Factors associated with early hydroxychloroquine-induced retinal toxicity in patients with systemic lupus erythematosus.

Adverse effects Hydroxychloroquine Lupus erythematosus Retinal diseases Risk Systemic Toxicity

Journal

Graefe's archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie
ISSN: 1435-702X
Titre abrégé: Graefes Arch Clin Exp Ophthalmol
Pays: Germany
ID NLM: 8205248

Informations de publication

Date de publication:
05 Apr 2024
Historique:
received: 11 11 2023
accepted: 20 03 2024
revised: 12 02 2024
medline: 5 4 2024
pubmed: 5 4 2024
entrez: 5 4 2024
Statut: aheadofprint

Résumé

Hydroxychloroquine is currently recommended for the treatment of systemic lupus erythematosus (SLE), but it can cause irreversible retinal toxicity. This study aimed to identify factors associated with early hydroxychloroquine-induced retinal toxicity in patients with SLE from a single centre for 20 years. SLE patients diagnosed between 1998 and 2017 and followed up for at least 1 year were included. Demographic, clinical, laboratory and therapeutic data were collected from the electronic medical records and retrospectively analysed. Early hydroxychloroquine-induced retinal toxicity was defined as the development of macular toxicity within the first 5 years of hydroxychloroquine treatment. A total of 345 patients followed for a median of 15 years were analysed; 337 (97.7%) patients received hydroxychloroquine, 38 (11.3%) of them presented with retinal toxicity, and 10 (3%) developed early retinal toxicity. These patients had a mean treatment duration of 3.3 years with a mean cumulative dose of 241 g. Patients were diagnosed by visual field (VF) and fundoscopy, and two were also assessed using spectral domain optical coherence tomography (SD-OCT). The median (IQR) age of patients with early toxicity was 56 (51-66) years, and 80% were female. Factors independently associated with early hydroxychloroquine-induced retinal toxicity were lupus anticoagulant positivity (OR 4.2; 95% CI 1.2-15.5) and hypercholesterolaemia (OR 5.6; 95% CI 1.5-21.5). Our results suggest that lupus anticoagulant positivity and hypercholesterolaemia among SLE patients may be risk factors for early hydroxychloroquine-induced retinal toxicity, regardless of the dose or duration of treatment.

Identifiants

DOI: 10.1007/s00417-024-06461-6 PMID: 38578332
pubmed: 38578332
doi: 10.1007/s00417-024-06461-6
pii: 10.1007/s00417-024-06461-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Kaul A, Gordon C, Crow MK et al (2016) Systemic lupus erythematosus. Nat Rev Dis Primer 2(1):1–21
doi: 10.1038/nrdp.2016.39
Fanouriakis A, Kostopoulou M, Andersen J et al (2024) EULAR recommendations for the management of systemic lupus erythematosus: 2023 update. Ann Rheum Dis 83(1):15–29. https://doi.org/10.1136/ard-2023-224762
doi: 10.1136/ard-2023-224762 pubmed: 37827694
Ruiz-Irastorza G, Ramos-Casals M, Brito-Zeron P et al (2010) Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: a systematic review. Ann Rheum Dis 69(01):20–28
pubmed: 19103632 doi: 10.1136/ard.2008.101766
Ruiz-Irastorza G, Martín-Iglesias D, Soto-Peleteiro A (2020) Update on antimalarials and systemic lupus erythematosus. Curr Opin Rheumatol 32(6):572–582
pubmed: 32890029 doi: 10.1097/BOR.0000000000000743
Dima A, Jurcut C, Chasset F et al (2022) Hydroxychloroquine in systemic lupus erythematosus: overview of current knowledge. Ther Adv Musculoskelet Dis 14. https://doi.org/10.1177/1759720X211073001
Costedoat-Chalumeau N, Dunogué B, Leroux G et al (2015) A critical review of the effects of hydroxychloroquine and chloroquine on the eye. Clin Rev Allergy Immunol 49(3):317–326
pubmed: 25672591 doi: 10.1007/s12016-015-8469-8
Ozawa H, Ueno S, Ohno-Tanaka A et al (2021) Ocular findings in Japanese patients with hydroxychloroquine retinopathy developing within 3 years of treatment. Jpn J Ophthalmol 65(4):472–481
pubmed: 34014447 doi: 10.1007/s10384-021-00841-9
Wolfe F, Marmor MF (2010) Rates and predictors of hydroxychloroquine retinal toxicity in patients with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Care Res 62(6):775–784
doi: 10.1002/acr.20133
Melles RB, Marmor MF (2014) The risk of toxic retinopathy in patients on long-term hydroxychloroquine therapy. JAMA Ophthalmol 132(12):1453–1460
pubmed: 25275721 doi: 10.1001/jamaophthalmol.2014.3459
Pelegrín L, Morató M, Araújo O et al (2023) Preclinical ocular changes in systemic lupus erythematosus patients by optical coherence tomography. Rheumatology (Oxford) 62(7):2475–2482
pubmed: 36331348 doi: 10.1093/rheumatology/keac626
Jorge A, Ung C, Young LH et al (2018) Hydroxychloroquine retinopathy — implications of research advances for rheumatology care. Nat Rev Rheumatol 14(12):693–703
pubmed: 30401979 doi: 10.1038/s41584-018-0111-8
Yusuf IH, Sharma S, Luqmani R et al (2017) Hydroxychloroquine retinopathy. Eye 31(6):828–845
pubmed: 28282061 pmcid: 5518824 doi: 10.1038/eye.2016.298
Ding HJ, Denniston AK, Rao VK et al (2016) Hydroxychloroquine-related retinal toxicity. Rheumatology (Oxford) 55(6):957–967
pubmed: 26428520 doi: 10.1093/rheumatology/kev357
Doyno C, Sobieraj DM, Baker WL (2021) Toxicity of chloroquine and hydroxychloroquine following therapeutic use or overdose. Clin Toxicol 59(1):12–23
doi: 10.1080/15563650.2020.1817479
Petri M, Elkhalifa M, Li J et al (2020) Hydroxychloroquine blood levels predict hydroxychloroquine retinopathy. Arthritis Rheumatol 72(3):448–453
pubmed: 31532077 pmcid: 7050401 doi: 10.1002/art.41121
Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725–1725
pubmed: 9324032 doi: 10.1002/art.1780400928
Aringer M, Costenbader K, Daikh D et al (2019) 2019 European League Against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus. Ann Rheum Dis 78(9):1151–1159
pubmed: 31383717 doi: 10.1136/annrheumdis-2018-214819
Yu CY, Kuo CF, Chou IJ et al (2022) Comorbidities of systemic lupus erythematosus prior to and following diagnosis in different age-at-onset groups. Lupus 31(8):963–973
pubmed: 35536913 doi: 10.1177/09612033221100908
Whelton PK, Carey RM, Aronow WS et al (2018) 2017 guideline for the prevention, detection, evaluation, and management of high blood pressure in adults: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 71(19):e127-248
pubmed: 29146535 doi: 10.1016/j.jacc.2017.11.006
ElSayed NA, Aleppo G, Aroda VR et al (2022) 2 Classification and diagnosis of diabetes: standards of care in diabetes—2023. Diabetes Care 46(Supplement 1):S19-40
pmcid: 9810477
Grundy SM, Stone NJ, Bailey AL et al (2019) 2018 guideline on the management of blood cholesterol: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 73(24):3168–3209
pubmed: 30423391 doi: 10.1016/j.jacc.2018.11.002
Webster AC, Nagler EV, Morton RL et al (2017) Chronic kidney disease. The Lancet 389(10075):1238–1252
doi: 10.1016/S0140-6736(16)32064-5
Marmor MF, Carr RE, Easterbrook M et al (2002) Recommendations on screening for chloroquine and hydroxychloroquine retinopathy: a report by the American Academy of Ophthalmology. Ophthalmology 109(7):1377–1382
pubmed: 12093666 doi: 10.1016/S0161-6420(02)01168-5
Marmor MF, Kellner U, Lai TYY et al (2011) Revised recommendations on screening for chloroquine and hydroxychloroquine retinopathy. Ophthalmology 118(2):415–422
pubmed: 21292109 doi: 10.1016/j.ophtha.2010.11.017
Marmor MF, Kellner U, Lai TYY et al (2016) Recommendations on screening for chloroquine and hydroxychloroquine retinopathy (2016 revision). Ophthalmology 123(6):1386–1394
pubmed: 26992838 doi: 10.1016/j.ophtha.2016.01.058
Marmor MF, Chien FY, Johnson MW (2013) Value of red targets and pattern deviation plots in visual field screening for hydroxychloroquine retinopathy. JAMA Ophthalmol 131(4):476–480
pubmed: 23710501 doi: 10.1001/jamaophthalmol.2013.1404
Anderson C, Blaha GR, Marx JL (2011) Humphrey visual field findings in hydroxychloroquine toxicity. Eye (Lond) 25(12):1535–1545
pubmed: 22094300 doi: 10.1038/eye.2011.245
Marmor MF (2012) Comparison of screening procedures in hydroxychloroquine toxicity. Arch Ophthalmol 130(4):461–469
pubmed: 22159170 doi: 10.1001/archophthalmol.2011.371
Chen E, Brown DM, Benz MS et al (2010) Spectral domain optical coherence tomography as an effective screening test for hydroxychloroquine retinopathy (the «flying saucer» sign). Clin Ophthalmol Auckl NZ 4:1151–1158
doi: 10.2147/OPTH.S14257
Araújo O, Hernández-Rodríguez J, Pelegrín L et al (2022) Why lupus patients discontinue antimalarials in real life: a 50 years-experience from a reference centre. Lupus 31(11):1344–1354
pubmed: 35848412 doi: 10.1177/09612033221115618
The Royal College of Ophthalmologists - Hydroxychloroquine and ocular toxicity recommendations on screening (2009) http://bmec.swbh.nhs.uk/wp-content/uploads/2013/03/OCULAR-TOXICITY-OF-HYDROXYCHLOROQUINE.pdf . Accessed 29 Aug 2023
Yusuf IH, Foot B, Galloway J et al (2018) The Royal College of Ophthalmologists recommendations on screening for hydroxychloroquine and chloroquine users in the United Kingdom: executive summary consensus-statement. Eye (Lond) 32(7):1168–1173
pubmed: 29887605 doi: 10.1038/s41433-018-0136-x
Yusuf IH, Foot B, Lotery AJ (2021) The Royal College of Ophthalmologists recommendations on monitoring for hydroxychloroquine and chloroquine users in the United Kingdom (2020 revision): executive summary. Eye (Lond) 35(6):1532–1537
pubmed: 33423043 doi: 10.1038/s41433-020-01380-2
Araújo O, Pelegrín L, Espinosa G et al (2021) Antimalarial-induced retinal toxicity. Rev Colomb Reumatol 28:132–143. https://doi.org/10.1016/j.rcreu.2021.05.010
doi: 10.1016/j.rcreu.2021.05.010
Garrity ST, Jung JY, Zambrowski O et al (2019) Early hydroxychloroquine retinopathy: optical coherence tomography abnormalities preceding Humphrey visual field defects. Br J Ophthalmol 103(11):1600–1604
pubmed: 30819690 doi: 10.1136/bjophthalmol-2018-313350
Elder M, Rahman AMA, McLay J (2006) Early paracentral visual field loss in patients taking hydroxychloroquine. Arch Ophthalmol 124(12):1729–1733
pubmed: 17159032 doi: 10.1001/archopht.124.12.1729
Jover JA, Leon L, Pato E et al (2012) Long-term use of antimalarial drugs in rheumatic diseases. Clin Exp Rheumatol 30(3):380–387
pubmed: 22339928
Almeida-Brasil CC, Hanly JG, Urowitz M et al (2022) Retinal toxicity in a multinational inception cohort of patients with systemic lupus on hydroxychloroquine. Lupus Sci Med 9(1):e000789. https://doi.org/10.1136/lupus-2022-000789
doi: 10.1136/lupus-2022-000789 pubmed: 36396267 pmcid: 9677013
Moschos MN, Moschos MM, Apostolopoulos M et al (2004) Assessing hydroxychloroquine toxicity by the multifocal ERG. Doc Ophthalmol 108(1):47–53
pubmed: 15104166 doi: 10.1023/B:DOOP.0000018385.99215.0d
Michaelides M, Stover NB, Francis PJ et al (2011) Retinal toxicity associated with hydroxychloroquine and chloroquine: risk factors, screening, and progression despite cessation of therapy. Arch Ophthalmol 129(1):30–39
pubmed: 21220626 doi: 10.1001/archophthalmol.2010.321
Farrell DF (2012) Retinal toxicity to antimalarial drugs: chloroquine and hydroxychloroquine: a neurophysiologic study. Clin Ophthalmol Auckl NZ 6:377–383
doi: 10.2147/OPTH.S27731
Manoj M, Sahoo RR, Singh A et al (2021) Prevalence of hydroxychloroquine retinopathy with long-term use in a cohort of Indian patients with rheumatic diseases. Rheumatol Int 41(5):929–937
pubmed: 33704526 doi: 10.1007/s00296-021-04831-5
Spinelli FR, Moscarelli E, Ceccarelli F et al (2018) Treating lupus patients with antimalarials: analysis of safety profile in a single-center cohort. Lupus 27(10):1616–1623
pubmed: 29954281 doi: 10.1177/0961203318781008
Mackenzie AH (1983) Dose refinements in long-term therapy of rheumatoid arthritis with antimalarials. Am J Med 75(1):40–5
pubmed: 6869410 doi: 10.1016/0002-9343(83)91269-X
Chiang E, Jampol LM, Fawzi AA (2014) Retinal toxicity found in a patient with systemic lupus erythematosus prior to 5 years of treatment with hydroxychloroquine. Rheumatol (Oxford, England) 53(11):2001
doi: 10.1093/rheumatology/keu317
Pasaoglu I, Onmez FE (2019) Macular toxicity after short-term hydroxychloroquine therapy. Indian J Ophthalmol 67(2):289–292
pubmed: 30672499 pmcid: 6376838 doi: 10.4103/ijo.IJO_732_18
Hernández Bel L, MonferrerAdsuara C, Hernández Garfella M et al (2018) Toxicidad macular precoz tras 2 meses de tratamiento con hidroxicloroquina. Arch Soc Esp Oftalmol 93(3):e20–e21
pubmed: 29395216 doi: 10.1016/j.oftal.2017.12.004
Flammer J, Konieczka K, Bruno RM et al (2013) The eye and the heart. Eur Heart J 34(17):1270–1278
pubmed: 23401492 pmcid: 3640200 doi: 10.1093/eurheartj/eht023
Hage MP, Badri MR, Azar ST (2014) A favorable effect of hydroxychloroquine on glucose and lipid metabolism beyond its anti-inflammatory role. Ther Adv Endocrinol Metab 5(4):77–85
pubmed: 25343023 pmcid: 4206615 doi: 10.1177/2042018814547204
Tsang AC, Ahmadi Pirshahid S, Virgili G et al (2015) Hydroxychloroquine and chloroquine retinopathy: a systematic review evaluating the multifocal electroretinogram as a screening test. Ophthalmology 122(6):1239-1251.e4
pubmed: 25824328 doi: 10.1016/j.ophtha.2015.02.011

Auteurs

Olga Araújo (O)

Department of Autoimmune Diseases, Member of the European Reference Centres (ERN) Re-CONNET and RITA, Reference Centre for Systemic Autoimmune Diseases, Vasculitis and Autoinflammatory Diseases of the Catalan and Spanish Health Systems, Hospital Clínic de Barcelona. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Villarroel 170, 08036, Barcelona, Catalonia, Spain.
ORCID: 0000-0003-1763-1880

Halbert Hernández-Negrín (H)

Department of Autoimmune Diseases, Member of the European Reference Centres (ERN) Re-CONNET and RITA, Reference Centre for Systemic Autoimmune Diseases, Vasculitis and Autoinflammatory Diseases of the Catalan and Spanish Health Systems, Hospital Clínic de Barcelona. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Villarroel 170, 08036, Barcelona, Catalonia, Spain.
ORCID: 0000-0002-9992-9148

Ricardo P Casaroli-Marano (RP)

Department of Ophthalmology, Hospital Clínic de Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Barcelona, Catalonia, Spain.
ORCID: 0000-0003-1812-9323

José Hernández-Rodríguez (J)

Department of Autoimmune Diseases, Member of the European Reference Centres (ERN) Re-CONNET and RITA, Reference Centre for Systemic Autoimmune Diseases, Vasculitis and Autoinflammatory Diseases of the Catalan and Spanish Health Systems, Hospital Clínic de Barcelona. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Villarroel 170, 08036, Barcelona, Catalonia, Spain.
ORCID: 0000-0002-2357-2015

Alfredo Adán (A)

Department of Ophthalmology, Hospital Clínic de Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Barcelona, Catalonia, Spain.
ORCID: 0000-0002-0849-8814

Gerard Espinosa (G)

Department of Autoimmune Diseases, Member of the European Reference Centres (ERN) Re-CONNET and RITA, Reference Centre for Systemic Autoimmune Diseases, Vasculitis and Autoinflammatory Diseases of the Catalan and Spanish Health Systems, Hospital Clínic de Barcelona. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Villarroel 170, 08036, Barcelona, Catalonia, Spain. gespino@clinic.cat.
ORCID: 0000-0003-1336-0163

Laura Pelegrín (L)

Department of Ophthalmology, Hospital Clínic de Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Barcelona, Catalonia, Spain.
ORCID: 0000-0003-2861-5173

Ricard Cervera (R)

Department of Autoimmune Diseases, Member of the European Reference Centres (ERN) Re-CONNET and RITA, Reference Centre for Systemic Autoimmune Diseases, Vasculitis and Autoinflammatory Diseases of the Catalan and Spanish Health Systems, Hospital Clínic de Barcelona. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Villarroel 170, 08036, Barcelona, Catalonia, Spain.
ORCID: 0000-0001-6085-492X

Classifications MeSH