Connection between Celiac Disease and Systemic Lupus Erythematosus in Children—A Development Model of Autoimmune Diseases Starting from What We Inherit to What We Eat

Celiac disease (CD) and systemic lupus erythematosus (SLE) are two diseases intensively studied in all age groups, with an increasing incidence at the global level, possibly due to the increased awareness of the diseases and their accurate diagnosis and as a consequence of the new research and innovation technologies that have appeared in medicine. The first is a controllable condition found in approximately 1% of the entire population in the form of a reaction to environmental stimuli affecting individuals with genetic susceptibility, causing gluten intolerance, gastrointestinal and extradigestive symptoms, starting from subclinical stages and culminating in severe malabsorption. On the other hand, lupus is an autoimmune disease with chameleon-like symptoms and found mainly in the female sex, which leaves its clinical mark on most organs, from the skin, eyes, and kidneys to the cardiovascular, pulmonary, neurological, osteoarticular, and hematological systems. Current studies focus on the correlation between celiac disease and other autoimmune pathologies such as autoimmune thyroiditis (Hashimoto and Graves–Basedow), type I diabetes, and systemic lupus erythematosus. The current review aims to present a summary of the data from the specialized literature regarding the intercurrents between celiac disease and lupus by analyzing the most recent studies published on PubMed.

[1]  Silvia L. Fotea,et al.  The Implication of the Gut Microbiome in Heart Failure , 2023, Cells.

[2]  U. de la Cruz-Mosso,et al.  Methyl Donor Micronutrients: A Potential Dietary Epigenetic Target in Systemic Lupus Erythematosus Patients , 2023, International journal of molecular sciences.

[3]  I. Miron,et al.  Difficulties in Adaptation of the Mother and Newborn via Cesarean Section versus Natural Birth—A Narrative Review , 2023, Life.

[4]  A. Azoicăi,et al.  Pediatric Systemic Lupus Erythematous in COVID-19 Era , 2023, Viruses.

[5]  M. Bodinier,et al.  Immunomodulation of B Lymphocytes by Prebiotics, Probiotics and Synbiotics: Application in Pathologies , 2023, Nutrients.

[6]  S. Esposito,et al.  The Effects of COVID-19 Pandemic and Lockdown on Pediatric Nutritional and Metabolic Diseases: A Narrative Review , 2022, Nutrients.

[7]  C. Strisciuglio,et al.  Role of Vitamin D in Celiac Disease and Inflammatory Bowel Diseases , 2022, Nutrients.

[8]  F. Marcu,et al.  The Gut Microbiome and Its Implication in the Mucosal Digestive Disorders , 2022, Biomedicines.

[9]  Muhammad Ali Tariq,et al.  An Overview of Systemic Lupus Erythematosus (SLE) Pathogenesis, Classification, and Management , 2022, Cureus.

[10]  C. Kelly,et al.  American College of Gastroenterology Guidelines Update: Diagnosis and Management of Celiac Disease. , 2022, The American journal of gastroenterology.

[11]  S. Rednic,et al.  An Update on the Effects of Vitamin D on the Immune System and Autoimmune Diseases , 2022, International journal of molecular sciences.

[12]  M. Barone,et al.  Pivotal Role of Inflammation in Celiac Disease , 2022, International journal of molecular sciences.

[13]  K. Kosidou,et al.  Association between parental mental illness and autoimmune diseases in the offspring - A nationwide register-based cohort study in Sweden. , 2022, Journal of psychiatric research.

[14]  B. Lucchini,et al.  What about TSH and Anti-Thyroid Antibodies in Patients with Autoimmune Thyroiditis and Celiac Disease Using a Gluten-Free Diet? A Systematic Review , 2022, Nutrients.

[15]  A. K. Hansen,et al.  Gluten-free diet reduces autoimmune diabetes mellitus in mice across multiple generations in a microbiota-independent manner. , 2022, Journal of autoimmunity.

[16]  Lei Zhang,et al.  Causal Relationship Between Gut Microbiota and Autoimmune Diseases: A Two-Sample Mendelian Randomization Study , 2022, Frontiers in Immunology.

[17]  M. Aringer,et al.  Classification of systemic lupus erythematosus in children and adults. , 2021, Clinical immunology.

[18]  T. Alexander,et al.  Systemic lupus erythematosus - Are children miniature adults? , 2021, Clinical immunology.

[19]  M. Ishii,et al.  The Effects of Vitamin D on Immune System and Inflammatory Diseases , 2021, Biomolecules.

[20]  G. Cappellano,et al.  How to Tackle the Relationship between Autoimmune Diseases and Diet: Well Begun Is Half-Done , 2021, Nutrients.

[21]  A. Schwarting,et al.  Vascular Inflammation and Dysfunction in Lupus-Prone Mice-IL-6 as Mediator of Disease Initiation , 2021, International journal of molecular sciences.

[22]  C. Hedrich,et al.  Systemic Lupus Erythematosus in Children and Young People , 2021, Current Rheumatology Reports.

[23]  Cristina Municio,et al.  Therapies Targeting Trained Immune Cells in Inflammatory and Autoimmune Diseases , 2021, Frontiers in Immunology.

[24]  I. Korponay-Szabó,et al.  Clinical Presentation in Children with Coeliac Disease in Central Europe. , 2020, Journal of pediatric gastroenterology and nutrition.

[25]  T. Kanneganti,et al.  The innate immune system and cell death in autoinflammatory and autoimmune disease. , 2020, Current opinion in immunology.

[26]  F. Sztajnbok,et al.  RELATIONSHIP BETWEEN FIBER INTAKE AND CARDIOVASCULAR RISK FACTORS IN ADOLESCENTS WITH SYSTEMIC LUPUS ERYTHEMATOSUS , 2020, Revista paulista de pediatria : orgao oficial da Sociedade de Pediatria de Sao Paulo.

[27]  S. Ménard,et al.  Psychological Stress, Intestinal Barrier Dysfunctions, and Autoimmune Disorders: An Overview , 2020, Frontiers in Immunology.

[28]  J. Frederiksen,et al.  Current Evidence on the Efficacy of Gluten-Free Diets in Multiple Sclerosis, Psoriasis, Type 1 Diabetes and Autoimmune Thyroid Diseases , 2020, Nutrients.

[29]  F. Alsohaibani,et al.  The Value of Screening for Celiac Disease in Systemic Lupus Erythematosus: A Single Experience of a Tertiary Medical Center , 2020, Rheumatology and Therapy.

[30]  C. Comba,et al.  Celiac disease does not influence markers of ovarian reserve in adolescent girls , 2020, Archives of Gynecology and Obstetrics.

[31]  Chao Lu,et al.  Vitamin D status and vitamin D receptor genotypes in celiac disease: a meta-analysis , 2020, Critical reviews in food science and nutrition.

[32]  G. Orozco,et al.  Functional genomics in autoimmune diseases , 2020, Human molecular genetics.

[33]  C. Mathieu,et al.  Vitamin D’s Effect on Immune Function , 2020, Nutrients.

[34]  V. Polzonetti,et al.  Possible Role of Vitamin D in Celiac Disease Onset , 2020, Nutrients.

[35]  J. Inamo Association between celiac disease and systemic lupus erythematosus: a Mendelian randomization study. , 2020, Rheumatology.

[36]  C. Venter,et al.  Nutrition and the Immune System: A Complicated Tango , 2020, Nutrients.

[37]  C. Selmi,et al.  The clinical implications of selective IgA deficiency , 2019, Journal of translational autoimmunity.

[38]  G. Gkoutos,et al.  Allergic diseases and long-term risk of autoimmune disorders: longitudinal cohort study and cluster analysis , 2019, European Respiratory Journal.

[39]  Junpeng Wang,et al.  [Advance in effect of aerobic exercise on immune system and autoimmune diseases]. , 2019, Sheng li xue bao : [Acta physiologica Sinica].

[40]  S. Kimura,et al.  The Roles of Peyer's Patches and Microfold Cells in the Gut Immune System: Relevance to Autoimmune Diseases , 2019, Front. Immunol..

[41]  N. Rose,et al.  Fatigue, Sleep, and Autoimmune and Related Disorders , 2019, Front. Immunol..

[42]  Gheyath K Nasrallah,et al.  Viruses and Autoimmunity: A Review on the Potential Interaction and Molecular Mechanisms , 2019, Viruses.

[43]  S. Parthasarathy,et al.  Negative Effects of a High-Fat Diet on Intestinal Permeability: A Review. , 2019, Advances in nutrition.

[44]  David D. Odineal,et al.  The Epidemiology and Clinical Manifestations of Autoimmunity in Selective IgA Deficiency , 2019, Clinical Reviews in Allergy & Immunology.

[45]  M. Villa,et al.  Nutritional Deficiencies in Children with Celiac Disease Resulting from a Gluten-Free Diet: A Systematic Review , 2019, Nutrients.

[46]  D. Sanders,et al.  European Society for the Study of Coeliac Disease (ESsCD) guideline for coeliac disease and other gluten-related disorders , 2019, United European gastroenterology journal.

[47]  M. Carroll,et al.  Diet patterns in an ethnically diverse pediatric population with celiac disease and chronic gastrointestinal complaints. , 2019, Clinical nutrition ESPEN.

[48]  A. Gabrielli,et al.  Celiac Disease Prevalence Is Increased in Primary Sjögren’s Syndrome and Diffuse Systemic Sclerosis: Lessons from a Large Multi-Center Study , 2019, Journal of clinical medicine.

[49]  C. Gordon,et al.  2019 update of the EULAR recommendations for the management of systemic lupus erythematosus , 2019, Annals of the rheumatic diseases.

[50]  Meiping Lu,et al.  Immunological pathogenesis and treatment of systemic lupus erythematosus , 2019, World Journal of Pediatrics.

[51]  Vaishali R. Moulton Sex Hormones in Acquired Immunity and Autoimmune Disease , 2018, Front. Immunol..

[52]  K. Kurppa,et al.  Screening for coeliac disease in children , 2018, Acta paediatrica.

[53]  H. Brunner,et al.  Childhood-Onset Systemic Lupus Erythematosus: A Review and Update. , 2018, The Journal of pediatrics.

[54]  M. Lipowska,et al.  Physical Activity and Cognitive Functioning of Children: A Systematic Review , 2018, International journal of environmental research and public health.

[55]  Y. Shoenfeld,et al.  Prolactin and Autoimmunity , 2018, Front. Immunol..

[56]  Daniel E. Miller,et al.  Transcription factors operate across disease loci, with EBNA2 implicated in autoimmunity , 2018, Nature Genetics.

[57]  D. Lipsker,et al.  The Cutaneous Spectrum of Lupus Erythematosus , 2017, Clinical Reviews in Allergy & Immunology.

[58]  Aline Zazeri Leite,et al.  Intestinal dysbiosis and probiotic applications in autoimmune diseases , 2017, Immunology.

[59]  B. Rovin,et al.  Update on Lupus Nephritis. , 2017, Clinical journal of the American Society of Nephrology : CJASN.

[60]  A. Dima,et al.  Immune and autoimmune gluten-related phenomenon in systemic lupus erythematosus , 2017, Lupus.

[61]  X. Puéchal,et al.  Eosinophilic gastrointestinal disorders associated with autoimmune connective tissue disease. , 2016, Joint, bone, spine : revue du rhumatisme.

[62]  S. Crowe,et al.  Complex Relationships Between Food, Diet, and the Microbiome. , 2016, Gastroenterology clinics of North America.

[63]  C. Bizzarri,et al.  Autoimmune diseases and celiac disease which came first: genotype or gluten? , 2016, Expert review of clinical immunology.

[64]  V. De Rosa,et al.  Nutritional control of immunity: Balancing the metabolic requirements with an appropriate immune function. , 2015, Seminars in immunology.

[65]  Cisca Wijmenga,et al.  Autoimmune Disease in First-Degree Relatives and Spouses of Individuals With Celiac Disease. , 2015, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[66]  T. Serwold,et al.  The Autoimmunity-Associated Gene CLEC16A Modulates Thymic Epithelial Cell Autophagy and Alters T Cell Selection. , 2015, Immunity.

[67]  Z. Tian,et al.  PTPN22 R620W Polymorphism and ANCA Disease Risk in White Populations: A Metaanalysis , 2015, The Journal of Rheumatology.

[68]  L. Hammarström,et al.  IgA deficiency: what is new? , 2012, Current opinion in allergy and clinical immunology.

[69]  Mark Daly,et al.  What have we learned from six years of GWAS in autoimmune diseases, and what is next? , 2012, Current opinion in immunology.

[70]  Roman Teimer,et al.  Influence of Dietary Components on Regulatory T Cells , 2012, Molecular medicine.

[71]  L. Criswell,et al.  Emerging patterns of genetic overlap across autoimmune disorders , 2012, Genome Medicine.

[72]  P. Visscher,et al.  Five years of GWAS discovery. , 2012, American journal of human genetics.

[73]  C. Hsieh,et al.  Dietary factors regulate cytokines in murine models of systemic lupus erythematosus. , 2011, Autoimmunity reviews.

[74]  B. Thapa,et al.  Lupus anticoagulant in a child with celiac disease: a rare association , 2011, Rheumatology International.

[75]  K. Kaukinen,et al.  Antibodies in celiac disease: implications beyond diagnostics , 2011, Cellular and Molecular Immunology.

[76]  S. Al-Mogairen Lupus protein-losing enteropathy (LUPLE): A systematic review , 2011, Rheumatology International.

[77]  S. Yasmeen,et al.  Multiple autoimmune syndrome: Hashimoto's thyroiditis, coeliac disease and systemic lupus erythematosus (SLE). , 2010, JPMA. The Journal of the Pakistan Medical Association.

[78]  K. Tsuneyama,et al.  Nutrition, geoepidemiology, and autoimmunity. , 2010, Autoimmunity reviews.

[79]  A. Fasano,et al.  Pediatric celiac disease , 2009, Current opinion in pediatrics.

[80]  J. Rioux,et al.  Autoimmune diseases: insights from genome-wide association studies. , 2008, Human molecular genetics.

[81]  I. Santin,et al.  The functional R620W variant of the PTPN22 gene is associated with celiac disease. , 2008, Tissue antigens.

[82]  C. Wijmenga,et al.  MYO9B gene polymorphisms are associated with autoimmune diseases in Spanish population. , 2007, Human immunology.

[83]  W. Caspary,et al.  Celiac disease , 2006, Orphanet journal of rare diseases.

[84]  Javier Martín,et al.  C1858T functional variant of PTPN22 gene is not associated with celiac disease genetic predisposition. , 2005, Human immunology.

[85]  A. Fasano,et al.  Coeliac disease in children. , 2005, Best practice & research. Clinical gastroenterology.

[86]  D. Sanders,et al.  Gluten sensitivity masquerading as systemic lupus erythematosus , 2004, Annals of the rheumatic diseases.

[87]  S. Makni,et al.  Systemic lupus erythematosus with celiac disease: a report of five cases. , 2004, Joint, bone, spine : revue du rhumatisme.

[88]  A. Patwari,et al.  Serum prolactin in celiac disease. , 2004, Journal of tropical pediatrics.

[89]  A. Leaños-Miranda,et al.  Analysis of anti-prolactin autoantibodies in systemic lupus erythematosus , 2001, Lupus.

[90]  P. Parisi,et al.  Latent coeliac disease in a child with epilepsy, cerebral calcifications, drug-induced systemic lupus erythematosus and intestinal folic acid malabsorption associated with impairment of folic acid transport across the blood-brain barrier , 2001, European Journal of Pediatrics.

[91]  L. Harbige Dietary n-6 and n-3 fatty acids in immunity and autoimmune disease , 1998, Proceedings of the Nutrition Society.

[92]  R. Hall,et al.  Characterization of circulating and cutaneous IgA immune complexes in patients with dermatitis herpetiformis. , 1985, Journal of immunology.

[93]  J. Heck,et al.  IgA-containing circulating immune complexes in dermatitis herpetiformis, Henoch-Schönlein purpura, systemic lupus erythematosus and other diseases. , 1980, Clinical and experimental immunology.

[94]  E. Holborow,et al.  MULTIPLE IMMUNE COMPLEXES AND HYPOCOMPLEMENTÆMIA IN DERMATITIS HERPETIFORMIS AND CŒLIAC DISEASE , 1976, The Lancet.

[95]  A. Hrõbjartsson,et al.  Hepatology and Nutrition Guidelines for Diagnosing Coeliac Disease 2020 , 2020 .

[96]  M. Faresjö The Link between Psychological Stress and Autoimmune Response in Children. , 2015, Critical reviews in immunology.

[97]  P. Gregersen,et al.  Selective IgA Deficiency in Autoimmune Diseases , 2011, Molecular medicine.