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© Borgis - Postępy Nauk Medycznych 10/2014, s. 678-683
*Izabela Rogozińska1, Beata Pyrżak1, Grażyna Miszkurka1, Angelika Kalińska2, Maria Dąbkowska3, Dorota Olczak-Kowalczyk2
Czynniki sprzyjające rozwojowi chorób błony śluzowej jamy ustnej oraz dziąseł u dzieci z cukrzycą typu 1
Factors contributing to the development of diseases of the oral mucosa and gums in children with type 1 diabetes
1Department of Pediatrics and Endocrinology, Medical University of Warsaw
Head of Department: Beata Pyrżak, MD, PhD
2Department of Pediatric Dentistry, Medical University of Warsaw
Head of Department: prof. Dorota Olczak-Kowalczyk, MD, PhD
3Department of Medical Microbiology, Medical University of Warsaw
Head of Department: Ewa Swoboda-Kopeć, MD, PhD
Streszczenie
Wstęp. Uważa się, że u osób z cukrzycą 1 typu częściej niż u zdrowych występują infekcje błony śluzowej jamy ustnej.
Cel pracy. Celem pracy była analiza czynników sprzyjających chorobom błony śluzowej jamy ustnej i dziąseł u dzieci z cukrzycą typu 1.
Materiał i metody. Grupa badana liczyła 41 dzieci z cukrzycą: 18 chłopców i 23 dziewczynki w wieku 5,33-17,83 roku (średni wiek 12,92 ± 3,02), grupa kontrolna – 39 dzieci: 19 chłopców i 20 dziewczynek w wieku 4-17,75 roku (średni wiek 11 ± 3,82). U wszystkich przeprowadzono badanie stomatologiczne oceniające stan higieny jamy ustnej (ang. Oral Hygiene Index-Simplified – OHI-S), błony śluzowej, dziąseł (wskaźnik dziąsłowy, ang. Gingival Index – GI) i zębów (wskaźnik PUW/puw), pobrano materiał do badania bakteriologicznego, mikologicznego oraz oceny parametrów fizykochemicznych śliny. Oceniono wybrane wykładniki wyrównania cukrzycy.
Wyniki. Nie stwierdzono różnic w odsetku obecności Candida spp. między grupami dzieci z cukrzycą i kontrolną, zapalenie dziąseł występowało z porównywalną częstością, odsetek dzieci bez cech stanu zapalnego dziąseł był istotnie wyższy w grupie kontrolnej (20 vs. 33%), łagodne zapalenie dziąseł częściej występowało u dzieci z cukrzycą (68 vs. 46%). Występowanie zakażeń Candida spp. było częstsze u dzieci z podwyższonym poziomem HbA1c. U dzieci z cukrzycą częściej występowały zapalenia kącików ust oraz zanikowe zapalenie języka, poziom HbA1c pozytywnie korelował z zanikowym zapaleniem języka, zapaleniem dziąseł, zapaleniem kącików ust, obecnością Lactobacillus acidophillus.
Wnioski. Zaburzenia wyrównania metabolicznego w cukrzycy sprzyjają pojawianiu się chorób błony śluzowej jamy ustnej i dziąseł. Brak różnicy w częstości występowania grzybów Candida spp. oraz zapaleń dziąseł między grupami badaną i kontrolną tłumaczyć można częstszymi kontrolami pediatrycznymi wynikającymi z prowadzenia cukrzycy oraz częstszą kontrolą stomatologiczną tych dzieci.
Summary
Introduction. Oral mucosal infections occur more often in patients with diabetes mellitus type 1 than in healthy population.
Aim. The aim of the study was to analyze factors contributing to diseases of the oral mucosa and gums in diabetic children.
Material and methods. Study group: 41 children with diabetes type 1 (18 boys and 23 girls of 5.33-17.83 years, mean age 12.92 ± 3.02); control group included 39 children (19 boys and 20 girls aged 4-17.75 years, mean age 11 ± 3.82). Dental examinations were performed to assess oral hygiene status (OHI-S), the state of oral mucous membrane, gums (GI) and teeth (DMFT/dmft). Material was collected for bacteriological and mycological examination and for evaluation of the physical and chemical properties of saliva. Laboratory rated exponents for control of diabetes were performed.
Results. No differences were found in the percentage of Candida spp. between study group and control. Gingivitis was observed with comparable frequency in both groups. The percentage of children with no signs of gingivitis was significantly higher in the control group (20 vs. 33%), while mild gingivitis was more often observed in children with diabetes (68 vs. 46%). Candida spp. infections were more frequent in children with elevated HbA1c. Cheilitis and atrophic glossitis were more often reported for diabetic children. HbA1c level positively correlated with atrophic glossitis, gingivitis, cheilitis and the presence of Lactobacillus acidophilus.
Conclusions. Metabolic disorders characteristic for diabetes favor the emergence of oral mucosa and gum diseases. No differences in the incidence rate for fungal gingivitis were observed between diabetic children and controls which may be attributed to more frequent pediatric and dental inspections associated with special care and monitoring of diabetic children.



INTRODUCTION
Diabetes mellitus type 1 is a term used to describe a severe metabolic disorder induced by insulin-deficiency. The disease results from the destruction of insulin-producing pancreatic beta cells in Langerhans islets by a beta-cell specific autoimmune process which involves T lymphocytes and macrophages. In diabetes type 1 the destruction of pancreatic beta-cells (insulitis) as result of inflammatory-cell /lymphocyte infiltration of insulin-producing pancreatic inslets constitutes the initiary phase of autoagression. The process of beta-cell destruction involves subpopulations of T lymphocytes (mostly Th1, Th2), cytotoxic lymphocytes CD8+, NK cells, macrophages/monocytes and mediators of inflammation secreted by immunocompetent cells (cytokines, free radicals/cytokine-induced free radicals) (1-4).
Diabetes-induced complications range from acute ketoacidosis and coma to long-term complications in different organs (retinopathy, nephropathy, cardiomyopathy, neuropathy) with diabetic angiopathy as the underlying factor.
Adequate/Good glycaemic control is the main target in the management of diabetes.
Inadequate/Poor control of diabetes not only results in long-term complications but also enhances susceptibility to bacterial and fungal infections one of which is yeast colonization of the oral cavity. Such colonization is not univocal to infection; an effective immune system of healthy people protects them against yeast-like fungi invasion and no pathological lesions are observed. Colonization progresses to infection only when the natural host-fungi equilibrium is disturbed. Candida albicans is the most frequent cause of oral infections. Colonization and tissue invasion by this bacteria species is facilitated by its morphological diversity, ability to adhere to host epithelial and endothelial cells, extracellular enzyme production and immunomodulative effect of Candida spp. antigens (5).
An important role in the antifungal host defense system is attributed to the oral milieu (e.g. mucosal integrity, antifungal effect of saliva, fungi-microflora interaction), defense mechanisms particularly related to phagocytic cells/phagocytes (mostly neutrophils) as well as specific cellular response.
Yeast-like oral infection promoting factors are:
I. Changes in secretion flow and biochemical parameters/composition of saliva i.e. higher glucose level, lower salivary pH, elevated salivary amylase, and oral mucosal injury (thickened capillary endothelium impairs oxygen flow and metabolic waste removal). Pathogenesis of salivary secretion in diabetic patients is not yet fully recognized. Clinical symptoms presented by diabetic patients include swollen salivary glands, especially parotid glands. Labial salivary glands of diabetic children reveal lymphocyte infiltrations similar to pancreatic infiltrations; this may be suggestive of similar or even identical autoimmune pathology (6). Disorders in salivary secretion may also be attributed to: angiopathy, neuropathy, smaller number of receptors on the surface of gland cells. Lower salivary secretion may also be attributed to poliuria, water balance disorders as well as medication administered for treatment of diabetic complications (7-10).
In diabetic children changes in salivary parameters/composition have also been observed. Literature reports on this subject vary mostly likely due to different study methods. Some authors report a marked decrease in total protein level, increase of salivary α-amylase and lactate dehydrogenase especially in children with poor glycemic control (6). Low saliva volume impairs oral self-purification and therefore favours dental plaque retention (11). In addition, higher glucose concentration in saliva and gum fluid may alter the living-conditions of bacteria and modify the microbial composition of the oral cavity. This may induce the development of oral infections, dental caries and periodontal diseases (12). The crucial factor here is high salivary glucose level observed also in patients with adequate diabetes control. Infections may also be attributed to plaque-pathogens which promote fungal infections. It is believed that the oral microflora/bacterial flora of diabetics is specifically changed and by producing leukotoxins may disturb neutrophil activity and bring on the inflammatory process (13).
II. The immunological response may also be disturbed by nonspecific factors such as:
1. Impairment of such neutrophil activity as: phagocytosis, intra-cellular pathogen elimination, adhesion and chemotaxis (14-16). Disturbance of the activity of these cells is closely related to the level of metabolic disorders observed in diabetic patients with poor diabetic control, elevated HbA1c levels and chronic/long-term diabetes (17).
In a hyperglicemic environment nonenzymatic glycosylation occurs on many proteins. The advanced glycation end products (AGE) play an important role in cell migration, phagocytic activity of macrophages/monocytes and finally lead to abundance of pathogenic bacterial and fungal flora in the oral cavity. Infection intensifies the oxidative stress and insulin resistance and so disturbs the regulatory secretion of proinflammatory TNF-α and IL-1. Oral infections may be induced by hyperglicemia, insulin resistance, accumulation of AGE proteins which cause degradation, destruction and proliferation of the connective tissue proteins. As result of non-enzymatic protein glycation there occurs disturbance in collagen synthesis, maturation and homeostasis followed by lower collagen resistance to change and impairment of blood vessel integrity (18-20).
In diabetic patients the level of immunoglobulin glycation has also been reported as higher for IgM than for IgG as well as impaired agglutination of IgM. It is believed that the high level of glycolized IgM reported in the early phase of acute infection negatively affect the immunological response (21, 22).
2. Cellular immunodeficiency
It has been demonstrated that in response to Candida spp. antigens there occurs a type Th1 immunological response characterized by high/increased interleukin 2 (IL-2) and IFN-gamma (IFN-γ) production while the levels of interleukin 4 (IL-4) and interleukin 10 (IL-10) production are low or null. Lower levels of T lymphocytes with regulatory CD+4 phenotype have also been demonstrated (23, 24).
Inadequate diabetic control leads to predominance of catabolic over anabolic processes with negative impact on inflammatory processes (23). Gingivitis and higher risk of parodontosis have been more frequently observed in diabetic children and adolescents than in healthy persons. These are fostered by: dental plaque, vascular changes in the marginal gingival, collagen metabolism disturbances and increased collagenase induced by hyperglycemia and wound healing impairment (25).
Up-to-date studies report that diabetes not only increases the risk of oral mucosa diseases but also impairs clinical treatment. Nowadays, the negative impact of oral diseases especially paradontium on management of diabetic patients is being strongly emphasized. It has been demonstrated that any inflammatory condition impairs diabetic control of a diabetic patient. Infections markedly increase insulin intake and therefore impede reaching normal range blood glucose levels (26).
AIM
The aim of the study was to assess the oral status of children with type 1 diabetes and analysis of factors that foster oral mucosa and gum diseases.
MATERIAL AND METHODS
The study included 41 children with type 1 diabetes (18 boys and 23 girls aged 5.33 to 17.83 years; mean age 12.92 ± 3.02) all patients of the Endocrinological Department and the out-patient clinic. The group was diversified for disease duration, age and control of diabetes.
Dental examination was performed during control visits at the outpatient clinic or during hospitalization. Management was based on insulin analogous (personal insulin pump) or intensive injection therapy. The control group comprised 39 healthy children (no diabetes or any other chronic disease). It consisted of 19 boys and 20 girls aged 4.17-17.75 years (mean age 11 ± 3.82).
All children were subjected to dental examination which included assessment of oral mucosa (frequency rate, site and scope of such specific lesions as cheilitis, atrophic glossitis, linea alba, lingual/tongue coating, mappy tongue), dental status according to DMFT index as well as micro hardness of mineralized tooth tissues. Oral hygiene status was assessed using the simplified Greene and Vermillion Oral Hygiene Index (OHI-S) (28) with mean OHI-S index values as baseline. Index values of 0.0-1.0, > 1.0-2.0 and > 2.0-3 indicated good, satisfactory and poor oral hygiene status respectively (28).

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otrzymano: 2014-07-02
zaakceptowano do druku: 2014-09-19

Adres do korespondencji:
*Izabela Rogozińska
Department of Pediatrics and Endocrinology Medical University of Warsaw
ul. Marszałkowska 24, 00-576 Warszawa
tel. +48 (22) 629-06-05
izabela.rogozinska@wp.pl

Postępy Nauk Medycznych 10/2014
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