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By Irina-Georgeta Sufaru 1, Silvia Teslaru 1, * , Liliana Pasarin 1, * , Gianina Iovan 2, Simona Stoleriu 2 and Sorina Mihaela Solomon 1
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Department of Cariology and Restorative Dental Therapy, Grigore T. Popa University of Medicine and Pharmacy, Universitatii Street 16, 700115 Iasi, Romania
Received: July 5, 2022 / Revised: August 12, 2022 / Accepted: August 17, 2022 / Published: August 18, 2022
The host inflammatory response in periodontitis is the phenomenon underlying the onset and course of periodontal destructive phenomena. A number of systemic factors, such as diabetes mellitus (DM), can negatively affect the patient with periodontitis, just as periodontitis can worsen the condition of the DM patient. Host Response Modulation Therapy involves the use of anti-inflammatory and antioxidant products aimed at resolving inflammation, halting destructive processes and promoting periodontal healing, all of which are important aspects in patients with high tissue loss, such as diabetic patients. This article reviews the data available in the literature on the relationship between DM and periodontitis, the main substances that modulate the inflammatory response (non-steroidal anti-inflammatory drugs, sub-antimicrobial doses of doxycycline or omega-3 fatty acids and their derivatives, specialized pro-solvent mediators), as well as their application in diabetic patients.
Periodontitis is an inflammatory disease of multifactorial etiology [1, 2], affecting the tissues that serve to maintain and function teeth in the dental arches. Periodontitis is characterized by the progressive loss of the periodontal attachment, which over time leads to bone destruction and even loss of teeth; negative endpoints included a significant deterioration in the functions of the stomatognathic system and the patient’s quality of life [3]. The etiology of periodontitis is multifactorial. It is based on abnormal immune function, a condition that can be caused by multiple causes of an oral or systemic nature. Periodontal inflammation is caused by periodontal pathogens, with a modification of the oral ecosystem, in favor of gram-negative bacteria [4], which will exacerbate the inflammatory responses. Therefore, the occurrence of dysbiosis is attributed to the onset of inflammation rather than the action of a single microorganism [5]. Periodontitis is the result of complex interactions between genetic and environmental factors, including the host’s inflammatory response to the microbial community (a bacterial biofilm) [6].
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The course of periodontitis, as has already been shown and observed in common practice, is non-linear and heterogeneous. Periodontitis often develops by alternating periods of activity, characterized by tissue loss, and periods of remission [7]. In addition, the evolution can differ enormously from one patient to another. In addition, evolution can lead to changes in the patient’s life, aging processes, the occurrence and/or evolution of certain systemic pathologies [8], or epigenetic changes [9], which will alter the ability an adequate immune response.
The dysregulated immune response is overactive, with excessive inflammatory responses promoting dysbiotic changes and periodontal tissue degradation [10]. Polymorphonuclear cells (PMN) play an important role in this phenomenon by their hyperfunctionality, which will lead to the excessive secretion of pro-inflammatory cytokines and chemokines. It is important that these pro-inflammatory mediators are not confined to periodontal tissue, but enter the bloodstream, where they affect distant organs and systems [10]. In addition, hyperactive PMNs can increase the production of oxygen radicals (ROS) [11], increasing oxidative stress, and can contribute to the recruitment and activation of osteoclasts, cells that play an essential role in bone resorption [ 12]. Excessive production of endogenous ROS probably contributes to the degradation of periodontal tissue [13], activates matrix metalloproteinases (MMPs) and stimulates the activity of bacterial proteinases [14], molecules implicated in the degradation of periodontal tissue.
At the same time, negative influences on neutrophils were observed, including chemotaxis deficiency, phagocytosis disorders, respiratory burst and intracellular destruction [15]. Such phenomena, associated with the lack of leukocyte adhesion, will in fact cause an escalation of inflammatory reactions. These events can be accompanied by the activation of Th-17 cells, which will attempt to compensate for the immune deficiencies already mentioned [16]. These processes will contribute to an even more dysbiotic environment, essentially creating a vicious cycle that, clinically speaking, will lead to continued loss of periodontal tissue (Figure 1).
The resolution of inflammatory symptoms is a complex and well-organized process involving anti-inflammatory and antioxidant mediators. Anti-inflammatory mediators include lipoxins, maresins, protectins or resolvins whose synthesis is signaled by pro-inflammatory mediators produced during inflammation [17, 18]. Based on these findings, the concept of modulating the host inflammatory response was developed. These pharmacological strategies include anti-inflammatory effects and, more recently, achieving resolution of inflammation.
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In addition, pro-inflammatory and anti-inflammatory responses and processes can be characterized by genetic factors, pathological factors (systemic diseases such as cardiovascular disease [19], diabetes [20] or kidney disease [21]) , factors related to lifestyle (stress [22], smoking [23], diet [24], physical inactivity [25]) or factors related to the evolution of the dental arches (dental anomalies and bad treatment) [26]. . Often, these factors can act simultaneously and exert different influences on different individuals [3], contributing to the heterogeneity of periodontitis.
Diabetes mellitus (DM) is a disease in which the body’s ability to produce or respond to the hormone insulin is compromised [27]. The consequences are abnormal carbohydrate metabolism, as well as an increase in the level of glucose in the blood (hyperglycaemia) and urine (glycosuria) [28]. DM is characterized by a number of major complications of a macrovascular (coronary heart disease and stroke) or microvascular (nephropathy, retinopathy, neuropathy) nature, including periodontitis [28, 29]. Literature data suggest that metabolic changes in patients with type 1 diabetes are mainly due to dysfunction in insulin production. Type II diabetes is characterized by both innate and adaptive immune responses, leading to the development of insulin resistance [30].
Diabetes, or rather the level of glycated hemoglobin (HbA1c), has become a descriptive factor in the current classification of periodontitis [31]. This fact generates the need to find effective therapies to treat patients with diabetes mellitus and periodontal disease. Although scaling and root planing (SRP), as part of periodontal treatment, have proven their beneficial role in improving HbA1c levels, new strategies have been developed, including inflammatory response modulating agents of the host [27]. Of course, neither SRPs nor anti-inflammatory and pro-resolving therapies are considered a treatment for DM on their own. But if the treatment of a local pathology, such as periodontitis, could also bring about improvements at the systemic level, this would result in a precious bullet that is at the heart of interdisciplinarity and periodontal medicine.
The concept of host modulation therapy is not new, but it is constantly expanding. Its potential role in patients with periodontitis and systemic diseases is still a relatively unknown area. Therefore, the purpose of this article is to investigate known host response modulating therapies in the context of both periodontal disease and the presence of DM and their intertwined disease mechanisms. The MEDLINE/PubMed, ISI Web of Science, Scopus and Science Direct databases were searched and the following keywords were used: periodontitis, diabetes mellitus, host inflammatory response, inflammation, oxidative stress, host modulation therapy, inflammation resolution , and antioxidants . A total of 6173 results were identified, of which the 124 most important articles in English were analyzed between 1992 and 2022. A two-step selection process (titles and abstract, followed by a full-text analysis) was carried out by three independent examiners (I.-G.S., S.T and S.M.S.).
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Diabetes can increase susceptibility to periodontitis through mechanisms such as periodontal dysbiosis, host inflammatory/immune response, and direct destruction of periodontal tissue.
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