The global burden of SLE: Prevalence, health disparities and socioeconomic impact

Nature Reviews Rheumatology

Volumn 12, Issue 10, 2016, Pages 605-620

  Carter, Erin E ^a   Barr, Susan G ^a   Clarke, Ann E ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COGNITIVE DEFECT; DISEASE COURSE; DISEASE SEVERITY; ECONOMIC ASPECT; EDUCATION; ENVIRONMENTAL FACTOR; ETHNICITY; GEOGRAPHIC DISTRIBUTION; HEALTH CARE COST; HEALTH CARE SYSTEM; HEALTH DISPARITY; HEALTH INSURANCE; HUMAN; INCIDENCE; INCOME; MEDICATION COMPLIANCE; OCCUPATION; PATHOGENESIS; PHYSICAL DISABILITY; PREVALENCE; PRIORITY JOURNAL; PRODUCTIVITY; QUALITY OF LIFE; REVIEW; SOCIAL STATUS; SOCIAL SUPPORT; SOCIOECONOMICS; SYSTEMIC LUPUS ERYTHEMATOSUS; COST OF ILLNESS; ECONOMICS; GLOBAL HEALTH; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; RISK FACTOR; SEVERITY OF ILLNESS INDEX;

COST OF ILLNESS; GLOBAL HEALTH; HUMANS; INCIDENCE; LUPUS ERYTHEMATOSUS, SYSTEMIC; PREVALENCE; QUALITY OF LIFE; RISK FACTORS; SEVERITY OF ILLNESS INDEX;

EID: 84983391698     PISSN: 17594790     EISSN: 17594804     Source Type: Journal    
DOI: 10.1038/nrrheum.2016.137     Document Type: Review

References (203)

1. Tsokos, G. C. Systemic lupus erythematosus. N. Engl. J. Med. 365, 2110-2121 (2011).
2. de Jesus, G. R., et al. Understanding and managing pregnancy in patients with lupus. Autoimmune Dis. 2015, http://dx.doi.org/10.1155/2015/943490 (2015).
3. Bernatsky, S., et al. Cancer risk in systemic lupus: an updated international multi-centre cohort study. J. Autoimmun. 42, 130-135 (2013).
4. Manzi, S., et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham study. Am. J. Epidemiol. 145, 408-415 (1997).
5. Aytan, J., & Bukhari, M. A. Use of biologics in SLE: a review of the evidence from a clinical perspective. Rheumatology (Oxford) 55, 775-779 (2016).
6. Uramoto, K. M., et al. Trends in the incidence and mortality of systemic lupus erythematosus, 1950-1992. Arthritis Rheum. 42, 46-50 (1999).
7. Borchers, A. T., Naguwa, S. M., Shoenfeld, Y., & Gershwin, M. E. The geoepidemiology of systemic lupus erythematosus. Autoimmun. Rev. 9, A277-A287 (2010).
8. Laustrup, H., Voss, A., Green, A., & Junker, P. Occurrence of systemic lupus erythematosus in a Danish community: an 8 year prospective study. Scand. J. Rheumatol. 38, 128-132 (2009).
9. Lerang, K., Gilboe, I., Garen, T., Thelle, D. S., & Gran, J. T. High incidence and prevalence of systemic lupus erythematosus in Norway. Lupus 21, 1362-1369 (2012).
10. Nossent, H. C. Systemic lupus erythematosus in the Arctic region of Norway. J. Rheumatol. 28, 539-546 (2001).
11. Alamanos, Y., et al. Epidemiology of systemic lupus erythematosus in northwest Greece 1982-2001. J. Rheumatol. 30, 731-735 (2003).
12. Hopkinson, N. D., Doherty, M., & Powell, R. J. The prevalence and incidence of systemic lupus erythematosus in Nottingham, UK, 1989-1990. Br. J. Rheumatol. 32, 110-115 (1993).
13. Nightingale, A. L., Farmer, R. D., & de Vries, C. S. Incidence of clinically diagnosed systemic lupus erythematosus 1992-1998 using the UK general practice research database. Pharmacoepidemiol. Drug Saf. 15, 656-661 (2006).
14. Rees, F., et al. The incidence and prevalence of systemic lupus erythematosus in the UK, 1999-2012. Ann. Rheum. Dis. 75, 136-141 (2016).
15. Nasonov, E., et al. The prevalence and incidence of systemic lupus erythematosus (SLE) in selected cities from three Commonwealth of Independent States countries (the Russian Federation, Ukraine and Kazakhstan). Lupus 23, 213-219 (2014).
16. Malaviya, A. N., Singh, R. R., Singh, Y. N., Kapoor, S. K., & Kumar, A. Prevalence of systemic lupus erythematosus in India. Lupus 2, 115-118 (1993).
17. Chiu, Y. M., & Lai, C. H. Nationwide population-based epidemiologic study of systemic lupus erythematosus in Taiwan. Lupus 19, 1250-1255 (2010).
18. Yeh, K. W., Yu, C. H., Chan, P. C., Horng, J. T., & Huang, J. L. Burden of systemic lupus erythematosus in Taiwan: a population-based survey. Rheumatol. Int. 33, 1805-1811 (2013).
19. Yu, K. H., See, L. C., Kuo, C. F., Chou, I. J., & Chou, M. J. Prevalence and incidence in patients with autoimmune rheumatic diseases: a nationwide population-based study in Taiwan. Arthritis Care Res. (Hoboken) 65, 244-250 (2013).
20. See, L. C., Kuo, C. F., Chou, I. J., Chiou, M. J., & Yu, K. H. Sex-And age-specific incidence of autoimmune rheumatic diseases in the Chinese population: a Taiwan population-based study. Semin. Arthritis Rheum. 43, 381-386 (2013).
21. Arnaud, L., et al. Prevalence and incidence of systemic lupus erythematosus in France: a 2010 nation-wide population-based study. Autoimmun. Rev. 13, 1082-1089 (2014).
22. Shim, J. S., Sung, Y. K., Joo, Y. B., Lee, H. S., & Bae, S. C. Prevalence and incidence of systemic lupus erythematosus in South Korea. Rheumatol. Int. 34, 909-917 (2014).
23. Ju, J. H., et al. Prevalence of systemic lupus erythematosus in South Korea: an administrative database study. J. Epidemiol. 24, 295-303 (2014).
24. Somers, E. C., et al. Population-based incidence and prevalence of systemic lupus erythematosus: the Michigan lupus epidemiology and surveillance program. Arthritis Rheumatol. 66, 369-378 (2014).
25. Lim, S. S., et al. The incidence and prevalence of systemic lupus erythematosus, 2002-2004: the Georgia Lupus Registry. Arthritis Rheumatol. 66, 357-368 (2014).
26. Gourley, I. S., Patterson, C. C., & Bell, A. L. The prevalence of systemic lupus erythematosus in Northern Ireland. Lupus 6, 399-403 (1997).
27. Farooqi, A., & Gibson, T. Prevalence of the major rheumatic disorders in the adult population of north Pakistan. Br. J. Rheumatol. 37, 491-495 (1998).
28. Moghimi, N., et al. WHO-ILAR COPCORD study (stage 1, urban study) in Sanandaj, Iran. Clin. Rheumatol. 34, 535-543 (2015).
29. Sandoughi, M., et al. Prevalence of musculoskeletal disorders in southeastern Iran: a WHO-ILAR COPCORD study (stage 1, urban study). Int. J. Rheum. Dis. 16, 509-517 (2013).
30. Davatchi, F., et al. Effect of ethnic origin (Caucasians versus Turks) on the prevalence of rheumatic diseases: a WHO-ILAR COPCORD urban study in Iran. Clin. Rheumatol. 28, 1275-1282 (2009).
31. Senna, E. R., et al. Prevalence of rheumatic diseases in Brazil: a study using the COPCORD approach. J. Rheumatol. 31, 594-597 (2004).
32. Granados, Y., et al. Prevalence of musculoskeletal disorders and rheumatic diseases in an urban community in Monagas State, Venezuela: a COPCORD study. Clin. Rheumatol. 34, 871-877 (2015).
33. Pelaez-Ballestas, I., et al. Epidemiology of the rheumatic diseases in Mexico. A study of 5 regions based on the COPCORD methodology. J. Rheumatol. Suppl. 86, 3-8 (2011).
34. Reyes-Llerena, G. A., et al. Community-based study to estimate prevalence and burden of illness of rheumatic diseases in Cuba: a COPCORD study. J. Clin. Rheumatol. 15, 51-55 (2009).
35. Wang, F., Wang, C. L., Tan, C. T., & Manivasagar, M. Systemic lupus erythematosus in Malaysia: a study of 539 patients and comparison of prevalence and disease expression in different racial and gender groups. Lupus 6, 248-253 (1997).
36. Al Rawi, Z., Al Shaarbaf, H., Al Raheem, E., & Khalifa, S. J. Clinical features of early cases of systemic lupus erythematosus in Iraqui patients. Br. J. Rheumatol. 22, 165-171 (1983).
37. Bossingham, D. Systemic lupus erythematosus in the far north of Queensland. Lupus 12, 327-331 (2003).
38. Shand, A. W., Algert, C. S., March, L., & Roberts, C. L. Second pregnancy outcomes for women with systemic lupus erythematosus. Ann. Rheum. Dis. 72, 547-551 (2013).
39. Segasothy, M., & Phillips, P. A. Systemic lupus erythematosus in Aborigines and Caucasians in central Australia: A comparative study. Lupus 10, 439-444 (2001).
40. Molokhia, M., McKeigue, P. M., Cuadrado, M., & Hughes, G. Systemic lupus erythematosus in migrants from west Africa compared with Afro-Caribbean people in the UK. Lancet 357, 1414-1415 (2001).
41. Alonso, M. D., et al. Systemic lupus erythematosus in northwestern Spain: a 20 year epidemiologic study. Medicine (Baltimore) 90, 350-358 (2011).
42. Lopez, P., Mozo, L., Gutierrez, C., & Suarez, A. Epidemiology of systemic lupus erythematosus in a northern spanish population: gender and age influence on immunological features. Lupus 12, 860-865 (2003).
43. Govoni, M., Castellino, G., Bosi, S., Napoli, N., & Trotta, F. Incidence and prevalence of systemic lupus erythematosus in a district of north Italy. Lupus 15, 110-113 (2006).
44. Nived, O., Sturfelt, G., & Wollheim, F. Systemic lupus erythematosus in an adult population in southern Sweden: incidence, prevalence and validity of ARA revised classification criteria. Br. J. Rheumatol. 24, 147-154 (1985).
45. Fessel, W. J. Systemic lupus erythematosus in the community. incidence, prevalence, outcome, and first symptoms; the high prevalence in black women. Arch. Intern. Med. 134, 1027-1035 (1974).
46. Hochberg, M. C., et al. Prevalence of self-reported physician-diagnosed systemic lupus erythematosus in the USA. Lupus 4, 454-456 (1995).
47. Phan, J. C., Bush, T. M., Donald, F., & Ward, M. Clinical and laboratory features of patients of Vietnamese descent with systemic lupus erythematosus. Lupus 8, 521-524 (1999).
48. Barnabe, C., et al. Prevalence of systemic lupus erythematosus and systemic sclerosis in the First Nations population of Alberta, Canada. Arthritis Care Res. (Hoboken) 64, 138-143 (2012).
49. Bernatsky, S., et al. A population-based assessment of systemic lupus erythematosus incidence and prevalence-results and implications of using administrative data for epidemiological studies. Rheumatology (Oxford) 46, 1814-1818 (2007).
50. Gudmundsson, S., & Steinsson, K. Systemic lupus erythematosus in Iceland 1975 through 1984. A nationwide epidemiological study in an unselected population. J. Rheumatol. 17, 1162-1167 (1990).
51. Nossent, J. C. Systemic lupus erythematosus on the Caribbean island of Curaçao: an epidemiological investigation. Ann. Rheum. Dis. 51, 1197-1201 (1992).
52. Zou, Y. F., et al. Prevalence of systemic lupus erythematosus and risk factors in rural areas of Anhui province. Rheumatol. Int. 34, 347-356 (2014).
53. Cakir, N., et al. The prevalences of some rheumatic diseases in western Turkey: Havsa study. Rheumatol. Int. 32, 895-908 (2012).
54. Anagnostopoulos, I., et al. The prevalence of rheumatic diseases in central Greece: a population survey. BMC Musculoskelet. Disord. 11, http://dx. doi.org/10.1186/1471-2474-11-98 (2010).
55. Mok, C. C., To, C. H., Ho, L. Y., & Yu, K. L. Incidence and mortality of systemic lupus erythematosus in a southern Chinese population, 2000-2006. J. Rheumatol. 35, 1978-1982 (2008).
56. Iseki, K., et al. An epidemiologic analysis of end-stage lupus nephritis. Am. J. Kidney Dis. 23, 547-554 (1994).
57. Stahl-Hallengren, C., Jonsen, A., Nived, O., & Sturfelt, G. Incidence studies of systemic lupus erythematosus in southern Sweden: increasing age, decreasing frequency of renal manifestations and good prognosis. J. Rheumatol. 27, 685-691 (2000).
58. Ferucci, E. D., et al. Prevalence and incidence of systemic lupus erythematosus in a population-based registry of American Indian and Alaska Native people, 2007-2009. Arthritis Rheumatol. 66, 2494-2502 (2014).
59. Feldman, C. H., et al. Epidemiology and sociodemographics of systemic lupus erythematosus and lupus nephritis among US adults with medicaid coverage, 2000-2004. Arthritis Rheum. 65, 753-763 (2013).
60. Scolnik, M., et al. Incidence and prevalence of lupus in Buenos Aires, Argentina: an 11 year health management organisation-based study. Lupus Sci. Med. 1, http://dx.doi.org/10.1136/lupus-2014-000021 (2014).
61. Naleway, A. L., Davis, M. E., Greenlee, R. T., Wilson, D. A., & McCarty, D. J. Epidemiology of systemic lupus erythematosus in rural Wisconsin. Lupus 14, 862-866 (2005).
62. Sardu, C., et al. Population based study of 12 autoimmune diseases in Sardinia, Italy: prevalence and comorbidity. PLoS ONE 7, http://dx.doi. org/10.1371/journal.pone.0032487 (2012).
63. Balluz, L., et al. Investigation of systemic lupus erythematosus in Nogales, Arizona. Am. J. Epidemiol. 154, 1029-1036 (2001).
64. Vilar, M. J., & Sato, E. I. Estimating the incidence of systemic lupus erythematosus in a tropical region (Natal, Brazil). Lupus 11, 528-532 (2002).
65. Garris, C., Shah, M., & Farrelly, E. The prevalence and burden of systemic lupus erythematosus in a Medicare population: retrospective analysis of Medicare claims. Cost Eff. Resour. Alloc. 13, http://dx.doi.org/10.1186/s12962-015-0034-z (2015).
66. McMurray, R. W., & May, W. Sex hormones and systemic lupus erythematosus: review and meta-Analysis. Arthritis Rheum. 48, 2100-2110 (2003).
67. Patel, M., Clarke, A. M., Bruce, I. N., & Symmons, D. P. The prevalence and incidence of biopsy-proven lupus nephritis in the UK: evidence of an ethnic gradient. Arthritis Rheum. 54, 2963-2969 (2006).
68. Molokhia, M., & McKeigue, P. Systemic lupus erythematosus: genes versus environment in high risk populations. Lupus 15, 827-832 (2006).
69. Molokhia, M., & McKeigue, P. Risk for rheumatic disease in relation to ethnicity and admixture. Arthritis Res. 2, 115-125 (2000).
70. Pons-Estel, G. J., Alarcon, G. S., Scofield, L., Reinlib, L., & Cooper, G. S. Understanding the epidemiology and progression of systemic lupus erythematosus. Semin. Arthritis Rheum. 39, 257-268 (2010).
71. Vincent, F. B., Bourke, P., Morand, E. F., Mackay, F., & Bossingham, D. Focus on systemic lupus erythematosus in indigenous Australians: towards a better understanding of autoimmune diseases. Intern. Med. J. 43, 227-234 (2013).
72. Alarcon, G. S., et al. Systemic lupus erythematosus in three ethnic groups. IX. Differences in damage accrual. Arthritis Rheum. 44, 2797-2806 (2001).
73. Alarcon, G. S., et al. Systemic lupus erythematosus in three ethnic groups: II. features predictive of disease activity early in its course. LUMINA study group (lupus in minority populations, nature versus nurture). Arthritis Rheum. 41, 1173-1180 (1998).
74. Anderson, E., Nietert, P. J., Kamen, D. L., & Gilkeson, G. S. Ethnic disparities among patients with systemic lupus erythematosus in South Carolina. J. Rheumatol. 35, 819-825 (2008).
75. Gonzalez, L. A., Toloza, S. M., McGwin, G., Jr., & Alarcon, G. S. Ethnicity in systemic lupus erythematosus (SLE): its influence on susceptibility and outcomes. Lupus 22, 1214-1224 (2013).
76. Ong, C., Nicholls, K., & Becker, G. Ethnicity and lupus nephritis: an Australian single centre study. Intern. Med. J. 41, 270-278 (2011).
77. Adelowo, O. O., & Oguntona, S. A. Pattern of systemic lupus erythematosus among Nigerians. Clin. Rheumatol. 28, 699-703 (2009).
78. Atisha-Fregoso, Y., Jakez-Ocampo, J., & Llorente, L. Systemic lupus erythematosus in Hispanics. Autoimmunity. 44, 555-561 (2011).
79. Pons-Estel, B. A., et al. The GLADEL multinational Latin American prospective inception cohort of 1, 214 patients with systemic lupus erythematosus: ethnic and disease heterogeneity among "Hispanics". Medicine (Baltimore) 83, 1-17 (2004).
80. Mok, M. Y., & Li, W. L. Do Asian patients have worse lupus? Lupus 19, 1384-1390 (2010).
81. Kaslow, R. A. High rate of death caused by systemic lupus erythematosus among U. S. residents of Asian descent. Arthritis Rheum. 25, 414-418 (1982).
82. Samanta, A., et al. High prevalence of systemic disease and mortality in Asian subjects with systemic lupus erythematosus. Ann. Rheum. Dis. 50, 490-492 (1991).
83. Nossent, J. C. Course and prognostic value of systemic lupus erythematosus disease activity index in black Caribbean patients. Semin. Arthritis Rheum. 23, 16-21 (1993).
84. Bernatsky, S., et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 54, 2550-2557 (2006).
85. Krishnan, E., & Hubert, H. B. Ethnicity and mortality from systemic lupus erythematosus in the US. Ann. Rheum. Dis. 65, 1500-1505 (2006).
86. Wadee, S., Tikly, M., & Hopley, M. Causes and predictors of death in South Africans with systemic lupus erythematosus. Rheumatology (Oxford) 46, 1487-1491 (2007).
87. Lau, C. S., Yin, G., & Mok, M. Y. Ethnic and geographical differences in systemic lupus erythematosus: An overview. Lupus 15, 715-719 (2006).
88. Gonzalez, L. A., Toloza, S. M., & Alarcon, G. S. Impact of race and ethnicity in the course and outcome of systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 40, 433-454, (2014).
89. Petri, M., Perez-Gutthann, S., Longenecker, J. C., & Hochberg, M. Morbidity of systemic lupus erythematosus: role of race and socioeconomic status. Am. J. Med. 91, 345-353 (1991).
90. Ward, M. M., & Studenski, S. Clinical manifestations of systemic lupus erythematosus. identification of racial and socioeconomic influences. Arch. Intern. Med. 150, 849-853 (1990).
91. Korbet, S. M., Schwartz, M. M., Evans, J. Lewis, E. J., & Collaborative Study Group. Severe lupus nephritis: racial differences in presentation and outcome. J. Am. Soc. Nephrol. 18, 244-254 (2007).
92. Nee, R., et al. Survival disparity of African American versus non-African American patients with ESRD due to SLE. Am. J. Kidney Dis. 66, 630-637 (2015).
93. Burgos, P. I., et al. US patients of Hispanic and African ancestry develop lupus nephritis early in the disease course: data from LUMINA, a multiethnic US cohort (LUMINA LXXIV). Ann. Rheum. Dis. 70, 393-394 (2011).
94. Thumboo, J., et al. A comparative study of the clinical manifestations of systemic lupus erythematosus in Caucasians in Rochester, Minnesota, and Chinese in Singapore, from 1980 to 1992. Arthritis Rheum. 45, 494-500 (2001).
95. Gomez-Puerta, J. A., et al. Racial and ethnic differences in mortality and cardiovascular events among patients with end-stage renal disease due to lupus nephritis. Arthritis Care Res. (Hoboken) 67, 1453-1462 (2015).
96. Heller, T., Ahmed, M., Siddiqqi, A., Wallrauch, C., & Bahlas, S. Systemic lupus erythematosus in Saudi Arabia: morbidity and mortality in a multiethnic population. Lupus 16, 908-914 (2007).
97. Alarcon, G. S., et al. Systemic lupus erythematosus in three ethnic groups: III. A comparison of characteristics early in the natural history of the LUMINA cohort. Lupus in Minority Populations: Nature versus Nurture. Lupus 8, 197-209 (1999).
98. Cooper, G. S., 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 11, 161-167 (2002).
99. Alarcon, G. S., et al. Systemic lupus erythematosus in a multiethnic cohort: LUMINA XXXV. Predictive factors of high disease activity over time. Ann. Rheum. Dis. 65, 1168-1174 (2006).
100. Malaviya, A. N., Chandrasekaran, A. N., Kumar, A., & Shamar, P. N. Systemic lupus erythematosus in India. Lupus 6, 690-700 (1997).
101. Connelly, K., Morand, E. F., & Hoi, A. Y. Asian ethnicity in systemic lupus erythematosus: an Australian perspective. Intern. Med. J. 43, 618-624 (2013).
102. Johnson, S. R., Urowitz, M. B., Ibanez, D., & Gladman, D. D. Ethnic variation in disease patterns and health outcomes in systemic lupus erythematosus. J. Rheumatol. 33, 1990-1995 (2006).
103. Reveille, J. D., et al. Systemic lupus erythematosus in three ethnic groups: I. The effects of HLA class II, C4, and CR1 alleles, socioeconomic factors, and ethnicity at disease onset. LUMINA study group. Lupus in Minority Populations, Nature versus Nurture. Arthritis Rheum. 41, 1161-1172 (1998).
104. Vina, E. R., Masi, C. M., Green, S. L., & Utset, T. O. A study of racial/ethnic differences in treatment preferences among lupus patients. Rheumatology (Oxford) 51, 1697-1706 (2012).
105. Karlson, E. W., et al. The relationship of socioeconomic status, race, and modifiable risk factors to outcomes in patients with systemic lupus erythematosus. Arthritis Rheum. 40, 47-56 (1997).
106. Odutola, J., & Ward, M. M. Ethnic and socioeconomic disparities in health among patients with rheumatic disease. Curr. Opin. Rheumatol. 17, 147-152 (2005).
107. Al Dhanhani, A. M., Gignac, M. A., Su, J., & Fortin, P. R. Work disability in systemic lupus erythematosus. Arthritis Rheum. 61, 378-385 (2009).
108. Baker, K., & Pope, J. Employment and work disability in systemic lupus erythematosus: a systematic review. Rheumatology (Oxford) 48, 281-284 (2009).
109. Baker, K., et al. Work disability in systemic lupus erythematosus is prevalent and associated with socio-demographic and disease related factors. Lupus 18, 1281-1288 (2009).
110. Bertoli, A. M., Fernandez, M., Alarcon, G. S., Vila, L. M., & Reveille, J. D. Systemic lupus erythematosus in a multiethnic US cohort LUMINA (XLI): factors predictive of self-reported work disability. Ann. Rheum. Dis. 66, 12-17 (2007).
111. Campbell, R., Jr., Cooper, G. S., & Gilkeson, G. S. The impact of systemic lupus erythematosus on employment. J. Rheumatol. 36, 2470-2475 (2009).
112. Drenkard, C., et al. Burden of systemic lupus erythematosus on employment and work productivity: data from a large cohort in the southeastern United States. Arthritis Care Res. (Hoboken) 66, 878-887 (2014).
113. Lau, C. S., & Mak, A. The socioeconomic burden of SLE. Nat. Rev. Rheumatol. 5, 400-404 (2009).
114. Walsh, S. J., & Gilchrist, A. Geographical clustering of mortality from systemic lupus erythematosus in the United States: contributions of poverty, Hispanic ethnicity and solar radiation. Lupus 15, 662-670 (2006).
115. Richiardi, L., Bellocco, R., & Zugna, D. Mediation analysis in epidemiology: methods, interpretation and bias. Int. J. Epidemiol. 42, 1511-1519 (2013).
116. Alarcon, G. S. Lessons from LUMINA: a multiethnic US cohort. Lupus 17, 971-976 (2008).
117. Alarcon, G. S., et al. Systemic lupus erythematosus in three ethnic groups. XIV. Poverty, wealth, and their influence on disease activity. Arthritis Rheum. 51, 73-77 (2004).
118. Kasitanon, N., Magder, L. S., & Petri, M. Predictors of survival in systemic lupus erythematosus. Medicine (Baltimore) 85, 147-156 (2006).
119. Fangtham M., & Petri, M. 2013 Update: Hopkins lupus cohort. Curr. Rheumatol. Rep. 15 http://dx.doi. org/10.1007/s11926-013-0360-0 2013).
120. Burling, F., et al. Ethnic, clinical and immunological factors in systemic lupus erythematosus and the development of lupus nephritis: results from a multi-ethnic New Zealand cohort. Lupus 16, 830-837 (2007).
121. Barr, R. G., et al. Prognosis in proliferative lupus nephritis: the role of socio-economic status and race/ethnicity. Nephrol. Dial. Transplant. 18, 2039-2046 (2003).
122. Ward, M. M. Education level and mortality in systemic lupus erythematosus (SLE): evidence of underascertainment of deaths due to SLE in ethnic minorities with low education levels. Arthritis Rheum. 51, 616-624 (2004).
123. Escalante, A., & del Rincon, I. Epidemiology and impact of rheumatic disorders in the United States Hispanic population. Curr. Opin. Rheumatol. 13, 104-110 (2001).
124. Kumar, K., et al. Beliefs about medicines in patients with rheumatoid arthritis and systemic lupus erythematosus: a comparison between patients of South Asian and white British origin. Rheumatology (Oxford) 47, 690-697 (2008).
125. Costenbader, K. H., et al. Cigarette smoking and the risk of systemic lupus erythematosus: a meta-Analysis. Arthritis Rheum. 50, 849-857 (2004).
126. Jiang, F., Li, S., & Jia, C. Smoking and the risk of systemic lupus erythematosus: an updated systematic review and cumulative meta-Analysis. Clin. Rheumatol. 34, 1885-1892 (2015).
127. Hardy, C. J., Palmer, B. P., Muir, K. R., Sutton, A. J., & Powell, R. J. Smoking history, alcohol consumption, and systemic lupus erythematosus: a case-control study. Ann. Rheum. Dis. 57, 451-455 (1998).
128. Takvorian, S. U., Merola, J. F., & Costenbader, K. H. Cigarette smoking, alcohol consumption and risk of systemic lupus erythematosus. Lupus 23, 537-544 (2014).
129. Rubin, R. L., et al. Effect of cigarette smoke on autoimmunity in murine and human systemic lupus erythematosus. Toxicol. Sci. 87, 86-96 (2005).
130. Ghaussy, N. O., Sibbitt, W. Jr., Bankhurst, A. D., & Qualls, C. R. Cigarette smoking and disease activity in systemic lupus erythematosus. J. Rheumatol. 30, 1215-1221 (2003).
131. Ward, M. M., & Studenski, S. Clinical prognostic factors in lupus nephritis. The importance of hypertension and smoking. Arch. Intern. Med. 152, 2082-2088 (1992).
132. Wang, J., Pan, H. F., Ye, D. Q., Su, H., & Li, X. P. Moderate alcohol drinking might be protective for systemic lupus erythematosus: a systematic review and meta-Analysis. Clin. Rheumatol. 27, 1557-1563 (2008).
133. Bengtsson, A. A., Rylander, L., Hagmar, L., Nived, O., & Sturfelt, G. Risk factors for developing systemic lupus erythematosus: a case-control study in southern Sweden. Rheumatology (Oxford) 41, 563-571 (2002).
134. Wang, J., Kay, A. B., Fletcher, J., Formica, M. K., & McAlindon, T. E. Alcohol consumption is not protective for systemic lupus erythematosus. Ann. Rheum. Dis. 68, 345-348 (2009).
135. Formica, M. K., Palmer, J. R., Rosenberg, L., & McAlindon, T. E. Smoking, alcohol consumption, and risk of systemic lupus erythematosus in the Black Women?s Health study. J. Rheumatol. 30, 1222-1226 (2003).
136. Farhat, S. C., et al. Air pollution in autoimmune rheumatic diseases: a review. Autoimmun Rev. 11, 14-21 (2011).
137. Cooper, G. S., et al. Occupational and environmental exposures and risk of systemic lupus erythematosus: silica, sunlight, solvents. Rheumatology (Oxford) 49, 2172-2180 (2010).
138. Cooper, G. S., Miller, F. W., & Germolec, D. R. Occupational exposures and autoimmune diseases. Int. Immunopharmacol. 2, 303-313 (2002).
139. Parks, C. G., & Cooper, G. S. Occupational exposures and risk of systemic lupus erythematosus: a review of the evidence and exposure assessment methods in population-And clinic-based studies. Lupus 15, 728-736 (2006).
140. Parks, C. G., et al. Occupational exposure to crystalline silica and risk of systemic lupus erythematosus: a population-based, case-control study in the southeastern United States. Arthritis Rheum. 46, 1840-1850 (2002).
141. Conrad, K., Mehlhorn, J., Luthke, K., Dorner, T., & Frank, K. H. Systemic lupus erythematosus after heavy exposure to quartz dust in uranium mines: clinical and serological characteristics. Lupus 5, 62-69 (1996).
142. Sanchez-Roman, J., Wichmann, I., Salaberri, J., Varela, J. M., & Nunez-Roldan, A. Multiple clinical and biological autoimmune manifestations in 50 workers after occupational exposure to silica. Ann. Rheum. Dis. 52, 534-538 (1993).
143. Finckh, A., et al. Occupational silica and solvent exposures and risk of systemic lupus erythematosus in urban women. Arthritis Rheum. 54, 3648-3654 (2006).
144. Dahlgren, J., et al. Cluster of systemic lupus erythematosus (SLE) associated with an oil field waste site: a cross sectional study. Environ. Health 6, http://dx.doi.org/10.1186/1476-069X-6-8 (2007).
145. Bernatsky, S., et al. Associations between ambient fine particulate levels and disease activity in patients with systemic lupus erythematosus (SLE). Environ. Health Perspect. 119, 45-49 (2011).
146. Parks, C. G., & De Roos, A. J. Pesticides, chemical and industrial exposures in relation to systemic lupus erythematosus. Lupus 23, 527-536 (2014).
147. Cooper, G. S., et al. Occupational risk factors for the development of systemic lupus erythematosus. J. Rheumatol. 31, 1928-1933 (2004).
148. Kilburn, K. H., & Warshaw, R. H. Prevalence of symptoms of systemic lupus erythematosus (SLE) and of fluorescent antinuclear antibodies associated with chronic exposure to trichloroethylene and other chemicals in well water. Environ. Res. 57, 1-9 (1992).
149. Sahebari, M., Nabavi, N., & Salehi, M. Correlation between serum 25(OH)D values and lupus disease activity: an original article and a systematic review with meta-Analysis focusing on serum VitD confounders. Lupus 23, 1164-1177 (2014).
150. Breslin, L. C., Magee, P. J., Wallace, J. M., & McSorley, E. M. An evaluation of vitamin D status in individuals with systemic lupus erythematosus. Proc. Nutr. Soc. 70, 399-407 (2011).
151. de Souza, V. A., et al. Association of hypovitaminosis D with systemic lupus erythematosus and inflammation. J. Bras. Nefrol. 36, 430-436 (2014).
152. Fragoso, T. S., et al. 25 hydroxyivitamin D3 levels in patients with systemic lupus erythematosus and its association with clinical parameters and laboratory tests. Rev. Bras. Reumatol. 52, 60-65 (2012).
153. Hamza, R. T., Awwad, K. S., Ali, M. K., & Hamed, A. I. Reduced serum concentrations of 25 hydroxy vitamin D in Egyptian patients with systemic lupus erythematosus: relation to disease activity. Med. Sci. Monit. 17, CR711-CR718 (2011).
154. Abe, J., et al. Prevention of immunological disorders in Mrl/l mice by a new synthetic analogue of vitamin D3: 22 oxa 1a, 25 dihydroxyvitamin D3. J. Nutr. Sci. Vitaminol. (Tokyo) 36, 21-31 (1990).
155. Lemire, J. M., Ince, A., & Takashima, M. 1 25 dihydroxyvitamin D3 attenuates the expression of experimental murine lupus of Mrl/l mice. Autoimmunity 12, 143-148 1992).
156. Yap, K., et al. Association of low vitamin D with high disease activity in an Australian systemic lupus erythematosus cohort. Lupus Sci. Med. 2, http://dx.doi.org/10.1136/lupus-2014-000064 (2015).
157. Mok, C. C., et al. Vitamin D deficiency as marker for disease activity and damage in systemic lupus erythematosus: a comparison with anti-dsDNA and anti C1q. Lupus 21, 36-42 (2012).
158. McGhie, T. K., DeCeulaer, K., Walters, C. A., Soyibo, A., & Lee, M. G. Vitamin D levels in Jamaican patients with systemic lupus erythematosus. Lupus 23, 1092-1096 (2014).
159. Barbhaiya, M., & Costenbader, K., H. Ultraviolet radiation and systemic lupus erythematosus. Lupus 23, 588-595 (2014).
160. Schneider, L., et al. Vitamin D levels and cytokine profiles in patients with systemic lupus erythematosus. Lupus 24, 1191-1197 (2015).
161. Munoz-Ortego, J., Torrente-Segarra, V., Prieto-Alhambra, D., Salman-Monte, T. C., & Carbonell-Abello, J. Prevalence and predictors of vitamin D deficiency in non-supplemented women with systemic lupus erythematosus in the Mediterranean region: a cohort study. Scand. J. Rheumatol. 41, 472-475 (2012).
162. Schneider, L., Dos Santos, A. S., Santos, M., da Silva Chakr, R. M., & Monticielo, O. A. Vitamin D and systemic lupus erythematosus: state of the art. Clin. Rheumatol. 33, 1033-1038 (2014).
163. Somers, E. C., Thomas, S. L., Smeeth, L., Schoonen, W. M., & Hall, A. J. Incidence of systemic lupus erythematosus in the United Kingdom, 1990-1999. Arthritis Rheum. 57, 612-618 (2007).
164. Szeto, C. C., et al. Climatic influence on the prevalence of noncutaneous disease flare in systemic lupus erythematosus in Hong Kong. J. Rheumatol. 35, 1031-1037 (2008).
165. Duarte-Garcia, A., Fang, H., To, C. H., Magder, L. S., & Petri, M. Seasonal variation in the activity of systemic lupus erythematosus. J. Rheumatol. 39, 1392-1398 (2012).
166. Panopalis, P., et al. Health care costs and costs associated with changes in work productivity among persons with systemic lupus erythematosus. Arthritis Rheum. 59, 1788-1795 (2008).
167. Huscher, D., et al. Cost of illness in rheumatoid arthritis, ankylosing spondylitis, psoriatic arthritis and systemic lupus erythematosus in Germany. Ann. Rheum. Dis. 65, 1175-1183 (2006).
168. Jonsen, A., et al. Total cost and cost predictors in systemic lupus erythematosus-8 years follow up of a Swedish inception cohort. Lupus 24, 1248-1256 (2015).
169. Bexelius, C., Wachtmeister, K., Skare, P., Jonsson, L., & Vollenhoven, R. Drivers of cost and health-related quality of life in patients with systemic lupus erythematosus (SLE): a Swedish nationwide study based on patient reports. Lupus 22, 793-801 (2013).
170. Doria, A., et al. Annual direct medical cost of active systemic lupus erythematosus in five European countries. Ann. Rheum. Dis. 73, 154-160 (2014).
171. Sutcliffe, N., Clarke, A. E., Taylor, R., Frost, C., & Isenberg, D. A. Total costs and predictors of costs in patients with systemic lupus erythematosus. Rheumatology (Oxford) 40, 37-47 (2001).
172. Cho, J., et al. Costs of illness and quality of life in patients with systemic lupus erythematosus in South Korea. Lupus 23, 949-957 (2014).
173. Zhu, T. Y., Tam, L. S., Lee, V. W., Lee, K. K., & Li, E. K. Systemic lupus erythematosus with neuropsychiatric manifestation incurs high disease costs: a cost of illness study in Hong Kong. Rheumatology (Oxford) 48, 564-568 (2009).
174. Zhu, T. Y., Tam, L. S., Lee, V. W., Lee, K. K., & Li, E. K. The impact of flare on disease costs of patients with systemic lupus erythematosus. Arthritis Rheum. 61, 1159-1167 (2009).
175. Li, T., et al. Long-Term medical costs and resource utilization in systemic lupus erythematosus and lupus nephritis: a five-year analysis of a large Medicaid population. Arthritis Rheum. 61, 755-763 (2009).
176. Garris, C., et al. Healthcare utilization and cost of systemic lupus erythematosus in a US managed care health plan. J. Med. Econ. 16, 667-677 (2013).
177. Kan, H., et al. A longitudinal analysis of costs associated with change in disease activity in systemic lupus erythematosus. J. Med. Econ. 16, 793-800 (2013).
178. Kan, H. J., et al. Healthcare utilization and costs of systemic lupus erythematosus in Medicaid. Biomed. Res. Int. 2013, http://dx.doi. org/10.1155/2013/808391 (2013).
179. Narayanan, S., Wilson, K., Ogelsby, A., Juneau, P., & Durden, E. Economic burden of systemic lupus erythematosus flares and comorbidities in a commercially insured population in the United States. J. Occup. Environ. Med. 55, 1262-1270 (2013).
180. Furst, D. E., et al. Medical costs and healthcare resource use in patients with lupus nephritis and neuropsychiatric lupus in an insured population. J. Med. Econ. 16, 500-509 (2013).
181. Furst, D. E., et al. Resource utilization and direct medical costs in adult systemic lupus erythematosus patients from a commercially insured population. Lupus 22, 268-278 (2013).
182. Oglesby, A., et al. Impact of early versus late systemic lupus erythematosus diagnosis on clinical and economic outcomes. Appl. Health Econ. Health Policy 12, 179-190 (2014).
183. Pelletier, E. M., Ogale, S., Yu, E., Brunetta, P., & Garg, J. Economic outcomes in patients diagnosed with systemic lupus erythematosus with versus without nephritis: results from an analysis of data from a US claims database. Clin. Ther. 31, 2653-2664 (2009).
184. Carls, G., et al. Direct and indirect costs to employers of patients with systemic lupus erythematosus with and without nephritis. J. Occup. Environ. Med. 51, 66-79 (2009).
185. Clarke, A. E., et al. SLE patients with renal damage incur higher health care costs. Rheumatology (Oxford) 47, 329-333 (2008).
186. Clarke, A. E., et al. The systemic lupus erythematosus Tri-Nation Study: absence of a link between health resource use and health outcome. Rheumatology (Oxford) 43, 1016-1024 (2004).
187. Clarke, A. E., Urowitz, M. B., Monga, N., & Hanly, J. G. Costs associated with severe and nonsevere systemic lupus erythematosus in Canada. Arthritis Care Res. (Hoboken) 67, 431-436 (2015).
188. Aghdassi, E., et al. Healthcare cost and loss of productivity in a Canadian population of patients with and without lupus nephritis. J. Rheumatol. 38, 658-666 (2011).
189. Gordon, C., et al. The substantial burden of systemic lupus erythematosus on the productivity and careers of patients: a European patient-driven online survey. Rheumatology (Oxford) 52, 2292-2301 (2013).
190. Panopalis, P., et al. The systemic lupus erythematosus Tri-Nation study: cumulative indirect costs. Arthritis Rheum. 57, 64-70 (2007).
191. Scofield, L., Reinlib, L., Alarcon, G. S., & Cooper, G. S. Employment and disability issues in systemic lupus erythematosus: a review. Arthritis Rheum. 59, 1475-1479 (2008).
192. Mok, C. C., Cheung, M. Y., Ho, L. Y., Yu, K. L., & To, C. H. Risk and predictors of work disability in Chinese patients with systemic lupus erythematosus. Lupus 17, 1103-1107 (2008).
193. Yelin, E., et al. Work loss and work entry among persons with systemic lupus erythematosus: comparisons with a national matched sample. Arthritis Rheum. 61, 247-258 (2009).
194. Zhu, T. Y., Tam, L. S., & Li, E. K. Labour and non-labour market productivity in Chinese patients with systemic lupus erythematosus. Rheumatology (Oxford) 51, 284-292 (2012).
195. Yelin, E., et al. Work dynamics among persons with systemic lupus erythematosus. Arthritis Rheum. 57, 56-63 (2007).
196. Schmeding, A., & Schneider, M. Fatigue, health-related quality of life and other patient-reported outcomes in systemic lupus erythematosus. Best Pract. Res. Clin. Rheumatol. 27, 363-375 (2013).
197. Mau, W., Listing, J., Huscher, D., Zeidler, H., & Zink, A. Employment across chronic inflammatory rheumatic diseases and comparison with the general population. J. Rheumatol. 32, 721-728 (2005).
198. Utset, T. O., et al. Work disability, lost productivity and associated risk factors in patients diagnosed with systemic lupus erythematosus. Lupus Sci. Med. 2, http://dx.doi.org/10.1136/lupus-2014-000058 (2015).
199. Jetha, A., et al. Unpacking early work experiences of young adults with rheumatic disease: an examination of absenteeism, job disruptions and productivity loss. Arthritis Care Res. (Hoboken) 67, 1246-1254 (2015).
200. Garris, C., Oglesby, A., Sulcs, E., & Lee, M. Impact of systemic lupus erythematosus on burden of illness and work productivity in the United States. Lupus 22, 1077-1086 (2013).
201. Al Dhanhani, A. M., Gignac, M. A., Beaton, D. E., Su, J., & Fortin, P. R. Work factors are associated with workplace activity limitations in systemic lupus erythematosus. Rheumatology (Oxford) 53, 2044-2052 (2014).
202. Dua, A. B., Touma, Z., Toloza, S., & Jolly, M. Top 10 recent developments in health-related quality of life in patients with systemic lupus erythematosus. Curr. Rheumatol. Rep. 15, http://dx.doi.org/10.1007/s11926-013-0380-9 (2013).
203. Mosca, M., et al. European league against rheumatism recommendations for monitoring patients with systemic lupus erythematosus in clinical practice and in observational studies. Ann. Rheum. Dis. 69, 1269-1274 (2010).