Publications by authors named "Yago Leira"

29 Publications

  • Page 1 of 1

Periodontal Inflamed Surface Area Mediates the Link between Homocysteine and Blood Pressure.

Biomolecules 2021 Jun 12;11(6). Epub 2021 Jun 12.

Clinical Research Unit (CRU), Egas Moniz Interdisciplinary Research Center, Egas Moniz-Cooperativa de Ensino Superior, 2829-511 Almada, Portugal.

Here, we assess the association between homocysteine (Hcy) serum levels and periodontal status in a large representative sample of the National Health and Nutrition Examination Survey (NHANES). Using the 2001-2002 and 2003-2004 NHANES databases, participants with a periodontal examination, medical self-reported data, blood pressure (BP) and blood samples to determine complete blood count, C-reactive protein (CRP) and Hcy levels. We then calculated the periodontal inflamed surface area (PISA) and the periodontal epithelial surface area (PESA). Multivariable regression analysis explored the association between Hcy, periodontal measures and BP. Mediation analysis was performed to understand the effect of PISA and PESA in the link between Hcy and BP. 4021 participants fulfilled the inclusion criteria. Hcy levels showed significant correlations with systolic BP, diastolic BP, PISA, PESA and age. PESA showed to be significantly associated with Hcy both for the crude and adjusted models ( < 0.01), but not PISA ( > 0.05). In the association of Hcy with systolic BP, PISA significantly mediated 17.4% and PESA 0.9%. In the association of Hcy with diastolic BP, PISA significantly mediated 16.3% and PESA 47.2%. In conclusion, Hcy and periodontitis are associated. Further, both PISA and PESA significantly mediated the association of Hcy with systolic BP and diastolic BP. Future studies shall deepen the mechanisms by which Hcy levels increase in a clinical situation of periodontitis.
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http://dx.doi.org/10.3390/biom11060875DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8231519PMC
June 2021

Remote Ischemic Preconditioning Protects Against Endothelial Dysfunction in a Human Model of Systemic Inflammation: A Randomized Clinical Trial.

Arterioscler Thromb Vasc Biol 2021 Aug 10;41(8):e417-e426. Epub 2021 Jun 10.

Periodontology Unit, UCL Eastman Dental Institute and Hospital (M.O., Y.L., F.D.), University College London, United Kingdom.

[Figure: see text].
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http://dx.doi.org/10.1161/ATVBAHA.121.316388DOI Listing
August 2021

Network Protein Interaction in the Link between Stroke and Periodontitis Interplay: A Pilot Bioinformatic Analysis.

Genes (Basel) 2021 May 20;12(5). Epub 2021 May 20.

Evidence-Based Hub, Clinical Research Unit (CRU), Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Egas Moniz-Cooperativa de Ensino Superior, CRL, 2829-511 Caparica, Portugal.

The clinical interaction between stroke and periodontitis has been consistently studied and confirmed. Hence, exploring potentially new protein interactions in this association using bioinformatic strategies presents potential interest. In this exploratory study, we conducted a protein-protein network interaction (PPI) search with documented encoded proteins for both stroke and periodontitis. Genes of interest were collected via GWAS database. The STRING database was used to predict the PPI networks, first in a sensitivity purpose (confidence cut-off of 0.7), and then with a highest confidence cut-off (0.9). Genes over-representation was inspected in the final network. As a result, we foresee a prospective protein network of interaction between stroke and periodontitis. Inflammation, pro-coagulant/pro-thrombotic state and, ultimately, atheroma plaque rupture is the main biological mechanism derived from the network. These pilot results may pave the way to future molecular and therapeutic studies to further comprehend the mechanisms between these two conditions.
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http://dx.doi.org/10.3390/genes12050787DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8160956PMC
May 2021

Economic burden of periodontitis in the United States and Europe - an updated estimation.

J Periodontol 2021 May 30. Epub 2021 May 30.

Clinical Research Unit (CRU), Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Egas Moniz - Cooperativa de Ensino Superior, Almada, Portugal.

Background: The aim of this study is to estimate the direct and indirect economic burdens of periodontal disease in the US and in Europe.

Methods: We used the most recent data available for the US and for Europe (32 European countries) to estimate the cost of periodontal disease. Global health, dental and periodontal expenditures were estimated. We tried to estimate the direct and the indirect costs of periodontitis. Indirect costs, those related to productivity losses, are a consequence of periodontal disease proper, plus edentulism and caries because of periodontal disease.

Results: In 2018, the aggregate cost in the US was estimated at $3.49B and €2.52B in Europe. Indirect costs because of periodontal disease amounted to $150.57B (95% confidence interval [CI]: 103.32-189.87) in the US countries and €156.12B (95% CI: 123.72-221.86) in Europe. The majority of the projected indirect costs were because of edentulism related to periodontal disease and periodontal disease. Indirect costs were the majority of the estimated economic impact with an average of 0.73% (95% CI: 0.50%-0.93%) of annual gross domestic product in the US and 0.99% (95% CI: 0.78%-1.40%) in Europe.

Conclusions: Periodontal disease caused an estimated loss of $154.06B in the US and €158.64B in Europe, in 2018. These results show that the economic burden of periodontal disease is significant and its indirect costs are impactful.
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http://dx.doi.org/10.1002/JPER.21-0111DOI Listing
May 2021

The Role of Inflammatory Diet and Vitamin D on the Link between Periodontitis and Cognitive Function: A Mediation Analysis in Older Adults.

Nutrients 2021 Mar 12;13(3). Epub 2021 Mar 12.

Evidence-Based Hub, Clinical Research Unit, Centro de Investigação Interdisciplinar Egas Moniz, 2829-511 Almada, Portugal.

Patients suffering from periodontitis are at a higher risk of developing cognitive dysfunction. However, the mediation effect of an inflammatory diet and serum vitamin D levels in this link is unclear. In total, 2062 participants aged 60 years or older with complete periodontal diagnosis and cognitive tests from the National Health and Nutrition Examination Survey (NHANES) 2011-2012 and 2013-2014 were enrolled. The Consortium to Establish a Registry for Alzheimer's disease (CERAD) word learning subtest (WLT) and CERAD delayed recall test (DRT), the animal fluency test (AFT) and the digit symbol substitution test (DSST) was used. Dietary inflammatory index (DII) was computed via nutrition datasets. Mediation analysis tested the effects of DII and vitamin D levels in the association of mean probing depth (PD) and attachment loss (AL) in all four cognitive tests. Periodontitis patients obtained worse cognitive test scores than periodontally healthy individuals. DII was negatively associated with CERAD-WLT, CERAD-DRT, AFT and DSST, and was estimated to mediate between 9.2% and 36.4% of the total association between periodontitis with cognitive dysfunction ( < 0.05). Vitamin D showed a weak association between CERAD-DRT, AFT and DSST and was estimated to between 8.1% and 73.2% of the association between periodontitis and cognitive dysfunction ( < 0.05). The association between periodontitis and impaired cognitive function seems to be mediated both by a proinflammatory dietary load and vitamin D deficiency. Future studies should further explore these mediators in the periodontitis-cognitive decline link.
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http://dx.doi.org/10.3390/nu13030924DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8001166PMC
March 2021

Mild systemic inflammation enhances response to OnabotulinumtoxinA in chronic migraineurs.

Sci Rep 2021 01 13;11(1):1092. Epub 2021 Jan 13.

Clinical Neurosciences Research Laboratory, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, Spain.

The anti-inflammatory effect of OnabotulinumtoxinA (OnabotA) has been a matter of discussion for many years. In chronic migraine, however, increased pro-inflammatory state is associated with good response to OnabotA. We aimed to investigate whether a mild systemic inflammatory state elicited by a common oral infection (periodontitis) could enhance treatment response to OnabotA. In this study, we included 61 chronic migraineurs otherwise healthy treated with OnabotA of which 7 were poor responders and 54 good responders. Before receiving OnabotA therapy, all participants underwent a full-mouth periodontal examination and blood samples were collected to determine serum levels of calcitonin gene-related peptide (CGRP), interleukin 6 (IL-6), IL-10 and high sensitivity C-reactive protein (hs-CRP). Periodontitis was present in 70.4% of responders and 28.6% of non-responders (P = 0.042). Responders showed greater levels of inflammation than non-responders (IL-6: 15.3 ± 8.7 vs. 9.2 ± 4.7 ng/mL, P = 0.016; CGRP: 18.8 ± 7.6 vs. 13.0 ± 3.1 pg/mL, P = 0.002; and hs-CRP: 3.9 ± 6.6 vs. 0.9 ± 0.8 mg/L, P = 0.003). A linear positive correlation was found between the amount of periodontal tissue inflamed in the oral cavity and markers of inflammation (IL-6: r = 0.270, P = 0.035; CGRP: r = 0.325, P = 0.011; and hs-CRP: r = 0.370, P = 0.003). This report shows that in presence of elevated systemic inflammatory markers related to periodontitis, OnabotA seems to reduce migraine attacks. The changes of scheduled inflammatory parameters after treatment and subsequent assessment during an adequate period still need to be done.
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http://dx.doi.org/10.1038/s41598-020-80283-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7806961PMC
January 2021

Iron Deposits in Periaqueductal Gray Matter Are Associated with Poor Response to OnabotulinumtoxinA in Chronic Migraine.

Toxins (Basel) 2020 07 28;12(8). Epub 2020 Jul 28.

Department of Neurology, Headache Unit, Hospital Clinico Universitario, Universidade de Santiago de Compostela, 15706 Santiago de Compostela, Spain.

Previous studies have reported increased brain deposits of iron in patients with chronic migraine (CM). This study aims to determine the relation between iron deposits and outcome after treatment with OnabotulinumtoxinA (OnabotA). Demographic and clinical data were collected for this study through a prospective cohort study including 62 CM patients treated with OnabotA in the Hospital Clínico Universitario de Santiago de Compostela (Spain). Demographic and clinical variables were registered. Selected biomarkers in plasma during interictal periods (calcitonin gene-related peptide (CGRP) and pentraxin-3 (PTX3)) and neuroimaging changes (iron deposits in the red nucleus (RN), substantia nigra (SN), globus pallidus (GP), and periaqueductal gray matter (PAG), and white matter lesions (WML)) were determined. Subjects were classified in responders (≥50% reduction in headache days) or non-responders (<50%). Responders to treatment were younger (mean age difference = 12.2; 95% confidence interval (CI): 5.4-18.9, = 0.001), showed higher serum levels of CGRP (≥50 ng/mL) and PTX3 (≥1000 pg/mL) and smaller iron deposits in the GP and PAG (mean difference = 805.0; 95% CI: 37.9-1572.1 μL, = 0.040 and mean difference = 69.8; 95% CI: 31.0-108.6 μL, = 0.008; respectively). Differences in PAG iron deposits remained significant after adjusting for age (mean difference = 65.7; 95% CI: 22.8-108.6 μL, = 0.003) and were associated with poor response to OnabotA after adjustment for clinical and biochemical variables (odds ratio (OR) = 0.963; 95% CI: 0.927-0.997, = 0.041). We conclude that larger PAG iron deposits are associated with poor response to OnabotA in CM.
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http://dx.doi.org/10.3390/toxins12080479DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7472356PMC
July 2020

Association between Periodontitis and High Blood Pressure: Results from the Study of Periodontal Health in Almada-Seixal (SoPHiAS).

J Clin Med 2020 May 23;9(5). Epub 2020 May 23.

Clinical Research Unit (CRU), Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Instituto Universitário Egas Moniz (IUEM), 2829-511 Caparica, Portugal.

Periodontitis is a common chronic inflammatory disease which could have an important impact on blood pressure (BP). This study aimed to explore (a) the association between periodontal health and BP in a large representative cohort, (b) the predictive value of diagnosis of periodontitis in undiagnosed raised BP and (c) whether age is a mediator of this relationship. In total, 1057 randomly recruited individuals (mean age, 60.9 ± 16.3 years, 57.7% women) underwent periodontal clinical assessment and one-single BP measurement using an automated sphygmomanometer device. Logistic and linear regression models were used to estimate the odds of hypertension based on periodontitis case definitions. Mediation analysis was performed to understand the effect of age on the association of periodontitis with hypertension. Adjusted logistic model for gender, smoking habits and body mass index confirmed the association between high BP and periodontitis (OR = 2.31, 95%CI: 1.75-3.04, < 0.001). Among 168 participants with undiagnosed high BP (15.9% of the study sample), 62.5% had periodontitis ( = 105). In this study, the association between periodontitis with both systolic blood pressure (SBP) (77.6%, < 0.001) and diastolic blood pressure (DBP) (66.0%, < 0.001) was mediated by age. Periodontitis is closely linked to BP in a representative Portuguese population.
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http://dx.doi.org/10.3390/jcm9051585DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7291060PMC
May 2020

Pentraxin 3 (PTX3): A Molecular Marker of Endothelial Dysfunction in Chronic Migraine.

J Clin Med 2020 Mar 20;9(3). Epub 2020 Mar 20.

Headache Unit, Department of Neurology, University Clinical Hospital, Universidade de Santiago de Compostela, 15706 Santiago de Compostela, Spain.

Even though endothelial dysfunction is known to play a role in migraine pathophysiology, studies regarding levels of endothelial biomarkers in migraine have controversial results. Our aim was to evaluate the role of pentraxin 3 (PTX3) and soluble tumour necrosis factor-like weak inducer of apoptosis (sTWEAK) as potential biomarkers of endothelial dysfunction in chronic migraine (CM). We performed a case-control study including 102 CM patients and 28 control subjects and measured serum levels of markers of endothelial dysfunction (PTX3 and sTWEAK) and inflammation [high-sensitivity C-reactive protein (hs-CRP)] as well as brachial artery flow-mediated dilation (FMD) during interictal periods. Interictal serum levels of PTX3 and sTWEAK were higher in CM patients than in controls (1350.6 ± 54.8 versus 476.1 ± 49.4 pg/mL, < 0.001 and 255.7 ± 21.1 versus 26.4 ± 2.6 pg/mL, < 0.0001; respectively). FMD was diminished in CM patients compared to controls (9.6 ± 0.6 versus 15.2 ± 0.9%, < 0.001). Both PTX3 and sTWEAK were negatively correlated with FMD (r = -0.508, < 0.001 and r = -0.188, = 0.033; respectively). After adjustment of confounders, PTX3 remained significantly correlated to FMD (r = -0.250, = 0.013). Diagnosis of CM was 68.4 times more likely in an individual with levels of PTX3 ≥ 832.5 pg/mL, suggesting that PTX3 could be a novel biomarker of endothelial dysfunction in CM.
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http://dx.doi.org/10.3390/jcm9030849DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7141491PMC
March 2020

Periodontitis and systemic markers of neurodegeneration: A case-control study.

J Clin Periodontol 2020 05 12;47(5):561-571. Epub 2020 Mar 12.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Santiago de Compostela, Spain.

Aim: To investigate whether periodontitis is associated with amyloid beta (Aβ) peptides and whether systemic inflammation could act as a potential mediator of this link.

Materials And Methods: A case-control study was designed including 75 patients with periodontitis (cases) and 75 age-balanced and gender-matched participants without periodontitis (controls). Full-mouth periodontal evaluation was performed in all participants. Demographic, clinical and behaviour data were also recorded. Fasting blood samples were collected, and serum levels of interleukin 6 (IL-6), high-sensitivity C-reactive protein (hs-CRP), Aβ and Aβ were determined.

Results: Cases showed higher levels of IL-6 (8.7 ± 3.2 vs. 4.8 ± 0.5 pg/ml), hs-CRP (3.3 ± 1.2 vs. 0.9 ± 0.7 mg/L), Aβ (37.3 ± 6.0 vs. 30.3 ± 1.8 pg/ml) and Aβ (54.5 ± 10.6 vs. 36.5 ± 10.0 pg/ml) when compared to controls (all p < .001). Diagnosis of periodontitis was statistically significantly associated with circulating Aβ (  = 6.9, 95% CI: 5.4-8.3; p < .001) and Aβ (  = 17.8, 95% CI: 14.4-21.3; p < .001). Mediation analysis confirmed hs-CRP and IL-6 as mediators of this association.

Conclusions: Periodontitis is associated with increased peripheral levels of Aβ. This finding could be explained by enhanced systemic inflammation that can be seen in patients with periodontitis.
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http://dx.doi.org/10.1111/jcpe.13267DOI Listing
May 2020

Subgingival instrumentation for treatment of periodontitis. A systematic review.

J Clin Periodontol 2020 07;47 Suppl 22:155-175

Department of Periodontology, Institute of Odontology, The Sahlgrenska Academy at University of Gothenburg, Gothenburg, Sweden.

Objectives: To evaluate the efficacy of subgingival instrumentation (PICOS-1), sonic/ultrasonic/hand instruments (PICOS-2) and different subgingival instrumentation delivery protocols (PICOS-3) to treat periodontitis.

Methods: Systematic electronic search (CENTRAL/MEDLINE/EMBASE/SCOPUS/LILACS) to March 2019 was conducted to identify randomized controlled trials (RCT) reporting on subgingival instrumentation. Duplicate screening and data extraction were performed to formulate evidence tables and meta-analysis as appropriate.

Results: As only one RCT addressed the efficacy of subgingival instrumentation compared with supragingival cleaning alone (PICOS-1), baseline and final measures from 9 studies were considered. The weighted pocket depth (PD) reduction was 1.4 mm (95%CI: 1.0 1.7) at 6/8 months, and the proportion of pocket closure was estimated at 74% (95%CI: 64-85). Six RCTs compared hand and sonic/ultrasonic instruments for subgingival instrumentation (PICOS-2). No significant differences were observed between groups by follow-up time point or category of initial PD. Thirteen RCTs evaluated quadrant-wise versus full-mouth approaches (PICOS-3). No significant differences were observed between groups irrespective of time-points or initial PD. Five studies reported patient-reported outcomes, reporting no differences between groups.

Conclusions: Nonsurgical periodontal therapy by mechanical subgingival instrumentation is an efficacious means to achieve infection control in periodontitis patients irrespective of the type of instrument or mode of delivery. Prospero ID: CRD42019124887.
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http://dx.doi.org/10.1111/jcpe.13245DOI Listing
July 2020

Cell-Based Therapies for Alveolar Bone and Periodontal Regeneration: Concise Review.

Stem Cells Transl Med 2019 12 6;8(12):1286-1295. Epub 2019 Nov 6.

Unit of Periodontology, UCL Eastman Dental Institute, London, United Kingdom.

Current regenerative strategies for alveolar bone and periodontal tissues are effective and well adopted. These are mainly based on the use of a combination of synthetic/natural scaffolds and bioactive agents, obviating the incorporation of cells. However, there are some inherent limitations associated with traditional techniques, and we hypothesized that the use of cell-based therapies as part of comprehensive regenerative protocols may help overcome these hurdles to enhance clinical outcomes. We conducted a systematic review of human controlled clinical trials investigating the clinical and/or histological effect of the use of cell-based therapies for alveolar bone and periodontal regeneration and explored the translational potential of the different cell-based strategies identified in the included trials. A total of 16 studies (11 randomized controlled trials, 5 controlled clinical trials) were included for data synthesis and qualitative analysis with meta-analyses performed when appropriate. The results suggest a clinical benefit from the use of cell therapy. Improved outcomes were shown for alveolar ridge preservation, lateral ridge augmentation, and periodontal regeneration. However, there was insufficient evidence to identify best-performing treatment modalities amongst the different cell-based techniques. In light of the clinical and histological outcomes, we identify extraction socket and challenging lateral and vertical bone defects requiring bone block grafts as strong candidates for the adjuvant application of mesenchymal stem cells. Given the complexity, invasiveness, and costs associated with techniques that include "substantial manipulation" of tissues and cells, their additional clinical benefit when compared with "minimal manipulation" must be elucidated in future trials. Stem Cells Translational Medicine 2019;8:1286&1295.
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http://dx.doi.org/10.1002/sctm.19-0183DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6877771PMC
December 2019

Periodontitis and vascular inflammatory biomarkers: an experimental in vivo study in rats.

Odontology 2020 Apr 3;108(2):202-212. Epub 2019 Oct 3.

Clinical Neurosciences Research Laboratory, Clinical University Hospital, Health Research Institute of Santiago de Compostela (IDIS), Travesa da Choupana s/n, 15706, Santiago de Compostela, Spain.

The objective of this preclinical in vivo study was to determine changes in vascular inflammatory biomarkers in systemic circulation after injection of lipopolysaccharide (LPS) from Porphyromonas gingivalis (Pg) in rats. Experimental periodontitis was induced by injections of Pg-LPS. Gingival soft and hard tissues changes were analysed by means of magnetic resonance imaging and micro computed tomography. Serum levels of interleukin (IL)-6, IL-10, pentraxin (PTX) 3, and soluble fragment of tumor necrosis factor-like weak inducer of apoptosis (sTWEAK) were determined at baseline and 24 h, 7, 14, and 21 days after periodontal induction. Significant periodontal inflammation and alveolar bone loss were evident at the end of periodontal induction. Experimental periodontitis posed an acute systemic inflammatory response with increased serum levels of IL-6 and PTX3 at 24 h post-induction, followed by a significant overexpression of sTWEAK at 7 days. This inflammatory state was maintained until the end of the experiment (21 days). As expected, IL-10 serum levels were significantly lower during the follow-up compared to baseline concentrations. In the present animal model, experimental periodontitis is associated with increased systemic inflammation. Further studies are needed to confirm whether PTX3 and sTWEAK could be useful biomarkers to investigate potential mechanisms underlying the relationship between periodontitis and atherosclerotic vascular diseases.
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http://dx.doi.org/10.1007/s10266-019-00461-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7066291PMC
April 2020

Severe periodontitis is linked with increased peripheral levels of sTWEAK and PTX3 in chronic migraineurs.

Clin Oral Investig 2020 Feb 20;24(2):597-606. Epub 2019 May 20.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Santiago de Compostela, Spain.

Objectives: Periodontitis (PD) and chronic migraine (CM) have been recently linked, and inflammatory processes and vascular endothelial changes are hypothesized as potential mediators of this relationship. The aim of this cross-sectional analysis was to investigate the potential association of PD with vascular systemic inflammation and complement activation in patients with CM.

Materials And Methods: Ninety-four chronic migraineurs underwent a full-mouth periodontal evaluation and a measure of PD activity and severity, namely the periodontal inflamed surface area (PISA) was calculated for each patient. We divided CM patients according to their periodontal status: mild PD (N = 14), moderate PD (N = 22), severe PD (N = 19), and non-PD (N = 39). Serum levels of C-reactive protein (CRP), pentraxin 3 (PTX3), soluble tumor necrosis factor-like weak inducer of apoptosis (sTWEAK), and complements C3 and C4 were measured outside of migraine attacks.

Results: We found that severe periodontal patients had significantly higher circulating levels of PTX3 and sTWEAK compared with those without PD (2475.3 ± 1646.8 pg/mL vs. 516.6 ± 1193.8 pg/mL, P < 0.0001 and 672.4 ± 118.2 pg/mL vs. 485.7 ± 112.2 pg/mL, P < 0.0001; respectively). For the remaining biomarkers, no significant differences were found between groups. Severe PD was independently associated with higher levels of PTX3 (β = 1997.6, P < 0.0001) and sTWEAK (β = 187.1, P < 0.0001) but not with CRP, C3, and C4. PISA positively correlated to PTX3 (r = 0.475, P < 0.0001) and sTWEAK (r = 0.386, P < 0.0001).

Conclusions: Based on these preliminary results, severe PD was linked with vascular systemic inflammation in patients with CM. However, further longitudinal studies should be performed to confirm these findings.

Clinical Relevance: sTWEAK and PTX3 measured in serum could be used as biomarkers in the PD-CM link.
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http://dx.doi.org/10.1007/s00784-019-02950-9DOI Listing
February 2020

Periodontal inflammation is related to increased serum calcitonin gene-related peptide levels in patients with chronic migraine.

J Periodontol 2019 10 27;90(10):1088-1095. Epub 2019 May 27.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Santiago de Compostela, Spain.

Background: Recently, a relationship was found between periodontitis and chronic migraine. Calcitonin gene-related peptide (CGRP) is a key element in migraine pathophysiology. However, no information exists of the potential association between periodontal inflammation and CGRP in chronic migraine. The aim of the study was, therefore, to investigate whether there is a link between periodontitis and peripheral levels of CGRP in a cohort of patients with chronic migraine.

Methods: We included 102 chronic migraineurs and 77 age- and sex-matched individuals free of headache/migraine. Full-mouth periodontal parameters were recorded and the periodontal inflamed surface area (PISA) was calculated to quantify the periodontal inflammatory status for each participant. Sociodemographic data and comorbidities were assessed by means of a standard questionnaire. We collected blood samples and serum concentrations were done for CGRP, interleukin (IL)-6 and IL-10.

Results: In the chronic migraine group, patients with periodontitis had greater levels of serum CGRP (19.7 ± 6.5 versus 15.3 ± 6.2 pg/mL, P < 0.0001) and IL-6 (15.1 ± 9.2 versus 9.6 ± 6.3 pg/mL, P < 0.0001) while non-significant differences were observed with IL-10 (2.0 ± 1.0 versus 2.8 ± 1.5 pg/mL, P = 0.675) concentrations than those without periodontitis. PISA was independently associated with CGRP in patients with chronic migraine (β = 0.003; 95% confidence interval: 0.001 to 0.006, P = 0.031). PISA correlated positively with CGRP (r = 0.236; P = 0.017) and IL-6 (r = 0.262; P = 0.008) in chronic migraine.

Conclusions: Periodontal inflammation is associated with increased circulating levels of CGRP in chronic migraineurs. Elucidating the exact mechanisms through which periodontitis and CGRP are linked in these patients deserves further investigation.
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http://dx.doi.org/10.1002/JPER.19-0051DOI Listing
October 2019

Self-reported periodontitis and migraine: results from a multicenter, cross-sectional survey in Spain.

Odontology 2019 Oct 27;107(4):530-535. Epub 2019 Apr 27.

Periodontology Unit, UCL Eastman Dental Institute and Hospital, University College London, 256 Gray's Inn Road, London, WC1X 8LD, UK.

The aim of this study was to evaluate self-reported periodontitis (PD) prevalence in migraineurs as well as to investigate the association between both diseases. A cross-sectional survey was carried out including patients diagnosed with migraine attending 12 Spanish Headache Units. We determined diagnosis of PD administering a validated self-reported questionnaire. Socio-demographic, clinical and medical information, comorbidities, daily habits, migraine characteristics and medication were collected using a questionnaire. Of the 651 consecutive migraineurs included in the study, 393 suffered from chronic migraine (CM). Self-reported PD was detected in 327 patients with migraine (50.2%). Migraineurs with self-reported PD were significantly older and had a previous history of fibromyalgia, stress, anxiety, depression, and allodynia (all P < 0.001). Additionally, this group of patients consumed more topiramate (P = 0.008) and simple analgesics (P < 0.001) than patients with migraine and without self-reported PD. Also, they were less active physically and belonged to a low education level (both P < 0.001). Prevalence of self-reported PD was significantly higher in chronic migraineurs compared to those diagnosed with episodic migraine (EM) (53.9% vs. 44.6%, P = 0.019). Logistic regression analyses showed that self-reported PD was associated with CM (OR 1.456; 95% CI 1.062-1.997, P = 0.020). However, after adjusting for significant confounders, the association was attenuated (OR 1.100; 95% CI 0.784-1.543, P = 0.581). We concluded that self-reported PD was significantly more frequent in CM compared to EM. Self-reported PD was associated with the presence of CM, although some comorbidities shared by both diseases could have an effect on this association.
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http://dx.doi.org/10.1007/s10266-019-00430-wDOI Listing
October 2019

Autophagy in periodontal disease: Evidence from a literature review.

Arch Oral Biol 2019 Jun 1;102:55-64. Epub 2019 Apr 1.

Periodontology Unit, UCL Eastman Dental Institute and Hospital, University College London, London, UK; Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Medical-Surgical Dentistry (OMEQUI) Research Group, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, Spain.

Objective: To summarize evidence and data relating to the implications of autophagy in periodontal disease (PD) and to describe potential nutraceuticals or pharmaceuticals that could modulate this cell death subtype.

Design: Literature searches of various electronic databases (Medline via PubMed, SCOPUS, Web of Science, and EMBASE) using appropriate keywords (e.g., periodontal disease, periodontitis, alveolar bone loss, periodontal infection, tooth loss, autophagy, programmed cell death, and type 2 cell death) were performed. Then, a comprehensive literature review of the current understanding of this link was elaborated.

Results: Autophagy plays a pivotal role in PD, and its regulation seems to be an interesting avenue for future periodontal research, according to several in vivo and in vitro reports.

Conclusion: Today's research has ascertained the role of autophagy in PD, especially its role in the host's defence against periodontal disease drivers. A bulk of the research recognised several pharmaceuticals and nutraceuticals that could potentially modulate this kind of cell death and serve as useful therapies. However, further research is warranted to reach a clinical translation, which could help in the discovery of novel host modulation therapies for PD.
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http://dx.doi.org/10.1016/j.archoralbio.2019.03.029DOI Listing
June 2019

Porphyromonas gingivalis lipopolysaccharide-induced periodontitis and serum amyloid-beta peptides.

Arch Oral Biol 2019 Mar 16;99:120-125. Epub 2019 Jan 16.

Clinical Neurosciences Research Laboratory, Clinical University Hospital, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, Spain. Electronic address:

Objective: The aim of this investigation was to determine the circulating levels of amyloid beta (Aβ) peptides using the Porphyromonas gingivalis (Pg) lipopolysaccharide (LPS) model to induce periodontitis.

Methods: Experimental periodontitis was induced in 6 male Sprague-Dawley rats. Alveolar bone loss was measure by micro computed tomography. Serum concentrations of Aβ and Aβ prior to periodontal induction, at 24 h, 7, 14, and 21 days the last injection of Pg-LPS.

Results: The distance between the cemento-enamel junction and the bone crest (i.e., alveolar bone loss) was significantly higher at the end of periodontal induction compared to baseline (2.92 ± 0.29 mm vs. 3.8 ± 0.28 mm, P < 0.001). Periodontitis evoked a slight acute elevation of Aβ serum levels that were maintained during the whole experiment. Aβ peptide levels peak at the end of the study. A positive strong correlation was observed between alveolar bone loss and Aβ serum levels at 7 days (r = 0.695, P = 0.012) and as well as with serum Aβ concentrations at 21 days (r = 0.968, P = 0.002).

Conclusions: Periodontitis induced Pg-LPS produced increased serum levels of Aβ peptides. Further studies are needed to confirm our results and to investigate the mechanisms by which periodontitis could be associated with an overexpression of Aβ.
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http://dx.doi.org/10.1016/j.archoralbio.2019.01.008DOI Listing
March 2019

Periodontitis is associated with systemic inflammation and vascular endothelial dysfunction in patients with lacunar infarct.

J Periodontol 2019 05 29;90(5):465-474. Epub 2018 Nov 29.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Medical-Surgical Dentistry (OMEQUI) Research Group, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, Spain.

Background: Periodontitis has been associated with lacunar infarct (LI), a type of cerebral small vessel disease. The objective of this study was to ascertain whether periodontitis is associated with increased circulating levels of systemic inflammation and endothelial dysfunction biomarkers in patients with LI.

Methods: One hundred twenty patients with LI and 120 healthy controls underwent a full-mouth periodontal examination. The periodontal inflamed surface area (PISA) was calculated for each participant. Demographic, medical, and neurological information were recorded from all of them. In addition, blood samples were collected in order to investigate differences in terms of interleukin (IL)-6, IL-10, pentraxin (PTX) 3, soluble fragment of tumor necrosis factor-like weak inducer of apoptosis (sTWEAK) and amyloid-beta (Aβ) peptides (i.e., Aβ , and Aβ ) measured in serum.

Results: Periodontitis was independently associated with increased levels of IL-6 (R = 0.656, P < 0.001), PTX3 (R = 0.115, P < 0.001), sTWEAK (R = 0.527, P < 0.001), and Aβ (R = 0.467, P < 0.001) in patients with LI. Within patients with poor outcome, PISA positively correlated with IL-6 (r = 0.738, P < 0.001), PTX3 (r = 0.468, P = 0.008), sTWEAK (r = 0.771, P < 0.001), and Aβ (r = 0.745, P < 0.001).

Conclusions: Our data suggest a link between periodontitis, systemic inflammatory response, and disruption of the vascular endothelial function in patients with LI. Experimental studies are needed to elucidate possible pathways through which periodontitis could lead to this systemic inflammatory state with impairment of the endothelial function in LI. Further longitudinal studies with large samples are warranted to confirm our findings.
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http://dx.doi.org/10.1002/JPER.18-0560DOI Listing
May 2019

Periodontitis as a risk indicator and predictor of poor outcome for lacunar infarct.

J Clin Periodontol 2019 01 29;46(1):20-30. Epub 2018 Nov 29.

Periodontology Unit, Faculty of Medicine and Odontology, Medical-Surgical Dentistry (OMEQUI) Research Group, Health Research Institute of Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, Spain.

Aim: To investigate the association between periodontitis (PD) and lacunar infarct (LI) as well as to analyse whether PD could be a predictor of poor functional prognosis in patients with LI.

Material And Methods: Full-mouth periodontal examination was done in 120 cases (patients with LI) and 157 healthy controls. Demographic, clinical, medical and neurological information were collected from all of them. In addition, a measure of periodontal inflammation and disease activity, namely the periodontal inflamed surface area (PISA), was also calculated for each patient. Poor functional outcome was considered as a modified Rankin Scale >2 at 3 months.

Results: PD was independently associated with the presence of LI (OR = 3.3, p < 0.001). Poor outcome was observed in 31 patients with LI (25.8%), of which 90.3% had PD. A PISA value ≥727 mm was an independent predictor of poor prognosis, after adjusting for clinical confounders (OR = 6.5, p = 0.001).

Conclusions: PD and LI were associated. Active moderate to severe PD predicted poor prognosis in patients with LI. Further evidence is warranted to confirm our results and investigate potential mechanisms behind this association.
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http://dx.doi.org/10.1111/jcpe.13032DOI Listing
January 2019

Available patient-centered Internet information on peri-implantitis. Can our patients understand it?

Clin Oral Investig 2019 Apr 21;23(4):1569-1574. Epub 2018 Aug 21.

Oral Medicine, Oral Surgery and Implantology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Santiago de Compostela, Spain.

Objectives: The aim of this study was to evaluate the quality, readability, and popularity of patient-oriented online information about peri-implantitis.

Materials And Methods: The term "peri-implantitis" was searched in Google® and in Yahoo!®. The first 100 websites of each search engine were considered for further analysis. Quality was measured by DISCERN tool, and JAMA benchmarks. Readability was analyzed by Flesch Reading Ease Score (FRES), Flesch-Kinkaid Reading Grade (FKRG), Gunning Fog index (GFI), and Simple Measure of Gobbledygook (SMOG) index. Popularity was assessed by Alexa Popularity Rank (APR).

Results: Only 28 websites remained after applying the exclusion criteria. The median overall DISCERN rating was 2.0 [2.0-3.0], which demonstrates the low quality of the information related to peri-implantitis. None of the websites achieved all the four JAMA benchmarks. Legibility indices showed ranges within the scores of difficult to read (FRES, 37.3 [26.9-53.9]; FKRGL, 12.8 [10.5-15.4]; GFI, 15.3 [12.5-18.0]; and SMOG, 11.1 [8.8-13.0]). Median APR was 2,228,599.0 [302,352.0-8,125,885.5].

Conclusions: Available English-written e-health information on peri-implantitis is poor in terms of quality and the analyzed websites are beyond the reading level recommended for comprehension. The popularity measurement showed great divergences between different Web pages.

Clinical Relevance: Information about peri-implantitis on the Internet is difficult to read by patients, which they are not capable of understand.
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http://dx.doi.org/10.1007/s00784-018-2583-yDOI Listing
April 2019

Association between periodontitis and chronic migraine: a case-control study.

Odontology 2019 Jan 12;107(1):90-95. Epub 2018 Apr 12.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Rúa Entrerríos S/N, 15782, Santiago de Compostela, Spain.

The aim of this investigation was to examine whether chronic periodontitis (CP) is a risk indicator of chronic migraine (CM). We performed a case-control study consisted of 102 cases (patients diagnosed with CM) and 91 controls (non-CM individuals) matched by age and gender. Full-mouth periodontal charts, demographic, medical, clinical, as well as neurological data were obtained. In addition, high sensitive C-reactive protein serum levels were determined from blood samples of both cases (taken during migraine interictal period) and controls. The prevalence of CP was significantly higher in patients with CM compared to those without CM (58.8 vs. 30.8%, p < 0.0001). Logistic regression analysis showed that CP was significantly associated with the presence of CM, independently of well-known chronifying factors of migraine (OR 2.4; 95% CI 1.2-4.7; p = 0.012). Based on our results, CP could be considered as a risk indicator of CM. However, more evidence is necessary to investigate if this relationship is causal or not.
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http://dx.doi.org/10.1007/s10266-018-0360-7DOI Listing
January 2019

High serum procalcitonin levels in patients with periodontitis and chronic migraine.

J Periodontol 2018 09 14;89(9):1069-1074. Epub 2018 Aug 14.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Santiago de Compostela, Spain.

Background: To evaluate the contribution of chronic periodontitis (CP) to serum procalcitonin (proCT) levels in chronic migraine (CM) patients in a cross-sectional study.

Methods: We included 138 subjects divided into 4 groups based on clinical features of CM and periodontal parameters: systemically and periodontally healthy individuals (n = 37), systemically healthy and CP patients (n = 19), CM and periodontally healthy patients (n = 34), and CM+CP patients (n = 48). Demographic, neurological, clinical data as well as full-mouth periodontal records were obtained. ProCT and high sensitive C-reactive protein (hs-CRP) serum levels were determined from blood samples taken during migraine interictal period.

Results: Patients from the CP+CM group (0.056±0.006 ng/mL) had significantly higher serum proCT levels in comparison with the systemically and periodontally healthy group (0.029±0.019 ng/mL), CM group (0.041±0.002 ng/mL), or CP group (0.034±0.014 ng/mL) (p < 0.001). There were no significant differences in hs-CRP between groups (p = 0.081). Multiple linear regression analysis showed that CP was associated with increased proCT levels in CM patients (R = 0.293, p < 0.001).

Conclusions: CP independently contributes to elevated serum proCT levels in CM patients. These findings suggest that CP could play a role in migraine chronification.
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http://dx.doi.org/10.1002/JPER.17-0603DOI Listing
September 2018

Periodontal inflamed surface area and periodontal case definition classification.

Acta Odontol Scand 2018 Apr 11;76(3):195-198. Epub 2017 Nov 11.

a Periodontology Unit, Faculty of Medicine and Odontology , Odontología Médico-Quirúrgica (OMEQUI) Research Group, Health Research Institute of Santiago de Compostela (IDIS), University of Santiago de Compostela , Santiago de Compostela , Spain.

Objective: To assess whether a higher periodontal inflamed surface area (PISA) may reflect more severe periodontitis, and if so, to calculate which cut-off point should be used to classify a patient as suffering from periodontitis.

Material And Methods: Eighty subjects were selected based on their periodontal status and were divided into 4 groups of 20 each; periodontally healthy, mild periodontitis, moderate periodontitis and severe periodontitis. In addition, demographic data, smoking status and socioeconomic status were also recorded.

Results: The highest mean PISA value was obtained for the severe periodontitis group (2309.42 ± 587.69 mm) and the least for the periodontally healthy (34.30 ± 16.48 mm). The PISA values corresponding to the three categories of periodontitis severity were significantly higher than the periodontally healthy group. When receiver operating characteristic (ROC) analysis was performed, a PISA value ≥130.33 mm predicted the presence of periodontitis with a sensitivity of 98% and a specificity of 100%.

Conclusions: PISA is a periodontal parameter that may be used in conjunction with the Centers for Disease Control and Prevention - American Academy of Periodontology case definition classification in periodontal medicine research.
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http://dx.doi.org/10.1080/00016357.2017.1401659DOI Listing
April 2018

The role of leptin as a biomarker in the relationship between periodontitis and chronic migraine.

J Clin Periodontol 2017 Dec 17;44(12):1208-1214. Epub 2017 Nov 17.

Periodontology Unit, Faculty of Medicine and Odontology, University of Santiago de Compostela, Santiago de Compostela, Spain.

Aim: To evaluate the prevalence of periodontitis (CP) and its contribution to serum leptin levels in chronic migraine (CM).

Material And Methods: In this case-control study, we included 150 subjects divided into healthy controls (n = 58) and CM patients (n = 92). Demographic, neurological, clinical data as well as full-mouth periodontal records were obtained. Serum leptin levels were measured by ELISA technique.

Results: Both the prevalence of CP and mean serum leptin levels were significantly higher in patients with CM in comparison with controls (57.6% versus 36.2%, p = .01 and 16.4 versus 7.2 ng/ml, p < .0001, respectively). Patients from the CM group who had CP showed significantly higher leptin concentrations than CM patients without CP (19.8 versus 11.8 ng/ml, p < .0001). Multivariable linear regression analysis showed that CP was an independent contributor to raised leptin levels in CM patients (R = 0.270, p = 0.013).

Conclusions: CP is prevalent in CM patients and when present it contributes to elevated serum leptin levels, independently of other confounding factors. Therefore, it seems that CP via leptin could be involved in the process of migraine chronification.
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http://dx.doi.org/10.1111/jcpe.12819DOI Listing
December 2017

Periodontal disease as a potential factor of migraine chronification.

Med Hypotheses 2017 May 14;102:94-98. Epub 2017 Mar 14.

Department of Neurology, Headache Unit, Clinical Neurosciences Research Laboratory, Hospital Clínico Universitario, Health Research Institute of Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, Spain.

Migraine is a hereditary constitutional base disorder, which is characterized by recurrent episodes of headache pulsatile characteristics associated with photophobia/phonophobia, nausea and/or vomiting. The main complication in migraine is the chronicity of the process, now recognized as a chronic migraine. Although pathogenic mechanisms that may influence the pathophysiology of migraine and its possible chronicity are not fully understood, previous studies have shown in patients with migraine molecular alterations of systemic inflammation, neurogenic inflammation, endothelial dysfunction, innate immunity, dysfunction of matrix proteases and blood-brain barrier. Periodontal disease is an inflammatory lesion caused by bacteria. After the bacterial infection begins, an immune response that will be responsible for individual susceptibility appears. More advanced forms of periodontitis have demonstrated molecular alterations of inflammation, endothelial dysfunction, dysfunction of matrix proteases and innate immunity, similar to those observed in migraine. Furthermore, the main molecular mediators of neurogenic inflammation related to activation of the trigeminovascular system, which are characteristic of migraine, are overexpressed in gingival crevicular fluid and mucosa in patients with periodontal disease. Hypertension, hypercholesterolemia, insulin resistance, stroke or coronary artery disease are comorbidities that periodontal disease and migraine could share. Therefore, several mechanisms and hypotheses could explain the possible association between both diseases. However, epidemiological and molecular studies will be necessary to provide a better understanding of this potential association, which could be implicated in the chronification of migraine.
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http://dx.doi.org/10.1016/j.mehy.2017.03.019DOI Listing
May 2017

Is Periodontal Disease Associated with Alzheimer's Disease? A Systematic Review with Meta-Analysis.

Neuroepidemiology 2017 21;48(1-2):21-31. Epub 2017 Feb 21.

Department of Periodontology, School of Dentistry, University of Santiago de Compostela, Santiago de Compostela, Spain.

Background: In the last decade, several observational studies have suggested that there exists an association between periodontal disease (PD) and Alzheimer's disease (AD). The aim of this systematic review was to investigate whether or not this link exists.

Summary: The Preferred Reporting Items for Systematic Reviews and Meta-Analysis guideline for systematic review was used and registered at PROSPERO (CRD42016035377). The search strategy included using electronic databases and by hand searching articles published up to January 2016. MEDLINE via PubMed, EMBASE and Web of Science were searched by 2 independent reviewers. Observational studies including patients meeting criteria for both AD and PD were eligible to be included in the analysis. Quality assessment of selected studies was performed by the Newcastle-Ottawa Scale. From a total of 550 titles and abstracts, 5 studies were included (2 cross-sectional, 2 case-control and one cohort study) in the review. A fixed effects meta-analysis showed that the presence of PD is associated with the presence of AD (OR 1.69, 95% CI 1.21-2.35). When only severe forms of PD were evaluated, a significant association was also observed (OR 2.98, 95% CI 1.58-5.62). Key Messages: In the present review, a significant association was observed between PD and AD. Further studies should be carried out in order to investigate the direction of the association and factors that may confound it.
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http://dx.doi.org/10.1159/000458411DOI Listing
March 2018

Association between periodontitis and ischemic stroke: a systematic review and meta-analysis.

Eur J Epidemiol 2017 01 14;32(1):43-53. Epub 2016 Jun 14.

Clinical Neurosciences Research Laboratory, Department of Neurology, Neurovascular Area, Health Research Institute of Santiago de Compostela (IDIS), Hospital Clínico Universitario, University of Santiago de Compostela, Santiago de Compostela, Spain.

Several observational studies have suggested an association between periodontitis and cerebral ischemia. This meta-analysis aimed to investigate whether this link exists, and if so, the degree to which it is significant. The Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guideline for systematic review was used. The search strategy included using electronic databases and hand searching works published up to March 2015. MEDLINE via PubMed, EMBASE, Proceedings Web of Science and Current Contents Connect were searched by two independent reviewers. Case-control, cross-sectional or cohort studies including patients with measures of periodontitis and ischemic stroke were eligible to be included in the analysis. Quality assessments of selected studies were performed. From a total of 414 titles and abstracts, 57 potentially relevant full text papers were identified. After inclusion criteria were applied, 8 studies were included in the present systematic review (5 case-control and 3 cohort studies). Although it was not the intention, cross-sectional studies were excluded due to eligibility criteria were not accomplished. Therefore, meta-analyses were conducted with data retrieved from the 8 studies included. These meta-analyses showed statistically significant association between periodontitis and ischemic stroke in both cohort pooled relative risks at 2.52 (1.77-3.58), and case-control studies pooled relative risks at 3.04 (1.10-8.43). In conclusion, the present meta-analysis demonstrated an association between periodontitis and ischemic stroke. However, well-designed prospective studies should be carried out to provide robust evidence of the link between both diseases. In regards to ischemic stroke subtypes, further case-control studies should be carried out to investigate whether there is any association between the different subtypes of cerebral infarcts and periodontitis.
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http://dx.doi.org/10.1007/s10654-016-0170-6DOI Listing
January 2017

[Association between periodontal disease and cerebrovascular disease. A review of the literature].

Rev Neurol 2015 Jul;61(1):29-38

Universidad de Santiago de Compostela, Santiago de Compostela, Espana.

Periodontal disease and cerebrovascular disease are two of the most prevalent processes in elderly people. Various studies have shown an association between them, although some methodological differences exist and this difficult the data interpretation. The aim of this paper is to conduct a critical review of the studies published about this association. Eleven prospective studies and 11 retrospective studies are included in this review. We analyse the different methodological outcomes (study population, periodontal diagnosis, cerebrovascular disease definition, adjusted outcomes and odds ratio/relative risk). Furthermore, we review several pathogenic mechanisms implicated in the progression and the relationship between both processes.
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July 2015
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