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Diabetes and periodontitis: A bidirectional relationship
Diabetes y periodontitis: una relación bidireccional
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AGE, advanced glycation end-products; MMP, matrix metalloproteinases; PMN, polymorphonuclear lymphocytes; RAGE, receptor for advanced glycation end-products.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Diabetes mellitus (DM) is a group of metabolic diseases characterised by hyperglycaemia resulting from a defect in insulin secretion, a defect in its action, or a combination of both.<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">1,2</span></a> The current prevalence of DM in Spain is around 8% in women and 12% in men, although a growing tendency has also been observed in recent years, both in Spain and on a global level.<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">3,4</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Periodontitis was traditionally considered to be a localised oral infection that only affected the periodontium, but is now regarded as a chronic localised infection of the oral cavity that can trigger the host inflammatory immune response at both local and systemic level, and can also be a source of bacteraemia. It is difficult to determine the prevalence of periodontitis. Some authors have estimated that gingivitis affects 50% of the US population, with the prevalence of periodontitis being 14%, although probably higher. It should be taken into account, however, that these estimations depend to a large extent on the diagnostic criteria established by each study.<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">5</span></a> Nowadays, it is known that periodontitis affects the pathogenesis of certain systemic diseases, and that it can increase their risk of presentation, which has led to the emergence and development of “Periodontal Medicine”.<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">6</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Interrelationship between the two entities</span><p id="par0015" class="elsevierStylePara elsevierViewall">The biological relationship between DM and periodontal disease is well documented. In the mid-1990s, after 30 years of exhaustive research and almost 90 published epidemiological studies, enough scientific evidence had been found to associate DM with periodontitis, which has become known as the sixth complication of DM.<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">7</span></a> DM was first shown to be a risk factor for periodontitis, and then an inverse influence was proposed, i.e., that periodontitis could be a risk factor for diabetic decompensation, a relationship backed up by various studies. This would therefore suggest a complex, two-way relationship between DM and periodontitis, creating a vicious circle that would exacerbate both diseases when both occur in the same individual.</p><p id="par0020" class="elsevierStylePara elsevierViewall">The association between DM and periodontal disease has been extensively studied. Shlossman et al.<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">8</span></a> evaluated the periodontal status of 3219 individuals from the Pima Indian population (a population with a high prevalence of type 2 DM), and found a significantly higher prevalence of periodontitis in diabetics than in non-diabetics, with age being an independent factor. Following on from this study, Emrich et al.,<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">9</span></a> Nelson et al.<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">10</span></a> and Taylor et al.<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">11</span></a> found similar results in this same population. Taylor et al.<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">12</span></a> showed that advanced periodontitis is significantly associated with a risk of worsening glycaemic control.</p><p id="par0025" class="elsevierStylePara elsevierViewall">According to published articles, several authors agree that DM acts as a risk factor in periodontal disease. Mealey<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">13</span></a> states that, after adjusting for other confounding factors such as age or sex, DM appears to increase the probability of presenting periodontitis 3-fold.</p><p id="par0030" class="elsevierStylePara elsevierViewall">A systematic review by Borgnakke et al.<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">14</span></a> included 17 articles; based on these, they determined that there is little evidence to support a negative effect of periodontal disease on glycaemic control, DM complications and development of type 2 DM, and possibly gestational diabetes.</p><p id="par0035" class="elsevierStylePara elsevierViewall">However, other reviews carried out in recent years have clearly established the effect of DM on periodontal diseases.<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">15,16</span></a> There is also evidence of a relationship between the severity of periodontitis and type 2 DM complications; moderate-to-severe periodontitis is associated with an increase in macroalbuminuria, end-stage renal disease, atheromatous plaque calcification, carotid intima-media thickening and cardiorenal mortality.<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">17</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">Some biochemical markers of DM are altered by periodontal disease. Glycated haemoglobin (HbA1c) is used as a marker of glycaemia, and since the 2013 Workshop on DM<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">13</span></a>, has been used as a standard response variable in the control of DM.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Pathogenesis</span><p id="par0045" class="elsevierStylePara elsevierViewall">Periodontitis is a chronic inflammatory disease in which periodontal tissue inflammation is stimulated by the prolonged presence of subgingival biofilm. The inflammatory response is characterised by unregulated secretion of host-derived mediators of inflammation and tissue destruction. The most extensively studied are interleukin (IL)-1β, IL-6, prostaglandin E2 (PGE2), tumour necrosis factor (TNF)-α, RANKL and matrix metalloproteinases (MMPs, especially MMP-8, MMP-9 and MMP-13), as well as regulatory T cells that produce cytokines (e.g. IL-12 and IL-18) and chemokines. The cytokine network in the pathogenesis of periodontal disease is quite complex, and there is also considerable heterogeneity in the nature of the inflammatory response among individuals.<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">18,19</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">Inflammation is the most central characteristic in the pathogenesis of both DM and periodontal disease. Both type 1 and type 2 DM are associated with high levels of systemic inflammatory markers. The elevated inflammatory state in DM contributes to both macrovascular and microvascular complications, and hyperglycaemia can result in the activation of pathways that increase inflammation, oxidative stress and apoptosis. High IL-6 and TNF-α levels have been found in DM and obesity. The onset of type 2 DM can be predicted through serum IL-6 and C-reactive protein (CRP) levels. High CRP levels are also associated with insulin resistance, type 2 DM and cardiovascular disease. Acute-phase proteins, including CRP, are mainly induced by TNF-α and IL-6, which also damage intracellular insulin signalling, potentially contributing to insulin resistance. Serum IL-6 and CRP levels are also high in patients with periodontitis, and there is a correlation between the IL-6 values and the extent of the periodontal disease. As such, the systemic inflammation associated with periodontal disease could encourage development of a diabetic state.<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">18,19</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">DM increases inflammation in the periodontal tissues. PGE2 and IL-1β values in gingival crevicular fluid (GCF) are higher in patients with type 1 DM and gingivitis or periodontitis compared to non-diabetic individuals with the same degree of periodontal disease. In a study of patients with type 2 DM, those with HbA1c >8% had significantly higher IL-1β values in the GCF than patients with HbA1c <8%, and the HbA1c and glucose values were independent predictors of a high IL-1β value in the GCF.<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">18,19</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">Following the damage caused by the lipopolysaccharide, the monocytes in patients with type 1 diabetes produce significantly higher concentrations of TNF-α, IL-1β and PGE2 than the monocytes of non-diabetic patients. Various studies have even shown defects in polymorphonuclear (PMN) leucocyte activity in diabetic patients, including impaired chemotaxis, phagocytosis and bactericidal functions. PMNs need energy to perform these functions, so these defects may be related to the metabolic changes that occur in DM. Diabetic patients with advanced periodontitis have been shown to have decreased chemotaxis compared to diabetic patients with mild periodontitis, as well as defective PMN apoptosis. This can cause an increase in PMN retention in the periodontal tissues, leading to increased tissue destruction due to the continuous secretion of MMP and reactive oxygen species (ROS). DM prolongs the inflammatory response to <span class="elsevierStyleItalic">Porphyromonas gingivalis</span>, with an increase in the production of TNF-α as an inflammatory mediator. However, periodontal treatment reduces the serum values of inflammatory mediators such as IL-6, TNF-α, CRP and MMP in patients with or without DM.<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">18,19</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">DM is considered to generate a hyperinflammatory phenotype in specific cells as a result of the action of advanced glycation end-products (AGE) on these cells. These complications are related to long-term hyperglycaemia; the hyperglycaemia leads to the formation of AGE. AGEs affect the endothelial cells and monocytes, making them more susceptible to the stimuli that induce the cells to produce inflammatory mediators. The accumulation of AGEs in plasma and tissues in diabetic patients has been associated with various complications. The gingival tissue containing AGEs is said to have greater vascular permeability, undergo greater breakdown of collagen fibres and show accelerated destruction of connective tissue and bone. These mechanisms—apart from accumulation of AGEs—are very similar to those of periodontal disease. Moreover, accumulation of AGEs in periodontal tissues also plays another role in the overexpression of periodontal inflammation in individuals with DM. Binding of AGE to its receptor leads to overproduction of inflammatory mediators such as IL-1β, TNF-α and IL-6.<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">18–20</span></a> The formation of these molecules causes ROS production, which increases oxidative stress. The subsequent cellular changes that occur contribute to the vascular damage involved in many DM complications.<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">15,21–24</span></a> AGEs also increase the respiratory burst in PMNs, which has the potential to increase the localised tissue damage in periodontitis. They also have a damaging effect on bone metabolism, leading to impaired bone repair and formation, and to lower extracellular matrix production. Apoptosis can also play a role in the increased susceptibility to periodontitis associated with DM, and apoptosis of matrix-producing cells can limit the opportunities for repair in inflamed tissues<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">19</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Clinical studies</span><p id="par0070" class="elsevierStylePara elsevierViewall">Attempts have been made to demonstrate the effect of periodontal treatment on glycaemic control in DM, and there seems to be good evidence to support this hypothesis. Studies have been conducted which show an improvement in both the clinical and immunological parameters of periodontitis, such us long-term glycaemic control of DM following treatment for periodontal disease.<a class="elsevierStyleCrossRefs" href="#bib0330"><span class="elsevierStyleSup">25–29</span></a> Although there are also studies that have failed to find a relationship, and few randomised clinical trials have been conducted, there is currently considered to be enough evidence to justify researching the effects of treatment and prevention of periodontitis as a means of contributing to better metabolic control in diabetic patients.</p><p id="par0075" class="elsevierStylePara elsevierViewall">Some authors also suggest that the prevention and control of periodontal disease should be considered an integral part of DM control.<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">30</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">Kiran et al.<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">26</span></a> conducted a randomised, controlled clinical study in 44 patients with type 2 DM and periodontal disease ranging from gingivitis to mild periodontitis. Treatments performed were prophylaxis, scaling and root planing. They achieved a 50% reduction in the prevalence of bleeding after 3 months in the treated patients. A 0.8% improvement in glycaemic control was observed compared to the control group, which did not receive treatment. However, in 2006, Faria-Almeida et al.<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">27</span></a> clearly demonstrated that the treatment of periodontal disease significantly improves metabolic control of DM. They conducted a 6-month controlled clinical study in 20 patients divided into two groups. The results showed an improvement in both the clinical and metabolic variables (HbA1c in this case), thus establishing that periodontal treatment improves metabolic control of DM.</p><p id="par0085" class="elsevierStylePara elsevierViewall">Several medical literature and systematic reviews have been carried out in recent years. Teeuw et al.<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">31</span></a> performed a systematic review and meta-analysis that included five controlled studies in which the patients in the control group did not receive periodontal treatment and had a follow-up period of over 3 months. The meta-analysis showed an improvement in HbA1c values in type 2 diabetic patients who received periodontal treatment, although the authors suggest that the data should be treated with caution due to the heterogeneity of the studies.</p><p id="par0090" class="elsevierStylePara elsevierViewall">The 2010 Cochrane Collaboration systematic review and meta-analysis<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">32</span></a> included seven studies; its conclusions were similar to those of Teeuw et al.,<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">31</span></a> finding an improvement in HbA1c values in diabetic patients after periodontal treatment, with follow-up of 3-4 months. However, they state that few studies have been conducted and that these have been of poor quality, which do not allow any definite conclusions to be drawn.</p><p id="par0095" class="elsevierStylePara elsevierViewall">In 2012, Gurav<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">33</span></a> carried out a systematic review to identify the effect of periodontal treatment on glycaemic control in patients with type 2 DM. The author concluded that periodontal treatment could be an adjuvant procedure in glycaemic control in these patients, although it does not improve control when used in isolation. He also highlighted the need for multicentre, randomised, controlled clinical studies.</p><p id="par0100" class="elsevierStylePara elsevierViewall">Engebretson and Kocher<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">34</span></a> carried out a systematic review in order to determine the effect of periodontal treatment on DM. They analysed nine articles comparing the change in HbA1c from the baseline level to the end of each study. After breaking down and analysing the various studies, they performed a meta-analysis in which a modest improvement in the response variable (HbA1c) was obtained, given the high risk of bias and the small sample size of the studies, as well as the different periodontal treatments used in each study. As such, the authors believe that further studies are required, although it appears that this improvement in the metabolic control of DM brought about by the treatment of periodontal disease does indeed exist.</p><p id="par0105" class="elsevierStylePara elsevierViewall">On the other hand, scientific evidence confirms that poor glycaemic control contributes to poor periodontal status,<a class="elsevierStyleCrossRefs" href="#bib0380"><span class="elsevierStyleSup">35–38</span></a> as was also shown in the systematic reviews by Taylor in 2001,<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">39</span></a> and Taylor and Borgnakke in 2008.<a class="elsevierStyleCrossRef" href="#bib0405"><span class="elsevierStyleSup">40</span></a> The inflammatory state induced by the cytokines in periodontal disease contributes to the low-grade systemic inflammation that takes place in DM. This low-grade inflammation is characterised by chronic activation of the patient's innate immunity, and, as a result, it can aggravate insulin resistance and negatively affect glycaemic control.<a class="elsevierStyleCrossRefs" href="#bib0380"><span class="elsevierStyleSup">35,38</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">This ultimately, as Watanabe<a class="elsevierStyleCrossRef" href="#bib0410"><span class="elsevierStyleSup">41</span></a> says, leads to one clear clinical implication: the need for direct collaboration between physicians and dentists for the treatment of diabetic patients with periodontal disease. When this happens, we will be able to better understand the interactions between these two highly prevalent diseases.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Conclusions</span><p id="par0115" class="elsevierStylePara elsevierViewall">The interrelationship between DM and periodontitis highlights the importance of the need for good communication between the diabetic patient's physician and dentist, always considering the possibility that the two conditions may occur simultaneously, to guarantee early diagnosis of both. Studies have shown that the association between DM and periodontitis is a reality today, and it has been clearly established that glycaemic control improves periodontal status and that control of periodontal infection improves glycaemia in diabetic patients. However, the clinical implications of this should be further investigated. Nevertheless, the possibility that the two diseases could share some common pathogenic aspects should always be kept in mind to ensure early diagnosis of both.</p><p id="par0120" class="elsevierStylePara elsevierViewall">Given the high prevalence of both diseases and the potential seriousness of their repercussions, the physician has an important role to play in recommending that patients regularly visit their dentist to control risk factors, such as the continuous presence of bacterial plaque in the periodontal pockets. Oral health professionals must also keep in mind that altered glucose metabolism can affect the development and severity of periodontal disease.</p><p id="par0125" class="elsevierStylePara elsevierViewall">Large-scale, clinical, microbiological, biochemical and epidemiological studies are required, in the form of multicentre, randomised, controlled clinical trials that include both type 1 and type 2 diabetics, to compare the different treatment modalities in order to establish a clear protocol of action and multidisciplinary treatment of diabetic patients with periodontal disease.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conflict of interests</span><p id="par0130" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interests.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres605073" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec619146" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres605072" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec619145" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Interrelationship between the two entities" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Pathogenesis" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Clinical studies" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Conclusions" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Conflict of interests" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2014-06-01" "fechaAceptado" => "2014-07-07" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec619146" "palabras" => array:3 [ 0 => "Diabetes mellitus" 1 => "Periodontal deseases" 2 => "Periodontal medicine" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec619145" "palabras" => array:3 [ 0 => "Diabetes mellitus" 1 => "Periodontitis" 2 => "Medicina periodontal" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Diabetes mellitus is a group of metabolic diseases characterised by hyperglycemia resulting from defects in insulin secretion, a defect in insulin action or a combination of both. Periodontitis is now considered a chronic localised infection of the oral cavity that can trigger inflammatory host immune responses at local and systemic levels, and can also be a source of bacteremia. It is now known that periodontitis has an influence on the pathogenesis of certain systemic diseases. The biological relationship between diabetes and periodontal disease is well documented. In the mid-90s sufficient scientific support for the association between diabetes and periodontitis was published, and periodontitis was designated as the sixth complication of diabetes. There have been studies that show an improvement in both clinical and immunological parameters of periodontitis and glycemic control in long-term diabetes after treatment of periodontal disease. In addition, scientific evidence confirms that poorer glycemic control contributes to a worse periodontal condition.</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The interplay between the two conditions highlights the importance of the need for a good communication between the internist and dentist about diabetic patients, considering always the possibility that the two diseases may be occurring simultaneously in order to ensure an early diagnosis of both.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La diabetes mellitus es un grupo de enfermedades metabólicas caracterizadas por una hiperglucemia resultante de un defecto en la secreción de insulina, un defecto en la acción de esta, o bien una combinación de ambos. La periodontitis se considera actualmente una infección crónica localizada en la cavidad oral, que puede activar la respuesta inmunitaria inflamatoria del hospedador a nivel local y sistémico, y que además puede ser una fuente de bacteriemia. Hoy en día se sabe que la periodontitis tiene una influencia sobre la patogénesis de ciertas enfermedades sistémicas. La relación biológica entre la diabetes y la enfermedad periodontal está bien documentada. A mediados de la década de 1990 se encontró soporte científico suficiente para la asociación entre la diabetes y la periodontitis, que se comenzó a designar como la sexta complicación de la diabetes. Se han realizado estudios que muestran una mejora tanto en los parámetros clínicos e inmunológicos de la periodontitis como en el control glucémico a largo plazo de la diabetes tras el tratamiento de la enfermedad periodontal. Además, la evidencia científica confirma que un peor control glucémico contribuye a un peor estado periodontal.</p><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">La interrelación entre ambas afecciones deja constancia de la importancia de la necesidad de una buena comunicación entre el médico internista y el odontólogo de los pacientes diabéticos, teniendo siempre en cuenta la posibilidad de que ambas enfermedades puedan estar ocurriendo simultáneamente, para garantizar el diagnóstico precoz de ambas.</p></span>" ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Bascones-Martínez A, Muñoz-Corcuera M, Bascones-Ilundain J. Diabetes y periodontitis: una relación bidireccional. Med Clin (Barc). 2015;145:31–35.</p>" ] ] "multimedia" => array:1 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1285 "Ancho" => 2170 "Tamanyo" => 167971 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Biological plausibility of the relationship between diabetes and periodontitis. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2017 October | 11 | 4 | 15 |
| 2017 September | 6 | 4 | 10 |
| 2017 August | 7 | 0 | 7 |
| 2017 July | 3 | 6 | 9 |
| 2017 June | 1 | 0 | 1 |
