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Systemic lupus erythematosus in native sub-Saharan Africans: A systematic review and meta-analysis
Background: The prevalence and phenotype of systemic lupus erythematosus (SLE) have not been thoroughly investigated in Native sub-Saharan Africans despite knowledge that the highest burden of SLE occurs in people of African descent. Through this systematic review of literature and meta-analysis, we wished to fill this gap.
Methods: PubMed, EMBASE, Web of Science, African Journals Online, and Global Index Medicus, as well as references of retrieved papers, were searched to select studies that addressed SLE in Native sub-Saharan Africans and had been published between January 1, 2008 and October 7, 2018. The prevalence of SLE and its characteristics were pooled through narrative review and random-effects model. Heterogeneity (I²) was assessed via the χ² test. Pooled estimates are expressed with 95% confidence intervals. This study is registered with PROSPERO: registration number CRD42019139226.
Results: Out of 1502 papers, 15 hospital-based studies were included. The pooled prevalence of SLE among 28575 participants was 1.7% (0.8-2.9), with substantial heterogeneity between studies (I2 = 96.9% [94.8%; 98.1%], τ2 = 0.0020, p < 0.0001). The mean age at diagnosis ranged from 28.8 to 39.2 years. The female proportion varied from 88% to 100%. Rheumatological (5.1%-99.9%), dermatological (4.3%-100%) and haematological (1.4-86.9%) manifestations were the most common clinical features of SLE. Patients had a high seroprevalence for anti-ribonucleoprotein 57.9% (36.4-77.9), anti-Smith 53.5% (40.4-66.2), anti-Sjogren syndrome antigen A 45.6% (19.2-73.4) and anti-Sjogren syndrome antigen B 33.7% (13.6-57.6) autoantibodies. The most used treatments were corticosteroids 99% (94.9-100) and antimalarials 62. 8 % (23.3-94.1). The pooled mortality rate was 10.3% (3.3-20.6) and death was mainly due to infections, kidney disease and neurological involvement.
Conclusion: SLE is not rare among native sub-Saharan Africans and its featured characteristics were earlier onset, female predominance, and high seropositivity for extractable nuclear antigen autoantibodies. Corticosteroids and antimalarials were the standard treatments. The mortality rate was high. Population prevalence and incidence as well as full description of SLE characteristics in Native sub-Saharan Africans are needed.
References
[1] Rees F, Doherty M, Grainge MJ, Lanyon P, Zhang W, (2018) The worldwide incidence and prevalence of systemic lupus erythematosus: systematic review of epidemiological studies. Rheumatol (Oxford). 56 (11) 1945-1961.[2] Carter EE, Barr SG, Clarke AE, (2016) The global burden of SLE: prevalence, health disparities and socioeconomic impact. Nat Rev Rheumatol. 12 (10) 605-20.
[3] Yen EY, Singh RR, (2018) Lupus-an unrecognized leading cause of death in young women: population-based study using nationwide death certificates, 2000-2015. Arthritis Rheumatol. 70 (8) 1251-1255.
[4] Lee YH, Choi SJ, Ji JD, Song GG, (2016) Overall and cause-specific mortality in systemic lupus erythematosus: an updated meta-analysis. Lupus. 0 1-8.
[5] Lewis MJ, Jawad AS, (2016) The effect of ethnicity and genetic ancestry on the epidemiology, clinical features and outcome of systemic lupus erythematosus. Rheumatol (Oxford). 56 (suppl_1) i67-i77.
[6] Agrawal M, Shah S, Patel A, Pinotti R, Colombel J-F, Burisch J, (2019), Changing epidemiology of immune-mediated inflammatory diseases in immigrants: A systematic review of population-based studies. J Autoimmun. https://doi.org/10.1016/j.jaut.2019.07.002.
[7] Bae S-C, Fraser P, Liang MH, (1999) The epidemiology of systemic lupus erythematosus in populations of African ancestry. Arthritis rheum. 41 (12) 2090-2099.
[8] Tiffin N, Hodkinson B, Okpechi I, (2014) Lupus in Africa: can we dispel the myths and face the challenges? Lupus. 23 102-111.
[9] Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25 (11) 1271-77.
[10] Hochberg MC, (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40(9) 1725-1734.
[11] Hoy D, Brooks P, Woolf A, et al, (2012) Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. Journal of Clinical Epidemiology. 65, 934-9.
[12] Cochran WG, (1954) The Combination of Estimates from Different Experiments. Biometrics. 10 101-29.
[13] Adelowo OO and Oguntona SA, (2009) Pattern of systemic lupus erythematosus among Nigerians. Clinical Rheumatology. 28, 699-703.
[14] Adelowo OO, Ojo O and Oduenyi I, (2012) Auto antibodies in Nigerian lupus patients. African journal of medicine and medical sciences. 41, 177-81.
[15] Budhoo A, Mody GM, Dubula T, Patel N and Mody PG, (2017) Comparison of ethnicity, gender, age of onset and outcome in South Africans with systemic lupus erythematosus. Lupus. 26, 438-46.
[16] Diallo MS, Mbengue B, Seck A, Ndao AC, Niang MS, Cissoko Y, et al, (2014) Evolution of autoantibodies profile in systemic lupus erythematosus according to age and clinical manifestations. Annales de biologie clinique. 72351-8.
[17] Doualla MB, Luma Namme H, Ashuntantang G, Epée H, Kwedi F, Kemta LF, et al, (2014) Clinical presentation, treatment and outcome of patients with systemic lupus erythematosus seen at a rheumatology clinic in Douala, Cameroon. Health and Sciences Diseases. 15 1-5.
[18] Dubula T and Mody GM, (2015) Spectrum of infections and outcome among hospitalized South Africans with systemic lupus erythematosus. Clinical Rheumatology. 34, 479-488.
[19] Dzifa D, Boima V, Yorke E, Yawson A, Ganu V and Mate-Kole C, (2017) Predictors and outcome of systemic lupus erythematosus (SLE) admission rates in a large teaching hospital in sub-Saharan Africa. Lupus. 0,1-7.
[20] Ekwom PE (2013) Systemic lupus erythematosus (SLE) at the Kenyatta National Hospital. Clinical Rheumatology. 32, 1215-1217.
[21] Gbané-Koné M, Ouattara B, Djaha KJM, Megne E, Ngandeu NA, Coulibaly KA, et al, (2015) Autoantibodies in Systemic Lupus Erythematosus, on Black African Subject, in Abidjan. Open Journal of Rheumatology and Autoimmune Diseases. 5, 28-35.
[22] Iba-Ba J, Biteghe B, Missounga L, Ibouili BR, Mipinda JB, Coniquet S, et al, (2009) Elevated C reactive protein rate in 23 black African patients with systemic lupus erythematosus and without opportunistic infectious disease. Sante (Montrouge, France). 19, 67-71.
[23] Kombate K, Saka B, Oniankitan OI, Sodonougbo P, Mouhari-Toure A, Tchangai-Walla K, et al, (2008) Systemic lupus erythematosus in Lomé, Togo. Medecine Tropicale. 68, 283-6.
[24] Malemba JJ and Mbuyi-Muamba JM, (2008) Clinical and epidemiological features of rheumatic diseases in patients attending the university hospital in Kinshasa. Clinical Rheumatology. 27 47-54.
[25] Ndiaye FS, Ndongo S, Fall S, Dioum A, Pouye A, Moreira-Diop T, et al, (2008) Frequency of hematological and immunological manifestations of lupus in Dakar. Dakar médical. 53, 192-197.
[26] Ngaïdé AA, Ly F, Ly K, Diao M, Mbaye AAK, Aw FML, et al, (1990) Cardiovascular manifestations in systemic lupus erythematosus in Dakar: Descriptive study about 50 cases. Bulletin de la Societe de pathologie exotique, 109 (2016) 345-352.
[27] Zavier Z, Michee A, Anthelme A, Felix A, Marcelle G and Martin A, (2014) Pattern of systemic lupus erythematosus in Benin and west African patients. Tunisie Medicale. 92, 707-710.
[28] McGill PE, Oyoo GO, (2002) Rheumatic disorders in sub-Saharan Africa. East Afr Med J. 79 (4) 214-216.
[29] Jeandel P, Roux H, (2002) Epidémiologie des affections rhumatologiques en Afrique subsaharienne. Rev Rhum. 69, 764-76.
[30] Monekosso GL, (2014) A brief history of medical education in sub-Saharan Africa. Acad Med. 89 (8) S11-S15.
[31] Parks CG, Sntos ASE, Barbhaiya M, Costenbader KH, (2017) Understanding the role of environmental factors in the development of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 31(3) 306-320.
[32] Magitta NF, (2018) Epidemiology of tobacco use and dependence in sub-Saharan Africa: a systematic review. J Pulmonol Clin Res. 2 (1) 9-15.
[33] Fayiga AO, Ipinmoroti MO, Chirenje T, (2018) Environmental pollution in Africa. Environ Dev Sustain. 20 (1) 41-73.
[34] Fenollar F, Mediannikov O, (2018) Emerging infectious diseases in Africa in the 21 st century. New microbe and new infect. 26, S10-S18.
[35] Lemoine M, Eholie S, Lacombe K, (2015) Reducing the burden of neglected viral hepatitis in Africa: strategies for a global approach. J Hepatol. 62, 469-76.
[36] Alarcon GS, Friedman AW, Straaton KV, Moulds JM, Lisse J, Bastian HM, et al, (1999) Systemic lupus erythematosus in three ethnic groups: III A comparison of disease characteristics early in the natural history of the LUMINA cohort. Lupus. 8, 197-209.
[37] Kamen DL, Barron M, Parker TM, Shaftman SR, Bruner GR, Aberle T, et al, (2008) Autoantibody prevalence and lupus characteristics in a Unique African American population. Arthritis Rheum. 58 (5) 1237-1247.
[38] Pons-Estel BA, Catoggio LJ, Cardiel MH, Soriano ER, Gentiletti S, Villa AR, et al, (2004) The GLADEL multinational Latin American prospective inception cohort of 1214 patients with systemic lupus erythematosus. Medicine. 83 (1) 1-17.
[39] Peschken CA, Katz SJ, Silvermann E, Pope JE, Fortin PR, Pineau C, et al, (2009) The 1000 Canadian faces of lupus: determinants of disease outcome in a large multiethnic cohort. J Rheumatol. 36 1200-8.
[40] Deligny C, Thomas L, Dubreuil F, Théodose C, Garsaud AM, Numéric P, et al, (2002) Lupus systémique en Martinique: enquête épidémiologique. Rev Med Intern. 23 21-29.
[41] Ameh OI, Kengne AP, Jayne D, Bello AK, Hodkinson B, Gcelu A, et al (2016) Standard of treatment and outcomes of adults with lupus nephritis in Africa: a systematic review. Lupus. 0, 1-9.
[42] Gonzalez LA, Toloza SMA, Jr McGwin G, Alarcon GS, (2013) Ethnicity in systemic lupus erythematosus (SLE): its influence on susceptibility and outcomes. Lupus. 22, 1214-1224.
[43] Morais SA, Isenberg DA, (2016) A study of the influence of ethnicity on serology and clinical features in lupus. Lupus. 0, 1-10.
[44] Arroyo-Avila M, Santiago-Casas Y, Jr McGwin G, Cantor RS, Petri M, Ramsay-Goldman R, et al, (2015) Clinical associations of anti-Smith antibodies in PROFILE: a multi-ethnic lupus cohort. Clin Rheumatol. 34 (7) 1217-23.
[45] Bruner BF, Guthridge JM, Lu R, Vidal G, Kelly JA, Robertson JM, et al, (2012) Comparison of autoantibody specificities between traditional and bead-based assays in a large, diverse collection of SLE patients and family members. Arthritis Rheum. 64 (11) 3677-3686.
[46] Choi MY, Clarke AE, St Pierre Y, Hanly JG, Urowitz MB, Romero-Diaz J, et al (2019) Antinuclear antibody-negative systemic lupus erythematosus in an international inception cohort. 71 (7) 893-902.
[47] Flower CH, Hennis AJM, Liang MH, (2011) Report of an international symposium on narrowing gap in the treatment and study of SLE worldwide: minimum best practices in the management and monitoring of moderate to severe SLE and improving outcomes in constrained environments. Curr Rev Musculoskelet Med. 4, 105-112.
[48] Bruce II, O’keeffe AG, Farewell V, Hanly JG, Manzi S, Su L, et al, (2015 ) Factors associated with damage accrual in patients with systemic lupus erythematosus: results from the Systemic Lupus International Collaborating Clinics (SLICC) Inception Cohort. Ann Rheum Dis. 74 (9) 1706-13.
[49] Appel GB, Contreras G, Dooley MA, Ginzler EM, Isenberg D, Jayne D, et al, (2009) Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis. J Am Soc Nephrol. 20, 1103-1112.
[50] Centre de référence pour le Lupus, le Syndrome des antiphospholipides et autres maladies auto-immunes rares. (2017), Protocle National de Diagnostic de Soins (PNDS). Lupus systémique. [Internet]. [Cited on July 04, 2019]. Available from: https://www.has-sante.fr
[51] Alarcon GS, Jr McGwin G, Bastian HM, Roseman J, Lisse J, Fessler BJ, et al, (2001) Systemic lupus erythematosus in three ethnic groups. VIII. Predictors of early mortality in the LUMINA cohort. Arthritis Care Res. 45 ,191-202.
[52] Ocampo-Piraquive V, Nieto A, Canas CA, Tobon GJ, (2018), Mortality in systemic lupus erythematosus: causes, predictors and interventions. Exp Rev Clin Immunol. 14 (12) 1043-1053.
[53] Phuti A, Schneider M, Makan K, Tikly M, Hodkinson B, (2019) Living with systemic lupus erythematosus in South Africa: a bitter pill to swallow. Health and Quality of Life Outcomes. 17, 65.
[54] Tektonidou MG, Lewandowski LB, Hu J, Dasgupta A, Ward MM, (2017) Survival in adults and children with systemic lupus erythematosus: a systematic review and Bayesian meta-analysis of studies from 1950 to 2016. Ann Rheum Dis. 0, 1-8.
[55] Alarcon GS, (2008) Lessons from LUMINA: a multiethnic US cohort. Lupus. 17, 971-976.
[56] Pons-Estel GJ, Catoggio LJ, Cardiel MH, Bonfa E, Caeiro F, Sato E, et al, (2015) Lupus in Latin-American patients: lessons from the GLADEL cohort. Lupus. 0, 1-10.
[57] Cervera R, (2006) Systemic lupus erythematosus in Europa at the change of the millenium: “Lessons from the Euro-Lupus Project”. Autoimmunity Rev. 5, 180-86.
[58] Lekoubou A, Awah P, Fezeu L, Sobngwi E, Kengne AP, (2010) Hypertension, diabetes mellitus and task shifting in their management in sub-Saharan Africa. Int J Environ Res Public Health. 7, 353-363.
[59] Dzudie A, Djomou A, Ba H, Njume E, Ndom MS, Mfekeu LK, et al, (2019) MMM-17 Cameroon, analysis and opportunities-Sub-Saharan Africa. Eur Heart 21 (Suppl D) D31-D33.
[60] Rees F, Doherty M, Grainge MJ, et al, (2016) The incidence and prevalence of systemic lupus erythematosus in the UK, 1999-2012. Ann Rheum Dis 75 (1) 136-41.
{61] Izmirly PM, Wan I, Sahl S, et al, (2017) The incidence and prevalence of systemic lupus erythematosus in New York county (Manhattan), New York. Arthritis Rheumatol. 69 (10) 2006-2017.
[62] Pons-Estel GJ, Saurit V, Alarcon GS, Hachuel L, Boggio G, Wojdyla D, et al, (2012) The impact of rural residency on the expression and outcome of systemic lupus erythematosus: data from a multiethnic latin american cohort. Lupus. 0, 1-8.
[63] Gergianaki I, Fanouriakis A, Adamichou C, Spyrou G, Mihalopoulos N, Kazadzis S, et al, (2018) Is systemic lupus erythematosus different in urban versus rural living environment? Data from the Cretan Lupus Epidemiology and Surveillance Regitry. Lupus. 0, 1-10.
[64] Unlu O, Zuily S, Erkan D, (2016) The clinical significance of antiphospholipid antibodies in systemic lupus erythematosus. Eur J Rheumatol. 3, 75-84.
[65] Aringer M, Costenbader K, Daikh D, Brinks R, Mosca M, Ramsey-Goldman R, et al, (2019 ) 2019 European League Against Rheumatism/American College of Rheumatology Classification criteria for Systemic Lupus Erythematosus. Arthritis Rheum. 0 (0) 1-13.
Written By
Mickael Essouma
Faculty of Medicine and Biomedical Sciences
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