|Year : 2016 | Volume
| Issue : 6 | Page : 637-642
|Presence of Aggregatibacter actinomycetemcomitans in saliva and cardiac tissue samples of children with congenital heart disease
Elif Bozdogan1, Nursen Topcuoglu2, Gurkan Cetin3, Ismail Haberal3, Guven Kulekci2, Oya Aktoren1
1 Department of Pediatric Dentistry, Faculty of Dentistry, Istanbul University, Istanbul, Turkey
2 Department of Microbiology, Faculty of Dentistry, Istanbul University, Istanbul, Turkey
3 Department of Cardiovascular Surgery, Institute of Cardiology, Istanbul University, Istanbul, Turkey
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|Date of Submission||10-May-2016|
|Date of Decision||08-Jun-2016|
|Date of Acceptance||29-Jul-2016|
|Date of Web Publication||7-Feb-2017|
| Abstract|| |
Aim: The purpose of this study was to analyze the presence of Aggregatibacter actinomycetemcomitans in saliva and cardiac tissue samples of children requiring cardiac surgery in Istanbul, Turkey.
Subjects and Methods: Twenty-five patients (mean age: 6.24 ± 2.93) undergoing surgery for congenital heart defects (CHDs) and an age/gender-matched control group of 25 healthy children were enrolled in the study. Saliva samples were collected from all children; plaque index (PI) and gingival index (GI) were also determined. In CHD group, cardiac tissue samples were received during surgery. All samples were evaluated for the presence of A. actinomycetemcomitans and its highly leukotoxic JP2 clonal strains using polymerase chain reaction. The findings were analyzed by Mann–Whitney U, Chi-square, and Fisher's exact tests.
Results: No significant differences were found in PI and GI values between the groups. A. actinomycetemcomitans was not detected in cardiac tissue samples. A. actinomycetemcomitans in saliva was detected in 2 (8%) of the CHD and 5 (20%) of the control children (p > 0.05). A. actinomycetemcomitans JP2 clonal strains were determined from 1 (4%) of the control group while it was not determined from the samples of the CHD group.
Conclusions: Early colonization of A. actinomycetemcomitans in oral cavities could be assessed as a risk marker for periodontal disease. Periodontal pathogens may enter bloodstream through bacteremia; thus, the presence of periodontal pathogens in the oral cavity of children should be assessed as a risk marker for cardiac diseases in older ages.
Keywords: Aggregatibacter actinomycetemcomitans, cardiac disease, polymerase chain reaction
|How to cite this article:|
Bozdogan E, Topcuoglu N, Cetin G, Haberal I, Kulekci G, Aktoren O. Presence of Aggregatibacter actinomycetemcomitans in saliva and cardiac tissue samples of children with congenital heart disease. Indian J Dent Res 2016;27:637-42
Oral health care is of vital importance in children with cardiac disabilities. Cardiac diseases complicate dental care in children and make them more susceptible to bad oral conditions., Parents' negligence of oral hygiene as a result of a greater concern with cardiac disease, chronic intake of sweetened liquid medications could affect the oral and periodontal health in children with cardiac disabilities.,
|How to cite this URL:|
Bozdogan E, Topcuoglu N, Cetin G, Haberal I, Kulekci G, Aktoren O. Presence of Aggregatibacter actinomycetemcomitans in saliva and cardiac tissue samples of children with congenital heart disease. Indian J Dent Res [serial online] 2016 [cited 2019 Nov 17];27:637-42. Available from: http://www.ijdr.in/text.asp?2016/27/6/637/199590
Positive associations between periodontal diseases and cardiovascular diseases have been reported. Periodontal disease comprises a group of conditions that affect gingival, periodontal ligament, cementum, alveolar bone, and tissue structures that support the teeth. The initiation and progression of periodontal diseases are caused by the accumulation of periodontal pathogens in the oral cavity. It is of particular importance to investigate early colonization of periodontal pathogens which can be an important approach for prevention and treatment of periodontal disease. Especially in children with mixed dentition, it is possible that periodontal pathogens remain in the area surrounding exfoliating primary teeth and continue to survive in the gingival sulcus around permanent teeth; thus, periodontal pathogens survive in the mouth without demonstrating any kind of periodontitis.,
Various dental procedures and routine oral hygiene habits may lead to the entry of periodontal pathogens into the bloodstream, which may invade coronary endothelium. Dental treatment procedures, which generally cause bleeding are known to be the major causative agent for bacteremia.,
Aggregatibacter actinomycetemcomitans, a Gram-negative facultative anaerobic coccobacillus, is an important periodontal pathogen which occurs in the oral cavity quite early in childhood.,A. actinomycetemcomitans is mainly related to aggressive periodontitis; however, it has also been associated with chronic periodontitis., Studies have reported the capability of A. actinomycetemcomitans to invade the coronary endothelium and the presence of viable A. actinomycetemcomitans in human atherosclerotic plaque.,
The JP2 clone of A. actinomycetemcomitans characterized by a 530-base pair (bp) deletion in the promoter region of the leukotoxin gene operon resulting in increased leukotoxin production has most frequently been detected in individuals of African descent. Studies have demonstrated a positive association between the presence of JP2 clone and occurrence of early-onset periodontitis.
The aim of this study is to analyze the presence of A. actinomycetemcomitans and its highly leukotoxic JP2 clonal strain in saliva samples and cardiac tissue specimens of children requiring cardiac surgery.
| Materials and Methods|| |
Patient selection and sample collection
Twenty-five patients attending the Istanbul University, Institute of Cardiology, Department of Cardiovascular Surgery, at 3–12 years of age (mean age: 6.24 ± 2.93) undergoing elective surgery for congenital heart defects (CHDs) with cardiopulmonary bypass under general anesthesia were enrolled in the study. An age- and gender-matched group of healthy children who attended the Pediatric Dentistry Clinic of Istanbul University Faculty of Dentistry, Istanbul, Turkey, was analyzed as controls. For control group, exclusion criteria were any systemic health problem that may affect oral health and dental plaque retention, and for CHD group, any systemic health problem not associated with the cardiac disease. All clinical procedures were approved by the Local Ethics Committee of Istanbul University Faculty of Medicine (2011/118–457) and informed consent was obtained from each parent before initiating the study.
Oral examinations of CHD and control group were performed by one examiner (Elif Bozdogan) at Pediatric Dentistry Clinic of Istanbul University, Faculty of Dentistry, following biosecurity principles. In CHD group, oral examinations were performed before hospitalization and cardiac surgery. The patients were examined on a medical examination table under good incident light.
Oral hygiene of groups was assessed using Silness–Löe plaque index (PI) which is based on recording both soft debris and mineralized deposits on the teeth. Each of the four surfaces of the teeth (buccal, lingual, mesial, and distal) were given a score from 0 to 3 (score 0 = no dental plaque in the gingiva area, score 1 = a film of dental plaque adhering to the free gingival margin (only upon probing), score 2 = moderate accumulation of dental plaque at the gingival margin (seen by naked eye), score 3 = abundant dental plaque in the gingival margin) and calculated scores were recorded for the PI.
Gingival condition and qualitative changes in the gingiva of CHD and control group were assessed using Löe and Silness gingival index (GI). The bleeding was assessed by probing gently along the wall of soft tissue of the gingival sulcus; the marginal and interproximal tissues scored 0–3 (0 = normal gingiva, 1 = mild inflammation, 2 = moderate inflammation, 3 = severe inflammation) and calculated scores were recorded for the GI.
After oral examinations, paraffin-stimulated saliva samples were collected for 5 min from both CHD and control group. Children were asked to chew a sugar-free gum expectorate into a sterile container. Swab samples from dental surfaces were taken using sterile swab sticks in smaller children, who were unable to chew. The swab samples were then placed in 2-ml sterile saline and homogenized by vortexing. The samples were pooled in a sterile empty tube and stored at −20°C until use. In CHD group, saliva samples were obtained before hospitalization and cardiac tissue samples were received during surgery.
Cardiac tissue specimens of CHD were collected under aseptic conditions during cardiac surgery and placed in 30 ml of prereduced transport medium immediately. The tissue was transported to the laboratory facility where a fraction of it was removed in a laminar-flow hood at aseptic conditions and used for DNA isolation. During the transfer of the cardiac tissues, it was presumed that the remnants of the microcapillary blood from the tissue, estimated at 50 mg/g tissue in vivo, leaked into the medium.
All samples and specimens in CHD and control groups were evaluated for the presence of A. actinomycetemcomitans and its highly leukotoxic JP2 clonal strains.
Polymerase chain reaction (PCR) techniques were used for bacterial detection. For each sample, bacterial DNA was extracted and purified with the High Pure PCR Template Preparation Kit (Roche, Mannheim, Germany) according to the manufacturer's instructions.
The species-specific primers used in this study are listed in [Table 1].,, Primers specific to the lkt A gene sequences were used for A. actinomycetemcomitans detection in saliva samples.
A. actinomycetemcomitans positive samples were then analyzed to identify the members of the JP2 clone using the primers span, the Δ530 deletion present in the clone. Escherichia More Details coli 16S ribosomal RNA universal primers common to all bacterial species were also used to detect the presence of nonspecific bacteria in the cardiac specimens.
The final volume of the reaction mixture for each PCR assay was 25 µl consisting of 2.5 µl of DNA sample, 0.25 mM of each deoxynucleotide triphosphate (MBI-Fermentas), 2.5 µl of 10X Standard Taq Reaction Buffer (670 mM Tris-HCL, pH 8.8, 166 mM (NH4)2 SO4, 0.1% Tween 20), 1.5 mM (MBI-Fermentas), 0.5 µM of each primer, 1.25U Taq DNA polymerase (MBI-Fermentas), and distilled water. PCRs were performed in a thermal cycler (Eppendorf AG, Master Cycler Personel 22331, Hamburg, Germany) under optimized conditions for each microorganism with an initial denaturation step of 2 min at 95°C [Table 1]. The amplification products were analyzed by 2% agarose gel electrophoresis. The gels were stained with ethidium bromide (0.5 µg/ml) and PCR products were visualized using a computer-aided imaging system (DNR Bio-imaging Systems Ltd, Jerusalem, Israel). The size of the PCR products was estimated using Φ X174 DNA-HAE III Digest (MBI-Fermentas) as a molecular weight marker. The sensitivity of all the PCR methods was evaluated using reference strains: A. actinomycetemcomitans ATCC 33384, A. actinomycetemcomitans ATCC 700685, and E. coli ATCC 25922. The detection limit for simultaneous PCR was determined as 1000 cells using the known numbers of bacterial cells diluted in sterile distilled water.
The findings were analyzed by Mann–Whitney U, Chi-square, and Fisher's exact tests. The sample size was determined using Power and Sample size software: VARYANS Statistics, Istanbul, Turkey. Power analysis in the study of GI for the parameter Δ: 2.3, standard deviation: 2.5, Power: 0.80, and α: 0.05 determined for the minimum number of samples for each group, n = 20, respectively.
| Results|| |
Demographic data and clinical measurements of GI and PI of CHD and control groups are presented in [Table 2]. No significant differences were found in PI and GI values between the groups. Two (8%) of the 25 children with CHD carried A. actinomycetemcomitans in their saliva samples compared to 5/25 (20%) of the healthy children. The difference was not shown to be statistically significant (p > 0.05). No significant differences were found between the age groups and the prevalence of A. actinomycetemcomitans in saliva samples of the groups [Table 3]. A. actinomycetemcomitans was detected in 8.3% and 16.7% of cardiac and healthy children under the age of 6. The minimum age of a subject positive for A. actinomycetemcomitans was 3 years old and in CHD group. Our results showed no significance in the prevalence of A. actinomycetemcomitans between the males and females in groups [Table 4]. In control group, saliva sample of one child was positive for A. actinomycetemcomitans JP2 clonal strain. [Table 5] shows the demographic data and the presence of JP2 clonal strain of positive saliva samples in CHD and control groups, respectively. No cardiac tissue samples yielded positive results for bacterial DNA in CHD group.
|Table 2: Demographic data of subjects and index values determined in groups|
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|Table 3: Prevalence of Aggregatibacter actinomycetemcomitans in saliva samples of groups according to age|
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|Table 4: Prevalence of Aggregatibacter actinomycetemcomitans in groups according to gender|
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|Table 5: Demographic data for the presence of Aggregatibacter actinomycetemcomitans and JP2 clone in congenital heart defect and control groups|
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| Discussion|| |
This study reports the presence of A. actinomycetemcomitans in saliva and cardiac tissue samples of children with congenital heart disease.
A. actinomycetemcomitans has been identified in dental and saliva specimens of children using PCR method. Okada et al., Yuan et al., and Ashimoto et al. detected the prevalence of A. actinomycetemcomitans in plaque samples of healthy children as 7.7%, 5.5%, and 14%, respectively. Another study reported that 20% of saliva samples of healthy children were positive for A. actinomycetemcomitans. In addition, Kulekci et al. detected A. actinomycetemcomitans in 24% of saliva samples of healthy children.
In our study, saliva is used for the microbiological analysis of A. actinomycetemcomitans in the oral cavity. Current studies report that proportions of bacterial species differ significantly on different intraoral surfaces. Although the microbiota of saliva is most similar to that of the dorsal and lateral surfaces of the tongue, it is worth mentioning that several of the known periodontal pathogens have similar percentages of DNA count in saliva compared to supra and subgingival tooth surfaces. Microorganisms in dental plaque can survive in saliva and can utilize salivary components as a substrate. Furthermore, saliva contains a variety of bacteria from different oral sites; and saliva sampling offers a rapid, noninvasive, and easy source for bacterial examination.,
Steelman et al.  reported 25% of subgingival plaques of cardiac children were positive for A. actinomycetemcomitans compared to the healthy children that had no bacteria in their subgingival plaque samples. In another study, author stated 8/12 of subgingival samples of cardiac patients had A. actinomycetemcomitans as compared with 2/12 controls (p < 0.05). In the present study, the detection prevalence of A. actinomycetemcomitans in saliva samples of cardiac and healthy children were 8% and 20%, respectively. Unlike Steelman et al., findings, these results show that children with cardiac disease had a lower frequency of A. actinomycetemcomitans in their saliva samples compared to healthy children.
Early colonization of periodontal pathogens is suggested as a risk factor for future periodontal diseases for the susceptible host. Tanner et al. detected A. actinomycetemcomitans as 30% in tongue samples of children aged 6–18 months. Rotimi et al. reported that A. actinomycetemcomitans was detected in 7.5% of the children under the age of 6. On the other hand, Frisken et al. reported that A. actinomycetemcomitans was not detected in the children under the age of 2.5, Könönen et al. reported that A. actinomycetemcomitans was not found in saliva and plaque samples of children under the age of 4. In this study, A. actinomycetemcomitans was detected in 8.3% and 16.7% of cardiac and healthy children under the age of 6, respectively. These results supported the studies that reporting A. actinomycetemcomitans was detected in the primary dentition. The youngest child in this study who was found to be positive for A. actinomycetemcomitans was in cardiac group and he was 3 years old.
Some of the studies suggest that prevalence of A. actinomycetemcomitans increases with age;, however, our results have shown no significant differences between the age groups. Although a relationship between the colonization of periodontopathic bacteria and sex hormones has been reported,, the findings in this study showed no significant differences between sex and prevalence of A. actinomycetemcomitans.
Studies have shown that A. actinomycetemcomitans isolates, which demonstrate highly leukotoxic activity, all belong to the JP2 clone. Patients who harbor the JP2 clone have more advanced stages of early-onset periodontitis than patients without the clone. There is a strong association between the occurrence of the JP2 clone and localized aggressive periodontitis. Haubek et al. indicated that infection with the JP2 clone of A. actinomycetemcomitans might happen early in life. Åberg et al. reported that 8.8% of the subgingival samples of adolescents were positive for JP2 clone. Fine et al. detected JP2 clone in 4.8% of school-children who were positive for A. actinomycetemcomitans. In our study, JP2 clone was not detected in cardiac group; and 4% of control group (one child) was positive for JP2 clone.
Studies suggest that periodontal pathogens are associated with infective endocarditis (IE) and cardiovascular diseases.,A. actinomycetemcomitans is grouped in the HACEK group of bacteria (Haemophilus species, A. actinomycetemcomitans, Cardiobacterium hominis, Eikenella corrodens, and Kingella kingae) and it has been reported that members of this group of bacteria cause 3% of all cases and endocarditis due to A. actinomycetemcomitans is rare., Nakatani et al. indicated 49.5% and 31.7% of the causative microorganism of patients with IE were streptococci and staphylococci, respectively. Niwa et al. reported streptococci and staphylococci are the major pathogens of IE.
Nakano et al. used PCR and found A. actinomycetemcomitans in 35% of heart valves and 30.2% of aneurysms. Haraszthy et al., Ishihara et al., and Padilla et al. detected A. actinomycetemcomitans in atherosclerotic plaques using PCR as 18%, 23.3%, and 16,6%, respectively. However, detection of A. actinomycetemcomitans in cardiovascular tissues has not been confirmed by other studies. Aquino et al. used PCR and found periodontal bacteria in subgingival biofilms of patients but not in carotid atheromas. Furthermore, other study reported that A. actinomycetemcomitans was not found in aortic tissue and atherosclerotic plaques using PCR method.
In our study, no cardiac tissue samples yielded positive results for bacterial DNA. It has been estimated that young ages of children for developing atherosclerotic plaques can be a result for negative bacterial DNA isolations; and the findings of this study have shown no invasion of bacteria to cardiovascular tissues.
| Conclusions|| |
Data from the present study have shown that children yielded positive results for A. actinomycetemcomitans in their saliva samples; thus, early colonization of this periodontal pathogen is a risk marker for periodontal diseases in older ages. Cardiac specimens collected from children undergoing cardiac surgery showed negative results for A. actinomycetemcomitans; however, periodontal pathogens may enter bloodstream through bacteremia; thus, positive saliva samples of children should be assessed as a risk marker for cardiac diseases in older ages.
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Conflicts of interest
There are no conflicts of interest
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Dr. Elif Bozdogan
Department of Pediatric Dentistry, Faculty of Dentistry, Istanbul University, Istanbul
Source of Support: None, Conflict of Interest: None
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
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