Advertisement

Late-onset systemic lupus erythematosus: characteristics and outcome in comparison to juvenile- and adult-onset patients—a multicenter retrospective cohort

  • Basma M MedhatEmail author
  • Mervat Essam Behiry
  • Nesreen Sobhy
  • Yomna Farag
  • Huda Marzouk
  • Noha Mostafa
  • Iman Khalifa
  • Marwa Elkhalifa
  • Basma M. Eissa
  • Eman Hassan ElSayed Hassan
Original Article
  • 51 Downloads

Abstract

Introduction

The aim of this study was to investigate the characteristics and outcome of systemic lupus erythematosus (SLE) among elderly-onset patients.

Methods

This study included 575 SLE patients managed at Cairo, Alexandria, and Helwan universities from August 2014 to 2018: of whom 49 (8.5%), 420 (73%), and 106 (18.4%) were elderly- (> 50 years), adult- (17–50 years), and juvenile- (≤ 16 years) onset patients, respectively. Cumulative characteristics were recorded. Disease activity at the last visit was investigated through the Systemic Lupus Erythematosus Disease Activity Index-2K (SLEDAI-2K), whereby lupus low disease activity (LLDA) was defined as a SLEDAI-2K score ≤ 4. The disease outcome was assessed through investigating disease damage (Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index (SDI)) and the prevalence of mortality. Quantitative and categorical data were compared using Kruskal–Wallis and Mann–Whitney tests, and chi-square (χ2) test, respectively.

Results

Late-onset SLE (LSLE) patients demonstrated the lowest prevalence of constitutional and mucocutaneous manifestations (p < 0.001), serositis (p = 0.006), nephritis (p < 0.001), neuropsychiatric involvement (p < 0.001), and hypocomplementinemia (p < 0.001), but showed the highest prevalence of comorbidities and multimorbidity (comorbidities ≥ 2) (p < 0.001), and positive anti-ds DNA antibodies (p < 0.001). Elderly-onset patients demonstrated the lowest SLEDAI-2K and SDI scores, achieved LLDA the most (p < 0.001), and developed any damage (SDI ≥ 1) the least (p < 0.001). The prevalence of mortality was comparable across the three age groups (p = 0.6).

Conclusions

Late-onset SLE patients (8.5%) showed the lowest prevalence of major organ involvement and the highest prevalence of comorbidities, and demonstrated more favorable disease activity and damage indices.

Key Points

• The disease characteristics and outcome among LSLE patients are characterized by being controversial, with studies from the Middle East being limited. Our cohort constituted of 8.5% elderly-onset SLE patients—who were characterized by the lowest prevalence of major organ involvement and the lowest activity and damage indices—making the disease pattern more favorable in this age group, despite being characterized by the highest prevalence of comorbidities.

Keywords

Characteristics Disease outcome Elderly onset Juvenile Late onset Systemic lupus erythematosus 

Notes

Compliance with ethical standards

The study was approved by the local Ethics Committee, according to the provisions of the World Medical Association Declaration of Helsinki.

Disclosures

None.

References

  1. 1.
    Lahita RG (1999) The role of sex hormones in systemic lupus erythematosus. Cur Opin Rheumatol 11(5):352–356.  https://doi.org/10.1097/00002281-199909000-00005 CrossRefGoogle Scholar
  2. 2.
    Sousa S, Gonçalves MJ, Inês LS, Eugénio G, Jesus D, Fernandes S, Terroso G, Romao VC, Cerqueira M, Raposo A, Couto M (2016) Clinical features and long-term outcomes of systemic lupus erythematosus: comparative data of childhood, adult and late-onset disease in a national register. Rheumatol Int 36(7):955–960.  https://doi.org/10.1007/s00296-016-3450-2 CrossRefPubMedGoogle Scholar
  3. 3.
    Bertoli AM, Alarcón GS, Calvo-Alén J, Fernández M, Vilá LM, Reveille JD (2006) Systemic lupus erythematosus in a multiethnic US cohort: clinical features, course, and outcome in patients with late-onset disease. Arthritis Rheum 54(5):1580–1587.  https://doi.org/10.1002/art.21765 CrossRefPubMedGoogle Scholar
  4. 4.
    Tomic-Lucic A, Petrovic R, Radak-Perovic M, Milovanovic D, Milovanovic J, Zivanovic S, Pantovic S, Veselinovic M (2013) Late-onset systemic lupus erythematosus: clinical features, course, and prognosis. Clin Rheumatol 32(7):1053–1058.  https://doi.org/10.1007/s10067-013-2238-y CrossRefPubMedGoogle Scholar
  5. 5.
    Rovenský J, Tuchyňová A (2008) Systemic lupus erythematosus in the elderly. Autoimmun Rev 7(3):235–239.  https://doi.org/10.1016/j.autrev.2007.11.014 CrossRefPubMedGoogle Scholar
  6. 6.
    Theis KA, Brady TJ, Helmick CG (2017) No one dies of old age anymore: a coordinated approach to comorbidities and the rheumatic diseases. Arthritis Care Res 69(1):1–4.  https://doi.org/10.1002/acr.23114 CrossRefGoogle Scholar
  7. 7.
    Sayarlioglu M, Cefle A, Kamali S, Gul A, Inanc M, Ocal L, Aral O, Konice M (2005) Characteristics of patients with late onset systemic lupus erythematosus in Turkey. Int J Clin Pract 59(2):183–187.  https://doi.org/10.1111/j.1742-1241.2004.00283.x CrossRefPubMedGoogle Scholar
  8. 8.
    Petri M, Orbai AM, Alarcón GS, Gordon C, Merrill JT, Fortin PR, Bruce IN, Isenberg D, Wallace DJ, Nived O, Sturfelt G (2012) Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 64(8):2677–2686.  https://doi.org/10.1002/art.34473 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    van den Akker M, Buntinx F, Knottnerus JA (1996) Comorbidity or multimorbidity: what’s in a name? A review of literature. Eur J Gen Pract 2(2):65–70.  https://doi.org/10.3109/13814789609162146 CrossRefGoogle Scholar
  10. 10.
    Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, DE Groot PG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannopoulos PG, Krilis SA (2006) International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 4(2):295–306.  https://doi.org/10.1111/j.1538-7836.2006.01753.x CrossRefPubMedGoogle Scholar
  11. 11.
    Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index. J Rheumatol 29(2):288–291PubMedGoogle Scholar
  12. 12.
    Franklyn K, Lau CS, Navarra SV, Louthrenoo W, Lateef A, Hamijoyo L, Wahono CS, Le Chen S, Jin O, Morton S, Hoi A (2016) Definition and initial validation of a lupus low disease activity state (LLDAS). Ann Rheum Dis 75(9):1615–1621.  https://doi.org/10.1136/annrheumdis-2015-207726 CrossRefPubMedGoogle Scholar
  13. 13.
    Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Sanchez-Guerrero J, Urowitz M, Bacon P, Bombardieri S, Hanly J, Jones J (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39(3):363–369CrossRefGoogle Scholar
  14. 14.
    Buttgereit F, Da Silva JA, Boers M, Burmester GR, Cutolo M, Jacobs J, Kirwan J, Köhler L, van Riel PL, Vischer T, Bijlsma JW (2002) Standardized nomenclature for glucocorticoid treatment regimens: current questions and tentative answers in rheumatology. Ann Rheum Dis 61(8):718–722.  https://doi.org/10.1136/ard.61.8.718 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Cervera R, Doria A, Amoura Z, Khamashta M, Schneider M, Guillemin F, Maurel F, Garofano A, Roset M, Perna A, Murray M (2014) Patterns of systemic lupus erythematosus expression in Europe. Autoimmun Rev 13(6):621–629.  https://doi.org/10.1016/j.autrev.2013.11.007 CrossRefPubMedGoogle Scholar
  16. 16.
    Boddaert J, Huong DLT, Amoura Z, Wechsler B, Godeau P, Piette JC (2004) Late-onset systemic lupus erythematosus: a personal series of 47 patients and pooled analysis of 714 cases in the literature. Medicine (Baltimore) 83(6):348–359.  https://doi.org/10.1097/01.md.0000147737.57861.7c CrossRefGoogle Scholar
  17. 17.
    Houman MH, Smiti-Khanfir M, Ben GI, Miled M (2004) Systemic lupus erythematosus in Tunisia: demographic and clinical analysis of 100 patients. Lupus 13(3):204–211.  https://doi.org/10.1191/0961203303lu530xx CrossRefPubMedGoogle Scholar
  18. 18.
    Choi JH, Park DJ, Kang JH, Yim YR, Lee KE, Lee JW, Wen L, Kim TJ, Park YW, Lee JK, Lee SS (2015) Comparison of clinical and serological differences among juvenile-, adult-, and late-onset systemic lupus erythematosus in Korean patients. Lupus 24(12):1342–1349.  https://doi.org/10.1177/0961203315591024 CrossRefPubMedGoogle Scholar
  19. 19.
    das Chagas Medeiros MM, Bezerra MC, Braga FH, da Justa Feijão MM, Gois AR, Rebouças VD, de Carvalho TA, Carvalho LS, Ribeiro ÁM (2016) Clinical and immunological aspects and outcome of a Brazilian cohort of 414 patients with systemic lupus erythematosus (SLE): comparison between childhood-onset, adult-onset, and late-onset SLE. Lupus 25(4):355–363.  https://doi.org/10.1177/0961203315606983 CrossRefPubMedGoogle Scholar
  20. 20.
    Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, DomÉnech I, Aydintug AO, Jedryka-Góral AN, The European Working Party on Systemic Lupus Erythematosus (1993) Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1,000 patients. Medicine (Baltimore) 72(2):113–124CrossRefGoogle Scholar
  21. 21.
    Catoggio LJ, Soriano ER, Imamura PM, Wojdyla D, Jacobelli S, Massardo L, Chacón Díaz R, Guibert-Toledano M, Alvarellos A, Saurit V, Manni JA (2015) Late-onset systemic lupus erythematosus in Latin Americans: a distinct subgroup? Lupus 24(8):788–795.  https://doi.org/10.1177/0961203314563134 CrossRefPubMedGoogle Scholar
  22. 22.
    Cartella S, Cavazzana I, Ceribelli A, Inverardi F, Tincani A, Franceschini F (2013) Evaluation of mortality, disease activity, treatment, clinical and immunological features of adult and late onset systemic lupus erythematosus. Autoimmunity 46(6):363–368.  https://doi.org/10.3109/08916934.2013.794793 CrossRefPubMedGoogle Scholar
  23. 23.
    Stefanidou S, Gerodimos C, Benos A, Galanopoulou V, Chatziyannis I, Kanakoudi F, Aslanidis S, Boura P, Sfetsios T, Settas L, Katsounaros M (2013) Clinical expression and course in patients with late onset systemic lupus erythematosus. Hippokratia 17(2):153–156PubMedPubMedCentralGoogle Scholar
  24. 24.
    Al Arfaj AS, Khalil N (2009) Clinical and immunological manifestations in 624 SLE patients in Saudi Arabia. Lupus 18(5):465–473.  https://doi.org/10.1177/0961203308100660 CrossRefPubMedGoogle Scholar
  25. 25.
    Formiga F, Moga I, Pac M, Mitjavila F, Rivera A, Pujol R (1999) Mild presentation of systemic lupus erythematosus in elderly patients assessed by SLEDAI. Lupus 8(6):462–465.  https://doi.org/10.1177/096120339900800609 CrossRefPubMedGoogle Scholar
  26. 26.
    Padovan M, Govoni M, Castellino G, Rizzo N, Fotinidi M, Trotta F (2007) Late onset systemic lupus erythematosus: no substantial differences using different cut-off ages. Lupus 24(8):788–795.  https://doi.org/10.1007/s00296-006-0284-3 CrossRefGoogle Scholar
  27. 27.
    Sassi RH, Hendler JV, Piccoli GF, Gasparin AA, da Silva Chakr RM, Brenol JC, Monticielo OA (2017) Age of onset influences on clinical and laboratory profile of patients with systemic lupus erythematosus. Clin Rheumatol 36(1):89–95.  https://doi.org/10.1007/s10067-016-3478-4 CrossRefPubMedGoogle Scholar
  28. 28.
    Maddison PJ (1987) Systemic lupus erythematosus in the elderly. J Rheumatol 14:182–187Google Scholar
  29. 29.
    Lewis MJ, Jawad AS (2016) The effect of ethnicity and genetic ancestry on the epidemiology, clinical features and outcome of systemic lupus erythematosus. Rheumatology 56:i67–i77.  https://doi.org/10.1093/rheumatology/kew399 CrossRefGoogle Scholar
  30. 30.
    Sohn IW, Joo YB, Won S, Bae SC (2018) Late-onset systemic lupus erythematosus: is it “mild lupus”? Lupus 27(2):235–242.  https://doi.org/10.1177/0961203317716789 CrossRefPubMedGoogle Scholar
  31. 31.
    Feng X, Zou Y, Pan W, Wang X, Wu M, Zhang M, Tao J, Zhang Y, Tan K, Li J, Chen Z (2014) Associations of clinical features and prognosis with age at disease onset in patients with systemic lupus erythematosus. Lupus 23(3):327–334.  https://doi.org/10.1177/0961203313513508 CrossRefPubMedGoogle Scholar
  32. 32.
    Lalani S, Pope J, De Leon F, Peschken C (2010) Clinical features and prognosis of late-onset systemic lupus erythematosus: results from the 1000 faces of lupus study. J Rheumatol 37(1):38–44.  https://doi.org/10.3899/jrheum.080957 CrossRefPubMedGoogle Scholar
  33. 33.
    Prasad R, Ibanez D, Gladman D, Urowitz M (2006) Anti-dsDNA and anti-Sm antibodies do not predict damage in systemic lupus erythematosus. Lupus 15(5):285–291.  https://doi.org/10.1191/0961203306lu2302oa CrossRefPubMedGoogle Scholar
  34. 34.
    Al Sawah S, Zhang X, Zhu B, Magder LS, Foster SA, Iikuni N, Petri M (2015) Effect of corticosteroid use by dose on the risk of developing organ damage over time in systemic lupus erythematosus—the Hopkins lupus cohort. Lupus Sci Med 2(1):e000066.  https://doi.org/10.1136/lupus-2014-000066 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Nossent J, Kiss E, Rozman B, Pokorny G, Vlachoyiannopoulos P, Olesinska M, Marchesoni A, Mosca M, Påi S, Manger K, Schneider M (2010) Disease activity and damage accrual during the early disease course in a multinational inception cohort of patients with systemic lupus erythematosus. Lupus 19(8):949–956.  https://doi.org/10.1177/0961203310366572 CrossRefPubMedGoogle Scholar
  36. 36.
    Somers EC, Richardson BC (2014) Environmental exposures, epigenetic changes and the risk of lupus. Lupus 23(6):568–576.  https://doi.org/10.1177/0961203313499419 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2019

Authors and Affiliations

  • Basma M Medhat
    • 1
    Email author
  • Mervat Essam Behiry
    • 2
  • Nesreen Sobhy
    • 1
  • Yomna Farag
    • 3
  • Huda Marzouk
    • 3
  • Noha Mostafa
    • 3
  • Iman Khalifa
    • 4
  • Marwa Elkhalifa
    • 5
  • Basma M. Eissa
    • 1
  • Eman Hassan ElSayed Hassan
    • 5
  1. 1.Rheumatology and Rehabilitation Department, Faculty of MedicineCairo UniversityCairoEgypt
  2. 2.Internal Medicine Department, Faculty of MedicineCairo UniversityCairoEgypt
  3. 3.Pediatric Rheumatology Department, Faculty of MedicineCairo UniversityCairoEgypt
  4. 4.Pediatric Department, Faculty of MedicineHelwan UniversityHelwanEgypt
  5. 5.Rheumatology Unit, Internal Medicine Department, Faculty of MedicineAlexandria UniversityAlexandriaEgypt

Personalised recommendations