bergamo, Italy 
m Dermatology Unit, Santa Chiara Hospital, Trento, Italy 
n Center for Dermatology Research, Department of Dermatology, Wake Forest School of Medicine, Winston-Salem, NC 
o Clinica Dermacross, Santiago, Chile 
p Jeffrey Cheah School Of Medicine and Health Sciences, Monash University, Subang Jaya, Selangor 
q Centro Studi GISED, Bergamo, Italy 
r Department of Dermatology, Ghent University, Ghent, Belgium 
s Department of Dermatology, Amsterdam Public Health/Infection and Immunology, Amsterdam University Medical Centers, Location AMC, Amsterdam, The Netherlands 
t Department of Dermatology, Edouard Herriot Hospital, Hospices Civils de Lyon, Lyon, France 
u Department of Dermatology, AP-HP Hôpital Saint-Louis, Paris, France 
v INSERM U1163, Imagine Institute for Human Genetic Diseases, Université de Paris, Paris, France 
w Harvard Medical School, Boston, Mass 
x Department of Dermatology, Massachusetts General Hospital, Harvard Medical School, Boston, Mass 
y Section of Dermatology and Venereology, University of Verona, Verona, Italy 
z Department of Dermatology, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain 
aa St. John’s Institute of Dermatology, School of Basic & Medical Biosciences, Faculty of Life Sciences & Medicine, King's College London, London, United Kingdom 
bb Faculty of Epidemiology, and Population Health, London School of Hygiene and Tropical Medicine, London, United Kingdom 

Corresponding author: Catherine Smith, MD, FRCP, St. John’s Institute of Dermatology, Guy’s and St Thomas’ NHS Foundation Trust, Great Maze Pond, London, SE1 9RT, UK.St. John’s Institute of DermatologyGuy’s and St Thomas’ NHS Foundation TrustGreat Maze PondLondonSE1 9RTUK

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Abstract

Background

The multimorbid burden and use of systemic immunosuppressants in people with psoriasis may confer greater risk of adverse outcomes of coronavirus disease 2019 (COVID-19), but the data are limited.

Objective

Our aim was to characterize the course of COVID-19 in patients with psoriasis and identify factors associated with hospitalization.

Methods

Clinicians reported patients with psoriasis with confirmed/suspected COVID-19 via an international registry, Psoriasis Patient Registry for Outcomes, Therapy and Epidemiology of COVID-19 Infection. Multiple logistic regression was used to assess the association between clinical and/or demographic characteristics and hospitalization. A separate patient-facing registry characterized risk-mitigating behaviors.

Results

Of 374 clinician-reported patients from 25 countries, 71% were receiving a biologic, 18% were receiving a nonbiologic, and 10% were not receiving any systemic treatment for psoriasis. In all, 348 patients (93%) were fully recovered from COVID-19, 77 (21%) were hospitalized, and 9 (2%) died. Increased hospitalization risk was associated with older age (multivariable-adjusted odds ratio [OR] = 1.59 per 10 years; 95% CI = 1.19-2.13), male sex (OR = 2.51; 95% CI = 1.23-5.12), nonwhite ethnicity (OR = 3.15; 95% CI = 1.24-8.03), and comorbid chronic lung disease (OR = 3.87; 95% CI = 1.52-9.83). Hospitalization was more frequent in patients using nonbiologic systemic therapy than in those using biologics (OR = 2.84; 95% CI = 1.31-6.18). No significant differences were found between classes of biologics. Independent patient-reported data (n = 1626 across 48 countries) suggested lower levels of social isolation in individuals receiving nonbiologic systemic therapy than in those receiving biologics (OR = 0.68; 95% CI = 0.50-0.94).

Conclusion

In this international case series of patients with moderate-to-severe psoriasis, biologic use was associated with lower risk of COVID-19–related hospitalization than with use of nonbiologic systemic therapies; however, further investigation is warranted on account of potential selection bias and unmeasured confounding. Established risk factors (being older, being male, being of nonwhite ethnicity, and having comorbidities) were associated with higher hospitalization rates.

Le texte complet de cet article est disponible en PDF.

Key words : COVID-19, hospitalization, psoriasis, risk factors, biologics, immunosuppressants

Abbreviations used : BMI, IBD, IMID, IQR, OR, PsoProtect


Plan


 We acknowledge financial support from the Department of Health via the National Institute for Health Research (NIHR) Biomedical Research Centre based at Guy's and St Thomas' NHS Foundation Trust and King's College London, the NIHR Manchester Biomedical Research Centre and the Psoriasis Association. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, or the Department of Health and Social Care. S.K.M. is funded by a Medical Research Council Clinical Academic Research Partnership award (MR/T02383X/1). N.D. is funded by Health Data Research UK (MR/S003126/1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council; Economic and Social Research Council; Department of Health & Social Care (England); Chief Scientist Office of the Scottish Government Health and Social Care Directorates; Health and Social Care Research and Development Division (Welsh Government); Public Health Agency (Northern Ireland); British Heart Foundation; and Wellcome. Z.Z.N.Y is funded by a NIHR Academic Clinical Lectureship through the University of Manchester. C.E.M.G. is an NIHR Emeritus Senior Investigator and is funded in part by the Medical Research Council (MR/101 1808/1). C.E.M.G. and R.B.W. are in part supported by the NIHR Manchester Biomedical Research Centre. S.M.L. is supported by a Wellcome Senior Research Fellowship in clinical science (205039/Z/16/Z). S.M.L. is also supported by Health Data Research UK (grant LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh government), Public Health Agency (Northern Ireland), British Heart Foundation ,and Wellcome Trust.
 Disclosure of potential conflict of interest: T. Mackenzie has received honoraria from AbbVie, Sanofi, and Leo. C. H. Smith has received departmental research funding from AbbVie, Novartis, Pfizer, and Sanofi and has served as an investigator on Medical Research Council– and Horizon 2020–funded consortia with industry partners (see psort.org.uk and biomap—imi.eu); SOBI provided the drug for a National Institute for Health Research–funded trial in pustular psoriasis. S. K. Mahil has received departmental funding from AbbVie, Celgene, Eli Lilly, Janssen-Cilag, Novartis, Sanofi, and UCB. K. J. Masib has received honoraria from Janssen, LEO Pharma, Lilly, and Novartis. P. Di Meglio has received research grants from UCB and consultancy/speaker honoraria from Novartis, UCB, and Janssen. F. Capon has received funding and consulting fees from Boehringer Ingelheim and AnaptysBio. E. Mahe has received honoraria from AbbVie, Celgene, Amgen, Janssen CIlag, Novartis, Lilly, and Leo Pharma. L. Moorhead has received honoraria from AbbVie, Celgene, Janssen, Leo, Novartis, and UCB. R. Rivera has been a consultant and adviser and/or received speaking fees and/or grants and/or served as an investigator in clinical trials for AbbVie, Almirall, Amgen, Boehringer, Celgene, Janssen, LEO Pharma, Lilly, MSD, Novartis, Pfizer, and UCB. L. Puig has perceived consultancy/speaker honoraria from and/or participated in clinical trials sponsored by AbbVie, Almirall, Amgen, Baxalta, Biogen, Boehringer Ingelheim, Celgene, Gebro, Janssen, JS BIOCAD, Leo-Pharma, Lilly, Merck-Serono, MSD, Mylan, Novartis, Pfizer, Regeneron, Roche, Sandoz, Samsung-Bioepis, Sanofi, and UCB. J. N. Barker has received honoraria and/or research grants from AbbVie, Almirall, Amgen, Boehringer-Ingelheim, Bristol-Myers Squibb, Celgene, Janssen, Leo, Lilly, Novartis, Samsung, and Sun Pharma. C. E. M. Griffiths has received honoraria and/or research grants from AbbVie, BMS, Almirall, Amgen, Celgene, Eli Lilly Galderma, LEO Pharma, Stiefel GSK, Janssen, MSD, Novartis, Pfizer, Sandoz, Sun Pharmaceuticals, and UCB Pharma. R. B. Warren has received grants and/or honoraria from AbbVie, Almirall, Amgen, Boehringer Ingelheim, Celgene, Janssen, Lilly, Leo Pharma, Novartis, Pfizer, Sanofi, UCB Pharma, and Xenoport. S. R. Feldman has received research, speaking and/or consulting support from Galderma, GSK/Stiefel, Almirall, Leo Pharma, Boehringer Ingelheim, Mylan, Celgene, Pfizer, Valeant, AbbVie, Samsung, Janssen, Lilly, Menlo, Merck, Novartis, Regeneron, Sanofi, Novan, Qurient, National Biological Corporation, Caremark, Advance Medical, Sun Pharma, Suncare Research, Informa, UpToDate, and the National Psoriasis Foundation; he is founder and majority owner of www.DrScore.com and founder and part owner of Causa Research, a company dedicated to enhancing patients’ adherence to treatment. H. McAteer is employed by the Psoriasis Association, which has received grants from Almirral, AbbVie, Amgen, Celgene, Dermal Laboratories, Eli Lilly, Janssen, LEO Pharma, T and R Derma, and UCB; the Psoriasis Association has a policy that no more than 15% of income can come from the pharmaceutical industry. H. Bachelez has had paid consulting activities for AbbVie, Almirall, Biocad, Boehringer-Ingelheim, Janssen, Kyowa Kirin, Novartis, and UCB, and received grant support from Janssen, Leo Pharma, and Pfizer. D. Jullien has acted as, participated in, or received consultancy for the following: speaker bureau, clinical research, honoraria, scientific officer, steering committees, advisory boards for AbbVie, Almiral Amgen, Biogen, Celgene, Fresenius-Kabi, Janssen-Cilag, Leo, Lilly, MEDAC, Novartis, Pfizer, Sanofi, and UCB. C. De La Cruz has been a speaker or principal investigator for AbbVie, Pfizer, Lilly, Janssen, Novartis, Amgen, Boehringer Ingelheim, and Sanofi. P. Spuls has done consultancies in the past for Sanofi 111017 and AbbVie 041217 (unpaid), received a departmental independent research grant for TREAT NL registry LeoPharma December 2019; he is involved in performing clinical trials with many pharmaceutical industries that manufacture drugs used for the treatment of diseases such as psoriasis and atopic dermatitis, for which financial compensation is paid to the department/hospital; and he is chief investigator of the systemic and phototherapy atopic eczema registry (TREAT NL) for adults and children, as well as one of the main investigators of the SECURE-AD registry. The rest of the authors declare that they have no relevant conflicts of interest.


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