Role of the Microbiome and Its Metabolites in Primary Sjögren’s Syndrome
Abstract
1. Introduction
2. Microbiome in Health: Oral, Ocular, Gut, and Blood
2.1. Oral Microbiome
- Gram-positive cocci: Abiotrophia, Peptostreptococcus, Streptococcus, and Stomatococcus.
- Gram-positive bacilli: Actinomyces, Bifidobacterium, Corynebacterium, Eubacterium, Lactobacillus, Propionibacterium, Pseudoramibacter, and Rothia.
- Gram-negative cocci: Moraxella, Neisseria, and Veillonella.
- Gram-negative bacilli: Campylobacter, Capnocytophaga, Desulfobacter Desulfovibrio, Eikenella, Fusobacterium, Haemophilus, Leptotrichia, Prevotella, Selenomonas, Simonsiella, Treponema, and Wolinella.
- Fungi: Candida, Cladosporium, Aureobasidium, Saccharomycetales, Aspergillus, Fusarium, and Cryptococcus.
- Virus: Bacteriophages [8].
2.2. Ocular Microbiome
2.3. Gut Microbiome
2.4. Blood Microbiome
3. Dysbiosis in pSS
4. Bacterial Metabolites and Their Importance in pSS
4.1. Short-Chain Fatty Acids (SCFAs)
4.2. Choline, Trimethylamine (TMA), and Trimethylamine-N-Oxide (TMAO)
4.3. Taurine
4.4. Serine (Another Important Amino Acid)
4.5. Lactate
4.6. Tryptophan and Kynurenine
4.7. Additional Metabolites of Interest
5. Clinical Applications
6. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Longhino, S.; Chatzis, L.G.; Dal Pozzolo, R.; Peretti, S.; Fulvio, G.; La Rocca, G.; Garcia, I.C.N.; Orlandi, M.; Quartuccio, L.; Baldini, C.; et al. Sjögren’s syndrome: One year in review 2023. Clin. Exp. Rheumatol. 2023, 41, 2343–2356. [Google Scholar] [CrossRef]
- Negrini, S.; Emmi, G.; Greco, M.; Borro, M.; Sardanelli, F.; Murdaca, G.; Indiveri, F.; Puppo, F. Sjögren’s syndrome: A systemic autoimmune disease. Clin. Exp. Med. 2022, 22, 9–25. [Google Scholar] [CrossRef] [PubMed]
- Shiboski, C.H.; Shiboski, S.C.; Seror, R.; Criswell, L.A.; Labetoulle, M.; Lietman, T.M.; Rasmussen, A.; Scofield, H.; Vitali, C.; Bowman, S.J.; et al. 2016 American College of Rheumatology/European League Against Rheumatism Classification Criteria for Primary Sjögren’s Syndrome: A Consensus and Data-Driven Methodology Involving Three International Patient Cohorts. Arthritis Rheumatol. 2017, 69, 35–45. [Google Scholar] [CrossRef] [PubMed]
- Björk, A.; Mofors, J.; Wahren-Herlenius, M. Environmental factors in the pathogenesis of primary Sjögren’s syndrome. J. Intern. Med. 2020, 287, 475–492. [Google Scholar] [CrossRef] [PubMed]
- Deng, C.; Xiao, Q.; Fei, Y. A Glimpse Into the Microbiome of Sjögren’s Syndrome. Front. Immunol. 2022, 13, 918619. [Google Scholar] [CrossRef]
- Liu, J.; Tan, Y.; Cheng, H.; Zhang, D.; Feng, W.; Peng, C. Functions of Gut Microbiota Metabolites, Current Status and Future Perspectives. Aging Dis. 2022, 13, 1106–1126. [Google Scholar] [CrossRef]
- Hou, K.; Wu, Z.-X.; Chen, X.-Y.; Wang, J.-Q.; Zhang, D.; Xiao, C.; Zhu, D.; Koya, J.B.; Wei, L.; Li, J.; et al. Microbiota in health and diseases. Signal Transduct. Target. Ther. 2022, 7, 135. [Google Scholar] [CrossRef]
- Morrison, A.G.; Sarkar, S.; Umar, S.; Lee, S.T.M.; Thomas, S.M. The Contribution of the Human Oral Microbiome to Oral Disease: A Review. Microorganisms 2023, 11, 318. [Google Scholar] [CrossRef]
- Aragona, P.; Baudouin, C.; Benitez del Castillo, J.M.; Messmer, E.; Barabino, S.; Merayo-Lloves, J.; Brignole-Baudouin, F.; Inferrera, L.; Rolando, M.; Mencucci, R.; et al. The ocular microbiome and microbiota and their effects on ocular surface pathophysiology and disorders. Surv. Ophthalmol. 2021, 66, 907–925. [Google Scholar] [CrossRef]
- GEM Project Research Consortium; Turpin, W.; Espin-Garcia, O.; Xu, W.; Silverberg, M.S.; Kevans, D.; Smith, M.I.; Guttman, D.S.; Griffiths, A.; Panaccione, R.; et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat. Genet. 2016, 48, 1413–1417. [Google Scholar] [CrossRef]
- Dupont, H.L.; Jiang, Z.D.; Dupont, A.W.; Utay, N.S. the intestinal microbiome in human health and disease. Trans. Am. Clin. Climatol. Assoc. 2020, 131, 178. [Google Scholar]
- Païssé, S.; Valle, C.; Servant, F.; Courtney, M.; Burcelin, R.; Amar, J.; Lelouvier, B. Comprehensive description of blood microbiome from healthy donors assessed by 16S targeted metagenomic sequencing. Transfusion 2016, 56, 1138–1147. [Google Scholar] [CrossRef] [PubMed]
- Tan, C.C.S.; Ko, K.K.K.; Chen, H.; Liu, J.; Loh, M.; Chia, M.; Nagarajan, N. No evidence for a common blood microbiome based on a population study of 9770 healthy humans. Nat. Microbiol. 2023, 8, 973–985. [Google Scholar] [CrossRef]
- Li, M.; Zou, Y.; Jiang, Q.; Jiang, L.; Yu, Q.; Ding, X.; Yu, Y. A preliminary study of the oral microbiota in Chinese patients with Sjögren’s syndrome. Arch. Oral Biol. 2016, 70, 143–148. [Google Scholar] [CrossRef]
- De Paiva, C.S.; Jones, D.B.; Stern, M.E.; Bian, F.; Moore, Q.L.; Corbiere, S.; Streckfus, C.F.; Hutchinson, D.S.; Ajami, N.J.; Petrosino, J.F.; et al. Altered Mucosal Microbiome Diversity and Disease Severity in Sjögren Syndrome. Sci. Rep. 2016, 6, 23561. [Google Scholar] [CrossRef]
- Siddiqui, H.; Chen, T.; Aliko, A.; Mydel, P.M.; Jonsson, R.; Olsen, I. Microbiological and bioinformatics analysis of primary Sjögren’s syndrome patients with normal salivation. J. Oral Microbiol. 2016, 8, 31119. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.C.; Ham, B.; Kang, K.D.; Yun, J.M.; Kwon, M.J.; Kim, H.S.; Bin Hwang, H. Bacterial distribution on the ocular surface of patients with primary Sjögren’s syndrome. Sci. Rep. 2022, 12, 1715. [Google Scholar] [CrossRef]
- Song, H.; Xiao, K.; Chen, Z.; Long, Q. Analysis of Conjunctival Sac Microbiome in Dry Eye Patients with and Without Sjögren’s Syndrome. Front. Med. 2022, 9, 841112. [Google Scholar] [CrossRef] [PubMed]
- van der Meulen, T.A.; Harmsen, H.J.M.; Vila, A.V.; Kurilshikov, A.; Liefers, S.C.; Zhernakova, A.; Fu, J.; Wijmenga, C.; Weersma, R.K.; de Leeuw, K.; et al. Shared gut, but distinct oral microbiota composition in primary Sjögren’s syndrome and systemic lupus erythematosus. J. Autoimmun. 2019, 97, 77–87. [Google Scholar] [CrossRef]
- Mandl, T.; Marsal, J.; Olsson, P.; Ohlsson, B.; Andréasson, K. Severe intestinal dysbiosis is prevalent in primary Sjögren’s syndrome and is associated with systemic disease activity. Arthritis Res. Ther. 2017, 19, 237. [Google Scholar] [CrossRef]
- Cao, Y.; Lu, H.; Xu, W.; Zhong, M. Gut microbiota and Sjögren’s syndrome: A two-sample Mendelian randomization study. Front. Immunol. 2023, 14, 1187906. [Google Scholar] [CrossRef] [PubMed]
- Santacroce, L.; Charitos, I.A.; Colella, M.; Palmirotta, R.; Jirillo, E. Blood Microbiota and Its Products: Mechanisms of Interference with Host Cells and Clinical Outcomes. Hematol. Rep. 2024, 16, 440–453. [Google Scholar] [CrossRef]
- Hammad, D.B.M.; Hider, S.L.; Liyanapathirana, V.C.; Tonge, D.P. Molecular Characterization of Circulating Microbiome Signatures in Rheumatoid Arthritis. Front. Cell Infect. Microbiol. 2020, 9, 498741. [Google Scholar] [CrossRef] [PubMed]
- Acharya, A.; Chan, Y.; Kheur, S.; Kheur, M.; Gopalakrishnan, D.; Watt, R.; Mattheos, N. Salivary microbiome of an urban Indian cohort and patterns linked to subclinical inflammation. Oral Dis. 2017, 23, 926–940. [Google Scholar] [CrossRef]
- Li, B.-Z.; Zhou, H.-Y.; Guo, B.; Chen, W.-J.; Tao, J.-H.; Cao, N.-W.; Chu, X.-J.; Meng, X. Dysbiosis of oral microbiota is associated with systemic lupus erythematosus. Arch. Oral Biol. 2020, 113, 104708. [Google Scholar] [CrossRef] [PubMed]
- Qi, Y.; Wan, Y.; Li, T.; Zhang, M.; Song, Y.; Hu, Y.; Sun, Y.; Li, L. Comparison of the Ocular Microbiomes of Dry Eye Patients with and Without Autoimmune Disease. Front. Cell. Infect. Microbiol. 2021, 11, 716867. [Google Scholar] [CrossRef]
- De Luca, F.; Shoenfeld, Y. The microbiome in autoimmune diseases. Clin. Exp. Immunol. 2018, 195, 74–85. [Google Scholar] [CrossRef]
- Bellando-Randone, S.; Russo, E.; Venerito, V.; Matucci-Cerinic, M.; Iannone, F.; Tangaro, S.; Amedei, A. Exploring the Oral Microbiome in Rheumatic Diseases, State of Art and Future Prospective in Personalized Medicine with an AI Approach. J. Pers. Med. 2021, 11, 625. [Google Scholar] [CrossRef]
- Zhao, T.; Wei, Y.; Zhu, Y.; Xie, Z.; Hai, Q.; Li, Z.; Qin, D. Gut microbiota and rheumatoid arthritis: From pathogenesis to novel therapeutic opportunities. Front. Immunol. 2022, 13, 1007165. [Google Scholar] [CrossRef]
- Haase, S.; Haghikia, A.; Wilck, N.; Müller, D.N.; Linker, R.A. Impacts of microbiome metabolites on immune regulation and autoimmunity. Immunology 2018, 154, 230–238. [Google Scholar] [CrossRef]
- Furusawa, Y.; Obata, Y.; Fukuda, S.; Endo, T.A.; Nakato, G.; Takahashi, D.; Nakanishi, Y.; Uetake, C.; Kato, K.; Kato, T.; et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013, 504, 446–450. [Google Scholar] [CrossRef]
- Kim, D.S.; Woo, J.S.; Min, H.-K.; Choi, J.-W.; Moon, J.H.; Park, M.-J.; Kwok, S.-K.; Park, S.-H.; Cho, M.-L. Short-chain fatty acid butyrate induces IL-10-producing B cells by regulating circadian-clock-related genes to ameliorate Sjögren’s syndrome. J. Autoimmun. 2021, 119, 102611. [Google Scholar] [CrossRef]
- Yang, L.; Xiang, Z.; Zou, J.; Zhang, Y.; Ni, Y.; Yang, J. Comprehensive Analysis of the Relationships Between the Gut Microbiota and Fecal Metabolome in Individuals with Primary Sjogren’s Syndrome by 16S rRNA Sequencing and LC–MS-Based Metabolomics. Front. Immunol. 2022, 13, 874021. [Google Scholar] [CrossRef]
- Woo, J.S.; Hwang, S.-H.; Yang, S.C.; Lee, K.H.; Lee, Y.S.; Choi, J.W.; Park, J.-S.; Jhun, J.; Park, S.-H.; Cho, M.-L. Lactobacillus acidophilus and propionate attenuate Sjögren’s syndrome by modulating the STIM1-STING signaling pathway. Cell Commun. Signal. 2023, 21, 135. [Google Scholar] [CrossRef] [PubMed]
- Alt-Holland, A.; Huang, X.; Mendez, T.; Singh, M.L.; Papas, A.S.; Cimmino, J.; Bairos, T.; Tzavaras, E.; Foley, E.; Pagni, S.E.; et al. Identification of Salivary Metabolic Signatures Associated with Primary Sjögren’s Disease. Molecules 2023, 28, 5891. [Google Scholar] [CrossRef] [PubMed]
- Teo, A.W.J.; Zhang, J.; Zhou, L.; Liu, Y.C. Metabolomics in Corneal Diseases: A Narrative Review from Clinical Aspects. Metabolites 2023, 13, 380. [Google Scholar] [CrossRef]
- Wei, Y.; Asbell, P.A. sPLA2-IIa participates in ocular surface inflammation in humans with dry eye disease. Exp. Eye Res. 2020, 201, 108209. [Google Scholar] [CrossRef]
- Chittim, C.L.; Martínez del Campo, A.; Balskus, E.P. Gut bacterial phospholipase Ds support disease-associated metabolism by generating choline. Nat. Microbiol. 2018, 4, 155–163. [Google Scholar] [CrossRef] [PubMed]
- Caradonna, E.; Abate, F.; Schiano, E.; Paparella, F.; Ferrara, F.; Vanoli, E.; Difruscolo, R.; Goffredo, V.M.; Amato, B.; Setacci, C.; et al. Trimethylamine-N-Oxide (TMAO) as a Rising-Star Metabolite: Implications for Human Health. Metabolites 2025, 15, 220. [Google Scholar] [CrossRef]
- Salah, M.; Shemies, R.S.; Elsherbeny, M.; Faisal, S.; Enein, A. The Gut Microbe-Derived Metabolite Trimethylamine N-Oxide in Patients with Systemic Lupus Erythematosus. Scr. Med. 2024, 55, 43–52. [Google Scholar] [CrossRef]
- Stec, A.; Maciejewska, M.; Paralusz-Stec, K.; Michalska, M.; Giebułtowicz, J.; Rudnicka, L.; Sikora, M. The Gut Microbial Metabolite Trimethylamine N-Oxide is Linked to Specific Complications of Systemic Sclerosis. J. Inflamm. Res. 2023, 16, 1895–1904. [Google Scholar] [CrossRef] [PubMed]
- Coras, R.; Kavanaugh, A.; Boyd, T.; Huynh, D.; Lagerborg, K.A.; Xu, Y.-J.; Rosenthal, S.B.; Jain, M.; Guma, M. Choline metabolite, Trimethylamine N-Oxide (TMAO), is associated with inflammation in psoriatic arthritis. Clin. Exp. Rheumatol. 2019, 37, 481. [Google Scholar] [PubMed]
- Ripps, H.; Shen, W. Review: Taurine: A “very essential” amino acid. Mol. Vis. 2012, 18, 2673. [Google Scholar] [PubMed]
- Qaradakhi, T.; Gadanec, L.K.; McSweeney, K.R.; Abraham, J.R.; Apostolopoulos, V.; Zulli, A. The Anti-Inflammatory Effect of Taurine on Cardiovascular Disease. Nutrients 2020, 12, 2847. [Google Scholar] [CrossRef]
- Herrala, M.; Mikkonen, J.J.W.; Pesonen, P.; Lappalainen, R.; Tjäderhane, L.; Niemelä, R.K.; Seitsalo, H.; Salo, T.; Myllymaa, S.; Kullaa, A.M. Variability of salivary metabolite levels in patients with Sjögren’s syndrome. J. Oral Sci. 2021, 63, 22–26. [Google Scholar] [CrossRef]
- Urbanski, G.; Assad, S.; Chabrun, F.; Chao de la Barca, J.M.; Blanchet, O.; Simard, G.; Lenaers, G.; Prunier-Mirebeau, D.; Gohier, P.; Lavigne, C.; et al. Tear metabolomics highlights new potential biomarkers for differentiating between Sjögren’s syndrome and other causes of dry eye. Ocul. Surf. 2021, 22, 110–116. [Google Scholar] [CrossRef] [PubMed]
- Nobuhara, Y.; Kawano, S.; Kageyama, G.; Sugiyama, D.; Saegusa, J.; Kumagai, S. Is SS-A/Ro52 a Hydrogen Peroxide-Sensitive Signaling Molecule? Antioxid. Redox Signal. 2007, 9, 385–391. [Google Scholar] [CrossRef]
- Ryo, K.; Yamada, H.; Nakagawa, Y.; Tai, Y.; Obara, K.; Inoue, H.; Mishima, K.; Saito, I. Possible Involvement of Oxidative Stress in Salivary Gland of Patients with Sjögren’s Syndrome. Pathobiology 2007, 73, 252–260. [Google Scholar] [CrossRef]
- Xu, J.; Chen, C.; Yin, J.; Fu, J.; Yang, X.; Wang, B.; Yu, C.; Zheng, L.; Zhang, Z. Lactate-induced mtDNA Accumulation Activates cGAS-STING Signaling and the Inflammatory Response in Sjögren’s Syndrome. Int. J. Med. Sci. 2023, 20, 1256–1271. [Google Scholar] [CrossRef]
- Apaydın, H.; Bicer, C.K.; Yurt, E.F.; Serdar, M.A.; Dogan, İ.; Erten, S. Elevated Kynurenine Levels in Patients with Primary Sjögren’s Syndrome. Lab. Med. 2023, 54, 166–172. [Google Scholar] [CrossRef]
- Pertovaara, M.; Raitala, A.; Uusitalo, H.; Pukander, J.; Helin, H.; Oja, S.S.; Hurme, M. Mechanisms dependent on tryptophan catabolism regulate immune responses in primary Sjögren’s syndrome. Clin. Exp. Immunol. 2005, 142, 155–161. [Google Scholar] [CrossRef] [PubMed]
- Eryavuz Onmaz, D.; Tezcan, D.; Abusoglu, S.; Sak, F.; Humeyra Yerlikaya, F.; Yilmaz, S.; Abusoglu, G.; Korez, M.K.; Unlu, A. Impaired kynurenine metabolism in patients with primary Sjögren’s syndrome. Clin. Biochem. 2023, 114, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Dehhaghi, M.; Kazemi Shariat Panahi, H.; Heng, B.; Guillemin, G.J. The Gut Microbiota, Kynurenine Pathway, and Immune System Interaction in the Development of Brain Cancer. Front. Cell Dev. Biol. 2020, 8, 562812. [Google Scholar] [CrossRef]
- de Oliveira, F.R.; Fantucci, M.Z.; Adriano, L.; Valim, V.; Cunha, T.M.; Louzada-Junior, P.; Rocha, E.M. Neurological and Inflammatory Manifestations in Sjögren’s Syndrome: The Role of the Kynurenine Metabolic Pathway. Int. J. Mol. Sci. 2018, 19, 3953. [Google Scholar] [CrossRef]
- Golpour, F.; Abbasi-Alaei, M.; Babaei, F.; Mirzababaei, M.; Parvardeh, S.; Mohammadi, G.; Nassiri-Asl, M. Short chain fatty acids, a possible treatment option for autoimmune diseases. Biomed. Pharmacother. 2023, 163, 114763. [Google Scholar] [CrossRef]
- Freguia, C.F.; Pascual, D.W.; Fanger, G.R. Sjögren’s Syndrome Treatments in the Microbiome Era. Adv. Geriatr. Med. Res. 2023, 5, e230004. [Google Scholar] [CrossRef]
- Low, C.E.; Loke, S.; Chew, N.S.M.; Lee, A.R.Y.B.; Tay, S.H. Vitamin, antioxidant and micronutrient supplementation and the risk of developing incident autoimmune diseases: A systematic review and meta-analysis. Front. Immunol. 2024, 15, 1453703. [Google Scholar] [CrossRef] [PubMed]
Oral Microbiome
|
Ocular Microbiome
|
Gut Microbiome
|
Blood Microbiome
| |
---|---|---|---|---|
Phyla and genera in HS | Abiotrophy, Peptostreptococcus, Streptococcus, Stomatococcus, Actinomyces, Bifidobacterium, Corynebacterium, Moraxella, Neisseria, Veillonella, Hemophilus, Leptotrichia, Prevotella, Selemonas, Treponema, Wolinella, and Fusobacterium nucleatum [8]. | Staphylococcus, Corynebacterium, Streptococcus, Micrococcus, Kokuria, Propionibacterium, Haemophilus spp., Neisseria spp., Pseudomonas spp., Acinetobacter, Sphingomonas, and Brevundimona [9]. | Firmicutes, Bacteroidetes, Actinomycetes, Faecalibacterium prausnitzii, Proteobacteria, Eubacterium, Ruminococcus, Lactobacillus, bifidobacterium, Escherichia, Bacteroides, Saccharomyces, and Clostridium [11]. | Staphylococcus spp. Proteobacteria, Cutibacterium acnes, Alcaligenes, Caulobacter, Bradyrhizobium, and Sphingomonas [12]. |
Phyla and genera in patients with pSS | ↑Proteobacteria and Streptoccocus ↓ Leucobacter, Delftia, Pseudochrobactrum, Ralstonia, Mitsuaria, Fusobacterium, Fretibacterium, and Porphyromonas [14,15,16]. | ↑Acinetobacter, Corynebacterium, and Geobacillus ↓Bacillus spp. [17,18]. | ↑Escherichia/Shigella and Streptococcus ↓ Alistipes, Bifidobacterium Faecalibacterium prausnitzii, Bacteroides fragilis, Lachnoclostridium, Roseburia, Lachnospira, and Ruminococcus [19,20,21]. | Not reported, possible participation of Actinomyces and Halomonas genera [22]. |
Phyla and genera in patients with SLE | ↑Lactobacillaceae, Veillonellaceae, and Moraxellaceae ↓Corynebacteriaceae, Micrococcaceae, Phyllobacteriaceae, Methylobacteriaceae, Sphingomonadaceae, Halomonadaceae, Pseudomonadaceae, and Xanthomonadaceae [25]. | ↑Actinobacteria, Firmicutes, Bacteroidetes, Corynebacterium, Streptococcus, and Prevotella ↓Pelomonas and Herbaspirillum [26]. | ↑Rhodococcus, Eggerthella, Klebsiella, Prevotella, Eubacterium, and Flavonifractor [27]. | ↑Desulfoconvexum, Desulfofrigus, Desulfovibrio, Draconibacterium, Planococcus, Psychrilyobacter, and Gemmatimonadete [22]. |
Phyla and genera in patients with RA | ↑Porphyromonas gingivalis, A. actinomycetemcomitans, Cryptobacterium curtum, P. intermedia/Tannerella forsythia Prevotella, and Leptotrichia [28]. | ↑Corynebacterium, Streptococcus, and Prevotella ↓Pelomonas and Herbaspirillum [27]. | ↑Prevotella copri, Lactobacillus spp., Lactobacillus salivarius, Collinsella, and Akkermansia ↓ Bacteroidetes, Bifidobacteria, Eubacterium rectale, and Haemophilus spp. [29]. | ↑Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria Halomonas, and Shewanella [23]. |
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Corona-Angeles, J.A.; Martínez-Pulido, R.L.; Oregon-Romero, E.; Palafox-Sánchez, C.A. Role of the Microbiome and Its Metabolites in Primary Sjögren’s Syndrome. Microorganisms 2025, 13, 1979. https://doi.org/10.3390/microorganisms13091979
Corona-Angeles JA, Martínez-Pulido RL, Oregon-Romero E, Palafox-Sánchez CA. Role of the Microbiome and Its Metabolites in Primary Sjögren’s Syndrome. Microorganisms. 2025; 13(9):1979. https://doi.org/10.3390/microorganisms13091979
Chicago/Turabian StyleCorona-Angeles, Jazz Alan, Roxana Lizbeth Martínez-Pulido, Edith Oregon-Romero, and Claudia Azucena Palafox-Sánchez. 2025. "Role of the Microbiome and Its Metabolites in Primary Sjögren’s Syndrome" Microorganisms 13, no. 9: 1979. https://doi.org/10.3390/microorganisms13091979
APA StyleCorona-Angeles, J. A., Martínez-Pulido, R. L., Oregon-Romero, E., & Palafox-Sánchez, C. A. (2025). Role of the Microbiome and Its Metabolites in Primary Sjögren’s Syndrome. Microorganisms, 13(9), 1979. https://doi.org/10.3390/microorganisms13091979