Patients with Systemic Lupus Erythematosus with Anxiety or Depression: Clinical Characteristics, Food Intake, and Gut Microbiota Profile

Authors

  • Meutia Gebrina Department of Internal Medicine, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia.
  • Alvina Widhani 1. Department of Internal Medicine, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia. 2. Department of Internal Medicine, Cipto Mangunkusumo Hospital, Jakarta, Indonesia. 3. Universitas Indonesia Hospital, Depok, Indonesia
  • Rudi Putranto 1. Department of Internal Medicine, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia. 2. Department of Internal Medicine, Cipto Mangunkusumo Hospital, Jakarta, Indonesia.
  • Murdani Abdullah 1. Department of Internal Medicine, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia. 2. Department of Internal Medicine, Cipto Mangunkusumo Hospital, Jakarta, Indonesia.
  • Ikhwan Rinaldi 1. Department of Internal Medicine, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia. 2. Department of Internal Medicine, Cipto Mangunkusumo Hospital, Jakarta, Indonesia.
  • samsuridjal djauzi 1. Department of Internal Medicine, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia. 2. Department of Internal Medicine, Cipto Mangunkusumo Hospital, Jakarta, Indonesia.
  • Franciscus Dhyanagiri Suyatna Department of Pharmacology and Therapeutics, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Beti Ernawati Dewi Department of Microbiology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Andi Yasmon Department of Microbiology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Susan Rahayu Molecular Biology Unit, Integrated Laboratory, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Amalia Shabrina Asih Husada Hospital, Banjar, West Java, Indonesia.

Keywords:

anxiety, depression, gut microbiota, systemic lupus erythematosus

Abstract

Background: Depression and anxiety are prevalent among patients with systemic lupus erythematosus (SLE), and gut microbiota may be a contributing factor. This study aimed to investigate the clinical characteristics, food intake, and gut microbiota profiles of SLE patients with anxiety or depression. Methods: An analysis of secondary data was conducted. The primary study was conducted at Cipto Mangunkusumo Hospital, Jakarta, Indonesia, in 2017–2018. The inclusion criteria were: a diagnosis of SLE, age 18‒60 years, and gastrointestinal symptoms. The data collected included clinical data, food intake, anxiety and depression scores, SLE disease activity, and stool samples. Sequencing of the 16S rRNA gene was performed to profile the gut microbiota using DNA was extracted from the stool samples. Results: After excluding those with incomplete data, 41 patients were analyzed. Among the subjects, 53.66% and 14.63% had anxiety and depression, respectively. SLE patients with anxiety were significantly more likely to harbor Bacteroides compared to those without anxiety (33.45% vs. 9.78%; p=0.02) and had lower levels of complement C3 (78.72 vs. 100.85 mg/dL; p=0.03). SLE patients with anxiety or depression had significantly lower fat intake compared to those without these conditions (38.78 vs. 48.43 g/day; p=0.04, and 31.48 vs. 45.27 g/day; p=0.04). A significant correlation was observed between the proportion of Bacteroides and SLE disease activity (p=0.02). Conclusion: SLE patients with anxiety showed a significantly higher proportion of Bacteroides and a lower C3 level compared to those without anxiety. Fat intake was significantly lower among SLE patients with anxiety or depression compared to those without either condition

References

Tselios K, Gladman DD, Touma Z, et al. Disease course patterns in systemic lupus ery-thematosus. Lupus. 2019;28:114–22. doi: 10.1177/0961203318817132.

Figueiredo-Braga M, Cornaby C, Cortez A, et al. Depression and anxiety in systemic lupus erythematosus: the crosstalk between immunological, clinical, and psychosocial factors. Medicine. 2018;97(28):e11376. doi: 10.1097/MD.0000000000011376.

Zhang L, Fu T, Yin R, et al. Prevalence of depression and anxiety in systemic lupus ery-thematosus: a systematic review and meta-analysis. BMC Psychiatry. 2017;17(1):70. doi: 10.1186/s12888-017-1234-1.

Yao H, Yang H, Wang Y, Xing Q, Yan L, Chai Y. Gut microbiome and fecal metabolic alter-ation in systemic lupus erythematosus patients with depression. Front Cell Infect Micro-biol. 2022;12:1040211. doi: 10.3389/fcimb.2022.1040211.

Xiang S, Qu Y, Qian S, et al. Association between systemic lupus erythematosus and dis-ruption of gut microbiota: a meta-analysis. Lupus Sci Med. 2022;9(1): e000599. doi: 10.1136/lupus-2021-000599.

de Oliveira GLV, Leite AZ, Higuchi BS, et al. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology. 2017;152(1):1-12. doi: 10.1111/imm.12765.

Rogers GB, Keating DJ, Young RL, et al. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol Psychiatry. 2016;21(6):738-48. doi: 10.1038/mp.2016.50.

Taylor AM, Holscher HD. A review of dietary and microbial connections to depression, anxiety, and stress. Nutr Neurosci. 2020;23(3):237-50. doi: 10.1080/1028415X.2018.1493808.

Chen Y, Lin J, Xiao L, et al. Gut microbiota in systemic lupus erythematosus: a fuse and a solution. J Autoimmun. 2022;132:102867. doi: 10.1016/j.jaut.2022.102867.

Yao K, Xie Y, Wang J, et al. Gut microbiota: a newly identified environmental factor in systemic lupus erythematosus. Front Immunol. 2023;14:1202850. doi: 10.3389/fimmu.2023.1202850.

Pan Q, Guo F, Huang Y, et al. Gut microbiota dysbiosis in systemic lupus erythematosus: novel insights into mechanisms and promising therapeutic strategies. Front Immunol. 2021;12:799788. doi: 10.3389/fimmu.2021.799788.

Jeon SW, Kim YK. Inflammation-induced depression: its pathophysiology and therapeutic implications. J Neuroimmunol. 2017;313:92-8. doi: 10.1016/j.jneuroim.2017.10.016.

Widhani A, Djauzi S, Suyatna FD, et al. Changes in gut microbiota and systemic inflam-mation after synbiotic supplementation in patients with systemic lupus erythematosus: a randomized, double-blind, placebo-controlled trial. Cells. 2022;11(21):3419. doi: 10.3390/cells11213419.

Ardini W, Bardosono S. Using the dietary inflammatory index for assessing inflammatory potential of traditional cuisine from four ethnic groups in Indonesia. Journal of Food and Nutrition Research. 2020;8(4):168-71. doi: 10.12691/jfnr-8-4-2

Shivappa N, Steck SE, Hurley TG, et al. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17(8):1689-96. doi: 10.1017/S1368980013002115

Kwan A, Marzouk S, Ghanean H, et al. Assessment of the psychometric properties of pa-tient-reported outcomes of depression and anxiety in systemic lupus erythematosus. Semin Arthritis Rheum. 2019;49(2) 260-6. doi: 10.1016/j.semarthrit.2019.03.004.

de Almeida Macêdo E, Appenzeller S, Lavras Costallat LT. Assessment of the Hospital Anxiety and Depression Scale (HADS) performance for the diagnosis of anxiety in pa-tients with systemic lupus erythematosus. Rheumatol Int. 2017;37(12):1999-2004. doi: 10.1007/s00296-017-3819-x.

Moustafa AT, Moazzami M, Engel L, et al. Prevalence and metric of depression and anxi-ety in systemic lupus erythematosus: a systematic review and meta-analysis. Semin Ar-thritis Rheum. 2020;50(1):84-94. doi: 10.1016/j.semarthrit.2019.06.017. Epub 2019 Jun 28.

Bai R, Liu S, Zhao Y, et al. Depressive and anxiety disorders in systemic lupus erythema-tosus patients without major neuropsychiatric manifestations. J Immunol Res. 2016;2016:2829018. doi: 10.1155/2016/2829018.

Shatri H, Purnamandala, Hidayat R, et al. The correlation of anxiety and depression with C3 and C4 Levels and systemic lupus erythematosus activity. BMC Psychiatry. 2023;23(1):785. doi: 10.1186/s12888-023-05285-8.

Liu R, Xu H, Guo X, et al. Genomic characterization of two Escherichia fergusonii isolates harboring the mcr-1 gene from the farm environment. Front Cell Infect Microbiol. 2022;12:774494. doi: 10.3389/fcimb.2022.774494.

Chen Z, Xie Y, Zhou F, et al. Featured gut microbiomes associated with the progression of chronic hepatitis B disease. Front Microbiol. 2020;11:383. doi: 10.3389/fmicb.2020.00383.

Marciano F, Vajro P. Oxidative stress and gut microbiota. In: Gracia-Sancho J, Salvadó J, editors. Gastrointestinal Tissue. Academic Press; 2017. p.113-23. https://doi.org/10.1016/B978-0-12-805377-5.00008-4.

Zhao Y, Lukiw WJ. Bacteroidetes neurotoxins and inflammatory neurodegeneration. Mol Neurobiol. 2018;55(12):9100-7. doi: 10.1007/s12035-018-1015-y.

Gibiino G, Lopetuso LR, Scaldaferri F, et al. Exploring Bacteroidetes: metabolic key points and immunological tricks of our gut commensals. Dig Liver Dis. 2018;50(7):635-9. doi: 10.1016/j.dld.2018.03.016.

Toumi E, Mezouar S, Plauzolles A, et al. Gut microbiota in SLE: from animal models to clinical evidence and pharmacological perspectives. Lupus Sci Med. 2023;10(1):e000776. doi: 10.1136/lupus-2022-000776.

Zhang L, Qing P, Yang H, et al. Gut microbiome and metabolites in systemic lupus ery-thematosus: link, mechanisms, and intervention. Front Immunol. 2021;12:686501. doi: 10.3389/fimmu.2021.686501.

Krupa-Kotara K, Gwiozdzik W, Nandzik S, et al. The role of microbiota pattern in anxiety and stress disorders—a review of the state of knowledge. Psych. 2023;5:602–18. doi: 10.3390/psych5030038

Zhang Y, Gan M, He Y, et al. Anxiety disorders and gut dysbiosis in primary Sjogren's syn-drome-mediated dry eye patients. Int J Gen Med. 2023;16:1735-46. doi: 10.2147/IJGM.S405225.

Jacobs JP, Lagishetty V, Hauer MC, et al. Multi-omics profiles of the intestinal microbi-ome in irritable bowel syndrome and its bowel habit subtypes. Microbiome. 2023;11(1):5. doi: 10.1186/s40168-022-01450-5.

Ritz NL, Brocka M, Butler MI, et al. Social anxiety disorder- associated gut microbiota in-creases social fear. Proc Natl Acad Sci USA. 2024;121(1):e2308706120. doi: 10.1073/pnas.2308706120.

Sudo N. Microbiome, HPA axis and production of endocrine hormones in the gut. Adv Exp Med Biol. 2014;817:177-94. doi: 10.1007/978-1-4939-0897-4_8.

Jiang H, Ling Z, Zhang Y, et al. Altered fecal microbiota composition in patients with ma-jor depressive disorder. Brain Behav Immun. 2015;48:186-94. doi: 10.1016/j.bbi.2015.03.016.

Nguyen TT, Kosciolek T, Maldonado Y, et al. Differences in gut microbiome composition between persons with chronic schizophrenia and healthy comparison subjects. Schizophr Res. 2019;204:23-9. doi: 10.1016/j.schres.2018.09.014.

Qing Y, Xu L, Cui G, et al. Salivary microbiome profiling reveals a dysbiotic schizophrenia-associated microbiota. NPJ Schizophr. 2021;7(1):51. doi: 10.1038/s41537-021-00180-1.

Mosca A, Leclerc M, Hugot JP. Gut microbiota diversity and human diseases: Should we reintroduce key predators in our ecosystem? Front Microbiol. 2016;7:1–12. doi: 10.3389/fmicb.2016.00455.

Chen J, Siliceo SL, Ni Y, et al. Identification of robust and generalizable biomarkers for microbiome-based stratification in lifestyle interventions. Microbiome. 2023;11(1):178. doi: 10.1186/s40168-023-01604-z.

Hiippala K, Kainulainen V, Kalliomäki M, et al. Mucosal prevalence and interactions with the epithelium indicate commensalism of Sutterella spp. Front Microbiol. 2016;7:1706. doi: 10.3389/fmicb.2016.01706.

Van den Abbeele P, Belzer C, Goossens M, et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J. 2013;7(5):949-61. doi: 10.1038/ismej.2012.158.

Zhang P. Influence of foods and nutrition on the gut microbiome and implications for in-testinal health. Int J Mol Sci. 2022;23(17):9588. doi: 10.3390/ijms23179588.

Kumar A, Pramanik J, Goyal N, et al. Gut microbiota in anxiety and depression: Unveiling the relationships and management options. Pharmaceuticals (Basel). 2023;16(4):565. doi: 10.3390/ph16040565.

Downloads

Additional Files

Published

2025-10-03

How to Cite

Gebrina, M., Widhani, A., Putranto, R., Abdullah, M., Rinaldi, I., djauzi, samsuridjal, Suyatna, F. D., Dewi, B. E., Yasmon, A., Rahayu, S., & Shabrina, A. (2025). Patients with Systemic Lupus Erythematosus with Anxiety or Depression: Clinical Characteristics, Food Intake, and Gut Microbiota Profile. Acta Medica Indonesiana, 57(3), 295. Retrieved from http://www.actamedindones.org/index.php/ijim/article/view/2803