Systemic lupus erythematosus among male patients in Malaysia: how are we different from other geographical regions?

Abstract

Background

Systemic lupus erythematosus (SLE) is an autoimmune disease which predominantly affects females. The disease characteristics in male SLE patients are reported to be distinct and may vary across ethnicities and geographical regions.

Objective

To determine and compare the clinical phenotype and organ damage between male and female patients with SLE in Malaysia.

Methodology

This was a cross-sectional study involving SLE patients from Universiti Kebangsaan Malaysia Medical Centre from June 2016 until June 2017. Information on their socio-demographics and disease characteristics were obtained from the clinical records. Disease damage was assessed using the Systemic Lupus International Collaborating Clinics/American College of Rheumatology (SLICC/ACR) damage index (SDI) scores. The disease characteristics, autoantibody profiles and organ damage were compared between male and female patients, and multivariable analysis using male sex as dependent variable was then performed.

Results

A total of 418 patients were recruited and a total of 59 (14.1%) patients were male. Male patients presented with lower SLE ACR criteria at initial presentation but a significantly higher number of them had renal involvement (lupus nephritis) (78.0% versus 63.8%, p = 0.04). Male patients had less musculoskeletal involvement (45.8% versus 63.0%, p = 0.02) and tended to have lesser mucocutaneous involvement. Immunologic profile revealed that a lower number of male patients had positive anti-Ro antibody (22.7% versus 44.7%, p = 0.04) and they tended to have positive lupus anticoagulant antibody (27.6% versus 14.3%, p = 0.06). Presence of organ damage (SDI score ≥ 1) was significantly higher among males (55.9% versus 39.6%, p = 0.02) with higher renal damage (25.4% versus 9.2%, p = 0.004) and cardiovascular event of ischaemic heart disease or stroke (20.3% versus 7.0%, p = 0.004). They were also inclined to develop damage much earlier as compared to female patients, 3 (interquartile range (IQR) 7.5) versus 5 (IQR 7) years, p = 0.08. The occurrence of disease damage was independently associated with male gender with odds ratio of 1.9 (95% confidence interval 1.1–3.5), p = 0.02.

Conclusion

Male patients with SLE have more severe disease with renal damage and cardiovascular event.

Keywords

Cardiovascular damage male systemic lupus erythematosus

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References

Ferretti

La Cava

Overview of the pathogenesis of systemic lupus erythematosus. In: Tsokos

(eds). Systemic lupus erythematosus: basic, applied and clinical aspects, London, UK: Elsevier, 2016, pp. 55–62. .

Hahn

. Harrison's principles of internal medicine, New York: McGraw-Hill Medical, 2008. .

Wallace

Hahn

. Dubois' lupus erythematosus, 6th ed. Philadelphia: Lippincott Williams & Wilkins, 2002. .

Murphy

Isenberg

. Effect of gender on clinical presentation in systemic lupus erythematosus. Rheumatology (Oxford) 2013; 52: 2108–2115.

Tan

Fang

Magder

Petri

. Differences between male and female systemic lupus erythematosus in a multiethnic population. J Rheumatol 2012; 39: 759–769.

Mok

Lau

Chan

Wong

. Clinical characteristics and outcome of southern Chinese males with systemic lupus erythematosus. Lupus 1999; 8: 188–196.

Voulgari

Katsimbri

Alamanos

Drosos

. Gender and age differences in systemic lupus erythematosus. A study of 489 Greek patients with a review of the literature. Lupus 2002; 11: 722–729.

Mongkoltanatus

Wangkaew

Kasitanon

Louthrenoo

. Clinical features of Thai male lupus: an age-matched controlled study. Rheumatol Int 2008; 28: 339–344.

Ding

Guo

, et al. Gender differences are associated with the clinical features of systemic lupus erythematosus. Chin Med J (Engl) 2012; 125: 2477–2481.

10.

Garcia

Marcos

, et al. Male systemic lupus erythematosus in a Latin-American inception cohort of 1214 patients. Lupus 2005; 14: 938–946.

11.

Miller

Urowitz

Gladman

Killinger

. Systemic lupus erythematosus in males. Medicine (Baltimore) 1983; 62: 327–334.

12.

Stefanidou

Benos

Galanopoulou

, et al. Clinical expression and morbidity of systemic lupus erythematosus during a post-diagnostic 5-year follow-up: a male:female comparison. Lupus 2011; 20: 1090–1094.

13.

Font

Cervera

Navarro

, et al. Systemic lupus erythematosus in men: clinical and immunological characteristics. Ann Rheum Dis 1992; 51: 1050–1052.

14.

Koh

Fong

Boey

Feng

. Systemic lupus erythematosus in 61 Oriental males. A study of clinical and laboratory manifestations. Br J Rheumatol 1994; 33: 339–342.

15.

Lahita

Chiorazzi

Gibofsky

Winchester

Kunkel

. Familial systemic lupus erythematosus in males. Arthritis Rheum 1983; 26: 39–44.

16.

Mok

. Do Asian patients have worse lupus?. Lupus 2010; 19: 1384–1390.

17.

Thumboo

Wee

H-L

. Systemic lupus erythematosus in Asia: is it more common and more severe?. APLAR J Rheumatol 2006; 9: 320–326.

18.

Hochberg

. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40: 1725.

19.

Tan

Cohen

Fries

, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982; 25: 1271–1277.

20.

Gladman

Ginzler

Goldsmith

, et al. The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 1996; 39: 363–369.

21.

Lau

Mak

. The socioeconomic burden of SLE. Nat Rev Rheumatol 2009; 5: 400–404.

22.

Manuel

Ugarte-Gil

GJP-E

Alarcón

Epidemiology. In: Tsokos

(eds). Systemic lupus erythematosus: basic, applied and clinical aspects, London, UK: Elsevier, 2016. .

23.

Dubois

Tuffanelli

. Clinical manifestations of systemic lupus erythematosus. Computer analysis of 520 cases. JAMA 1964; 190: 104–111.

24.

Andrade

Alarcon

Fernandez

, et al. Accelerated damage accrual among men with systemic lupus erythematosus: XLIV. Results from a multiethnic US cohort. Arthritis Rheum 2007; 56: 622–630.

25.

Jacobsen

Petersen

Ullman

, et al. A multicentre study of 513 Danish patients with systemic lupus erythematosus. I. Disease manifestations and analyses of clinical subsets. Clin Rheumatol 1998; 17: 468–477.

26.

Hwang

Lee

Ahn

, et al. Clinical characteristics of male and female Korean patients with systemic lupus erythematosus: a comparative study. Korean J Intern Med 2015; 30: 242–249.

27.

Lopez

Mozo

Gutierrez

Suarez

. Epidemiology of systemic lupus erythematosus in a northern Spanish population: gender and age influence on immunological features. Lupus 2003; 12: 860–865.

28.

Cooper

Parks

Treadwell

, et al. Differences by race, sex and age in the clinical and immunologic features of recently diagnosed systemic lupus erythematosus patients in the southeastern United States. Lupus 2002; 11: 161–167.

29.

Prete

Majlessi

Gilman

Hamideh

. Systemic lupus erythematosus in men: a retrospective analysis in a Veterans Administration Healthcare System population. J Clin Rheumatol 2001; 7: 142–1450.

30.

Renau

Isenberg

. Male versus female lupus: a comparison of ethnicity, clinical features, serology and outcome over a 30 year period. Lupus 2012; 21: 1041–1048.

31.

Molina

Drenkard

Molina

, et al. Systemic lupus erythematosus in males. A study of 107 Latin American patients. Medicine (Baltimore) 1996; 75: 124–130.

32.

de Carvalho

do Nascimento

Testagrossa

Barros

Bonfa

. Male gender results in more severe lupus nephritis. Rheumatol Int 2010; 30: 1311–1315.

33.

Kotokey

Rajkhowa

Chaliha

Pegu

. A study of cardiovascular manifestations in systematic lupus erythematosus in Upper Assam. J Indian Coll Cardiol 2012; 2: 29–32.

34.

Hari

Bagga

Mahajan

Dinda

. Outcome of lupus nephritis in Indian children. Lupus 2009; 18: 348–354.

35.

Vijay

Parveen

. Clinical and immunological profile of systemic lupus erythematosus in a pediatric population in North India. Egypt Rheumatol Rehabil 2014; 41: 148–151. .

36.

Kumar

Malaviya

Singh

, et al. Survival in patients with systemic lupus erythematosus in India. Rheumatol Int 1992; 12: 107–109.

37.

Wang

Tan

Manivasagar

. Systemic lupus erythematosus in Malaysia: a study of 539 patients and comparison of prevalence and disease expression in different racial and gender groups. Lupus 1997; 6: 248–253.

38.

Cervera R, Doria A, Amoura Z, Khamashta M, Schneider M, Guillemin F, et al. Patterns of systemic lupus erythematosus expression in Europe. Autoimmun Rev 2014; 13: 621–629.

39.

Keskin G, Tokgoz G, DUzgun N, Duman M, Kinikli G, Olmez U, et al. Systemic lupus erythematosus in Turkish men. Clin Exp Rheumatol 2000; 18: 114–115.

40.

Ward MM, Studenski S. Clinical manifestations of systemic lupus erythematosus. Identification of racial and socioeconomic influences 2010; 150: 849–853.