
==== Front
J Allergy Clin Immunol Glob
J Allergy Clin Immunol Glob
The Journal of Allergy and Clinical Immunology: Global
2772-8293
Elsevier

S2772-8293(24)00084-5
10.1016/j.jacig.2024.100288
100288
Review Article
Lupus and other autoimmune diseases: Epidemiology in the population of African ancestry and diagnostic and management challenges in Africa
Essouma Mickael MD essmic@rocketmail.com
a∗
Noubiap Jean Jacques MD, PhD b
a Network of Immunity in Infection, Malignancy and Autoimmunity (NIIMA), Universal Scientific Education and Research Network (USERN), Cameroon
b Division of Cardiology, Department of Medicine, University of California-San Francisco, San Francisco, Calif
∗ Corresponding author: Mickael Essouma, MD, Network of Immunity in Infection, Malignancy and Autoimmunity, Universal Scientific Education and Research Network (USERN), Yaounde, Cameroon. essmic@rocketmail.com
01 6 2024
11 2024
01 6 2024
3 4 10028830 9 2023
15 2 2024
23 2 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Autoimmune diseases are prevalent among people of African ancestry living outside Africa. However, the burden of autoimmune diseases in Africa is not well understood. This article provides a global overview of the current burden of autoimmune diseases in individuals of African descent. It also discusses the major factors contributing to autoimmune diseases in this population group, as well as the challenges involved in diagnosing and managing autoimmune diseases in Africa.

Key words

Lupus
autoimmune diseases
epidemiology
challenges
Africa
Abbreviations used

AD Autoimmune disease

ADMT Autoimmune disease–modifying therapy

ANA Antinuclear antibody

DEI Diversity, equity, and inclusion

ID Infectious disease

SAD Systemic autoimmune disease
==== Body
pmcAutoimmune diseases (ADs) are chronic diseases resulting primarily from the breakdown of tolerance against self-antigens.1,2 Besides the classic autoantibody-positive and seronegative AD subtypes,1,3,4 there are “borderline ADs” that exhibit both autoimmune (eg, autoantibodies in a subset of patients) and autoinflammatory (eg, excess pattern recognition receptor signaling) features.4,5 Examples of “borderline ADs” include sarcoidosis, inflammatory bowel disease, and psoriatic disease.6, 7, 8 Most ADs are treated with the same types of AD-modifying therapies (ADMTs) because they arise from a combination of similar patient-related and environmental factors driving similar pathogenetic and clinical features.5,9 This phenomenon is referred to as the “autoimmune tautology.”9 However, some ADs are mendelian disorders.5

The estimated prevalence of ADs outside Africa is 5% to 10%, with people of African ancestry being particularly affected.10, 11, 12 From 1965 (when ADs were officially recognized) to the 2000s, they were rarely reported in Africa.13, 14, 15, 16 Given the high burden of infectious diseases (IDs) in Africa,17 the “hygiene” or “old friend” hypothesis, which suggests an inverse association between IDs and ADs,18,19 was used to justify the scarcity of AD documentation in Africa. The scarcity of lupus (a prototypical AD) reports from West Africa in the 20th century and the high frequency of lupus in West African immigrants in America and Europe gave rise to the “lupus gradient” hypothesis.20, 21, 22 This hypothesis suggests that lupus is rare in West Africa owing to the high prevalence of malaria, which is the most common ID.20,23, 24, 25 However, infectious agents have been identified as risk factors for ADs.5,26 Current lupus data from Nigeria27 are inconsistent with data from the 20th century.21 Additionally, a universal definition of a "rare disease" is still awaited.28,29

In this article, we have narratively synthesized up-to-date epidemiologic data on lupus and other ADs in people of African ancestry. We also discuss potential determinants of the high burden of ADs in this population group and the challenges faced when it comes to managing ADs in Africa.

Epidemiology

Frequency

The combined frequency of organ-specific lupus and systemic lupus erythematosus (SLE) is unknown. The frequency of diagnosed SLE is highest in the United States (US) and Barbados (the Caribbean).30 The US Centers for Disease Control and Prevention estimated the prevalence of diagnosed SLE in the US at 72.8 of 100,000 in the general population, 230.9 of 100,000 in females of African ancestry, and 26.7 of 100,000 in males of African ancestry (vs 14.6 for all US males).31 In Barbados, the incidence of diagnosed SLE is 10.37 per 100,000 person years.30 Among low- and middle-income countries, the World Health Organization-Africa region had the second-highest (after American countries) standardized prevalence (60 per 100,000 of individuals with diagnosed SLE [95% CI = 40-1300]).32 Population-based prevalence data on SLE in Sub-Saharan Africa are scarce,32 but SLE was diagnosed in 1.7% of 28,175 natives in Sub-Saharan African internal medicine and rheumatology settings between 1987 and 2014 (95% CI = 0.8-2.9).15 It is also estimated that 9% of the global population of individuals who are younger than 16 years and have SLE reside in Eastern Africa.33

Scleroderma, type 1 diabetes mellitus, and sarcoidosis are more commonly diagnosed in individuals of African descent than in individuals of other ancestries.34, 35, 36 However, the frequencies of these conditions in Africa are not well known.37, 38, 39 Between 2004 and 2012, dermatomyositis and polymyositis were diagnosed in US Medicaid beneficiaries of African ancestry more frequently than in White people.40 In Africa,41 the frequency of diagnosed autoimmune inflammatory myopathy mirrors the frequency reported elsewhere.42 The incidence rates of dermatomyositis per 1,000,000 person years were approximately 7.5 and 1.2 in South Africa43 and Botswana,44 respectively. The incidence of polymyositis was 8.8 per 1,000,000 person years in Lybia,45 and its prevalence was 11 per 100,000 persons in Egypt (95% CI = 0-32).46 Data from Southern California in the US suggest that multiple sclerosis could be more prevalent among young people of African ancestry than among young people of other ancestries.47 In Africa, the prevalence of diagnosed multiple sclerosis saw a 59% increase from 2013 to 2020, with the latest prevalence rate at 8.76 per 100,000 individuals.48

Further research is needed to determine across age groups the magnitude of other ADs in individuals of African descent versus in individuals of other ancestries.15,33,49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60

Phenotype, severity and case fatality rate

In general, individuals of African ancestry tend to develop ADs earlier in life15,16,37,41,61, 62, 63; in addition, ADs have a higher female predilection16,54,64 and are characterized by more symptoms in individuals of African ancestry15,16,65 than in those of other ancestries.

Patients with SLE who are of African descent are more likely to develop lupus nephritis (the most severe manifestation of lupus), have higher disease activity scores, and experience more organ damage accrual than White patients do.65, 66, 67, 68, 69 It has been estimated that people of African ancestry have a higher frequency of biomarkers indicating severe SLE than people of other ancestries do.70,71 For example, the frequency of checked anti-Smith autoantibodies in Sub-Saharan Africans with SLE was found to be 53.5% (95% CI = 40.4%-66.2%),72 whereas the frequency of anti-Smith autoantibodies in the general population of people with SLE varies between 5% and 30%.73

Survival has improved markedly in patients with SLE who are living in developed countries.74,75 However, US Medicaid beneficiaries of African ancestry who had SLE had a 21% higher risk of death than did White people in 2000-2006 (hazard ratio = 1.21 [95% CI = 1.10-1.33),76 and SLE ranked fifth and sixth among causes of death in women of African descent aged 15 to 24 and 25 to 34 years compared with 10th and 14th in age-matched White American women.77 In Sub-Saharan Africa, SLE inpatient case fatality rate reaches as high as 43.1% (95% CI = 29.3%-57.8%), with death often occurring shortly after the diagnosis.72 IDs are the main causes of death.15,76,78 However, kidney disease is also a major cause of death in Sub-Saharan Africa.15,79 More robust studies are needed to clearly determine the burden of juvenile-onset SLE in individuals of African ancestry versus in individuals of other ancestries.80, 81, 82, 83

Individuals of African descent who have various ADs tend to have worse disease activity and outcomes than patients of other ancestries do. Examples of these ADs include, but are not limited to, type 1 diabetes mellitus, multiple sclerosis, autoimmune hepatitis, myasthenia gravis, autoimmune inflammatory myopathy, rheumatoid arthritis, and scleroderma.38,40,41,47,49,52,64,84, 85, 86 Scleroderma and SLE are 2 of the deadliest systemic ADs (SADs),87 with the highest case fatality rates found in individuals of African descent.76,85 In the US, the age-adjusted case fatality rate of scleroderma in people of African ancestry is 1.5 times higher than that in White individuals.85 In a study in South Africa, a 9% case fatality rate was reported among individuals with scleroderma who were receiving medical care.88 These high death rates are due mainly to scleroderma-associated interstitial lung disease.37,85,88

Determinants

There are cross-sectional studies linking ADs with sociologic and genetic factors in people of African ancestry. However, other environmental factors may also play a crucial role (Fig 1).5,89, 90, 91, 92, 93, 94, 95, 96, 97, 98, 99, 100, 101, 102, 103, 104, 105, 106, 107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117, 118, 119, 120, 121, 122, 123, 124, 125, 126Fig 1 Factors driving susceptibility and severity of multigenic ADs in individuals of African ancestry.5,89, 90, 91, 92, 93, 94, 95, 96, 97, 98, 99, 100, 101, 102, 103, 104, 105, 106, 107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117, 118, 119, 120, 121, 122, 123, 124, 125, 126 There is a specific gene in people of African descent that is strongly associated with ADs. This gene is called Apolipoprotein 1 (APOL1), and its G1 and G2 variants are linked to lupus nephritis and lupus-related end-stage kidney disease in people of African descent.89, 90, 91 Social determinants of health (SODHs) including low socioeconomic status and Diversity-Equity-Inclusion (DEI)-related matters are the best-known AD determinants in people of African ancestry.65,66,92, 93, 94, 95 Considering data from the general population with ADs, ecologic factors commonly found in neighborhoods of individuals of African ancestry (eg, infectious agents and pollutants) and other lifestyle-related SODHs such as food environments could also be major environmental AD determinants in the population of African ancestry.5,96, 98, 97, 99, 100, 102, 103, 104, 105, 106, 110, 107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117, 118, 119, 120, 121, 122, 123, 124, 125, 126 Geographic, spatial, and temporal factors, including latitude, longitude, altitude, temperature, precipitation, and humidity, may contribute as well.119

Sociologic determinants

Sociologic determinants refer mainly to psychosocial stressors that can increase the likelihood and severity of ADs.92, 93, 94, 95 They do this by affecting the body, increasing environmental exposures, and limiting access to optimal care.92,107, 108, 109,127,128 An important bodily consequence of these factors is the change in a person's genetic makeup, resulting in the development of “social epigenetic factors.”127 Additionally, these factors stimulate brain regions responsible for threat vigilance and emotions such as the amygdala, and the hypothalamic-pituitary-adrenal axis, leading to the sustained production of stress hormones and proinflammatory cytokines.107, 108, 109,128, 129, 130, 131

Low socioeconomic status

The socioeconomic status of an individual refers to his or her relative position in the hierarchic structure of society based on access to control over wealth, prestige, and power.92 The socioeconomic stratification of individuals has substantial effects on their self-perception and well-being.92,129,132,133 Socioeconomic stratification also affects mating behavior, which in turn affects the genetic diversity of populations.134

Low socioeconomic status is a psychosocial stressor that can lead to various diseases, including ADs, given that "health” encompasses physical, mental, and social well-being.92,107, 108, 109,132,135 Socioeconomic status is determined mainly by income, educational level and quality, occupational class, social class, and ancestry.92 This entails low socioeconomic status being associated with poverty and low educational level and quality, other psychosocial stressors, and driving factors of low self-health perception and unadvisable habits that have been associated with ADs in people of African descent.38,52,64,65,92, 93, 94, 95,136, 137, 138 For instance, in Nigeria, most individuals diagnosed with SLE between 2017 and 2020 had a monthly income below $100 US.27

Individuals with low socioeconomic status may be subject to neglect and social abuses such as rape and emotional abuse.82,111,112,130,139,140 They may also have limited social support and fewer opportunities to take advantage of available resources.111,112,132,138 This can help explain why patients of African ancestry, who experience multiple adverse life events and insecurities such as food and housing insecurity and low access to health care, are more likely to experience SLE severity and organ damage.65,79,82,93,111,112,130,139, 140, 141

Low socioeconomic status is associated with increased susceptibility, severity, and worse outcomes of ADs,65,92, 93, 94, 95,142 as well as with comorbidities111,112,142 such as infections, depression, and cardiovascular diseases, especially among individuals of African descent with SLE.65,92,93,142

Bias in implementation of the principles of DEI

The concept of “diversity, equity, and inclusion” (DEI) was developed in the US in the 1960s to close the socioeconomic gap across ancestral groups (see Beavers D.143). An unbiased implementation of DEI principles would have been helpful for people of African ancestry with ADs or predisposing factors had all forms of racial discrimination been eliminated in 1965, as was expected by the United Nations.93,121,137,139,140,143, 144, 145, 146 According to the 2015-2017 BeWell (Black Women’s Experiences Living with Lupus) study, perceived racist microaggressions and vicarious racism (unintended exposure to a racist act inflicted on someone else) were associated with SLE disease activity and organ damage, as well as with comorbid obesity.139,140 Racism is a psychosocial stressor.128 Its impact on susceptibility and outcomes of ADs could also be understood through the lens of low socioeconomic status, as racism amplifies stigma and common discriminations against people with ADs (eg, sex discrimination, ableism, and job discrimination).92,93,95,111,112,128,147,148

Besides interpersonal and structural racism outside the health system, people of African ancestry with ADs are being discriminated against within the health system.82,93,142,147 The provision of care for SADs is often influenced by rheumatologists, who may or may not have received formal training in internal medicine. This could be due to a reduced interest in autoimmunity among general internal medicine physicians, and there is no formal autoimmunology medical specialty.149, 150, 151, 152 African-specific phenotypes, such as skin and hematologic manifestations, data, and voices, are substantially underrepresented in rheumatology training, research, and management materials and frameworks.16,153, 154, 155, 156, 157, 158, 159, 160, 161 This leads to unequal opportunity for timely diagnosis and management of SADs in people of African descent versus in people of other ancestries.16,153,154 This inequality also limits the understanding of ADs, as data from individuals of African ancestry may have important educational value.153,154,162

Patients of African ancestry have often been underrepresented in studies on the effectiveness of ADMTs.16,163 This is due partly to inadequate counseling that does not take cultural sensitivities into consideration.163 It is also observed in Western rheumatology settings during treatment of patients of African ancestry with biologic ADMTs.164 However, providing appropriate counseling and ensuring equitable inclusion in clinical trials is crucial for patients of African ancestry with ADs.163,165 These patients may respond differently to ADMTs such as azathioprine and belimumab than do patients of other ancestries.166,167 It is important to note that African Americans carry the memories of historical injustices in medicine, such as the 1932-1972 Tuskegee syphilis experiment, during which drug treatment was withheld from males of African ancestry.163,168 Moreover, appropriate counseling has the potential to mitigate the increased risk of IDs in individuals of African ancestry treated with biologic ADMTs.65,67,169

Infectious agents

Infectious agents are well-known AD determinants.5,162,170 All types of pathogens can trigger autoimmunity through mechanisms such as molecular mimicry, epitope spreading, and bystander activation of autoreactive B and T lymphocytes.26,171, 172, 173, 174 According to epidemiologic and molecular data, the most incriminated infectious agents are viruses, particularly Epstein Barr Virus (EBV) and severe acute respiratory syndrome coronavirus 2.5,26,175, 176, 177, 178 A study conducted in Tunisia found that lymphocytic EBV infection was present in the salivary glands of patients with Sjögren disease but not in the control group.113 However, the reported absence of a significant association between EBV infection and Sjögren disease in that study was potentially due to a low statistical power.51 EBV, Human Immunodeficiency Virus, and Mycobacterium spp are potential major determinants of inflammatory bowel disease in people of African descent.17,26,57,58,179,180 Mycobacterium spp. are part of the “sarcoidosis autoantigenome,” although their pathogenetic mechanisms in this context are unclear.181,182 In the rest of this section, we take a look at the link between human malaria and human ADs.

Does malaria trigger polygenic ADs?

It has been observed in and outside Africa that Plasmodium falciparum triggers the production of numerous autoantibodies (eg, anti-smooth muscle antibody, anti-parietal cell antibody, anti-red blood cell antibody, antilymphocyte antibody, rheumatoid factor, antiphosphatidylserine, and antinuclear antibodies [ANAs]) in people with chronic and acutemalaria.171,183, 184, 185, 186, 187, 188, 189, 190 A study published in 2004 found that 27% of 124 West African immigrants in Italy who had previously experienced repetitive episodes of malaria and diarrhea in Africa were seropositive for ANAs. In comparison, only 3.5% of 375 White Italian relatives of patients with SLE were seropositive for ANAs. The data from West Africans were further divided on the basis of their duration of stay in Italy. The ANA frequencies were 35%, 19%, and 14% for groups having stayed in Italy since 3 months to 7 years, 8 to 14 years, and 15 to 21 years, respectively.191 IgM and IgG antiphosphatidylserine autoantibodies were also found in sera of people with Plasmodium malariae, Plasmodium knowlesi, and Plasmodium vivax malaria in Asia.192 A study from Nigeria suggested NETosis could be a mechanism for the production of the ANA termed anti-deoxyribonucleic acid in people with P falciparum malaria,185 as commonly observed in individuals with SLE.193 The development of cell-mediated immune responses has also been reported in individuals with malaria.188,194

Could malaria-induced autoimmunity be pathogenic?171,183 It has been reportd that human malaria autoantibodies are produced by a segment of age-associated B cell known as the autoantibody-producing segment (VH4-34), which is involved in the pathogenesis of ADs.23,195, 196, 197, 198, 199 IgG and IgM antiphosphatidylserine serum autoantibodies were correlated with anemia in Ugandans and Malaysians with malaria.188 Anti-deoxyribonucleic acid autoantibodies were correlated with anemia in Ugandan children with severe P falciparum malaria.200 It has also been reported that P falciparum malaria–related anti-deoxyribonucleic acid autoantibodies are nephritogenic,171,183,188,200 and both IgM and IgG anti-deoxyribonucleic acid autoantibodies that were found in people with a recent or past episode of malaria187 have been incriminated in SLE pathogenesis.2 In a study conducted in Brazil, the authors reported a destruction of infected red blood cells by cytotoxic CD8 T cells in people with P vivax malaria.201 Because of the cross-sectional nature of these studies, it remains unclear whether malaria autoantibodies are causally associated with the clinical expression of autoimmunity. However, it has been observed that antimalarial drugs are highly effective in reducing antiphospholipid antibody levels and associated thromboembolic events in antiphospholipid antibody–seropositive adults during follow-up.202 Additionally, there was an inverse association between maternal use of hydroxychloroquine during pregnancy and cardiac neonatal lupus in infants born to anti-Ro–seropositive women.203 These findings202,203 highlight the need for longitudinal studies assessing whether there is a causal link between malaria and the clinical expression of autoimmunity in humans.202, 203, 204

ANA seropositivity following malaria exposure could raise the suspicion for ADs5,158,205 such as scleroderma206 and lupus (Fig 2).23,25,70,80,89, 90, 91, 92, 93,96,102, 103, 104, 105, 106, 107, 108, 109,157,158,171,186, 187, 188, 189, 190,194,196, 197, 198, 199,207, 208, 209, 210, 211, 212, 213, 214, 215, 216, 217, 218, 219, 220, 221, 222, 223, 224, 225, 226, 227, 228, 229, 230, 231, 232, 233, 234, 235, 236, 237, 238, 239, 240, 241, 242, 243, 244, 245, 246 In a cross-sectional study involving 1297 unhealthy people, including individuals with unspecified IDs and 188 individuals with SLE, the specificity of ANAs for the SLE diagnosis increased with ANA titer and number of positive autoantibodies against nuclear antigens.247 Accordingly, future studies of malaria should specify participants' autoantibody titers to help guide the follow-up of malaria patients seropositive for ANAs.Fig 2 The “malaria-lupus tautology.”23,25,70,80,89, 90, 91, 92, 93,96,102, 103, 104, 105, 106, 107, 108, 109,157,158,171,186, 187, 188, 189, 190,194,196, 197, 198, 199,207, 208, 209, 210, 211, 212, 213, 214, 215, 216, 217, 218, 219, 220, 221, 222, 223, 224, 225, 226, 227, 228, 229, 230, 231, 232, 233, 234, 235, 236, 237, 238, 239, 240, 241, 242, 243, 244, 245, 246 The malaria features described refer mostly to P falciparum malaria, and the lupus features described refer mostly to SLE. Malaria and lupus share disease determinants and features and antimalarials (AMs) are used to treat both malaria and lupus.23,25,70,80,89, 90, 91, 92, 93,96,102, 103, 104, 105, 106, 107, 108, 109,157,158,171,186, 187, 188, 189, 190,194,196, 197, 198, 199,207, 208, 209, 210, 211, 212, 213, 214, 215, 216, 217, 218, 219, 220, 221, 222, 223, 224, 225, 226, 227, 228, 229, 230, 231, 232, 233, 234, 235, 236, 237, 238, 239, 240, 241, 242, 243, 244, 245, 246 Shared genetic factors include Human Leukocyte Antigen (HLA)96,194,207,208 and non-HLA89, 90, 91,96,194,208, 209, 210, 211 genes. Deoxyribonucleic acid (DNA) modification is an epigenetic mechanism incriminated in the pathogenesis of both malaria and lupus.212,213 Age-associated B cells (ABCs) responsible for the production of autoantibodies in individuals with malaria and those with lupus have been found to exhibit the following common characteristics: derivation from an interferon (IFN)-γ -mediated differentiation of naive B cells, identical autoimmune segment (VH4-34), and similar transcriptional profiles.23,197 The following ANAs have been found in individuals with malaria: IgG/IgM/IgA anti-single and double stranded deoxyribonucleic acid, and anti-Smith/ribonucleoprotein.171,186, 187, 188 Women of reproductive age at highest risk of contracting malaria are pregnant women,25 and available data do not highlight a striking risk difference for lupus across the age spectrum in the paediatric population.80 Whilst all AMs used in clinical practice have been shown to be variably effective in individuals with malaria,242 hydroxychloroquine and chloroquine have been the most tested and proven effective AMs in lupus patients.243, 244, 245aPL, Antiphospholipid antibody; CNS, central nervous system; ESKD, end-stage kidney disease; PRRs, pattern recognition receptors; RF, rheumatoid factor; Tfh, T follicular helper cell; TLR, Toll-like receptor; TNF, tumor necrosis factor.

Can malaria indirectly trigger ADs? It is common for humans to contract malaria alongside other endemic infections caused by intracellular pathogens known as triggers of ADs (eg, EBV infection).26,248 This is mainly because once in the human body, Plasmodium parasites can reactivate latent infectious agents with which they have phylogenetic links.248,249 In this light, Plasmodium parasites could be viewed as indirect triggers of ADs commonly triggered by EBV including lupus, Sjögren disease, rheumatoid arthritis, and multiple sclerosis.179,250, 251, 252 Besides their potential indirect triggering role, Plasmodium parasites may enhance AD activity directly by eliciting the production of anti-Smith autoantibodies, or indirectly through the reactivation of EBV with consequential production of anti-Smith autoantibodies.70, 71, 72, 73,179,248, 249, 250, 251 Another mechanism through which Plasmodium parasites could enhance AD activity is by upregulating interferon signaling directly232,233 and/or through the reactivation of viral infections.162,179,248,249

Have ADs evolved from Plasmodium-mediated genetic selection?

It has been reported that human ADs have evolved from the selection pressure of pathogens on the human genome.170,253 One such pathogen could be the Plasmodium parasite, which has been a major threat to human health for thousands of years across the globe, particularly in Africa.25,194,207,208,254 Plasmodium parasites have been dsecribed as the most powerful known pressure forces on the human genome.194,208 They reportedly have selected genes responsible for immune dysregulation and inflammation in humans.194,208 However, the specific human immune-related conditions shaped by malaria have not been clearly elucidated.194,208 Interestingly, shared immune response gene variants between human malaria and human lupus have been described, as shown in Fig 2. This suggests that human lupus, which has been known since the Middle Ages,255 could have resulted from selection pressure of Plasmodium on the human genome. Findings of an overlap of autoimmune pathways256 between lupus and sickle cell disease, which is a mendelian disease known to have resulted from selection pressure of Plasmodium on the human genome,194,207,208 may be an additional indirect argument for a potential evolutionary link between malaria and lupus.

Besides lupus, other ADs could have evolved from the selection pressure of Plasmodium parasites on the human genome, given the potential association between multiple ADs and glucose-6-phosphate dehydrogenase deficiency,257,258 which is another mendelian disease shaped by malaria.194,207,208 The causal role of lupus in other ADs, such as primary biliary cirrhosis,259 the “autoimmune tautology” phenomenon,9,220 and the overlap of clinicopathogenetic features between ADs and other immune-related conditions (eg, autoinflammatory diseases,4 primary immunodeficiencies,260,261 and atopic and Kikuchi-Fujimoto diseases2,262,263), are additional indirect arguments suggesting that if human malaria has shaped human lupus, then it has also potentially contributed to shaping other human ADs, autoimmune lymphoproliferative syndrome,264,265 and other diseases in immunology/allergy and hematology/oncology.266,267 In the same vein, malaria could have contributed to the shaping of multiple myeloma268,269; the bases for this assumption are data highlighting features of autoimmunity270 and a predominance of the African ancestry269 among patients with multiple myeloma, as well as the spectacular improvement of multiple myeloma manifestations which was observed in some patients following antimalarial drug treatment.267,271

Diagnostic and therapeutic challenges in africa

ADs are underdiagnosed and underreported in Africa.15,16,58,272 Table I provides a summary of the challenges in diagnosing ADs in Africa, especially sub-Saharan Africa.15,16,22,23,27,38,41,51,58,60,111,112,136,138,182,272, 273, 274, 275, 276, 277, 278, 279, 280Table I Barriers to the diagnosis of ADs in Africa

Level of barrier	Barrier	Comment	
Patient- and public-related	Low awareness for ADs and discrimination against individuals with ADs in the society	Limited awareness among patients, patients’ families/guardians, and the public: source of discrimination against, stigmatization and isolation of patients with consequential reluctance to attend to health care settings in some cases15,16,41,51,58,111,112,273,274	
	Unadvisable health-seeking behaviors	- Low self-health perception138

- Prioritization of self-management strategies (eg, use of over-the-counter glucocorticoids to relieve arthritis pain) and care from informal medicine retailers (street drug sellers, spiritual leaders) at the expense of hospital care136

	
	Low income	Unaffordability of autoimmunity diagnostic tests often carried out through subcontracting between local and international health laboratories15,16,27 For example, the estimation of detailed ANA assessment at 53.3 € through health laboratory subcontracting in Gabon275 provides a glimpse of the burden imposed on people with low income27 by costs of autoimmunity assessment in sub-Saharan Africa	
Disease-related	⁃ Overlap of disease features between ADs and other diseases highly prevalent on the continent such as IDs and SCD

⁃ Insidious forms of disease (eg, in AIH)60

⁃ Possibility for spontaneous disease remission (eg, in a subset of patients with sarcoidosis)182

	- Overlap of clinical features: barrier to the diagnosis of ADs when autoimmunity testing cannot be done22,27,58,256

- Overlap of autoantibodies: a barrier to the diagnosis of ADs in individuals with chronic IDs such as HCV infection, previous repetitive episodes of IDs (eg, malaria), or SCD22,23,58,256

- Overlap of morphologic (endoscopic/histopathologic) lesions: barrier to the attribution of an AD etiology to morphologic lesions (eg, tuberculous colitis and CD) and source of delayed diagnosis made only after the failure of a course of antibiotic (eg, antituberculosis) treatment58

	
Health system related: limited diagnostic capacity	Limited diagnostic offer due to health care setting deficiencies	Precarity of ambulatory, home and street based models of care	Limiting factor for a timely diagnosis of ADs in disabled patients unable to attend to health care settings276	
		Deficiencies in public and private health laboratories	- Limited availability of tests for autoimmunity and histopathologic (eg, renal and salivary gland) analyses15,16,51

- Limited availability of equipments for autoimmunity assessment15,16,38,272,277

	
	Limited diagnostic offer due to providers’ biases	- Shortage of health care professionals, especially physicians who represented 9% of 3.6 million health care professionals across 47 countries in Africa between 2018 and 2019278

- Limited awareness for ADs among health care professionals15,16,58,136,272,279

- Limited interest in ADs among aware health care professionals272,274

- Few local opportunities for training on autoimmunity and limited possibility for interested health care professionals to take advantage of online opportunities of training owing to low incomes58 and reduced access to optimal internet connexion280

	
AIH, Autoimmune hepatitis; CD, Crohn disease; HCV, hepatitis C virus; SCD, sickle cell disease.

Three main factors hinder the management of diagnosed ADs in Africa. These factors are deficiencies in the management framework, the huge burden of highly immunosuppressive IDs such as tuberculosis and Human Immunodeficiency Virus infection,17,281 and unadvisable patient behaviors such as low adherence to standard-of-care management and combination of multiple models of care (eg, ADMT-traditional African medicine combination) at the discretion of health care providers.16,136,272

An important deficiency in the management framework is the limited understanding of African-specific AD features, which reduces the possibility to implement personalized ADMTs.15,16,41,51,282 Additionally, there are few robust data on the effectiveness of current immunosuppressive and immunomodulatory ADMTs283 in Africa,16,41,51,58,169 as well as limited availability and affordability of those ADMTs.15,16,41,51,169

The limited availability of ADMTs in sub-Saharan Africa could be due to a limited universal health insurance coverage and implementation of the World Health Organization's essential medicines list for ADs (clearly considered for the first time in 2023) in many countries in Africa.284, 285, 286 Consequently, synthetic ADMTs are often available intermittently at unaffordable costs for many patients in private pharmacies surrounding the health care settings where those ADMTs are most frequently prescribed. Biologic ADMTs are prescribed infrequently because of their original compounds’ limited availability and the prohibitive cost of their biosimilar products.169 Regarding instrumental ADMTs, kidney dialysis is the most accessible.287 Transplantation288 (including chimeric antigen receptor T-cell therapy289) and apheresis290 are not readily available in many countries in sub-Saharan Africa.

Discussion

Current data highlight a growing number of individuals diagnosed with ADs and allergic diseases291,292 in Africa. There is also an association between IDs and ADs, which suggests that we need to reconsider the “hygiene” and “lupus gradient” hypotheses, which are supported primarily by animal data.23,293, 294, 295, 296 Furthermore, these data highlight the need for extensive confirmation bias–free297 research on the burden, determinants, and mechanisms of the more than 100 organ-specific ADs and SADs298,299 in individuals of African ancestry around the world (Box 1).5,51,92,99,110,114, 115, 116, 117, 118, 119,127,134,144,162,170,194,220,264,265,300, 301, 302, 303, 304, 305, 306, 307, 308Box 1 Suggested research pillars to improve the understanding of ADs in people of African descent5,51,92,99,110,114-119,127,134,144,162,170,194,220,264,265,300-308

General notes❖ Data disaggregation by ancestry subtype (i.e., African only versus African admixed), age, sex, birthplace, country of origin, tribe, geographic location (including the area (urban versus rural) and the migration status), and any other nondiscriminatory social identity deemed relevant

❖ Scrutiny of the causal relationships existing between different ADs

❖ Epidemiologic assessment of the autoimmune lymphoproliferative syndrome in the global population of African ancestry

❖ Tracing the history of ADs in Africa and people of African ancestry living outside Africa, including any information about a possible historical link with other diseases commonly found in Afro-descendants

Patient-related biologic determinants❖ Priority for studies of African genomic, “phenomic” (including blood groups), and “microbiomics” biomarkers of autoimmunity, including classic and “dark matter” biomarkers

Infectious agents❖ Scrutinity of the pathogenicity or protective effect of different autoantibodies from each Plasmodium spp. across different age groups, and if necessary, identification of predictors of transition from preclinical to clinically manifest AD → need for (1) long-term prospective cohort studies specifying the titers of autoantibodies in participants with acute, repetitive episodes, chronic ADs, or history of malaria; (2) studies tracking Plasmodium spp. in people with newly diagnosed ADs before the commencement of antimalarial drugs in and outside Africa

❖ Scrutiny of the possible interactions between Plasmodium spp. and typical AD determinants such as EBV infection and pollutants, as well as the putative independent role of other infectious agents

❖ Assessment of the long-term effect of malaria and other vaccines on the incidence of ADs in Africa

❖ Data disaggregation by antimalarial-resistance strain of Plasmodium

Pollutants and climate hazards❖ Long-term prospective cohort/case-control studies of the effect of different pollutants from forest fires, wood smoke, charcoal, fugitive dust, silica, and other sources on different ADs

❖ Studies of seasonal variations of ADs and the impact of climatic factors on ADs in Africa

Psychosociologic factors❖ Robust data on the association between psychological factors and ADs in people of African ancestry around the world

❖ Cohort/case-control studies on individual and intersecting sociologic determinants of different ADs in Africans around the world

❖ Scrutiny of the impact of sociologic factors on the African autoimmune genome and epigenome

	
To allow more accurate conclusions and comparisons of data from Afro-descendants within and across different regions of the world, future studies will need to consistently report patients’ ancestry. This is important given that the terms race and ethnicity are social constructs whose classification varies with the geographic region and is expected to evolve with the advancement of societies’ knowledge.307,308 Accordingly, the use of the terms race and ethnicity may lead to selection, analysis and interpretation biases in studies.144,307 Indeed, the population of African ancestry is a multiracial population, and even the dark skin tone most commonly found in sub-Saharan Africa is found in all regions of the world because of the settlement of some sub-Saharan Africans outside Africa during the transatlantic slave trade.308 The specification “African ancestry/descent/heritage” together with clear information about individuals' geographic locations, will also help to uncover the specific effects of settling environments in the pathogenesis of ADs in people of African descent.144

There is also an urgent need for improved AD care in people of African descent worldwide. To provide holistic management of ADs in this population group, complementary and alternative therapies309 valued by patients of African ancestry (eg, spirituality and African herbal medicines111,136,310) need to be tested in robust randomized clinical trials including those patients, and implemented if definitely proven effective.310,311 Proactive social care measures also need to be implemented for patients with low socioeconomic status.141,312 This requires an unbiased implementation of DEI to ensure that health care professionals and patient representatives of African ancestry, who are more aware of cultural sensitivities of and challenges faced by people of African ancestry, are equitably represented on the boards of AD clinician and patient organizations and funding bodies.313, 314, 315 In Africa, where there are competing health interests,15,16,41 the best approach to AD care provision would require a paradigm shift that regards all ADs as a single disease landscape151,152 in existing noncommunicable disease programs.15 When grouped, ADs that broadly require similar management and biopathologic diagnostic procedures5,9,151,152,220 are not infrequent.10, 11, 12 The capitalization on ID programs, which are the most important health programs in Africa,17,25 could also help provide some resources for AD care on the continent.

Regulatory implementation of advances in the artificial intelligence and Internet landscape are expected to help improve the management of and research on ADs in Africa.316,317 These advances provide a great opportunity for distance learning, which can further increase awareness and interest in ADs among health care professionals on the continent.280 Additionally, they have the potential to facilitate networking, advocacy, and telemedicine activities among enthusiasts of autoimmunology in people of African descent around the world.318,319 Finally, these advances enable accurate data recording.29,320 This means that governments in Africa need to extend the supply of a symmetric Internet bandwidth across the continent and further develop electronic health record systems for an accurate record of data on ADs in Africa.11,12,29,280,320,321

Good partnerships between public health care facilities and private autoimmunity centers of excellence322,323 (Fig 3)15,16,38,58,136,151,152,280,288,289,309,310,324,325 are also expected to contribute to improving research on and care provision for ADs in Africa, as seen with other diseases on the continent326 and with ADs on other continents.152,318,322Fig 3 Proposed road map for establishing an autoimmunity center of excellence with integrated digital clinic in Africa.15,16,38,58,136,151,152,280,288,289,309,310,324,325 The Human Heredity and Health in Africa (H3Africa) consortium involves a a collaboration between the NIH and Wellcome Trust and the African Society of Human Genetics that has successfully led to a better understanding of genetic determinants of many diseases highly prevalent in individuals of African descent.325

Conclusion

There are increasing numbers of individuals diagnosed with ADs in the global population of African ancestry, especially those of sub-Saharan African ancestry whose data represent the bulk of data highlighted in this review. The increasing magnitude of ADs in this population could be due to genetic and sociologic factors, as well as to exposure to IDs and pollutants. To improve care and research on ADs in people of African descent, it is important that DEI be embraced and that governments in Africa harness the power of digital health. This will enable timely diagnosis and proper management of ADs in all persons of African ancestry, regardless of their geographic location, or social identity, just as is done for any other person of any other ancestral group.

Disclosure statement

Disclosure of potential conflict of interest: No funding was received for this research. The authors declare that they have no relevant conflicts of interest.

We express our gratitude to the authors who published the data that are referred to in this article.
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