The Influence of Type 1 Diabetes Mellitus on Dental Caries and Salivary Composition

Ferizi, Lulëjeta; Dragidella, Fatmir; Spahiu, Lidvana; Begzati, Agim; Kotori, Vjosa

doi:https://doi.org/10.1155/2018/5780916

International Journal of Dentistry

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2018 | Article ID 5780916 | https://doi.org/10.1155/2018/5780916

The Influence of Type 1 Diabetes Mellitus on Dental Caries and Salivary Composition

Lulëjeta Ferizi,¹Fatmir Dragidella,²Lidvana Spahiu,³Agim Begzati,¹and Vjosa Kotori³

Academic Editor: Izzet Yavuz

Received01 Jun 2018

Accepted26 Aug 2018

Published02 Oct 2018

Abstract

Diabetes mellitus is the most common chronic disease that affects the oral health. The aim of the study is to evaluate the dental caries, salivary flow rate, buffer capacity, and Lactobacilli in saliva in children with type 1 diabetes mellitus compared to the control group. Methods. The sample consisted of 160 children of 10 to 15 years divided into two groups: 80 children with type 1 diabetes mellitus and 80 children as a control group. Dental caries was assessed using the DMFT index for permanent dentition. Stimulated saliva was collected among all children. Salivary flow rate and buffer capacity were measured, and the colonies of Lactobacillus in saliva were determined. The observed children have answered a number of questions related to their dental visits and parents’ education. The data obtained from each group were compared statistically using the chi-square test and Mann–Whitney U-test. The significant level was set at . Results. DMFT in children with type 1 diabetes was significantly higher than that in the control group (). Diabetic children have a low level of stimulated salivary flow rate compared to control children (0.86 ± 0.16 and 1.10 ± 0.14). The buffer capacity showed statistically significant differences between children with type 1 diabetes and control group (). Also, children with type 1 diabetes had a higher count and a higher risk of Lactobacillus compared to the control group ( and ). Conclusion. The findings we obtained showed that type 1 diabetes mellitus has an important part in children’s oral health. It appears that children with type 1 diabetes are exposed to a higher risk for caries and oral health than nondiabetic children.

1. Introduction

Diabetes mellitus (DM) is a common chronic disease that leads to hyperglycemia [1–3]. It is classified into four general categories: type 1, in which the pancreas β-cells lose their capacity to produce insulin; type 2, in which a defect in the β-cells or a reduction in tissue sensitivity to insulin is necessary for disease manifestation; gestational diabetes, defined as any degree of glucose intolerance with onset or first recognition during pregnancy; and specific types of diabetes due to other causes, e.g., monogenic diabetes syndromes (such as neonatal diabetes and maturity-onset diabetes of the young (MODY)), diseases of the exocrine pancreas (such as cystic fibrosis), and drug- or chemical-induced diabetes (such as with glucocorticoid use, in the treatment of HIV/AIDS, or after organ transplantation) [1].

The oral cavity structure can be affected by diabetes, which may result in several complications including dental caries, periodontal disease, oral mucosal diseases, and saliva dysfunction that have a significant effect on the quality of life of diabetic patients. Also, untreated oral diseases may increase the risk of poor metabolic control [4]. The relationship between diabetes and dental caries has received the attention of researchers because both of the diseases are associated with carbohydrates. The insulin deficiency in diabetes may lead to hyposalivation and elevated salivary glucose levels, which may put diabetic patients at a high risk of caries development [5]. Saliva composition is an important factor in determining the prevalence of caries and oral health. It maintains the integrity of oral tissues, provides protection against immunologic bacterial, fungal, and viral infections [6], and controls the equilibrium between demineralization and remineralization in a cariogenic environment. Also, salivary buffers can stabilize pH in plaque, thus preventing demineralization of enamel [7–9]. Patients with diabetes have been reported to complain of dry mouth and salivary dysfunction leading to a reduction of salivary flow rate, lower buffer capacity, increased risk for dental caries, and bacterial infections [10].

Increasing the level of glucose in saliva affects the activity of microorganisms. Streptococcus mutans and Lactobacillus are considered to be related to caries and are the most cariogenic bacteria [11] because they have the ability to create a low pH environment and progression of caries [12]. Research studies show that Streptococcus mutans and Lactobacillus found in stimulated saliva explain better the development of caries than Streptococcus mutans and Lactobacillus found in plaque [13, 14]. For this reason, the combined analysis of dental caries, salivary components, and bacterial pathogens in saliva is a powerful method of following the oral diseases in children with type 1 diabetes mellitus [15].

The parents’ role is very important in relation to oral health because they are the main caregivers of their children’s oral health [16]. The studies show that the parents of children with diabetes are often careless about untreated dental caries in their children and not conscious enough on the importance of their oral health and its influence in diabetes [17, 18].

The aim of the study was to assess the dental caries, salivary flow rate, buffer capacity, and bacterial count of Lactobacillus in saliva between children with type 1 diabetes mellitus and control group.

2. Materials and Methods

2.1. Study Sample

The study was conducted in 160 children, including 80 children with type 1 diabetes mellitus aged 10–15 years, who were attending the Pediatric Clinic at University Medical Centre of Prishtina, Republic of Kosovo. All diabetic children were treated with insulin but not with any other therapy within the last month. The control group aged 10–15 years included 80 healthy children with absence of active diseases and no history of drug therapy within the previous month.

2.2. Clinical and Microbiological Procedures

All children were examined by a researcher at the Department of Pediatric Dentistry, University Dentistry Clinical Centre of Kosovo (UDCCK). Before children’s examination, an informed consent was received from their parents. The clinical dental health status was measured using the Decayed, Missing and Filled Teeth (DMFT) Index for permanent teeth according to the WHO caries diagnostic criteria for epidemiological studies [19].

The results of examination of the saliva were compared with the results of a control group of healthy children, corresponding in number and age of studied diabetic children. The test for evaluation of saliva included salivary flow rate, buffer capacity, and colonies of Lactobacillus in stimulated saliva. For at least one hour before the test is conducted, patients should neither eat nor drink anything. Each subject was given a piece of paraffin pellet and asked to chew the paraffin and to expectorate the stimulated saliva into the sterile container. Flow rate (5 min production) was defined as the volume of saliva secreted per min. The CRT buffer is used to determine the buffer capacity of saliva by means of a test strip featuring a special indicator system (Ivoclar Vivadent, Liechtenstein). Pipetted stimulated saliva from the container was dropped in each of the three fields of the strip test. The color of the field changed immediately, but the results were assessed after the expiration of the manufacturer’s reaction time (5 minutes) in the color scale. Blue indicates a high buffer capacity, green indicates a medium buffer capacity, and yellow color indicates a low buffer capacity of saliva. The CRT buffer enables the buffering capacity of saliva to be quickly and efficiently determined. For the microbial count identification, saliva was used instead of dental plaque because the saliva is sufficiently representative of the available microflora in the oral cavity. The presence of Lactobacillus was determined using the CRT bacteria test (Ivoclar Vivadent, Liechtenstein) on the saliva previously stimulated by chewing paraffin. Bacterial counts were recorded as colony-forming units per milliliter (CFU/mL) of saliva. The number of Lactobacillus colonies was graded as follows: Class 1 (none detected), Class 2 (10²–10³ CFU/mL), Class 3 (10⁴–10⁵ CFU/mL), and Class 4 (CFU ≥ 10⁵/mL), according to the manufacturers’ scoring card.

2.3. Questionnaire

All study participants were asked to fill in a prepared questionnaire during their visit to the dental clinic. The questions were answered by the children under the parental supervision.

The questionnaire included sections related to the frequency of dental visits and parents’ education. The parents’ education level was categorized into those who completed low-level education (primary school), middle-level education (secondary school), and high-level education (university).

2.4. Ethical Aspects

This study was approved by the Ethical Committee of Medical Faculty of the University of Prishtina, Kosovo, with Reference Number 4000/2016. Written informed consent was obtained from parents of children that were included in this study.

2.5. Data Analysis

The statistical analysis was carried out using MS Excel (Microsoft Corporation, Redmond, WA, USA) and SPSS 17 (SPSS Inc., Chicago, Illinois, USA) software. Percentages were compared by using the chi-square test. The difference in the values of D, M, F, and DMFT index for permanent teeth, between type 1 diabetes mellitus and healthy children, was tested using the Mann–Whitney U-test. Differences were set to be statistically significant at .

3. Results

Children included in this study were divided into two groups as children with and without type 1 diabetes mellitus. The results shown in Table 1 refer to the age and buffer capacity among the two groups of children. No significant difference between two groups with respect to the age of children was found (). Regarding buffer capacity, children with type 1 diabetes have a low buffer capacity and a medium buffer capacity (45.0% and 33.7%), whereas children from the control group have a high buffer capacity and a medium buffer capacity (39.4% and 31.3%) (Table 1).

The difference between the DMFT index of diabetic children and nondiabetic children is presented in Table 2. The component D was significantly higher in diabetic children (), whereas component F was higher in the control group (). No significant difference between groups related to component M () was found. In total, the DMFT index of children with type 1 diabetes mellitus was higher () compared to the DMFT index of nondiabetic children.

The average and standard deviation of salivary flow rate in children with type 1 diabetes mellitus are lower (0.86 ± 0.16 mL/min) than those of children in the control group (1.10 ± 0.14 mL/min) (Table 3).

The results related to Lactobacillus in both groups of children are shown in Table 4. Children with type 1 diabetes have significantly lower levels of colonies of Lactobacillus in Class 1 and Class 2 (0% and 27.5%) than the control group (21.3% and 51.3%). The colonies of Class 3 (10⁴–10⁵ CFU/mL) tend to be similar in both groups, in terms of Lactobacillus (25.0% and 23.8%), but regarding Class 4 of Lactobacillus, children with type 1 diabetes have higher levels of colonies of Lactobacillus than the control group (47.5% and 3.8%). Type 1 diabetes children are predisposed to have a higher caries risk of Lactobacillus than the control group. Low risk for caries was found in 27.5% of children with type 1 diabetes mellitus and 72.5% of the control group, whereas high risk for caries was significantly higher in children with type 1 diabetes (72.5%) than in the control group (27.5%) (Table 4).

As shown in Table 5 regarding dental visits, there is a significant difference between groups. The majority of children with type 1 diabetes visited the dentist only when necessary, whereas children from the control group visited dentist once a year (). Related to the parents’ education, children with type 1 diabetes mostly have medium and low levels of parents’ education, with a difference from the control group, which dominates with the medium and higher levels of parents’ education ().

4. Discussion

The prevalence of dental caries and its burden on the general population are of significant public health interest. Therefore, it is important to identify patients who may be at a high risk of dental caries and oral disease [20]. Diabetes mellitus may increase one’s susceptibility to dental caries. In addition, people with diabetes are also more prone to infections, including dental abscesses that are a result of progressive dental caries [5].

The results from the present study show that oral health of children with type 1 diabetes in Kosovo is a serious health problem. Previous studies conducted in Kosovo regarding dental caries among children and healthy adults reported high scores of dental caries [21–24]. In our study, the prevalence of dental caries was significantly higher among diabetic patients than nondiabetic patients. Several authors have reported similar findings [25–27], others reported low prevalence of dental caries among diabetics [28, 29], and some authors did not find any significant difference in the DMFT index between type 1 diabetic children and control group [30, 31]. Increased risk of dental caries would be related to certain factors such as poor oral hygiene, rare dental visits, and lack of metabolic control of diabetes.

Most of the studies have shown that patients with diabetes manifested low salivary flow rates, high levels of glucose in saliva [32, 33], and complaints of dry mouth [28]. Salivary flow rates are reduced in diabetic patients, and this may increase the sensitivity to oral infections, especially when there is a poor metabolic control of the disease. The results of this study showed a significant decrease of stimulated salivary flow rate and buffer capacity in diabetic patients when compared with nondiabetic children. A similar finding was also reported by other studies [34, 35]. Salivary flow rate in the present study was decreased in diabetic patients, but this finding was in disagreement with studies by Edblad et al. [36], Belazi et al. [37], and Canepari et al. [38]. They showed no difference in the salivary flow rate between diabetic and control subjects. Among several reasons which contribute to the decreased salivary flow rate in diabetes is hyperglycemia and glucosuria which cause a lower secretion of saliva. Also, if the diabetes is uncontrolled, these changes are more expressive [39].

In saliva, there are three major systems contributing to the buffer capacity: bicarbonate, phosphate, and protein buffer systems. The buffer capacity of saliva is an important factor, which has an important role in the maintenance of salivary pH and in dental remineralization. It correlates with salivary flow rate, and if any factor that decreases the salivary flow rate, it declines also its buffer capacity and increases the risk of caries development [40–42]. In our study, there was a significant difference in the mean salivary buffering capacity among study groups (). The results obtained are in accordance with the study performed by Aral et al. [43]. In their study, the authors found that the percentage of individuals with low salivary buffer capacity was highest in the diabetic group and lowest in the control group. However, other studies have shown no considerable difference between children with type 1 diabetes mellitus and control group related to buffer capacity [36, 38].

The buffer capacity also was studied by Saes Busato et al. [44], among adolescents with type 1 diabetes mellitus (14–19 years) and nondiabetic group. The adolescents in the type 1 diabetes mellitus group were evaluated at a baseline (T₀) and after 15 months (T₁), and those in the nondiabetic group were only evaluated at baseline (T₀). The salivary buffering capacity was slightly reduced after 15 months in adolescents with type 1 diabetes mellitus; at T₀, it was 4.8, and at T₁, it was 3.9. The study suggests that the hyposalivation and duration of the disease associate with a reduction in the buffer capacity in children with type 1 diabetes.

Most of the studies in diabetic children have analyzed the presence of Streptococcus mutans and Lactobacillus in the saliva. But in our study, the main focus was on the colonies of Lactobacillus, and the results showed a correlation between different levels of Lactobacillus in saliva; high levels of Lactobacillus were found in classes with a higher risk for caries. The similar results related to salivary Lactobacilli have been reported in other studies conducted by De Tove et al. [45] and Al-Khayoun et al. [46]. The authors found high levels of Lactobacillus in saliva in children with type 1 diabetes and evaluated that the poor metabolic control of diabetes had a significant effect on the Lactobacillus level in the saliva. Unlike our study, other studies reported no differences between the levels of Lactobacillus among children with type 1 diabetes and control group [18, 36, 47].

Twetman et al. [48] evaluated the quantitative distribution of Streptococcus mutans and Lactobacillus in saliva of type 1 diabetic children (aged 4–19) compared to healthy children regarding the metabolic control of the disease. They found low levels of Lactobacillus in the diabetic children which correlated with glucose concentration in saliva. Their findings suggest that the dietary treatment of children with type 1 diabetes reduced the number of Lactobacilli in saliva.

Although the results in our study report that children with type 1 diabetes have a higher caries risk of Lactobacillus, López Del Valle et al. [47] found no difference between type 1 diabetic children and control group regarding the caries risk of Lactobacillus. Diminished salivary flow is a suitable environment for the establishment of Streptococcus mutans and Lactobacillus in the oral cavity of diabetic patients, especially among the uncontrolled diabetes group. High levels of these bacteria in saliva can be considered an indicator of a cariogenic environment in the mouths of diabetes subjects. Streptococcus mutans is the main bacterium responsible for the occurrence of dental caries, whereas Lactobacillus is more related to the progression of caries due to its ability to adhere to the tooth surface [47].

The present study reports that the children with type 1 diabetes visited the dentist only when necessary, and our results were consistent with the study conducted by Tagelsir et al. [49] where children with type 1 diabetes rarely visited the dentist. Unlike our study, other studies have shown that children with type 1 diabetes visited the dentists at least once a year [50, 51]. Surprisingly, Al-Khabbaz et al. [52] found that only 24% of the diabetic children had their first dental visit before the age of 4 years, and a large number of them (44%) had never visited the dentist before. Apparently, the current health service in Kosovo provides free access to dental care to all Kosovo’s children up to 15 years, and parents should be encouraged to use these services to maintain the oral health of their children with type 1 diabetes mellitus.

Parents’ education and the impact of family is a well-recognized risk factor for caries and metabolic control in children with type 1 diabetes mellitus. The level of parents’ education regarding diabetic children in our study was medium and low, whereas the control group dominated with the medium and higher levels of parents’ education. The findings of our study are similar to those of other studies related to the level of parents’ education [18, 53]. In disparity to the results of our study, Siudikiene et al. [54] in their study found that a mother’s education level was not an important predictor of high caries experience. Parents of children with type 1 diabetes have a lack of sufficient knowledge on their children’s oral health and its influence on general health and also on metabolic control of diabetes. Therefore, parents’ education and their active involvement in their child’s diabetes self-management are crucial tools to achieve the desired goals.

4.1. Study Limitation

The researcher did not collect the information regarding the well-controlled and poorly controlled diabetes which may affect the dental caries and bacterial count. The authors may suggest further studies.

5. Conclusion

Diabetes is a risk factor for oral health complications. The findings of this study showed that children with type 1 diabetes mellitus exhibited significantly more dental caries, low salivary flow rate and buffer capacity, and higher count of Lactobacillus than healthy children. In addition, diabetic children must do regular dental visits. Parents also play a major role in their children’s oral health, and the dentist and pediatrician should inform them of the importance of their children’s oral health and routine dental checkups.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request. The corresponding author possesses data and may make data available upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

The authors are thankful to the Endocrinology Department of Pediatric Clinic at the University Clinical Centre of Kosovo (UCCK) in Prishtina for its support and assistance in this work. Also, the authors thank all the patients and their parents who participated in this study.

References

American Diabetes Association, “Classification and diagnosis of diabetes,” Diabetes Care, vol. 40, no. 1, pp. S11–S24, 2017.
View at: Publisher Site | Google Scholar
M. Badran and I. Laher, “Type II diabetes mellitus in arabic-speaking countries,” International Journal of Endocrinology, vol. 2012, Article ID 902873, 11 pages, 2012.
View at: Publisher Site | Google Scholar
P. P. Brahmkshatriya, A. A. Mehta, B. D. Saboo, and R. K. Goyal, “Characteristics and prevalence of latent autoimmune diabetes in adults (LADA),” ISRN Pharmacology, vol. 2012, Article ID 580202, 8 pages, 2012.
View at: Publisher Site | Google Scholar
R. S. Leite, N. M. Marlow, and J. K. Fernandes, “Oral Health and type 2 diabetes,” American Journal of the Medical Sciences, vol. 345, no. 4, pp. 271–273, 2013.
View at: Publisher Site | Google Scholar
E. A. Malvania, S. A. Sheth, A. S. Sharma, S. Mansuri, F. Shaikh, and S. Sahani, “Dental caries prevalence among type II diabetic and nondiabetic adults attending a hospital,” Journal of International Society of Preventive and Community Dentistry, vol. 6, no. 9, pp. 232–236, 2016.
View at: Publisher Site | Google Scholar
L. P. Bretas, M. E. Rocha, M. S. Vieira, and A. Rodríguez, “Flow rate and buffering capacity of the saliva as indicators of the susceptibility to caries disease,” Pesquisa Brasileira em Odontopediatria e Clínica Integrada, vol. 8, no. 3, pp. 289–293, 2008.
View at: Publisher Site | Google Scholar
B. P. Preethi, D. Reshma, and P. Anand, “Evaluation of flow rate, pH, buffering capacity, calcium, total proteins and total antioxidant capacity levels of saliva in caries free and caries active children: an in vivo study,” Indian Journal of Clinical Biochemistry, vol. 25, no. 4, pp. 425–428, 2010.
View at: Publisher Site | Google Scholar
F. J. Dowd, “Saliva and dental caries,” Dental Clinics North of America, vol. 43, no. 4, pp. 579–597, 1999.
View at: Google Scholar
D. Animireddy, V. T. Reddy Bekkem, P. Vallala, S. B. Kotha, S. Ankireddy, and N. Mohammad, “Evaluation of pH, buffering capacity, viscosity and flow rate levels of saliva in caries-free, minimal caries and nursing caries children: an in vivo study,” Contemporary Clinical Dentistry, vol. 5, no. 3, pp. 324–328, 2014.
View at: Publisher Site | Google Scholar
A. Y. Al-Maskari, M. Y. Al-Maskari, and S. Al-Sudairy, “Oral manifestations and complications of diabetes mellitus: a review,” Sultan Qaboos University Medical Journal, vol. 11, no. 2, pp. 179–186, 2011.
View at: Google Scholar
J. A. Teixeira, A. V. C. Silva, V. E. Dos Santos Júnior et al., “Effects of a new nano-silver fluoride-containing dentifrice on deminaralization of enamel and streptococcus mutans adhesion and acidogenicity,” International Journal of Dentistry, vol. 2018, Article ID 1351925, 9 pages, 2018.
View at: Publisher Site | Google Scholar
I. Chase, R. J. Berkowitz, S. A. Mundorff-Shrestha, H. M. Proskin, P. Weinstein, and R. Billings, “Clinical outcomes for Early Childhood Caries (ECC): the influence of salivary mutans streptococci levels,” European Journal of Dentistry, vol. 5, no. 3, pp. 143–146, 2004.
View at: Google Scholar
Y. Li, S. Argimón, C. N. Schön, P. Saraithong, and P. W. Caufield, “Characterizing diversity of lactobacilli associated with severe early childhood caries: a study protocol,” Advances in Microbiology, vol. 5, no. 1, pp. 9–20, 2015.
View at: Publisher Site | Google Scholar
C. Badet and N. Thebaud, “Ecology of lactobacilli in the oral cavity: a review of literature,” Open Microbiology Journal, vol. 2, no. 1, pp. 38–48, 2008.
View at: Publisher Site | Google Scholar
H. G. Mohamed, S. B. Idris, M. Mustafa et al., “Influence of type 2 diabetes on prevalence of key periodontal pathogens, salivary matrix metalloproteinases, and bone remodeling markers in sudanese adults with and without chronic periodontitis,” International Journal of Dentistry, vol. 2016, Article ID 6296854, 9 pages, 2016.
View at: Publisher Site | Google Scholar
E. Bozorgmehr, A. Hajizamani, and T. Malek Mohammadi, “Oral health behavior of parents as a predictor of oral health status of their children,” ISRN Dentistry, vol. 2013, Article ID 741783, 5 pages, 2013.
View at: Publisher Site | Google Scholar
E. Dawkins, A. Michimi, G. Ellis-Griffith, T. Peterson, D. Carter, and G. English, “Dental caries among children visiting a mobile dental clinic in South Central Kentucky: a pooled cross-sectional study,” BMC Oral Health, vol. 13, no. 1, p. 19, 2013.
View at: Publisher Site | Google Scholar
M. El-Tekeya, M. El Tantawi, H. Fetouh, E. Mowafy, and N. Abo Khedr, “Caries risk indicators in children with type 1 diabetes mellitus in relation to metabolic control,” Pediatric Dental, vol. 34, no. 7, pp. 510–516, 2012.
View at: Google Scholar
World Health Organisation, Oral Health Surveys: Basic Methods, World Health Organisation, Geneva, Switzerland, 4th edition, 1997.
J. A. Ship, “Diabetes and oral health: an overview,” Journal of the American Dental Association, vol. 134, no. 1, pp. 4S–10S, 2003.
View at: Publisher Site | Google Scholar
L. Ferizi, F. Dragidella, G. Staka, V. Bimbashi, and S. Mrasori, “Oral health status related to social behaviors among 6–11 year old schoolchildren in Kosovo,” Acta Stomatologica Croatica, vol. 51, no. 2, pp. 122–132, 2017.
View at: Publisher Site | Google Scholar
L. F. Shabani, A. Begzati, F. Dragidella, V. H. Hoxha, V. H. Cakolli, and B. Bruçi, “The correlation between DMFT and OHI-S index among 10–15 years old children in Kosova,” International Journal of Dentistry and Oral Health, vol. 5, pp. 2002–2005, 2015.
View at: Publisher Site | Google Scholar
B. Kamberi, F. Koçani, A. Begzati et al., “Prevalence of dental caries in Kosovar adult population,” International Journal of Dentistry, vol. 2016, Article ID 4290291, 6 pages, 2016.
View at: Publisher Site | Google Scholar
A. Begzati, K. Meqa, D. Siegenthaler, M. Berisha, and W. Mautsch, “Dental health evaluation of children in Kosovo,” European Journal of Dentistry, vol. 5, no. 1, pp. 32–39, 2011.
View at: Google Scholar
E. S. Akpata, Q. Alomari, O. A. Mojiminiyi, and H. Al-Sanae, “Caries experience among children with type 1 diabetes in Kuwait,” Pediatric Dentistry, vol. 34, no. 7, pp. 468–472, 2012.
View at: Google Scholar
A. Arheiam and S. Omar, “Dental caries experience and periodontal treatment needs of 10- to 15-year old children with type 1 diabetes mellitus,” International Dental Journal, vol. 64, no. 3, pp. 150–154, 2014.
View at: Publisher Site | Google Scholar
S. Miko, S. J. Ambrus, S. Sahafian, E. Dinya, G. Tamas, and M. G. Albrecht, “Dental caries and adolescents with type 1 diabetes,” British Dental Journal, vol. 208, no. 6, p. E12, 2010.
View at: Publisher Site | Google Scholar
V. K. Gupta, S. Malhotra, V. Sharma, and S. S. Hiremath, “The influence of insulin dependent diabetes mellitus on dental caries and salivary flow,” International Journal of Chronic Diseases, vol. 2014, Article ID 790898, 5 pages, 2014.
View at: Publisher Site | Google Scholar
L. Bassir, R. Amani, M. Khaneh Masjedi, and F. Ahangarpor, “Relationship between dietary patterns and dental health in type I diabetic children compared with healthy controls,” Iranian Red Crescent Medical Journal, vol. 16, no. 1, p. 9684, 2014.
View at: Publisher Site | Google Scholar
A. F. Ismail, C. P. McGrath, and C. K. Y. Yiu, “Oral health status of children with type 1 diabetes: a comparative study,” Journal of Pediatric Endocrinology and Metabolism, vol. 30, no. 11, pp. 1155–1159, 2017.
View at: Publisher Site | Google Scholar
R. Rafatjou, Z. Razavi, S. Tayebi, M. Khalili, and M. Farhadian, “Dental health status and hygiene in children and adolescents with type 1 diabetes mellitus,” Journal of Research in Health Sciences, vol. 16, no. 3, pp. 122–126, 2016.
View at: Google Scholar
R. Harrison and W. H. Bowen, “Flow rate and organic constituents of whole saliva in insulin-dependent diabetic children and adolescents,” Pediatric Dentistry, vol. 9, no. 4, pp. 287–291, 1987.
View at: Google Scholar
R. M López-Pintor, E. Casañas, J. González-Serrano et al., “Xerostomia, hyposalivation, and salivary flow in diabetes patients,” Journal of Diabetes Research, vol. 2016, Article ID 4372852, 15 pages, 2016.
View at: Publisher Site | Google Scholar
B. Karthikeyan, L. S. Negi, S. B. Kondaveeti, S. Pragash, and R. Thayappan, “Glycated albumin levels in relation to dental caries, mutants streptococci lactobacilli and salivary status of type 2 diabetes mellitus patients,” Indian Journal of Mednodent and Allied Sciences, vol. 3, no. 2, pp. 82–89, 2015.
View at: Publisher Site | Google Scholar
J. Siudikiene, V. Machiulskiene, B. Nyvad, J. Tenovuo, and I. Nedzelskiene, “Dental caries and salivary status in children with type 1 diabetes mellitus, related to the metabolic control of the disease,” European Journal of Oral Sciences, vol. 114, no. 1, pp. 8–14, 2006.
View at: Publisher Site | Google Scholar
E. Edblad, S. A. Lundin, B. Sjodin, and J. Aman, “Caries and salivary status in young adults with type 1 diabetes,” Swedish Dental Journal, vol. 25, no. 2, pp. 53–60, 2001.
View at: Google Scholar
M. A. Belazi, A. Galli-Tsinopoulou, D. Drakoulakos, A. Fleva, and P. H. Papanayiotou, “Salivary alterations in insulin-dependent diabetes mellitus,” International Journal of Paediatric Dentistry, vol. 8, no. 1, pp. 29–33, 1998.
View at: Publisher Site | Google Scholar
P. Canepari, N. Zerman, and G. Cavalleri, “Lack of correlation between salivary Streptococcus mutans and lactobacilli counts and caries in IDDM children,” Minerva Stomatologica, vol. 43, no. 11, pp. 501–505, 1994.
View at: Google Scholar
A. Hoseini, A. Mirzapour, A. Bijani, and A. Shirzad, “Salivary flow rate and xerostomia in patients with type I and II diabetes mellitus,” Electron Physician, vol. 9, no. 9, pp. 5244–5249, 2017.
View at: Publisher Site | Google Scholar
C. Fenoll-Palomares, J. V. Muñoz Montagut, V. Sanchiz et al., “Unstimulated salivary flow rate, pH and buffer capacity of saliva in healthy volunteers,” Revista Española de Enfermedades Digestivas, vol. 96, no. 11, pp. 773–783, 2004.
View at: Publisher Site | Google Scholar
A. Bardow, D. Moe, B. Nyvad, and B. Nauntofte, “The buffer capacity and buffer systems of human whole saliva measured without loss of CO₂,” Archives of Oral Biology, vol. 45, no. 1, pp. 1–12, 2000.
View at: Publisher Site | Google Scholar
V. De Almeida Pdel, A. M. Grégio, M. Â. Machado, A. A. De Lima, and L. R. Azevedo, “Saliva composition and functions: a comprehensive review,” Journal of Contemporary Dental Practice, vol. 9, no. 3, pp. 72–80, 2008.
View at: Google Scholar
C. A. Aral, B. G. Nur, M. Altunsoy, and K. Demir, “Yeni tip 1 diabetes mellitus teşhisi konulan çocuklarda tükürük tamponlama kapasitesi ve akiş hizi değişiklikleri,” Turkiye Klinikleri Journal of Dental Sciences, vol. 22, no. 1, pp. 48–54, 2016.
View at: Publisher Site | Google Scholar
I. M. Saes Busato, C. C. Antoni, T. Calcagnotto, S. A. Ignácio, and L. R. Azevedo-Alanis, “Salivary flow rate, buffer capacity, and urea concentracion in adolescent with type 1 diabetes mellitus,” Journal of Pediatric Endocrinology and Metabolism, vol. 29, no. 12, pp. 1359–1363, 2016.
View at: Publisher Site | Google Scholar
M. M. S. De Tove, R. Bakayoko-Ly, and A. K. N’Guessan, “Relations entre le flux salivaire et le taux élevé des Streptocoques mutans et des Lactobacilles salivaires chez l’enfant diabétique de type 1,” Médecine Buccale Chirurgie Buccale, vol. 19, pp. 3–6, 2013.
View at: Publisher Site | Google Scholar
J. D. Al-Khayoun and B. S. Diab, “Dental caries, mutans streptococci, lactobacilli and salivary status of type 1 diabetic mellitus patients aged 18-22 years in relation to glycated haemoglobin,” Journal of Baghdad College of Dentistry, vol. 25, no. 1, pp. 153–158, 2013.
View at: Google Scholar
L. M. López Del Valle and C. Ocasio-López, “Comparing the oral health status of diabetic and non-diabetic children from puerto rico: a case-control pilot study,” Puerto Rico Health Sciences Journal, vol. 30, no. 3, pp. 123–127, 2011.
View at: Google Scholar
S. Twetman, S. Aronsson, and S. Björkman, “Mutans streptococci and lactobacilli in saliva from children with insulin-dependent diabetes mellitus,” Oral Microbiology and Immunology, vol. 4, no. 3, pp. 165–168, 1989.
View at: Publisher Site | Google Scholar
A. Tagelsir, R. Cauwels, S. Van Aken, J. Vanobbergen, and L. C. Martens, “Dental caries and dental care level (restorative index) in children with diabetes mellitus type 1,” International Journal of Paediatric Dentistry, vol. 21, no. 1, pp. 13–22, 2011.
View at: Publisher Site | Google Scholar
C. Alves, M. Brandao, J. Andion, and R. Menezes, “Oral health knowledge and habits in children with type 1 diabetes mellitus,” Brazilian Dental Journal, vol. 20, no. 1, pp. 70–73, 2009.
View at: Publisher Site | Google Scholar
S. Lai, M. G. Cagetti, F. Cocco et al., “Evaluation of the difference in caries experience in diabetic and non-diabetic children-a case control study,” PLoS One, vol. 12, no. 11, Article ID e0188451, 2017.
View at: Publisher Site | Google Scholar
A. K. Al-Khabbaz, K. F. Al-Shammari, A. Hasan, and M. Abdul-Rasoul, “Periodontal health of children with type 1 diabetes mellitus in kuwait: a case-control study,” Medical Principles and Practice, vol. 22, no. 2, pp. 144–149, 2013.
View at: Publisher Site | Google Scholar
H. A. Sohn and D. J. Rowe, “Oral health knowledge, attitudes and behaviors of parents of children with diabetes compared to those of parents of children without diabetes,” Journal of Dental Hygiene, vol. 89, no. 3, pp. 170–179, 2015.
View at: Google Scholar
J. Siudikiene, V. Maciulskiene, and I. Nedzelskiene, “Dietary and oral hygiene habits in children with type I diabetes mellitus related to dental caries,” Stomatologija, vol. 7, no. 2, pp. 58–62, 2005.
View at: Google Scholar

Copyright

Copyright © 2018 Lulëjeta Ferizi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

6466

Downloads

2532

Citations