Anti-Toxoplasma gondii antibodies as a risk factor for the prevalence and severity of systemic lupus erythematosus

Zhongzhen Li; Zhiwei Lei; Wanying Yang; Chunxia Jing; Xiaolin Sun; Guang Yang; Xiaozhen Zhao; Mingjiao Zhang; Miaomiao Xu; Yuanjia Tang; Qingwen Wang; Jing Zhao; Zixing Zhou; Zihao Wen; Xiaojing Chen; Qinglin Peng; Guochun Wang; Pingjing Zhang; Erwei Sun; Nan Shen; Weiguo Xu; Zhanguo Li; Hengwen Yang; Zhinan Yin

doi:10.1186/s13071-024-06141-8

Anti-Toxoplasma gondii antibodies as a risk factor for the prevalence and severity of systemic lupus erythematosus

Parasit Vectors. 2024 Jan 30;17(1):44. doi: 10.1186/s13071-024-06141-8.

Authors

Zhongzhen Li^#¹, Zhiwei Lei^#², Wanying Yang¹, Chunxia Jing^{3

4}, Xiaolin Sun⁵, Guang Yang⁶, Xiaozhen Zhao⁵, Mingjiao Zhang^{7

8}, Miaomiao Xu¹, Yuanjia Tang⁹, Qingwen Wang¹⁰, Jing Zhao⁵, Zixing Zhou³, Zihao Wen³, Xiaojing Chen³, Qinglin Peng¹¹, Guochun Wang¹¹, Pingjing Zhang⁹, Erwei Sun^{7

8}, Nan Shen⁹, Weiguo Xu¹², Zhanguo Li^#⁵, Hengwen Yang^#¹³, Zhinan Yin^#^{14

15}

Affiliations

¹ Guangdong Provincial Key Laboratory of Tumor Interventional Diagnosis and Treatment, Zhuhai Institute of Translational Medicine, Zhuhai People's Hospital (Zhuhai Clinical Medical College of Jinan University), Jinan University, Zhuhai, 519000, China.
² Department of Basic Medical Research, The Sixth Affiliated Hospital of Guangzhou Medical University, Qingyuan People's Hospital, Qingyuan, 511518, China.
³ Department of Epidemiology, School of Medicine, Jinan University, Guangzhou, 510632, China.
⁴ Guangdong Key Laboratory of Environmental Pollution and Health, Jinan University, Guangzhou, 510632, China.
⁵ Department of Rheumatology and Immunology, Peking University People's Hospital and Beijing Key Laboratory for Rheumatism Mechanism and Immune Diagnosis (BZ0135), Beijing, 100034, China.
⁶ Department of Pathogen Biology, School of Medicine, Jinan University, Guangzhou, 510632, China.
⁷ Department of Rheumatology and Immunology, The Third Affiliated Hospital, Southern Medical University, Guangzhou, 510630, China.
⁸ Institute of Clinical Immunology, Academy of Orthopedics Guangdong Province, Guangzhou, 510630, China.
⁹ Shanghai Institute of Rheumatology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200001, China.
¹⁰ Department of Rheumatism and Immunology, Peking University Shenzhen Hospital, Shenzhen, 518036, China.
¹¹ Department of Rheumatology, Beijing Key Lab for Immune-Mediated Inflammatory Diseases, China-Japan Friendship Hospital, Beijing, 100029, China.
¹² Guangdong Provincial Key Laboratory of Tumor Interventional Diagnosis and Treatment, Zhuhai Institute of Translational Medicine, Zhuhai People's Hospital (Zhuhai Clinical Medical College of Jinan University), Jinan University, Zhuhai, 519000, China. xwg315@163.com.
¹³ Guangdong Provincial Key Laboratory of Tumor Interventional Diagnosis and Treatment, Zhuhai Institute of Translational Medicine, Zhuhai People's Hospital (Zhuhai Clinical Medical College of Jinan University), Jinan University, Zhuhai, 519000, China. hengwenyang@jnu.edu.cn.
¹⁴ Guangdong Provincial Key Laboratory of Tumor Interventional Diagnosis and Treatment, Zhuhai Institute of Translational Medicine, Zhuhai People's Hospital (Zhuhai Clinical Medical College of Jinan University), Jinan University, Zhuhai, 519000, China. tzhinan@jnu.edu.cn.
¹⁵ Department of Basic Medical Research, The Sixth Affiliated Hospital of Guangzhou Medical University, Qingyuan People's Hospital, Qingyuan, 511518, China. tzhinan@jnu.edu.cn.

^# Contributed equally.

Abstract

Background: Systemic lupus erythematosus (SLE) is a complex systemic autoimmune disease characterized by the presence of numerous autoantibodies. The interaction of infectious agents (viruses, bacteria and parasites) and a genetically susceptible host may be a key mechanism for SLE. Toxoplasma gondii is a widespread intracellular parasite that has been implicated in the pathogenesis of autoimmune diseases. However, the relationship between T. gondii infection and the increased risk of SLE in Chinese populations remains unclear.

Methods: The seroprevalence of T. gondii infection was assessed in 1771 serum samples collected from Chinese individuals (908 healthy controls and 863 SLE patients) from different regions of China using an enzyme-linked immunosorbent assay. Serum autoantibodies and clinical information were obtained and analysed.

Results: Our observations revealed a higher prevalence of anti-T. gondii antibodies (ATxA) immunoglobulin G (IgG) in serum samples from SLE patients (144/863, 16.7%) than in those from the healthy controls (53/917, 5.8%; P < 0.0001), indicating a 2.48-fold increased risk of SLE in the ATxA-IgG⁺ population, after adjustment for age and sex (95% confidence interval [CI] 1.70-3.62, P < 0.0001). ATxA-IgG⁺ SLE patients also showed a 1.75-fold higher risk of developing moderate and severe lupus symptoms (95% CI 1.14-2.70, P = 0.011) compared to ATxA-IgG^- patients. Relative to ATxA-IgG^- patients, ATxA-IgG⁺ patients were more likely to develop specific clinical symptoms, including discoid rash, oral ulcer, myalgia and alopecia. Seven antibodies, namely anti-ribosomal RNA protein (rRNP), anti-double stranded DNA (dsDNA), anti-cell membrane DNA (cmDNA), anti-scleroderma-70 (Scl-70), anti-cardiolipin (CL), anti-beta2-glycoprotein-I (B2GPI) and rheumatoid factor (RF), occurred more frequently in ATxA-IgG⁺ patients. When combined with anti-dsDNA and RF/anti-rRNP/anti-cmDNA/ESR, ATxA-IgG significantly increased the risk for severe lupus.

Conclusions: Our results suggest that ATxA-IgG may be a significant risk factor for SLE prevalence and severity in Chinese populations.

Keywords: Autoantibody; Risk factor; SLE; Toxoplasma gondii.

MeSH terms

Autoantibodies*
DNA
Humans
Immunoglobulin G
Lupus Erythematosus, Systemic* / complications
Lupus Erythematosus, Systemic* / epidemiology
Prevalence
Risk Factors
Seroepidemiologic Studies

Substances

Autoantibodies
Immunoglobulin G
DNA

Abstract

MeSH terms

Substances

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