Indian Journal of Dental ResearchIndian Journal of Dental ResearchIndian Journal of Dental Research
HOME | ABOUT US | EDITORIAL BOARD | AHEAD OF PRINT | CURRENT ISSUE | ARCHIVES | INSTRUCTIONS | SUBSCRIBE | ADVERTISE | CONTACT
Indian Journal of Dental Research   Login   |  Users online: 1452

Home Bookmark this page Print this page Email this page Small font sizeDefault font size Increase font size         

 


 
Table of Contents   
ORIGINAL RESEARCH  
Year : 2013  |  Volume : 24  |  Issue : 3  |  Page : 342-346
Detection of putative periodontopathic bacteria in type 1 diabetic and healthy children: A comparative study


1 Department of Paedodontics and Preventive Dentistry, Sree Balaji Dental College and Hospital, Bharath University, Pallikaranai, Chennai, Tamilnadu, India
2 Department of Paedodontics and Preventive Dentistry, Sree Balaji Dental College and Hospital, Bharath University, Pallikaranai; Department of Paedodontics and Preventive Dentistry, Sri Venkateswara Dental College and Hospital, Chennai, Tamilnadu, India
3 Department of Microbiology, Dr. A.L.M. PG Institute of Basic Medical Sciences, University of Madras, Taramani, Chennai, Tamilnadu, India
4 Department of Microbiology, Sree Balaji Dental College and Hospital, Bharath University, Pallikaranai, Chennai, Tamilnadu, India

Click here for correspondence address and email

Date of Submission28-Dec-2011
Date of Decision08-Sep-2012
Date of Acceptance01-Feb-2013
Date of Web Publication12-Sep-2013
 

   Abstract 

Aim: The aim of this study was to compare and assess the risk of periodontitis due to the presence of four putative periodontopathic bacteria (Porphyromonas gingivalis, Treponema denticola, Tannerella forsythia, and Aggregatibacter actinomycetemcomitans) in type 1 diabetic and healthy children.
Materials and Methods: Fifty type 1 diabetic and 50 healthy children in the age group of 7-14 years were recruited for the study. Subgingival plaque samples collected from permanent first molars were subjected to polymerase chain reaction assay to detect 16S rRNA gene of P. gingivalis, T. forsythia, T. denticola and A. actinomycetemcomitans. The data were analyzed using Fisher exact test. The P < 0.05 was considered statistically significant.
Results: The prevalence of subgingival periodontal pathogens in diabetic and healthy children was 2% and 4% for P. gingivalis, 34% and 34% for T. denticola, 20% and 18% for A. actinomycetemcomitans and for T. forsythia, 4% and 34%, respectively. Significant statistical difference was not observed with regard to the prevalence of P. gingivalis, T. denticola, and A. actinomycetemcomitans among type 1 diabetic and healthy children (P = 1.00). Conversely, T. forsythia was less prevalent in diabetic children compared to healthy children.
Conclusion: Statistical significance was not observed for the prevalence of periodontopathic bacteria in type 1 diabetic subjects. The results of the present study thus reveal the absence of risk of periodontitis by these bacterial species in type 1 diabetic subjects.

Keywords: A. actinomycetemcomitans, P. gingivalis, T. denticola, T. forsythia, type I diabetes

How to cite this article:
Arangannal P, Santoshkumari, Krishnan P, Nichani MH, Krishnan M, Chamarthi V. Detection of putative periodontopathic bacteria in type 1 diabetic and healthy children: A comparative study. Indian J Dent Res 2013;24:342-6

How to cite this URL:
Arangannal P, Santoshkumari, Krishnan P, Nichani MH, Krishnan M, Chamarthi V. Detection of putative periodontopathic bacteria in type 1 diabetic and healthy children: A comparative study. Indian J Dent Res [serial online] 2013 [cited 2019 Dec 5];24:342-6. Available from: http://www.ijdr.in/text.asp?2013/24/3/342/118000
Diabetes mellitus is a group of metabolic disorder characterized by hyperglycemia resulting from defect in Insulin secretion or absorption or both. There are four different types of Diabetes mellitus but vast majority of cases of diabetes fall in two categories. They are Type 1 Diabetes Mellitus (T1DM) and Type 2 Diabetes Mellitus (T2DM). [1] T1DM is due to autoimmune destruction of the insulin-producing pancreatic beta cells resulting in absolute deficiency of insulin. The diagnosis of Type 1 diabetes can be made at any age, but it usually manifests in childhood, adolescence or early adulthood, before the age of 20. [2] According to the American Diabetes Association, Type 1 diabetes is present in 5-10% of patients with diabetes. [2]

Among the long-term systemic complications of uncontrolled diabetes, periodontal diseases is the 6 th most common complication. [3] Periodontal disease is caused by gram-negative anaerobic periodontopathic subgingival microflora. [4],[5] In recent years, much interest has focused on this subgingival microflora and its role in destructive periodontal disease. The gram-negative putative periodontopathic bacteria (Porphyromonas gingivalis, Tannerella forsythia, Treponema denticola, and Aggregatibacter actinomycetemcomitans) are known causative agents for periodontitis [4] and identification of these putative pathogens can act as marker for onset of the periodontal diseases. [5],[6] These gram-negative periodontal pathogens especially P. gingivalis has been detected in high numbers in adult long-duration insulin-dependent diabetics. [7]

Detection of anaerobic bacteria by culture methods are challenging because of their specific growth requirements like anaerobic environment and certain technical barriers. [8],[9] Advances in molecular biology such as polymerase chain reaction (PCR) have enabled the identification of specific bacteria in large number of periodontitis cases. The PCR is a relatively simple, sensitive and rapid test for successful detection of oral anaerobic bacterial pathogens. [9],[10]

The presence of gram-negative periodontopathic bacteria and its relation with periodontal disease is widely studied in adult (Type 2) diabetic population [11],[12],[13],[14],[15],[16] but there are hardly any reports in children. Hence, the purpose of the present study was to compare the prevalence and assess the risk of the four periodontopathic bacteria (P. gingivalis, T. denticola, T. forsythia, and A. actinomycetemcomitans) among the type 1 diabetic children and healthy children/adolescents between the age group of 7 and 14 years, using PCR.


   Materials and Methods Top


The present study was cleared by the institutional ethical committee of Sree Balaji Dental College and Hospital, Chennai and the Department of Endocrinology and Diabetology, Institute of Child Health and Hospital for Children (ICHS), Chennai. Diabetic children and adolescents were screened by a single examiner in the Dental Department ICHS and selected based on inclusion and exclusion criteria.

Fifty children with type I diabetic were recruited for the study. Confirmed diagnosis of T1DM, age between 7 and 14 years, presence of all permanent first molars, were the inclusion criteria. History of diabetic related systemic complications, professional dental cleaning and periodontal therapy for past 6 months, antibiotic therapy for past 3 months and history of orthodontic treatment were the exclusion criteria. Fifty healthy children and adolescents attending the Department of Paedodontics and Preventive Dentistry, Sree Balaji Dental College and Hospital, Chennai were included as control group. Absence of systemic diseases, age between 7 and 14 years and presence of all permanent first molars were the inclusion criteria for the control group. Informed consent was obtained from the parents/guardian of all children enrolled for the study.

Intra-oral examination was carried out for all the 100 selected subjects and clinical parameters such as plaque index (Silness and loe 1964) and gingival index (Silness and Loe 1967) were recorded. The level of bleeding on probing was more in T1DM patient. The probing depths ranged 3-5 mm. Clinical attachment levels were not measured. Subgingival plaque was collected using sterile Gracey curette from the buccal surface of all first permanent molars after careful removal of supragingival plaque with sterile cotton roll. The plaque was immediately transferred to sterile tubes containing 500 μl of sterile phosphate buffered saline (pH 7.8). The samples were then transferred with necessary precautions to the Department of Microbiology, Institute of Basic Medical Sciences Chennai and stored at −20° till assay.

PCR analysis

The Subgingival plaque was micro-centrifuged at 8,000 rpm for 5 min, the supernatant was discarded and the pellet was re-suspended with 250 μl of lysis buffer. DNA extraction was performed by boiling-lysis method and the supernatant was used as template for PCR assay. Species specific primers for the target organisms have been used as suggested by previous studies. [8],[9] PCR reaction mixture (50 μl) for the detection of 16S rRNA of the four bacterial species contained 5 μl of ×10 PCR buffer (pH 8.4), 1 U Taq DNA polymerase (Bangalore genei, India.), 0.25 mMol/L of each deoxyribonucleotides (dNTP) (Medox Biotech India Pvt., Ltd.), 1.5 mM MgCl 2 (Sigma-Aldrich Pvt., Ltd.) , 0.5 μM of each primer (Sigma-Aldrich Pvt., Ltd.) and 5 μl of the template. Bacterial sequences submitted to Gen Bank under accession no's HQ112349, HQ112350, HQ202265 and HQ188689 were used as positive controls and sterile millipore water served as blank control. PCR was carried out for 35 cycle with each cycle consisting of denaturation (94°C for 5 min), annealing (50°C for 1 min) and primer extension (72°C for 1.5 min). Amplified PCR products were detected by 1.5% gel electrophoresis (Bio-rad, USA).

Statistical analysis

Fisher exact test (two-tailed) was used to calculate the P value. SPSS software 15 was used for all statistical analysis. In the present study, P < 0.05 was considered statistically significant. The odds ratio at 95% confidence interval was calculated to assess the association of the bacterial species to type I diabetes.


   Results Top


PCR carried out with the subgingival plaque samples of type I diabetic children and healthy children amplified the 16S rRNA gene of P. gingivalis, T. forsythia, T. denticola and A. actinomycetemcomitans in the product size of 404 bp, 641b p, 316 bp and 443 bp, respectively. None of the samples showed non-specific amplification. [Table 1] shows the prevalence of four bacterial species in type I diabetic group and healthy subjects. The sample that was positive for P. gingivalis in type I diabetic and healthy subject was also positive for T. denticola. Two of the type I diabetic children showed co-occurrence of T. forsythia, A. actinomycetemcomitans and T. denticola. Co-occurrence of A. actinomycetemcomitans, and T. denticola was observed among six type I diabetic children. One healthy subject showed positive for all the four periodontopathic bacteria screened. T. forsythia and T. denticola co-occurred in eight healthy samples. A. actinomycetemcomitans and T. forsythia co-occurred in four healthy samples. The association between type I diabetes and healthy group with regard to P. gingivalis, T. denticola and A. actinomycetemcomitans is considered statistically insignificant as the two-tailed P = 1.000 by Fisher exact test. Conversely, good statistical difference was observed between type I diabetes and healthy group with regard to T. forsythia (two-tailed P = 0.0002 by Fisher exact test). [Table 2] shows the clinical parameters measured. Significant difference was not noticed in the PD between the T1DM and control group. The Plaque index was 0.35 and 0.37 for diabetic and healthy group, respectively. The gingival index was 0.88 and 0.44 for diabetic and healthy group respectively. The level of gingival bleeding (gingival index-0.88) on probing was more in T1DM children. Statistically significant difference was not observed for gingival index. The HbA1c Level of children withT1DM ranged 5.66-11.50%. About 45% of the T1DM children HbA1c readings were above 8.0%. The duration of diabetes among T1DM subjects ranged 3-7 years. The odds ratio (at 95% confidence interval) calculated for P. gingivalis, T. forsythia, T. denticola, and A. actinomycetemcomitans were 0.48 (0.043-5.58), 0.08 (0.017-0.37), 1 (0.44-2.29) and 1.13 (0.42-3.09) respectively.
Table 1: Percentage prevalence of periodontopathic bacteria among type I diabetes children and healthy subjects

Click here to view
Table 2: Clinical parameters measured

Click here to view



   Discussion Top


The etiology of periodontal disease is a result of interaction between the plaque biofilm, microbial by products and the host response. [5] Bacteria are the primary etiological factor of periodontal disease. It is a proven fact that diabetes mellitus is a risk-factor for development of periodontitis in adults. [3] The association between periodontal disease and diabetes mellitus with respect to gram-negative anaerobes in adult population has been extensively studied. [14],[15],[16] while, data regarding prevalence of periodontopathic bacteria among type I diabetic children are lacking.

The PCR method of detection is advantageous over routinely used culture techniques, owing to their greater specificity and sensitivity, and less labor intensive. [10] The 16S rRNA detection by PCR method is accurate, reproducible, highly sensitive test for identification of highly fastidious gram negative pathogens. [9]

In the present study, 2% and 4% of P. gingivalis, 34% and 34% of T. denticola, 20% and 18% of A. actinomycetemcomitans, 4% and 34% of T. forsythia was detected in diabetic and healthy group respectively. P. gingivalis, T. denticola, and T. forsythia are principal red complex periodontopathogenic bacteria which exist as a consortium in subgingival biofilms. [4],[5] Despite red complex A. actinomycetemcomitans was also screened due to its association with aggressive periodontitis, which is mostly reported in adolescence. [17]

The results of the present study are well in concurrence with Matto et al. [18] who has reported P. gingivalis in 5% of the healthy children between 5 and 10 years of age. In contrast to the present study, Kulekci et al. [19] (12%) and Gafan et al. [20] (49%) found higher prevalence of P. gingivalis in healthy children. The present study found a very low prevalence of P. gingivalis (2%) among T1DM children compared to higher prevalence in few earlier reports among adult T1DM diabetes. [7],[15]

The prevalence rate (34%) observed in both the groups for T. denticola is well in concurrence with few previous studies. [19],[21]

Among the healthy children, prevalence rate of A. actinomycetemcomitans found in this study is in accordance with Kulekci et al. [19] who had reported a prevalence of 24%. In Type 1 diabetic children 20% of prevalence was detected for A. actinomycetemcomitans, which is high when compared to Trevonen et al. [15] study (6.5%). The higher prevalence in the present study may be due to the PCR method of detection in contrast to immunoassay method by Trevonen et al. [15]

The prevalence of T. forsythia in the present study among healthy children is well in agreement with Gafan et al., [20] Okada et al. [22] and Campus et al.[13] Gafan et al. [20] concluded that there is 2.3 times greater chance of developing gingivitis in absence of T. forsythia as this micro-organism is mostly associated with dental plaque of healthy individuals.

There was no significant statistical difference between type 1 diabetic and healthy children/adolescent in the prevalence of P. gingivalis, T. denticola, and A. actinomycetemcomitans. Thus, the results of this study are in agreement with various other previous reports. [7],[13],[15],[21] On the contrary, similar plaque level was observed in both the groups. Although, periodontal pathogens are necessary for progression of periodontal disease, their presence alone is not responsible for development of the disease. The failure to establish any statistically significant difference between the bacterial profile of type 1 diabetic and healthy children in the present study and other studies, [7],[13],[15],[21] suggest that factors other than micro-organism are needed to initiate the disease. Van winkelhoff et al. [23] had suggested that mere presence of periodontal pathogens in subgingival plaque were not enough to initiate the destructive periodontal disease and apparently susceptible host is needed to initiate the disease.

Cianciola et al. [24] have proposed that altered host immune response has a vital role in the development and progression of periodontal disease. He found 9.8% prevalence of periodontal disease in type 1 diabetic children when compared to 1.7% in control group even though there was no difference in the periodontal pathogens levels. In spite of similar prevalence of periodontopathic bacteria in the 2 groups, there was increased bleeding on probing in the gingiva of type 1 diabetic children, which was similar to the findings of two previous reports on periodontal changes among type I diabetic children. [25],[26] The similar prevalence among type I diabetic and healthy children in the present study with respect to bacterial profiles is well in agreement with Lalla et al. [27] Alteration in the function of immune inflammatory cells and hyper-responsiveness of macrophage and monocyte results in increased production of tumor necrosis factor (TNFα), IL-1 in response to the periodontal pathogens leading to prolonged inflammatory response and host tissue destruction. [23],[24],[28],[29] The results of the present study is well in agreement with the study of Salvi et al. [29] who found that there was no difference in the bacterial composition in both type 1 diabetic and non-diabetic individual. Only a few studies on the T1DM children with reference to periodontal pathogen have been reported, while, plenty of studies in adult T1DM and periodontitis have been reported. Hence, the results of the present study have been compared with adult T1DM. [27],[29]

In conclusion, the odds ratio of P. gingivalis, T. forsythia, T. denticola, and A. actinomycetemcomitans revealed a negative association to type I diabetes and hence the risk of periodontitis in this group is absent due to the presence of these bacterial species. A large cohort study may help in identifying the risk of periodontitis due to these periodontopathic bacteria in type I diabetes.

 
   References Top

1.Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R, et al. Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 2003;26:3160-7.  Back to cited text no. 1
[PUBMED]    
2.Silverstein J, Klingensmith G, Copeland K, Plotnick L, Kaufman F, Laffel L, et al. Care of children and adolescents with type 1 diabetes: A statement of the American Diabetes Association. Diabetes Care 2005;28:186-212.  Back to cited text no. 2
[PUBMED]    
3.Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329-34.  Back to cited text no. 3
    
4.Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998;25:134-44.  Back to cited text no. 4
[PUBMED]    
5.Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000 2005;38:135-87.  Back to cited text no. 5
    
6.Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: The "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 2005;38:72-122.  Back to cited text no. 6
    
7.Thorstensson H, Dahlén G, Hugoson A. Some suspected periodontopathogens and serum antibody response in adult long-duration insulin-dependent diabetics. J Clin Periodontol 1995;22:449-58.  Back to cited text no. 7
    
8.Riggio MP, Macfarlane TW, Mackenzie D, Lennon A, Smith AJ, Kinane D. Comparison of polymerase chain reaction and culture methods for detection of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in subgingival plaque samples. J Periodontal Res 1996;31:496-501.  Back to cited text no. 8
[PUBMED]    
9.Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 1996;11:266-73.  Back to cited text no. 9
[PUBMED]    
10.Erlich HA, Gelfand D, Sninsky JJ. Recent advances in the polymerase chain reaction. Science 1991;252:1643-51.  Back to cited text no. 10
[PUBMED]    
11.Mealey BL, Ocampo GL. Diabetes mellitus and periodontal disease. Periodontol 2000:2007;44:127-53.  Back to cited text no. 11
    
12.Mealey BL. Periodontal disease and diabetes. A two-way street. J Am Dent Assoc 2006;137:26S-31.  Back to cited text no. 12
[PUBMED]    
13.Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: A case-control study. J Periodontol 2005;76:418-25.  Back to cited text no. 13
[PUBMED]    
14.Hintao J, Teanpaisan R, Chongsuvivatwong V, Ratarasan C, Dahlen G. The microbiological profiles of saliva, supragingival and subgingival plaque and dental caries in adults with and without type 2 diabetes mellitus. Oral Microbiol Immunol 2007;22:175-81.  Back to cited text no. 14
[PUBMED]    
15.Tervonen T, Oliver RC, Wolff LF, Bereuter J, Anderson L, Aeppli DM. Prevalence of periodontal pathogens with varying metabolic control of diabetes mellitus. J Clin Periodontol 1994;21:375-9.  Back to cited text no. 15
[PUBMED]    
16.Davila-Perez C, Amano A, Alpuche-Solis AG, Patiño-Marin N, Pontigo-Loyola AP, Hamada S, et al. Distribution of genotypes of Porphyromonas gingivalis in type 2 diabetic patients with periodontitis in Mexico. J Clin Periodontol 2007;34:25-30.  Back to cited text no. 16
    
17.Kinane DF, Podmore M, Murray MC, Hodge PJ, Ebersole J. Etiopathogenesis of periodontitis in children and adolescents. Periodontol 2000:2001;26:54-91.  Back to cited text no. 17
    
18.Mättö J, Saarela M, Alaluusua S, Oja V, Jousimies-Somer H, Asikainen S. Detection of Porphyromonas gingivalis from saliva by PCR by using a simple sample-processing method. J Clin Microbiol 1998;36:157-60.  Back to cited text no. 18
    
19.Kulekci G, Leblebicioglu B, Keskin F, Ciftci S, Badur S. Salivary detection of periodontopathic bacteria in periodontally healthy children. Anaerobe 2008;14:49-54.  Back to cited text no. 19
[PUBMED]    
20.Gafan GP, Lucas VS, Roberts GJ, Petrie A, Wilson M, Spratt DA. Prevalence of periodontal pathogens in dental plaque of children. J Clin Microbiol 2004;42:4141-6.  Back to cited text no. 20
[PUBMED]    
21.Sastrowijoto SH, Hillemans P, van Steenbergen TJ, Abraham-Inpijn L, de Graaff J. Periodontal condition and microbiology of healthy and diseased periodontal pockets in type 1 diabetes mellitus patients. J Clin Periodontol 1989;16:316-22.  Back to cited text no. 21
[PUBMED]    
22.Okada M, Hayashi F, Nagasaka N. PCR detection of 5 putative periodontal pathogens in dental plaque samples from children 2 to 12 years of age. J Clin Periodontol 2001;28:576-82.  Back to cited text no. 22
[PUBMED]    
23.van Winkelhoff AJ, Loos BG, van der Reijden WA, van der Velden U. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol 2002;29:1023-8.  Back to cited text no. 23
[PUBMED]    
24.Cianciola LJ, Park BH, Bruck E, Mosovich L, Genco RJ. Prevalence of periodontal disease in insulin-dependent diabetes mellitus (juvenile diabetes). J Am Dent Assoc 1982;104:653-60.  Back to cited text no. 24
[PUBMED]    
25.Lalla E, Cheng B, Lal S, Tucker S, Greenberg E, Goland R, et al. Periodontal changes in children and adolescents with diabetes: A case-control study. Diabetes Care 2006;29:295-9.  Back to cited text no. 25
[PUBMED]    
26.Pinson M, Hoffman WH, Garnick JJ, Litaker MS. Periodontal disease and type I diabetes mellitus in children and adolescents. J Clin Periodontol 1995;22:118-23.  Back to cited text no. 26
[PUBMED]    
27.Lalla E, Kaplan S, Chang SM, Roth GA, Celenti R, Hinckley K, et al. Periodontal infection profiles in type 1 diabetes. J Clin Periodontol 2006;33:855-62.  Back to cited text no. 27
[PUBMED]    
28.Salvi GE, Yalda B, Collins JG, Jones BH, Smith FW, Arnold RR, et al. Inflammatory mediator response as a potential risk marker for periodontal diseases in insulin-dependent diabetes mellitus patients. J Periodontol 1997;68:127-35.  Back to cited text no. 28
[PUBMED]    
29.Salvi GE, Kandylaki M, Troendle A, Persson GR, Lang NP. Experimental gingivitis in type 1 diabetics: A controlled clinical and microbiological study. J Clin Periodontol 2005;32:310-6.  Back to cited text no. 29
[PUBMED]    

Top
Correspondence Address:
Mahalakshmi Krishnan
Department of Microbiology, Sree Balaji Dental College and Hospital, Bharath University, Pallikaranai, Chennai, Tamilnadu
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0970-9290.118000

Rights and Permissions



 
 
    Tables

  [Table 1], [Table 2]

This article has been cited by
1 Extract of ice plant (Mesembryanthemum crystallinum) ameliorates hyperglycemia and modulates the gut microbiota composition in type 2 diabetic Goto-Kakizaki rats
Chengcheng Zhang,Weicheng Wu,Xiaoting Xin,Xiaoqiong Li,Daqun Liu
Food & Function. 2019; 10(6): 3252
[Pubmed] | [DOI]
2 Extract of ice plant (Mesembryanthemum crystallinum) ameliorates hyperglycemia and modulates the gut microbiota composition in type 2 diabetic Goto-Kakizaki rats
Chengcheng Zhang,Weicheng Wu,Xiaoting Xin,Xiaoqiong Li,Daqun Liu
Food & Function. 2019; 10(6): 3252
[Pubmed] | [DOI]
3 Frequency of putative periodontal pathogens among type 1 diabetes mellitus: a case–control study
Krishnan Mahalakshmi,Ponnudurai Arangannal,Ponnudurai Santoshkumari
BMC Research Notes. 2019; 12(1)
[Pubmed] | [DOI]
4 Frequency of putative periodontal pathogens among type 1 diabetes mellitus: a case–control study
Krishnan Mahalakshmi,Ponnudurai Arangannal,Ponnudurai Santoshkumari
BMC Research Notes. 2019; 12(1)
[Pubmed] | [DOI]
5 Type 1 Diabetes Mellitus (Juvenile Diabetes) – A Review for the Pediatric Oral Health Provider
E Bimstein,D Zangen,W Abedrahim,J Katz
Journal of Clinical Pediatric Dentistry. 2019; 43(6): 417
[Pubmed] | [DOI]
6 Type 1 Diabetes Mellitus (Juvenile Diabetes) – A Review for the Pediatric Oral Health Provider
E Bimstein,D Zangen,W Abedrahim,J Katz
Journal of Clinical Pediatric Dentistry. 2019; 43(6): 417
[Pubmed] | [DOI]
7 Detection of selected periodontal bacteria in preschool children affected by early childhood caries
Pavla Pantuckova,Michaela Bartosova,Zdenek Broukal,Martina Kukletova,Lydie Izakovicova Holla
Folia Microbiologica. 2016; 61(6): 533
[Pubmed] | [DOI]
8 Detection of selected periodontal bacteria in preschool children affected by early childhood caries
Pavla Pantuckova,Michaela Bartosova,Zdenek Broukal,Martina Kukletova,Lydie Izakovicova Holla
Folia Microbiologica. 2016; 61(6): 533
[Pubmed] | [DOI]



 

Top
 
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  
 


    Abstract
    Materials and Me...
   Results
   Discussion
    References
    Article Tables

 Article Access Statistics
    Viewed1581    
    Printed24    
    Emailed1    
    PDF Downloaded104    
    Comments [Add]    
    Cited by others 8    

Recommend this journal