Publications by authors named "Mario García-Carrasco"

85 Publications

Human mesenchymal stem cells for the management of systemic sclerosis. Systematic review.

Autoimmun Rev 2021 Apr 18;20(6):102831. Epub 2021 Apr 18.

Research Institute, Fundación Universitaria De Ciencias De La Salud, University of Health Sciences, Bogota, Colombia.

Introduction: Sistemic Sclerosis (SSc) is a heterogeneous autoimmune disease with a high rate of progression and therapeutic failure, and treatment is a challenge, new therapeutic proposals being needed, being mesenchymal stem cells (MSCs) considered as alternative therapy for SSc for its immunomodulatory capacity. We evaluated the efficacy and safety of human MSC (hMSC) in patients with SSc through a systematic literature review (SLR).

Methods: SLR (PRISMA guideline) on MEDLINE/OVID, LILACS, EMBASE, and Cochrane/OVID bases (until July 2020, without limits). All types of clinical studies were considered: patients ≥18 years old with SSc and treatment with hMSC.

Exclusion Criteria: animal models, autologous/allogenic hematopoietic stem cell transplants, narrative reviews, letters to the editor. MeSH and "Key word" terms were used. The level of evidence and the quality rating were rated [Joanna Briggs Institute (JBI) lists]. Registration in PROSPERO repository (ID CRD42020185245) The Synthesis Without Meta-analysis (SWiM) guideline was followed.

Results: We initially identified 508 articles, of which 11 were finally included (8 case series and 3 case reports). The 11 articles included 101 patients (85 female, age range 18-75 years). The level of evidence was mostly 4 (JBI); the quality of evidence was met (≥50% of JBI items). SWiM showed that vascular skin involvement (digital ulcers, necrosis, and gangrene) and associated pain were the predominant outcomes, while improvements were found in almost all cases. One patient died in the first month, and the frequency of complications was low. Expanded hMSCs were used in 24 patients and other cell sources in the remaining patients.

Conclusion: There is too little reported data to reach definite conclusions about the use of hMSC in SSc. Further studies with better epidemiological designs are needed to evaluate the benefit of hMSCs in SSc patients.
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http://dx.doi.org/10.1016/j.autrev.2021.102831DOI Listing
April 2021

A Retrospective Analysis of Longitudinal Changes in Bone Mineral Density in Women with Systemic Lupus Erythematosus.

Calcif Tissue Int 2021 Apr 17. Epub 2021 Apr 17.

Research in Health Coordination, Mexican Social Security Institute, Puebla, Puebla, Mexico.

Most prospective studies of bone mineral density (BMD) in systemic lupus erythematosus (SLE) patients have been of relatively short duration, with a maximum of 6 years. To describe long-term changes in BMD in women with SLE and identify risk factors associated with BMD loss. We retrospectively evaluated 132 adult Mexican-Mestizo women with SLE who underwent dual X-ray absorptiometry (DXA). Demographic and clinical data were collected and BMD at the lumbar spine (L1-L4) and total hip were collected at baseline and during the follow up. At baseline, the mean age of participants was 43.4 ± 12.5 years, 50.8% had osteopenia and 11% osteoporosis. The median follow-up was 13 (IQR 10.2-14.0) years. During follow up, 79% of patients used glucocorticoid (GCT). The mean percentage of changes in BMD during follow up were: - 14.03 ± 11.25% (- 1.49%/year) at the lumbar spine, and - 15.77 ± 11.57% (- 1.78%/year) at the total hip, with significant changes (p < 0.001 for both comparisons). Multivariate analysis showed older age, GCT use at baseline, and transition to the menopause during the follow-up were significantly associated with greater reductions in BMD. This retrospective longitudinal study found significant BMD loss at the lumbar spine and hip. Older age, menopausal transition and GCT use were independently associated with BMD decline in women with SLE.
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http://dx.doi.org/10.1007/s00223-021-00845-0DOI Listing
April 2021

Medication adherence is influenced by resilience in patients with systemic lupus erythematosus.

Lupus 2021 Apr 1:9612033211004722. Epub 2021 Apr 1.

Research Coordination, Mexican Social Security Institute, Puebla. México.

Objective: Evidence on the relationship between resilience and medication adherence in systemic lupus erythematosus (SLE) patients is lacking. We aimed to examine the impact of resilience on medication adherence in SLE patients.

Method: In a cross-sectional analysis SLE outpatients were assessed for resilience (Connor-Davison Resilience Scale, CD-RISC), depressive symptoms (CES-D) and medication adherence (Compliance Questionnaire for Rheumatology [CQR]). The disease activity index (mexSLEDAI) and damage (SLICC Damage Index) were administered. Factors independently associated with adherence were identified using multivariate logistic regression.

Results: Of the 157 patients, 152 (96.8%) were female with a median age of 45.9 (IQR: 39.0-55.5) years and disease duration of 14 (IQR: 10.0-19.0) years. Medication adherence (CQR ≥80%) and depressive symptoms were found in 74.5% and 43.9% of patients, respectively. Adherent patients had a lower CES-D score and a higher CD-RISC score. In the multivariate analysis adjusting for demographic and clinical confounders, resilience and older age protected against non-adherence (OR 0.96, [95% CI 0.94-0.99] and OR 0.96 [95% CI 0.93-0.98], respectively).

Conclusion: In SLE patients, resilience and older age, which possibly associated with better medication adherence, may protect against non-adherence.
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http://dx.doi.org/10.1177/09612033211004722DOI Listing
April 2021

The Cardio-Rheumatology Approach to Atherosclerotic Cardiovascular Disease.

Reumatol Clin 2020 Sep - Oct;16(5 Pt 1):311-312. Epub 2020 Jul 25.

Systemic Autoimmune Diseases Research Unit and Rheumatology/Immunology Department, BUAP School of Medicine, Puebla, Mexico. Electronic address:

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http://dx.doi.org/10.1016/j.reuma.2020.07.001DOI Listing
July 2020

Comparing cytology, colposcopy and human papillomavirus cervical intraepithelial lesion screening methods in women with systemic lupus erythematosus.

Lupus 2020 Aug 5;29(9):1060-1066. Epub 2020 Jun 5.

Gynaecology Service, Hospital Universitario de Puebla, México.

Objective: To compare the performance of cytology, colposcopy and human papillomavirus in detecting cervical intraepithelial lesions in women with systemic lupus erythematosus.

Methods: Papanicolaou smears (normal, low-grade squamous intraepithelial lesion, high grade squamous intraepithelial lesion), colposcopy findings, human papillomavirus and co-testing (Papanicolaou smear + human papillomavirus) were compared with cervical biopsy findings in women with systemic lupus erythematosus. Sensitivity, specificity, false-positive and false-negative rates, positive and negative predictive values and likelihood ratios of cytologic smears, colposcopy findings, human papillomavirus and co-testing were determined.

Results: Cytology and colposcopy were performed in 170 systemic lupus erythematosus women (mean age and disease duration of 43.7±12.1 years and 9.7±5.3 years, respectively) and biopsies were performed in 55 patients (38.2% normal, 60.0% low-grade squamous intraepithelial lesion and 1.8% high grade squamous intraepithelial lesion). The sensitivity, specificity, positive predictive value and negative predictive value of cytology were 14.7% (95% confidence interval 5.5-31.8%), 95.2% (95% confidence interval 74.1-99.7%), 83.3% (95% confidence interval 36.4-99.1%) and 40.8% (95% confidence interval 27.3-55.7%), respectively. The sensitivity, specificity and positive predictive value of colposcopy findings were 100.0% (95% confidence interval 87.3-100.0%), 0.0% (95% confidence interval 0.0-19.2%) and 61.8% (95% confidence interval 47.7-74.2%), respectively. The sensitivity and specificity of co-testing were 8.0% (95% confidence interval 1.3-27.5%) and 100.0% (95% confidence interval 71.6-100.0%). The positive predictive value and negative predictive values were 100.0% (95% confidence interval 19.7-100.0%) and 36.1% (95% confidence interval 33.5-38.8%), respectively.

Conclusions: In systemic lupus erythematosus patients, colposcopy impressions were more sensitive than cytology and co-testing. However, cytology and co-testing were the most specific tests. The results should be interpreted with caution due to the small sample size.
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http://dx.doi.org/10.1177/0961203320931176DOI Listing
August 2020

Systemic lupus erythematosus, endothelial progenitor cells and intracellular Ca signaling: A novel approach for an old disease.

J Autoimmun 2020 08 29;112:102486. Epub 2020 May 29.

Laboratory of General Physiology, Department of Biology and Biotechnology "L. Spallanzani", University of Pavia, via Forlanini 6, 27100, Pavia, Italy. Electronic address:

Systemic lupus erythematosus (SLE) is an autoimmune multisystem disease featured by an increased cardiovascular risk that may lead to premature patient's death. It has been demonstrated that SLE patients suffer from early onset endothelial dysfunction which is due to the impairment of endogenous vascular repair mechanisms. Vascular integrity and homeostasis are maintained by endothelial progenitor cells (EPCs), which are mobilized in response to endothelial injury to replace damaged endothelial cells. Two main EPCs subpopulations exist in peripheral blood: endothelial colony forming cells (ECFCs), which represent truly endothelial precursors and can physically engraft within neovessels, and myeloid angiogenic cells (MACs), which sustain angiogenesis in a paracrine manner. Emerging evidence indicates that ECFCs/MACs are down-regulated and display compromised angiogenic activity in SLE, thereby contributing to the pathogenesis of this disease. Intracellular calcium (Ca) signaling plays a crucial role in maintaining vascular integrity by stimulating migration, proliferation and tube formation in both ECFCs and MACs. Herein, we illustrate the evidences that support the role played by EPCs dysfunction in SLE. Subsequently, we discuss about the hypothesis that the Ca handling machinery is compromised in SLE-derived ECFCs and MACs, thereby resulting in their reduced pro-angiogenic activity. Finally, we speculate about the proposal to exploit intracellular Ca signaling to improve ECFCs' reparative phenotype and suggest this strategy as a new approach to treat SLE patients.
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http://dx.doi.org/10.1016/j.jaut.2020.102486DOI Listing
August 2020

[Therapeutic options for the management of severe Covid-19: A rheumatology perspective].

Reumatol Clin 2020 May 16. Epub 2020 May 16.

Coordinación de Investigación en Salud, Delegación Puebla, Instituto Mexicano del Seguro Social, Puebla, México.

The novel SARS-CoV-2 human coronavirus in Wuhan, China, has triggered a worldwide respiratory disease outbreak (COVID-19). Acute respiratory distress syndrome (ARDS), multiorgan dysfunction and thrombotic events are among the leading causes of death in critically ill patients with COVID-19. The elevated inflammatory cytokines suggest that a "cytokine storm", also known as cytokine release syndrome (CRS), may play a major role in the pathology of COVID-19. In addition to anti-viral therapy and supportive treatment in critically ill patients, unique medications for this condition are also under investigation. Here we reviewed therapeutic options, including the antibody therapy that might be an immediate strategy for SARS-CoV-2 therapy.
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http://dx.doi.org/10.1016/j.reuma.2020.05.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7229930PMC
May 2020

Endothelial dysfunction and arterial stiffness in patients with systemic lupus erythematosus: A systematic review and meta-analysis.

Atherosclerosis 2020 03 31;297:55-63. Epub 2020 Jan 31.

Department of Autoimmune Diseases, Hospital Clinic, Barcelona, Catalonia, Spain.

Background And Aims: Non-invasive surrogates of cardiovascular (CV) disease such as endothelial dysfunction (ED) and peripheral arterial stiffness (AS) have been evaluated in systemic lupus erythematosus (SLE) patients. The aim of this study was to systematically review and meta-analyze reports of cardiovascular disease (CVD) in SLE patients, as measured by ED and AS.

Methods: Studies analyzing the relationship of SLE with ED (flow-mediated dilatation [FMD], nitroglycerin-mediated dilatation [NMD] and peripheral arterial tonometry [PAT]) and AS (augmentation index [AIx], pulse wave velocity [PWV]) were systematically searched for in PubMed, Cochrane library, EMBASE, VHL, SciELO and Web of Science databases. Inclusion criteria included peer-review and English language. Mean differences (MD) and 95% confidence intervals (CIs) were estimated using the random effect model. The study was registered with PROSPERO, number CRD42019121068.

Results: The meta-analysis included 49 studies. FMD data from 18 studies including 943 SLE subjects (mean age = 38.71 [95%CI 36.21, 41.21] years) and 644 unaffected controls (mean age = 38.63 [95%CI 36.11, 41.15] years) were included. When compared with unaffected controls, FMD in SLE subjects was decreased by 4.3% (95%CI: -6.13%, -2.47%): p < 0.001). However, NMD did not significantly differ between SLE patients and controls (MD = - 2.68%; 95% CI -6.00, 0.62; p = 0.11). A significantly increased AS between SLE patients and controls according to overall PWV (MD = 1.12 m/s; 95% CI 0.72-1.52; p < 0.001) was observed, but not for the brachial-ankle PWV. AIx was also increased in SLE patients compared with healthy controls (MD = 4.55%; 95% CI 1.48-7.63; p = 0.003).

Conclusions: Overall, SLE patients showed impaired FMD, an independent predictor of CV events. There was a higher degree of AS in SLE patients compared with controls. ED and AS in SLE should be considered when planning preventive strategies and therapies.
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http://dx.doi.org/10.1016/j.atherosclerosis.2020.01.028DOI Listing
March 2020

Type 2 Diabetes Alters Intracellular Ca Handling in Native Endothelium of Excised Rat Aorta.

Int J Mol Sci 2019 Dec 30;21(1). Epub 2019 Dec 30.

Laboratory of General Physiology, Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.

An increase in intracellular Ca concentration ([Ca]) plays a key role in controlling endothelial functions; however, it is still unclear whether endothelial Ca handling is altered by type 2 diabetes mellitus, which results in severe endothelial dysfunction. Herein, we analyzed for the first time the Ca response to the physiological autacoid ATP in native aortic endothelium of obese Zucker diabetic fatty (OZDF) rats and their lean controls, which are termed LZDF rats. By loading the endothelial monolayer with the Ca-sensitive fluorophore, Fura-2/AM, we found that the endothelial Ca response to 20 µM and 300 µM ATP exhibited a higher plateau, a larger area under the curve and prolonged duration in OZDF rats. The "Ca add-back" protocol revealed no difference in the inositol-1,4,5-trisphosphate-releasable endoplasmic reticulum (ER) Ca pool, while store-operated Ca entry was surprisingly down-regulated in OZDF aortae. Pharmacological manipulation disclosed that sarco-endoplasmic reticulum Ca-ATPase (SERCA) activity was down-regulated by reactive oxygen species in native aortic endothelium of OZDF rats, thereby exaggerating the Ca response to high agonist concentrations. These findings shed new light on the mechanisms by which type 2 diabetes mellitus may cause endothelial dysfunction by remodeling the intracellular Ca toolkit.
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http://dx.doi.org/10.3390/ijms21010250DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6982087PMC
December 2019

Helicobacter pylori infection and gastroduodenal lesions in patients with systemic lupus erythematosus.

Clin Rheumatol 2020 Feb 12;39(2):463-469. Epub 2019 Nov 12.

Puebla Research Coordination, Highly Specialized Medical Unit, UMAE CMNMAC, Instituto Mexicano del Seguro Social, Puebla, México.

Objective: The aim of this study was to determine the frequency of Helicobacter pylori in SLE patients and to compare clinical characteristics and gastroduodenal lesions in patients with and without H. pylori infection.

Methods: Adult SLE patients were selected and subjected to endoscopy. Gastroduodenal lesions were examined by endoscopy and biopsy (antrum and corpus). Biopsies were evaluated by hematoxylin and eosin and Giemsa staining. Immunochromatographic membrane-based assay using amplification was used to test for H. pylori antigen (coproantigen) in stool samples in all participants. Clinical characteristics and gastroduodenal lesions were compared between patients with and without H. pylori infection.

Results: A total of 118 SLE patients were included (mean age 44.7 ± 11.7 years, mean disease duration 11.6 ± 6.0 years), of whom 101 (85.6%) were receiving non-steroidal anti-inflammatory drugs (NSAIDs). The coproantigen test was positive in 32 (27.1%) patients. H. pylori was present in twenty six patients (22.0%) in the gastric biopsy. The frequency of gastric erosions and gastric ulcers were 55.1% and 0.8%, respectively. Gastric erosions were less frequent in SLE patients with H. pylori infection than those without H. pylori (43.5.7% vs. 62.5%; p = 0.04). The age, disease duration, disease activity, chronic damage, gastroprotective drugs, and immunosuppressive therapy did not differ between the two groups.

Conclusions: We found a high frequency of H. pylori infection in SLE patients. The severity of SLE and reception of gastroprotective therapy do not seem to be related to H. pylori infection. Immunosuppressive therapy may not be protective against H. pylori infection in SLE patients.Key Points• In patients with systemic lupus erythematosus (SLE), the frequency of Helicobacter pylori infection was 39% and gastric erosions were frequent.• Disease activity, chronic damage, gastroprotective drugs, and immunosuppressive therapy may not affect the prevalence of H. pylori infection in SLE patients.
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http://dx.doi.org/10.1007/s10067-019-04805-wDOI Listing
February 2020

25-Hydroxyvitamin D concentrations and risk of metabolic syndrome in systemic lupus erythematosus women.

Int J Rheum Dis 2019 Nov 9;22(11):2067-2072. Epub 2019 Oct 9.

Laboratorios Clínicos de Puebla, Puebla, Mexico.

Objective: A protective function of vitamin D in metabolic syndrome (MetS) has been described. The objective of the present study was to examine the relationship between serum 25-hydroxyvitamin D (25(OH)D) concentrations and MetS in non-diabetic systemic lupus erythematosus (SLE) women.

Methods: Cross-sectional analyses of the relationship between concentrations of 25(OH)D, MetS, and its components were made in 160 non-diabetic SLE women. MetS was defined according to National Cholesterol Education Program Adult Treatment Panel III criteria. Serum 25(OH)D was measured by chemiluminescent immunoassay. Serum 25(OH)D concentrations were categorized into quartiles (<16.6, 16.6-21.1, 21.2-26.3, ≥26.4 ng/mL).

Results: A total of 79 (49.3%) SLE women had MetS. Without adjusting for body mass index (BMI) or smoking, the odds of having MetS decreased according to increasing quartiles of 25(OH)D concentrations (P for trend = .03). The odds ratio (OR) of having MetS was 0.4 (95% confidence interval: 0.2-0.9, P = .04) for the highest vs the lowest quartile of 25(OH)D concentrations when adjusted by age. The crude OR of having elevated hypertriglyceridemia decreased according to increasing quartiles of 25(OH)D concentrations (P for trend = .036). However, further adjustments for BMI and smoking removed the inverse association between 25(OH)D concentrations and MetS and its individual components.

Conclusion: In non-diabetic SLE women with mild activity, 25(OH)D concentrations are not associated with MetS and its components.
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http://dx.doi.org/10.1111/1756-185X.13715DOI Listing
November 2019

Systemic lupus erythematosus and hypertension.

Autoimmun Rev 2019 Oct 12;18(10):102371. Epub 2019 Aug 12.

Department of Autoimmune Disease, Hospital Clinic, Barcelona, Spain. Electronic address:

Systemic lupus erythematosus (SLE) is associated with a high burden of cardiovascular disease (CVD), which is in part imputed to classical vascular risk factors such as hypertension. Hypertension is frequent among patients with SLE and studies show it is more prevalent in SLE patients than in people without SLE. Despite the high frequency of hypertension in SLE patients, the pathophysiological mechanisms underlying the development of hypertension remain poorly understood. 24-h ambulatory blood pressure monitoring has emerged as a valuable tool in determining blood pressure (BP) in SLE patients in whom hypertension has been associated with damage accrual, stroke and cognitive dysfunction. Although prevalent, current guidelines neglect the specific management of hypertension in SLE patients in their recommendations. This review discusses the mechanisms that may lead to hypertension and the literature evaluating hypertension screening and management in SLE patients.
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http://dx.doi.org/10.1016/j.autrev.2019.102371DOI Listing
October 2019

Functional gastrointestinal disorders in women with systemic lupus erythematosus: A case-control study.

Neurogastroenterol Motil 2019 11 1;31(11):e13693. Epub 2019 Aug 1.

Laboratorio de Hígado, Páncreas y Motilidad (HIPAM), Unidad de Investigación en Medicina Experimental, Facultad de Medicina-Universidad Nacional Autónoma de México (UNAM)-Hospital General de México, Dr. Eduardo Liceaga., Mexico City, México.

Background: Systemic lupus erythematosus (SLE) is an autoimmune disease with multisystemic involvement. Gastrointestinal (GI) manifestations are frequent but functional gastrointestinal disorders (FGIDs) have scarcely been studied in SLE. To determine the prevalence of FGIDs and their potential risk factors in SLE female patients vs controls.

Methods: Systemic lupus erythematosus patients meeting the American College of Rheumatology (ACR) criteria and controls completed the Rome III questionnaire for FGIDs and a structured interview to assess sociodemographic, clinical, and treatment variables after excluding organic GI diseases. Logistic regression was used to determine risk factors (ie, alcohol drinking, medications) for FGIDs.

Key Results: Responders included 113 SLE patients and 122 age-matched controls. The presence of at least one FGIDs was higher in SLE (73.4%) vs controls (54.1%), P = .003. The most frequent FGIDs in SLE patients were nausea and vomiting disorders (NVD), belching disorders, globus, anorectal pain, functional heartburn (FH), and functional bloating (FB). After adjustment for confounding variables, SLE was associated with NVD (OR: 7.1, 95% CI: 2.7-19.1) globus (3.5, 1.3-9.3), anorectal pain (3.4, 1.4-8.4), and FH (2.5, 1.5-4.4). The simultaneous presence of >1 FGID was more common in SLE patients than controls (69.8% vs 31.8%). Glucocorticoids (5.2, 1.3-19.9) and non-steroidal anti-inflammatory drugs (NSAIDs; 3.0, 1.1-8.0) were associated with any FGID in SLE patients while alcohol drinking with gallbladder/sphincter of Oddi disorders 7.4 (1.1-47.3).

Conclusions And Inferences: Functional gastrointestinal disorders are more frequent in SLE patients compared with controls. Medication that may alter gastrointestinal homeostasis, such as glucocorticoids and NSAIDs, are potential risk factors for FGIDs in SLE.
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http://dx.doi.org/10.1111/nmo.13693DOI Listing
November 2019

Histamine induces intracellular Ca oscillations and nitric oxide release in endothelial cells from brain microvascular circulation.

J Cell Physiol 2020 02 16;235(2):1515-1530. Epub 2019 Jul 16.

Laboratory of General Physiology, Department of Biology and Biotechnology "L. Spallanzani", University of Pavia, Pavia, Italy.

The neuromodulator histamine is able to vasorelax in human cerebral, meningeal and temporal arteries via endothelial histamine 1 receptors (H Rs) which result in the downstream production of nitric oxide (NO), the most powerful vasodilator transmitter in the brain. Although endothelial Ca signals drive histamine-induced NO release throughout the peripheral circulation, the mechanism by which histamine evokes NO production in human cerebrovascular endothelial cells is still unknown. Herein, we exploited the human cerebral microvascular endothelial cell line, hCMEC/D3, to assess the role of intracellular Ca signaling in histamine-induced NO release. To achieve this goal, hCMEC/D3 cells were loaded with the Ca - and NO-sensitive dyes, Fura-2/AM and DAF-FM/AM, respectively. Histamine elicited repetitive oscillations in intracellular Ca concentration in hCMEC/D3 cells throughout a concentration range spanning from 1 pM up to 300 μM. The oscillatory Ca response was suppressed by the inhibition of H Rs with pyrilamine, whereas H R was abundantly expressed at the protein level. We further found that histamine-induced intracellular Ca oscillations were initiated by endogenous Ca mobilization through inositol-1,4,5-trisphosphate- and nicotinic acid dinucleotide phosphate-sensitive channels and maintained over time by store-operated Ca entry. In addition, histamine evoked robust NO release that was prevented by interfering with the accompanying intracellular Ca oscillations, thereby confirming that the endothelial NO synthase is recruited by Ca spikes also in hCMEC/D3 cells. These data provide the first evidence that histamine evokes NO production from human cerebrovascular endothelial cells through intracellular Ca oscillations, thereby shedding novel light on the mechanisms by which this neuromodulator controls cerebral blood flow.
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http://dx.doi.org/10.1002/jcp.29071DOI Listing
February 2020

Associations between resilience and sociodemographic factors and depressive symptoms in women with systemic lupus erythematosus.

J Psychosom Res 2019 07 9;122:39-42. Epub 2019 May 9.

Puebla Research Coordination, High-Specialty Medical Unit, Specialty Hospital of Puebla, Instituto Mexicano del Seguro Social, Puebla, Mexico.

Objective: To compare resilience in women with SLE and healthy women and determine whether sociodemographic factors and depressive symptoms were associated with resilience in patients with SLE.

Methods: This was a cross-sectional study. Participants were 123 women with SLE according to the ACR criteria and 132 age-matched healthy women (median = 45 (IQR = 34-54) years). Scales administered were: SLEDAI-2 K for disease activity, Graffar method, SLICC damage index, Center for Epidemiologic Studies Depression Scale, and the Spanish version of the Resilience Scale of Wagnild and Young. The statistical analysis was made using the Student t, Mann Whitney, Chi-square, and Spearman's Rho tests and multivariate analysis with a generalized linear model (GLM). Statistical significance was set as p < .05.

Results: There were no differences in resilience scores between women with SLE and healthy women (median = 80, IQR = 75-87 vs. median = 80, IQR = 74-86.75, p = .38), although patients with SLE had higher self-efficacy scores (median = 47 IQR = 43-50 vs. median = 45, IQR = 42-48, p = .002) and depressive symptoms (median = 10, IQR = 5-18 vs. median = 8, IQR = 5-18, p = .01). The overall resilience score correlated with depressive symptoms (r = -0.537, p < .01). The GLM showed no association between sociodemographic factors and resilience in patients with SLE.

Conclusions: Resilience did not differ between women with SLE and healthy women. In patients with SLE, depressive symptoms may influence resilience and its domains, but sociodemographic factors do not.

Public Health Significance Statement: The results suggest that resilience was similar between females with systemic lupus erythematosus (SLE) and age-matched healthy women. Depressive symptoms correlated negatively with resilience in patients with SLE. Sociodemographic factors were not associated with resilience in patients with SLE.
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http://dx.doi.org/10.1016/j.jpsychores.2019.05.002DOI Listing
July 2019

Clinical relevance of monitoring serum adalimumab levels in axial spondyloarthritis.

Rheumatol Int 2019 05 21;39(5):841-849. Epub 2019 Mar 21.

Clinical Medicine Department, Universitas Miguel Hernández, Elche, Alicante, Spain.

Our aim was to assess the relationship between serum adalimumab levels, anti-drug antibodies (ADA) and disease activity in patients with axial spondylarthritis (SpA). We have carried out a single-centre cross-sectional study. adalimumab and ADA levels were analysed with ELISA and correlated with SpA activity using BASDAI and ASDAS scores. Adalimumab cut-off value was calculated to discriminate inactive disease/low disease activity (BASDAI < 4; ASDAS < 2.1) from moderate/high disease activity (BASDAI ≥ 4; ASDAS ≥ 2.1), using a receiver operating characteristic (ROC) curve. Up to January 2016, 51 consecutive patients were included. The median (range) age was 46.6 (18-68) and 47.1% were women. ADA prevalence was 27.5%, with none detected in the 21.6% receiving concomitant disease-modifying antirheumatic drugs (DMARDs) (p = 0.021). Adalimumab level was normal (> 3 mg/l) in 36 patients (70.6%), all without ADA. Fifteen patients (29.4%) had subtherapeutic adalimumab levels (< 3 mg/l), with ADA in 14 (93%). Median adalimumab (mg/l) was significantly higher in patients with inactive disease/low disease activity: BASDAI < 4 vs ≥ 4: 9.5 vs 2.6 (p < 0.01); ASDAS-CRP < 2.1 vs ≥ 2.1: 9.3 vs 0.3 (p < 0.001); ASDAS-ESR < 2.1 vs ≥ 2.1: 9.9 vs 3.0 (p < 0.001), and this finding was consistent with the result of the multivariate model. Patients with inactive disease/low disease activity presented significantly lower ADA levels. The adalimumab level cut-offs and area under the curve (AUC) obtained in the ROC curves were: ASDAS-CRP (< 2.1) 4.6 mg/l (AUC 81.2%; 95% CI 67.5-94.9; p < 0.001); ASDAS-ESR (< 2.1) 7.7 mg/l (AUC 82.4%; 95% CI 69.3-95.5; p < 0.001); BASDAI (< 4) 6.4 mg/l (AUC 73.5%; 95% CI 58.6-88.3; p < 0.01). In conclusion, presence of ADA in axial SpA patients treated with adalimumab was associated with lower serum drug levels. ADA levels were lower and adalimumab levels were higher in patients with inactive disease/low disease activity based on BASDAI and ASDAS indices. Concomitant treatment with MTX reduces de likelihood of finding ADA. Serum adalimumab levels above 4.6 mg/l are recommended to avoid compromising efficacy.
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http://dx.doi.org/10.1007/s00296-019-04288-7DOI Listing
May 2019

Reply to the editor.

Autoimmun Rev 2019 04 10;18(4):435-436. Epub 2019 Feb 10.

Department of Autoimmune Diseases, Hospital Clinic, Barcelona, Catalonia, Spain. Electronic address:

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http://dx.doi.org/10.1016/j.autrev.2019.02.007DOI Listing
April 2019

The Role of Circulating Regulatory T Cell Levels on Subclinical Atherosclerosis and Cardiovascular Risk Factors in Women with Systemic Lupus Erythematosus.

Mediators Inflamm 2018 18;2018:3271572. Epub 2018 Dec 18.

Laboratorios Clínicos de Puebla, Puebla, Mexico.

The increase in cardiovascular disease (CVD) in patients with systemic lupus erythematosus (SLE) is not fully explained by traditional CVD risk factors. Regulatory T cells (Treg cells) are considered atheroprotective. We investigated the relationship between the absolute number of different phenotypes of Treg cells and abnormal carotid intima-media thickness (IMT) in women with SLE. Sixty-six women with SLE with no history of CV disease were included. Carotid IMT was quantified by ultrasound. Abnormal carotid IMT was defined as ≥0.8 mm and two groups were compared according to this definition. Flow cytometry was used to analyze Foxp3 and Helios expression in peripheral blood CD4 T cells. A significantly higher level of absolute CD4+CD25+FoxP3 T cells was present in patients with abnormal carotid IMT compared with those without (1.795 ± 4.182 cells/l vs. 0.274 ± 0.784 cells/l; = 0.003). However, no correlations were found between any Treg cell phenotypes and carotid IMT. Only the absolute number of CD4+CD45RA+FoxP3 T cells was significantly decreased in SLE patients with low HDL cholesterol compared with those with normal HDL cholesterol (0.609 ± 2.362 cells/l vs. 1.802 ± 4.647 cells/l; = 0.009 and 15.358 ± 11.608 cells/l vs. 28.274 ± 34.139; = 0.012, respectively). In conclusion, in SLE women, diminished levels of Treg cells based on flow cytometry were not a good indicator of abnormal carotid IMT.
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http://dx.doi.org/10.1155/2018/3271572DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6312616PMC
May 2019

Prevalence of cervical HPV infection in women with systemic lupus erythematosus: A systematic review and meta-analysis.

Autoimmun Rev 2019 Feb 18;18(2):184-191. Epub 2018 Dec 18.

Department of Autoimmune Diseases, Hospital Clinic, Barcelona, Catalonia, Spain. Electronic address:

Objective: The objectives of this systematic review and meta-regression were: 1) to compare the prevalence of cervical HPV infection between SLE patients and healthy controls and 2) to evaluate the relationship between cervical HPV infection and traditional and SLE-related risk factors for cervical HPV infection in these patients.

Methods: We conducted a systematic literature review (PubMed, Cochrane Library, Embase, Virtual Health Library and SciELO databases) following PRISMA guidelines and using meta-regression to investigate the pooled prevalence of cervical HPV infection in adult women with SLE. The articles included were independently evaluated by two investigators who extracted information on study characteristics, defined outcomes, risk of bias and summarized strength of evidence [Quality of evidence using the Oxford Centre for evidence-based medicine (EBM) Levels of Evidence]. Using meta-regression, we further analyzed whether factors such as multiple sexual partners and immunosuppressive therapy were associated with HPV prevalence. We evaluated the quality of evidence included using the Oxford Centre for EBM levels of evidence. Pooled odds ratios (ORs) and 95% confidence intervals (CI) were calculated for studies providing data on HPV prevalence in women with SLE and in healthy controls.

Results: A total of 687 articles were identified; 9 full-text articles examining the prevalence of cervical HPV infection in SLE women were included, comprising 751 SLE women. Eight studies employed PCR using general primers. The HPV prevalence varied from 3.1% to 80.7%. In the random effects meta-analysis, the pooled prevalence of cervical HPV infection in SLE vs. controls was 34.15% (95% CI: 19.6%-52.5%) vs. 15.3% (95% CI 0.79-27.8%), OR = 2.87 (95% CI: 2.20-3.76) p < .0001, with large between-study heterogeneity (I = 95.4%). When only SLE women were evaluated, meta-regression showed no significant differences between patients with and without a background of multiple sexual partners and any immunosuppressive therapy. In addition, the prevalence of cervical HPV infection did not significantly differ between SLE patients on azathioprine or cyclophosphamide.

Conclusions: This meta-analysis suggests that the prevalence of cervical HPV infection is higher in SLE women than in healthy controls. However, multiple sexual partners and any immunosuppressive therapy or specific immunosuppressive treatment (azathioprine and cyclophosphamide) were not associated with the prevalence of cervical HPV infection.
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http://dx.doi.org/10.1016/j.autrev.2018.09.001DOI Listing
February 2019

Phosphatidylethanolamine Induces an Antifibrotic Phenotype in Normal Human Lung Fibroblasts and Ameliorates Bleomycin-Induced Lung Fibrosis in Mice.

Int J Mol Sci 2018 Sep 14;19(9). Epub 2018 Sep 14.

Facultad de Medicina, Benemérita Universidad Autónoma de Puebla, Puebla 72410, Mexico.

Lung surfactant is a complex mixture of phospholipids and specific proteins but its role in the pathogenesis of interstitial lung diseases is not established. Herein, we analyzed the effects of three representative phospholipid components, that is, dipalmitoilphosphatidylcoline (DPPC), phosphatidylglycerol (PG) and phosphatidylethanolamine (PE), on collagen expression, apoptosis and Ca signaling in normal human lung fibroblasts (NHLF) and probed their effect in an experimental model of lung fibrosis. Collagen expression was measured with RT-PCR, apoptosis was measured by using either the APOPercentage assay kit (Biocolor Ltd., Northern Ireland, UK) or the Caspase-Glo 3/7 assay (Promega, Madison, WI, USA) and Ca signaling by conventional epifluorescence imaging. The effect in vivo was tested in bleomycin-induced lung fibrosis in mice. DPPC and PG did not affect collagen expression, which was downregulated by PE. Furthermore, PE promoted apoptosis and induced a dose-dependent Ca signal. PE-induced Ca signal and apoptosis were both blocked by phospholipase C, endoplasmic reticulum pump and store-operated Ca entry inhibition. PE-induced decrease in collagen expression was attenuated by blocking phospholipase C. Finally, surfactant enriched with PE and PE itself attenuated bleomycin-induced lung fibrosis and decreased the soluble collagen concentration in mice lungs. This study demonstrates that PE strongly contributes to the surfactant-induced inhibition of collagen expression in NHLF through a Ca signal and that early administration of Beractant enriched with PE diminishes lung fibrosis in vivo.
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http://dx.doi.org/10.3390/ijms19092758DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6164566PMC
September 2018

Role of Infectious Diseases in the Antiphospholipid Syndrome (Including Its Catastrophic Variant).

Curr Rheumatol Rep 2018 08 20;20(10):62. Epub 2018 Aug 20.

Department of Autoimmune Diseases, Hospital Clinic, Villarroel, 170, 08036, Barcelona, Catalonia, Spain.

Purpose Of Review: The antiphospholipid syndrome (APS) is characterized by the development of thrombotic events and pregnancy morbidity in the presence of antiphospholipid antibodies (aPL). An infectious etiology for this syndrome has been postulated. The present review is aimed to summarize recent evidence about the role of infections and vaccines in the pathogenesis of the APS (including its catastrophic variant).

Recent Findings: There is an increased risk of developing aPL in various infections, particularly in viral infections. The most frequent infection related to aPL has been hepatitis C virus. These antibodies may be associated with thromboembolic events, including catastrophic APS. There is a link between vaccinations, such as the tetanus toxoid and aPL, due to molecular mimicry between the two molecules. Accumulated evidence supports that the presence of aPL is associated with a variety of infections, including viruses, bacteria, fungi, and parasites, and the main mechanism to explain this correlation is molecular mimicry. Moreover, a link between vaccinations, such as the tetanus toxoid, and APS has also been described.
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http://dx.doi.org/10.1007/s11926-018-0773-xDOI Listing
August 2018

Bone mineral density and vertebral fractures in patients with systemic lupus erythematosus: A systematic review and meta-regression.

PLoS One 2018 13;13(6):e0196113. Epub 2018 Jun 13.

Department of Autoimmune Diseases, Hospital Clinic, Barcelona, Catalonia, Spain.

Background: Observational studies have indicated a high but heterogeneous prevalence of low bone mineral density (BMD) and vertebral fractures (VF) in patients with systemic lupus erythematosus (SLE). Therefore, the objectives of this systematic review and meta-regression were: 1) to compare BMD between SLE patients and healthy controls and 2) to evaluate the relationship between BMD and glucocorticoid therapy and VF in SLE patients.

Methods And Findings: Articles were identified from electronic databases (PubMed, Embase, VHL, SciELO and the Cochrane Library). Prospective longitudinal and cross-sectional studies were considered for review. We evaluated the quality of the evidence included using the Oxford Centre for evidence-based medicine (EBM) Levels of Evidence. In total, 38 articles were identified and analyzed (3442 SLE cases and 6198 controls) in the analysis of BMD (9232 women and 408 men). There were significant differences in mean BMD between SLE patients and controls. BMD mean difference in cases/controls: -0.0566 95% CI (-0.071, -0.0439; p = < 0.0001). When only SLE patients were analyzed, the BMD did not significantly differ between patients who had or had not received glucocorticoid (GCT) therapy. 694 SLE patients were included in the analysis of VF (189 with VF vs. 505 without VF). Patients with VF had lower BMD than patients without VF (BMD mean difference without VF/with VF: 0.033 (95%CI: 0.006-0.060); p-value: 0.0156).

Conclusions: Patients with SLE had lower BMD than healthy controls. Moreover, SLE patients with VF had lower BMD than patients without VF. However, our data did not show that GCT therapy had an impact on BMD.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0196113PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5999233PMC
November 2018

Inflammation and atherosclerosis: Cardiovascular evaluation in patients with autoimmune diseases.

Autoimmun Rev 2018 Jul 3;17(7):703-708. Epub 2018 May 3.

Department of Autoimmune Diseases, Institut Clínic de Medicina i Dermatologia, Hospital Clínic, IDIBAPS, University of Barcelona, Barcelona, Catalonia, Spain. Electronic address:

Evidence now indicates that inflammation contributes considerably to the initiation and progression of atherosclerosis and active inflammatory processes may trigger plaque rupture and enhance the risk of coronary thrombosis leading to a clinical ischemic event. Interest in characterizing inflammatory markers that predict clinical events have dominated clinical investigation. Such markers include C-reactive protein, Fibrinogen and a number of interleukins. Human macrophages avidly phagocytize cholesterol crystals. These cholesterol crystals induce a dose-dependent secretion of mature Interleukin 1-beta (IL-1β) from human monocytes and macrophages (an NLRP3 inflammasome-mediated pathway). Since IL-1β production leads to increased levels of IL-6 and C-reactive protein, this could be a mechanistic link between early deposition of cholesterol crystals within the vessel wall to the macrophage-monocyte interactions that initiate fatty streaks and promote local atherosclerotic progression. We have entered a time where a pure anti-inflammatory drug without significant effects on lipids or any other traditional cardiovascular risk factor decreased cardiovascular events. Patients with autoimmune diseases are at increase cardiovascular risk. In this review we describe the link between inflammation and atherosclerosis. Furthermore we explore the data regarding primary prevention, cardiac imaging for risk stratification and the implications of targeting inflammation in patients with autoimmune disease.
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http://dx.doi.org/10.1016/j.autrev.2018.01.021DOI Listing
July 2018

Vβ T cell receptor (TCR) genes in circulating cells of patients with systemic lupus erythematosus and their healthy relatives

Gac Med Mex 2018 ;154(1):74-79

Departamento de Inmunología y Reumatología, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Ciudad de México. México.

Objective: We investigated the proportion of Vβ T cell receptor (TCR) gene expression in peripheral CD3+ lymphocytes in familial and non-familial systemic lupus erythematosus (SLE) patients.

Method: The Vβ TCR repertoire was studied in 14 families in which several members had SLE. The Vβ TCR usage in SLE patients (n = 27) was compared with that in healthy members of these multiplex families (n = 47), in 37 sporadic SLE patients who had no relatives with SLE, and in 15 healthy unrelated controls. Vβ TCR repertoire expression was studied by multiparameter flow cytometry with the use of an array of 24 different Vβ TCR gene family-specific monoclonal antibodies.

Results: We found the same Vβ TCR expression profile in the comparisons between sporadic SLE and familial SLE cases and healthy relatives, which included increased expression of Vβ 5.2, Vβ 11 and Vβ 16, and lower expression of Vβ 3, Vβ 4, Vβ 7.1 and Vβ 17. Interestingly, solely Vβ 17 was differentially expressed among sporadic and familial SLE. Also, increased expression of Vβ 9 was the hallmark among familial SLE (casesand h ealthy relatives) in comparison to controls.

Conclusion: These results highlight the notion that the final profile of the Vβ TCR repertoire seen in familial and non-familial SLE seems to arise from the interaction of genetic, environmental, and immunoregulatory factors. Furthermore, it may contribute to the immunologic abnormalities affecting relatives of SLE patients.
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http://dx.doi.org/10.24875/GMM.17002697DOI Listing
June 2018

GRADE system, systematic and transparent evaluation.

Reumatol Clin 2018 Mar - Apr;14(2):65-67. Epub 2017 Oct 27.

Unidad de Investigación de Enfermedades Autoinmunes Sistémicas, Hospital General Regional N.(o) 36, IMSS, Puebla, Puebla, México; Departamento de Reumatología e Inmunología, Facultad de Medicina, Benemérita Universidad Autónoma de Puebla, Puebla, Puebla, México. Electronic address:

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http://dx.doi.org/10.1016/j.reuma.2017.07.010DOI Listing
October 2018

Clinical relevance of P-glycoprotein activity on peripheral blood mononuclear cells and polymorphonuclear neutrophils to methotrexate in systemic lupus erythematosus patients.

Clin Rheumatol 2017 Oct 14;36(10):2267-2272. Epub 2017 Jun 14.

Laboratorios Clínicos de Puebla, Puebla, México.

To elucidate the relationship between P-glycoprotein activity on peripheral blood leukocytes of systemic lupus erythematosus (SLE) patients with lupus arthritis and the clinical response to methotrexate. An observational study was made in patients with SLE according to ACR criteria 1997 who had arthralgia and arthritis and received methotrexate for ≥3 months. Methotrexate responders and non-responders were compared according to the Clinical Disease Activity Index. Mononuclear cells and polymorphonuclear neutrophils were isolated from SLE patients and P-glycoprotein expression was measured using the relative fluorescence index and percentage of positive cells. The chi-square test was used to compare P-glycoprotein activity between responders and non-responders. Thirty-two patients with a mean age of 45.4 ± 10.7 years were included: 34.4% had a response to methotrexate and 65.6% did not. Mean relative fluorescence units of both mononuclear cells and polymorphonuclear neutrophils were significantly lower in patients with a good response (7.0 ± 4.3 vs. 9.6 ± 3.8; p = 0.041 and 4.2 ± 3.5 vs. 7.6 ± 4.0; p = 0.004). The prevalence of low fluorescence levels (<6 relative fluorescence units), signifying higher P-glycoprotein activity of both mononuclear cells and polymorphonuclear neutrophils, was higher in methotrexate responders than in non-responders (27.3 vs. 4.8%; p = 0.10 and 81.8 vs. 23.8%; p = 0.003, respectively). In SLE patients with joint involvement treated with methotrexate, P-glycoprotein activity was higher in responders to methotrexate than in non-responders. Further studies are required to determine the mechanisms behind this finding and whether P-glycoprotein activity mediates alterations in methotrexate efficacy.
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http://dx.doi.org/10.1007/s10067-017-3728-0DOI Listing
October 2017

Incidence of Vertebral Fractures in Women with Systemic Lupus Erythematosus After 8 Years of Follow-Up.

Calcif Tissue Int 2017 09 15;101(3):291-299. Epub 2017 May 15.

Department of Autoimmune Diseases, Hospital Clinic, Catalonia, Spain.

The aim of this study was to evaluate possible associations between potential risk factors and the occurrence of established vertebral fractures (VF) in Mexican patients with systemic lupus erythematosus (SLE). Consecutive patients with SLE were enrolled in a prospective, observational study from 2006 to 2015. Information on potential risk factors, including demographics, clinical data, and bone mineral density (BMD) at the lumbar spine and hip on dual-energy X-ray absorptiometry was collected at baseline and follow-up. Semiquantitative analysis was used to determine incident VF on lateral thoracic and lumbar radiographs, defined as any vertebral body graded normal at baseline and at least mildly deformed (20-25% reduction or more in any vertebral height) during follow-up. Differences in baseline characteristics were assessed in patients with and without new radiographic VF. Of 110 SLE patients included, with a median follow-up of 8 (IQR 8-9) years, 22 (20%) had radiographic VF at baseline; 35 (32%) patients had a new VF. The annual incidence rate of new morphometric VF was 3.5 (95% CI 2.4-4.91) per 100 patient/years. Most fractures were mild or moderate and biconcave shaped. Incident VF were significantly associated with baseline BMD at the total hip and longer disease duration. Cumulative glucocorticoid dose, postmenopausal status, and previous prevalent VF were not associated with VF. In this SLE cohort in daily clinical practice, new VF were frequently present in SLE patients, especially those with longer disease duration and low-hip BMD.
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http://dx.doi.org/10.1007/s00223-017-0286-zDOI Listing
September 2017

Vitamin D and Sjögren syndrome.

Autoimmun Rev 2017 Jun 12;16(6):587-593. Epub 2017 Apr 12.

Department of Autoimmune Diseases, Hospital Clinic, Barcelona, Catalonia, Spain. Electronic address:

The immunomodulatory effects of vitamin D have been extensively studied in the context of autoimmunity. Multiple studies have demonstrated a high prevalence of vitamin D deficiency in autoimmune diseases. Recently, a possible protective role of vitamin D in autoimmunity has been described; however, this function remains controversial. Few studies have investigated the role of vitamin D in patients with Sjögren syndrome (SS). In this review, we compiled the main features of SS pathogenesis, the vitamin D immunomodulatory effects and the possible interaction between both. Data suggests that vitamin D may play a role in the SS pathogenesis. In addition, vitamin D low levels have been found in SS patients, which are associated with extra-glandular manifestations, such as lymphoma or neuropathy, suggesting a possible benefit effect of vitamin D in SS.
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http://dx.doi.org/10.1016/j.autrev.2017.04.004DOI Listing
June 2017