The Journal of the American Dental Association
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Am Dent Assoc, Vol 137, No 11, 1539-1546.
© 2006 American Dental Association
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lee, Y.
Right arrow Articles by Loesche, W. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lee, Y.
Right arrow Articles by Loesche, W. J.
Related Collections
Right arrow Periodontics

RESEARCH

JADA Continuing Education

The transmission of BANA-positive periodontal bacterial species from caregivers to children



Yun Lee, DDS, MS, Wen-Shiun S. Tchaou, DDS, Kathleen B. Welch, MPH and Walter J. Loesche, DMD, PhD


   ABSTRACT
TOP
 ABSTRACT
PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background. The purpose of the authors’ study was to use the N-benzoyl-DL-arginine-2-naphthy-lamide (BANA) test (BANAMet LLC, Ann Arbor, Mich.) to obtain information regarding the prevalence of an enzyme unique to certain periodontal pathogens in plaque samples of children, as well as the potential transmission of these pathogens from caregivers to children.

Methods. The authors tested 218 subjects (3 to 10 years old) and 195 care-givers at four pediatric dentistry clinics in Taipei, Taiwan.

Results. Forty-four percent of the children had at least one plaque sample that tested positive and/or weakly positive. Positive results were more frequent in the mixed dentition, as well as in children with gingivitis (P < .001). A logistic regression model showed that if the BANA test results for the care-giver were positive, the odds of the child’s also having positive test results were 55 times greater (P < .001; confidence interval [CI] = 14 to 224) than those for a child whose caregiver had negative BANA test results. Other predictors were the presence of a mixed dentition (P < .001; odds ratio [OR] = 11; CI = 3.5 to 33.5) and the children’s papillary bleeding scores (P < .001, OR = 3.1, CI = 2.0 to 4.7).

Conclusion. The BANA test results were positive for almost one-half of the children. A positive reaction was associated with gingivitis, a mixed dentition, a BANA-positive caregiver or a caregiver with a history of periodontal disease in the family.

Clinical Implications. The authors propose an anaerobic periodontal infection risk model in which children with a mixed dentition who have gingivitis and a caregiver with a history of periodontal disease would undergo the BANA test.

Key Words: Taiwanese children; BANA test; transmission; periodontal disease

Periodontal diseases often are neglected in childhood and adolescence.1 Although gingivitis is the most common form of periodontal disease, a localized aggressive form that causes bone loss around molars and incisors occurs in a small number of subjects, usually after puberty. This localized aggressive periodontitis is associated significantly with periodontal pathogens such as Porphyromonas gingivalis, Treponema denticola, Tannerella forsythia and Actinobacillus actinomycetemcomitans, which also are associated with adult periodontal disease.2,3 If the localized form is not treated properly, it may progress to a more aggressive periodontitis affecting many teeth. This finding is evidence that the bacterial species implicated in adult periodontal diseases actually colonizes the teeth in childhood.


   PERIODONTAL DISEASE
TOP
 ABSTRACT
 PERIODONTAL DISEASE
N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
These early forms of periodontal disease may have serious medical consequences later in life. Women with the type of periodontal disease that is associated often with P. gin-givalis, T. denticola and T. forsythia in subgingival plaque are at an increased risk of delivering low-birth-weight premature infants.4–6 Recently, Gatz and colleagues7 showed that tooth loss in people younger than 35 years is an independent risk factor for the development of Alzheimer’s disease in people 65 years and older. These medical conditions point to the need to detect the presence of these periodontal pathogens in children and treat them accordingly.

An infant’s oral flora is acquired from his or her primary caregiver, almost always the mother. Li and colleagues8 and Tedjosasongko and Kozai9 showed this initially with Streptococcus mutans, and it has been extended to include several periodontal pathogens. Kononen and colleagues10 reported that various anaerobic species colonize the edentulous mouths of infants, and maternal saliva may act as a source of some gram-negative anaerobes.11 Alaluusua and colleagues12 demonstrated that if a child harbored a periodontal pathogen, such as A. actinomycetemcomitans, at least one of his or her parents exhibited the same bacterial genotype. Tuite-McDonnell and colleagues13 found a significant association between colonization of P. gingivalis in the infant and in either of the parents.


   N-BENZOYL-DL-ARGININE-2-NAPHTHYLAMIDE
TOP
 ABSTRACT
 PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
T. denticola, P. gingivalis and T. forsythia possess a trypsin-like enzyme that hydrolyzes the synthetic substrate N-benzoyl-DL-arginine-2-naphthylamide (BANA). Clinicians can detect this enzyme within five to 10 minutes at chairside using the BANA test (BANAMet LLC, Ann Arbor, Mich.; distributed by OraTec, Manassas, Va.).14

Watson and colleagues15 reported that children 2 to 18 years of age whose parents or other care-givers’ oral cavities were colonized by BANA-positive bacteria had 9.8 times greater odds of their oral cavities’ being colonized by these bacteria than did children whose parents’ or care-givers’ oral cavities were not colonized by BANA-positive bacteria. In addition, Lee and colleagues16 conducted a study involving patients in a dental clinic; they found that children’s odds of having oral cavities colonized by BANA-positive species were 55 times greater in those whose parents or caregivers’ oral cavities were colonized by BANA-positive species than in children whose parents or other caregivers had negative BANA test findings. In both studies, children whose parents or care-givers had a history of periodontal disease were significantly more likely to have dentitions that were colonized by the BANA-positive species than were children whose parents or caregivers did not report having a history of periodontal disease. Watson and colleagues15 conducted examinations in the parents and found that children whose mothers had clinical evidence of periodontitis had 12 times greater odds of having oral cavities colonized by BANA-positive species than did children whose mothers did not have periodontal disease.

These findings are compatible with the hypothesis that children acquire the BANA-positive species from their parents or other caregivers, especially if any of their caregivers has periodontitis. We obtained these data from convenience samples in southwestern Michigan. To generalize these findings, we sought to determine whether the study could be replicated in caregiver-child pairs residing in Taiwan.

Taiwan is an island with an ethnic Chinese population of approximately 22 million people. The drinking water in Taiwan is nonfluoridated. In 2000, Tsai and colleagues17 reported that 95 percent of children aged 7 years had active dental caries. Peng and colleagues18 surveyed adults in Taipai using the Community Periodontal Index of Treatment Needs, which showed an 87 percent prevalence of gingivitis and a 33 percent prevalence of periodontitis. No data were available regarding the prevalence of gingivitis or aggressive periodontitis in Taiwanese children or adolescents, but Yuan and colleagues19 found a 5.5 percent prevalence rate of A. actinomycetemcomitans, which increased after the eruption of first molars and peaked near puberty.

We conducted a study, therefore, to determine the prevalence of anaerobic periodontal pathogens, as measured by the BANA test, in young Taiwanese children, as well as the potential transmission of BANA-positive species from caregivers to children.


   SUBJECTS, MATERIALS AND METHODS
TOP
 ABSTRACT
 PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Subjects. One of us (Y.L.) saw 218 subjects (aged 3 to 10 years) in the Pediatric Dentistry Clinic at the Taipei Medical University Hospital (n = 82), Pediatric Dentistry Clinic at the Chang Chung Memorial Children’s Hospital (n = 62), Bo-Lin Pediatric Dentistry Clinic (n = 42) and Der-Wei Pediatric Dentistry Clinic (n = 32), all in Taipei. There were 116 boys and 102 girls, all of whom had posterior teeth, were in good general health and were cooperative with dental treatment. All parents (n = 195) (some had two or more children in the study) agreed to undergo the BANA test. The Medical Health Ethics Committee of Taipei Medical University Hospital, Dental Department, reviewed and approved all procedures included in this research.

Experimental protocol. All children and their caregivers who came to the pediatric clinics during the winter of 2003 were invited to participate in the study. The dentist explained the purpose and design of the study to the caregiver (usually the mother). He explained to the caregivers that participation in the study was strictly voluntary and their decision would not influence further treatment of their children at the clinic. In addition, he described the dental examination, BANA test procedure and possible discomfort, as well as the benefits of the test to the caregiver. If he or she agreed to allow his or her child to participate in the study, as well as himself or herself, the clinician obtained signed consent before the examination. He also obtained oral consent from the 6- to 10-year-old children before the test.

The dentist asked the caregiver for relevant data about the child and himself or herself (such as birth date, sex and age). He also asked him or her to complete a simple questionnaire, written in Chinese, that inquired about such things as the number of people in the household, the periodontal history of the caregivers and previous use of antibiotics by the child. The dentist was present to help caregivers if they had difficulty filling out the questionnaire.

The same clinician then examined the child and recorded the type of dentition (primary, mixed or permanent), decayed, missing and filled teeth (dmft [primary] or DMFT [permanent]) index, caries status (that is, caries free, small pit-and-fissure caries, moderate occlusal caries, proximal caries or rampant caries) and the patient’s level of oral hygiene. The dentist also determined the plaque index (PI) at the interproximal site to be sampled for the BANA test.

The dentist collected interproximal/subgingival plaque samples for the BANA test. He used a plaque remover (STIM-U-DENT Plaque Removers, Johnson & Johnson, New Brunswick, N.J.) to obtain plaque samples from each quadrant. First, he removed any supragingival plaque from the site and inserted the plaque remover between the first and second molars in children with a primary dentition; between the second primary molar and first permanent molar in children with a mixed dentition; and between the second premolar and first permanent molar in children with a late mixed dentition or a permanent dentition. If the child had any missing teeth, the dentist removed the plaque sample from the mesial or distal side of the remaining tooth. This procedure was repeated for caregivers, except that the dentist sampled the site between the first molar and second premolar.

Papillary bleeding score (PBS). The PBS can indicate gingival inflammation and can be calculated at the same time that the plaque sample for the BANA test is obtained.16 After the dentist removed the plaque remover from the subject’s mouth, he or she recorded any bleeding in the interproximal area on a 0-to-5 scale (0 = no bleeding, tissue healthy; 1 = no bleeding, tissue not healthy; 2 = spotting of blood; 3 = bleeding that flows into the triangular fossa; 4 = bleeding to other teeth; 5 = spontaneous bleeding).16

BANA test. After removing the plaque remover from the interproximal site, the dentist wiped it onto the lower portion of the strip of the BANA test card to transfer any adherent plaque. He used a separate plaque remover for each plaque sample, so four distinct samples were obtained for each subject, for a total of five possible BANA outcomes (Table 1Go). After the dentist sampled all tooth sites, he used a cotton swab to lightly moisten the upper portion of the strip with distilled water. He then folded the BANA test card in half.


View this table:
[in this window]
[in a new window]
  		TABLE 1 Bacterial colonization based on BANA test,* by age and total DMFT.{dagger}

 
The dentist placed the card in an incubator at 55 C for five minutes. He then removed the card and discarded the lower portion of the strip in a manner appropriate for contaminated material. The dentist recorded the color on the upper end of the strip according to the consensus of one other examiner and himself (W.-S.S.T., Y.L.) as follows: no blue color (negative), a faint blue color (weakly positive) or a distinct blue color (positive). For statistical analysis, the examiners recorded both weakly positive and positive results as positive, because a previous study by Loesche and colleagues20 demonstrated that a weakly positive sample behaved more like a BANA-positive sample than a BANA-negative sample when compared with gingival health.

Statistical analysis. We used statistical software (SPSS 10.1 for Windows, SPSS, Chicago) for statistical analysis. We generated frequency tables for each categorical variable and obtained descriptive statistics for continuous variables. We performed {chi}2 tests to assess the significance of the relationship of the BANA test results to each of the categorical variables. In addition, we performed independent-samples t tests to determine if there was a difference in the means of continuous variables for BANA-positive and BANA-negative patients. We used a stepwise logistic regression analysis to determine the association between the various independent variables and the BANA-positive status of the child.


   RESULTS
TOP
 ABSTRACT
 PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
The mean (± standard deviation [SD]) dfmt index for the 106 children with a primary dentition was 8.5 (± 4.42). The mean dfmt index for the 111 children with a mixed dentition was 4.3 (± 2.26). The mean DMFT index for children with a permanent dentition was 2.0 (± 1.83).

The results of the BANA test were negative for 110 children (50.5 percent) for the plaque samples taken from the four quadrants. The results of the test were positive or weakly positive for 108 children (49.5 percent). Children with more BANA-positive samples tended to be older than children with BANA-negative plaque samples (Table 1Go).

The number of BANA-positive samples was not related to sex, PI, caries status, the history of dental visits, brushing habits or the antibiotic history of the subject (P > .05). New patients in the clinic were more likely to have negative BANA test results, because they tended to be younger and to have a primary dentition. Children with a mixed dentition had significantly more BANA-positive samples than did children with a primary dentition (P < .001) (Table 2Go). BANA-positive children were significantly older than were BANA-negative children. Thirty-five percent of the children aged 3 to 5 years had BANA-positive samples, compared with 63 percent of the children aged 6 to 10 years (P < .001) (Table 2Go). We found a tendency for the dmft index, but not the DMFT index, to be lower in BANA-positive children. However, the difference was not significant (P > .05). In addition, the BANA-positive children had significantly higher PBS scores (Table 3Go).


View this table:
[in this window]
[in a new window]
  		TABLE 2 Relationship of treatment, dentition and age to BANA* status.

 

View this table:
[in this window]
[in a new window]
  		TABLE 3 Relationship of clinical variables to BANA* status.

 
The BANA test results for one or more of the four plaque samples were positive or weakly positive for 123 caregivers (63 percent), while the test results were negative for 72 caregivers (37 percent). Seventy-six percent of the children whose caregivers had positive BANA test results also tested positive compared with 4 percent of the children whose caregivers had negative BANA test results (P < .001, {chi}2 test). In the 3- to 5-year-old age group, 36 (56 percent) of the children of BANA-positive caregivers had positive BANA test results, while only two (5 percent) of the children of BANA-negative care-givers had positive BANA test results (P < .001). This pattern was more pronounced in the 6- to 10-year-old age group; 69 (93 percent) of the children of BANA-positive caregivers had positive BANA test results compared with only one (3 percent) of the children of BANA-negative caregivers (P < .001).

Seventy-four percent of the children whose care-givers reported that they or a family member had periodontal disease had BANA-positive plaque samples, whereas 34 percent of the children whose caregivers reported having no history of periodontal disease had BANA-positive plaque samples ({chi}2 = 32.2, P < .001). Fifty-five percent of the children whose caregivers were 35 years or older had positive BANA test results. compared with 31 percent of the children whose caregivers were younger ({chi}2 = 9.1, P = .003). We found no effect of the number of caregivers on the BANA status of the child.

We performed a series of logistic regression analyses to determine the association between various independent variables and the positive test results for the children in this study. Table 4Go shows the results for each of these models, including the Nagelkerke R2, the odds ratio (OR) for each variable and the 95 percent confidence interval (CI).


View this table:
[in this window]
[in a new window]
  		TABLE 4 Significant predictors of BANA* status in children, using stepwise logistic regression analysis.

 
As shown in model 1, children with a BANA-positive caregiver had 82 times greater odds (95 percent CI = 24.2 to 276) of having a BANA-positive sample than did children with a BANA-negative caregiver. This single factor accounted for 58 percent of the explained variability in the BANA status of the child (that is, Nagelkerke R2 = 0.58). The large CI for the BANA status of the caregiver was due to the small number of children who had positive BANA test results when their caregiver had negative test results (only three of 80 children whose caregiver had negative BANA test results had positive BANA test results).

When we added the mean PBS of the child (model 2), the explained variability increased to 71 percent. In this model, the caregiver’s BANA status and PBS were about equally significant contributors to the child’s BANA status. When we added the child’s dentition status (primary versus mixed) (model 3), it also was significant, and the explained variability of the model increased to 77.4 percent. We should note that the ORs decreased for the BANA status of the caregiver as we included additional variables in the model, which reflects the colinearity among the various predictors. We emphasize the overall ability of the model to predict the BANA status of the child, rather than the importance of individual predictors.

The periodontal history of the family, when added to the model, was not significant, despite its importance in the bivariate analysis. This finding reflected our observation that the BANA-positive status of the caregiver and a history of periodontal disease in the family were so highly correlated that they could not behave as independent variables in the model (that is, 92 percent of the BANA-positive caregivers had a family history of periodontal disease). However, when we substituted a history of periodontal disease in the family for the BANA status of the caregiver (model 4), we estimated that a child with a family history of periodontal disease had 3.3 times greater odds of having a BANA-positive plaque sample than did a child without a family history of periodontal disease (Table 4Go). The Nagelkerke R2 for this model (R2 = .64), although not as high as that for the model including the BANA status of the caregiver, was impressive.

Other predictor variables, such as the care-giver’s age, number of family members with a history of periodontal disease, occlusal development stage and treatment status, that were associated significantly with the child’s BANA-positive results in the bivariate models (Tables 2Go and 3Go) were not significant when added to any of the logistic regression models.


   DISCUSSION
TOP
 ABSTRACT
 PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
The BANA status of caregivers was an important factor in the detection of BANA-positive plaque samples in young Taiwanese children in this study. This finding11 was identical to findings reached with the BANA test in convenience samples of U.S. children living in southwestern Michigan.16,21 Our finding also is in agreement with studies that showed a vertical transfer of species associated with subgingival plaque from mother to child using molecular fingerprinting and cultural techniques in Finland,11 Netherlands,22,23 Norway,24 France,25 Ohio,13,26 Saipan, Northern Mariana Islands,27,28 and Japan.29

Although these studies were performed in convenience samples (with the exception of the Saipan study), the uniformity of the results in mother-child pairs from different ethnic backgrounds and locations and in studies that used different detection methods indicates that organisms associated with periodontal disease are acquired in early childhood from the caregiver, almost always the mother. Li and colleagues30 observed a similar pattern with regard to the transmission of mutans streptococci from mother to child.

Our study and those carried out in U.S. children16,21 showed that BANA-positive plaque samples were found more frequently in children aged 6 to 10 years with a mixed dentition compared with younger children with a primary dentition. A possible explanation is that with increasing age, there is more time for the oral cavity to be colonized by outside sources of bacteria. Another possible explanation is that the microenvironment at interproximal sites in the mixed dentition (such as bleeding during eruption) promotes colonization of BANA-positive species from sites such as the tongue31 and the primary dentition. In this regard, the BANA species have nutrient requirements for host molecules such as hemin, progesterone, ceruloplasmin and acetyl muramic acid.32–34 The eruption of the permanent teeth increases the number of interproximal sites, which would provide a suitable environment for these anaerobic bacteria.

The BANA test has been used in epidemiologic studies of children,35–38 but there have been no reports, to our knowledge, regarding its use in children in a clinical practice. Because the prevalence of periodontal disease (especially aggressive early-onset periodontitis) in children in the United States and elsewhere is low,39,40 there has been no perceived need to address the presence of periodontopathic species in children, such as there is for the presence of mutans streptococci. However, the three BANA-positive bacteria associated with aggressive periodontitis (P. gingivalis,41 T. denticola2,3 and T. forsythia 3,42) also are associated with adult forms of periodontal disease. This is of interest because reports have suggested that periodontal disease and tooth loss, especially in people younger than 35 years, may be associated with cardiovascular disease,43,44 preterm births of low-birth-weight infants4,6 and Alzheimer’s disease.7 It is possible that advanced forms of periodontal disease in people 35 years or younger reflect a childhood colonization by periodontopathic bacteria.

While these studies associating periodontal disease with serious medical conditions are preliminary, they suggest that researchers and clinicians should be somewhat concerned regarding the transmission of odontopathogenic bacterial species from the mother or caregiver to the child. Our finding that the mother or other caregiver is the main source of the child’s BANA-positive plaque samples is of little practical value in this regard, because it is unlikely that the dentist would routinely determine the BANA status of the mother or caregiver. However, when we used the history of periodontal disease in the household as a surrogate for the BANA status of the caregiver, this history, in combination with the child’s PBS and the presence of a mixed dentition, yielded a model that was highly predictive of the child’s BANA status (Table 4Go). The information for this model can be obtained easily at the child’s first clinic visit.

Periodontal infection risk model. Accordingly, we can propose an anaerobic periodontal infection risk model from the results of our study. A likely scenario would be to administer the BANA test to children with a mixed dentition who have gingivitis and whose caregivers indicate having a history of periodontal disease. If the child’s BANA test results are positive and he or she has gingivitis (as determined by a PBS greater than 2), the clinician can provide oral hygiene instructions and/or prescribe topical antimicrobials to suppress the BANA-positive flora. Periodontal risk assessment of this nature would focus on children whose oral cavities are colonized demonstrably by periodontopathic bacteria, thereby saving time and reducing expenditures.

Study limitations. Because these recommendations are based on results obtained from convenience samples, researchers need to sample a larger, randomly selected population for the results to be applicable to the general population. A long-term follow-up of the children who had positive BANA test results would be necessary to determine whether the risk indicators identified were effective in predicting which children were more likely to develop aggressive periodontitis. Longitudinal studies in adults have shown that the presence of P. gingivalis, T. forsythia and BANA-positive plaque samples were risk factors for periodontal disease.45–47

The reduction in the OR when we substituted a history of periodontal disease for the BANA status of the caregiver (that is, 3.3 versus 55) (Table 4Go) might reflect the caregiver’s inaccurate reporting of this history, or that bacteria other than the BANA-positive species are contributing to the periodontal disease in the household. These bacteria include Prevotella intermedia, Fusobacterium nucleatum, A. actinomycetemcomitans and Campylobacter rectus, as well as others.48


   CONCLUSION
TOP
 ABSTRACT
 PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Although few children develop periodontitis, the periodontal bacteria associated with adult periodontitis can be found in many children. Because periodontal disease and tooth loss before age 35 years can be associated with serious medical conditions in later life, a preventive strategy would be to detect and treat colonizations of periodontopathic bacterial species in affected children. Some of these bacteria can be detected with the BANA test.

We propose an anaerobic periodontal infection risk model in which children with a mixed dentition who have gingivitis and a caregiver with a history of periodontal disease undergo the BANA test. In this model, clinicians would recommend treatment for children whose BANA test results are positive.


   FOOTNOTES
 

Dr. Lee is clinical director of the dental rehabilitation center for children, Taipei Medical University Hospital, Taiwan.


Dr. Tchaou is chairman, Department of Dentistry, Taipei Medical University Hospital, Taiwan.


Dr. Welch is a computer systems consultant, Center for Statistical Consultation and Research, and an adjunct assistant professor for biostatistics, University of Michigan, Ann Arbor.


Dr. Loesche is the Marcus Ward Professor emeritus, Department of Biologic and Materials Sciences, University of Michigan School of Dentistry, and a professor emeritus of microbiology and immunology, University of Michigan School of Medicine, 1011 N. University, Ann Arbor, Mich. 48109-1078, e-mail "wloesche{at}umich.edu". Address reprint requests to Dr. Loesche.


DISCLOSURE: Dr. Loesche is a partner in BANAMet LLC, Ann Arbor, Mich., which manufactures the BANA tests and incubators and provided them for use in this study.


This research was performed as part of Dr. Lee’s master’s thesis in pediatric dentistry at the University of Michigan, Ann Arbor.


The Department of Pediatric Dentistry, Taipei Medical University Hospital, Taiwan, provided access to clinic patients.


The authors gratefully acknowledge the advice and guidance of Lloyd Straffon, Kevin Hale and Jan Hu.


   REFERENCES
TOP
 ABSTRACT
 PERIODONTAL DISEASE
 N-BENZOYL-DL-ARGININE-2...
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

  1. Page RC. Gingivitis. J Clin Periodontol 1986;13(5):345–59.[Medline]

  2. Albandar JM, Brown LJ, Loe H. Putative periodontal pathogens in subgingival plaque of young adults with and without early-onset periodontitis. J Periodontol 1997;68(10):973–81.[Medline]

  3. Mullally BH, Dace B, Shelburne CE, Wolff LF, Coulter WA. Prevalence of periodontal pathogens in localized and generalized forms of early-onset periodontitis. J Periodontal Res 2000;35(4):232–41.[Medline]

  4. Lopez NJ, Smith PC, Gutierrez J. Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res 2002;81(1):58–63.[Abstract/Free Full Text]

  5. Offenbacher S, Katz V, Fertik G, et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 1996;67(10 supplement):1103–13.[Medline]

  6. Offenbacher S, Jared HL, O’Reilly PG, et al. Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Ann Periodontol 1998;3(1):233–50.[Medline]

  7. Gatz M, Mortimer JA, Fratiglioni L, et al. Potentially modifiable risk factors for dementia in identical twins. Alzheimer’s Dementia 2006;2:110–17.

  8. Li Y, Caufield PW, Dasanayake AP, Wiener HW, Vermund SH. Mode of delivery and other maternal factors influence the acquisition of Streptococcus mutans in infants. J Dent Res 2005;84(9):806–11.[Abstract/Free Full Text]

  9. Tedjosasongko U, Kozai K. Initial acquisition and transmission of mutans streptococci in children at day nursery. ASDC J Dent Child 2002;69(3):284–8, 34–5.[Medline]

  10. Kononen E, Asikainen S, Jousimies-Somer H. The early colonization of gram-negative anaerobic bacteria in edentulous infants. Oral Microbiol Immunol 1992;7(1):28–31.[Medline]

  11. Kononen E, Saarela M, Karjalainen J, Jousimies-Somer H, Alatu-usua S, Asikainen S. Transmission of oral Prevotella melaninogenica between a mother and her young child. Oral Microbiol Immunol 1994;9(5):310–4.[Medline]

  12. Alaluusua S, Asikainen S, Lai CH. Intrafamilial transmission of Actinobacillus actinomycetemcomitans. J Periodontology 1991;62(3):207–10.

  13. Tuite-McDonnell M, Griffen AL, Moeschberger ML, Dalton RE, Fuerst PA, Leys EJ. Concordance of Porphyromonas gingivalis colonization in families. J Clin Microbiol 1997;35(2):455–61.[Abstract]

  14. Loesche WJ, Bretz WA, Kerschensteiner D, et al. Development of a diagnostic test for anaerobic periodontal infections based on plaque hydrolysis of benzoyl-DL-arginine-naphthylamide. J Clin Microbiol 1990;28(7):1551–9.[Abstract/Free Full Text]

  15. Watson MR, Bretz WA, Loesche WJ. Presence of Treponema denticola and Porphyromonas gingivalis in children correlated with periodontal disease of their parents. J Dent Res 1994;73(10):1636–40.[Abstract/Free Full Text]

  16. Lee Y, Straffon LH, Welch KB, Loesche WJ. The transmission of anaerobic periodontopathic organisms. J Dent Res 2006;85(2):182–6.[Abstract/Free Full Text]

  17. Tsai AI, Hsiang CI, Johnsen DC. Caries levels and patterns in the primary dentition of preschool children in Taiwan. Chang Gung Med J 2000;23(1):22–7.[Medline]

  18. Peng TK, Yao JH, Shih KS, Dong YJ, Chen CK, Pai L. Assessment of periodontal disease in an adult population survey in Taipei city using CPITN and GPM/T indices. Zhonghua Ya Yi Xue Hui Za Zhi 1990;9(2):67–74.[Medline]

  19. Yuan K, Hsu PC, Tseng CC, Kiang D, Wang JR. Detection rate of Actinobacillus actinomycetemcomitans on the permanent 1st molars of primary school children in Taiwan by polymerase chain reaction. J Clin Periodontol 2001;28(4):348–52.[Medline]

  20. Loesche WJ, Kazor CE, Taylor GW. The optimization of the BANA test as a screening instrument for gingivitis among subjects seeking dental treatment. J Clin Periodontol 1997;24(10):718–26.[Medline]

  21. Watson MR, Lopatin DE, Bretz WA, Ertel IJ, Loesche WJ. Detection of two anaerobic periodontopathogens in children by means of the BANA and ELISA assays. J Dent Res 1991;70(7):1052–6.[Abstract/Free Full Text]

  22. Petit MD, van Steenbergen TJ, Scholte LM, van der Velden U, de Graaff J. Epidemiology and transmission of Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans among children and their family members: a report of 4 surveys. J Clin Periodontol 1993;20(9):641–50.[Medline]

  23. van Steenbergen TJ, Bosch-Tijhof CJ, Petit MD, Van der Velden U. Intra-familial transmission and distribution of Prevotella intermedia and Prevotella nigrescens. J Periodontal Res 1997;32(4):345–50.[Medline]

  24. Preus HR, Zambon JJ, Dunford RG, Genco RJ. The distribution and transmission of Actinobacillus actinomycetemcomitans in families with established adult periodontitis. J Periodontol 1994;65(1):2–7.[Medline]

  25. Suchett-Kaye G, Decoret D, Barsotti O. Intra-familial distribution of Fusobacterium nucleatum strains in healthy families with optimal plaque control. J Clin Periodontol 1999;26(6):401–4.[Medline]

  26. Lamell CW, Griffen AL, McClellan DL, Leys EJ. Acquisition and colonization stability of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in children. J Clin Microbiol 2000;38(3):1196–9.[Abstract/Free Full Text]

  27. Yang EY, Tanner AC, Milgrom P, et al. Periodontal pathogen detection in gingiva/tooth and tongue flora samples from 18- to 48-month-old children and periodontal status of their mothers. Oral Microbiol Immunol 2002;17(1):55–9.[Medline]

  28. Tanner AC, Milgrom PM, Kent R Jr, et al. Similarity of the oral microbiota of pre-school children with that of their caregivers in a population-based study. Oral Microbiol Immunol 2002;17(6):379–87.[Medline]

  29. Umeda M, Miwa Z, Takeuchi Y, et al. The distribution of periodontopathic bacteria among Japanese children and their parents. J Periodontal Res 2004;39(6):398–404.[Medline]

  30. Li Y, Dasanayake AP, Caufield PW, Elliott RR, Butts JT 3rd. Characterization of maternal mutans streptococci transmission in an African American population. Dent Clin North Am 2003;47(1):87–101.[Medline]

  31. Tanner AC, Milgrom PM, Kent R Jr, et al. The microbiota of young children from tooth and tongue samples. J Dent Res 2002;81(1):53–7.[Abstract/Free Full Text]

  32. Wyss C. Dependence of proliferation of Bacteroides forsythus on exogenous N-acetylmuramic acid. Infect Immun 1989;57(6):1757–9.[Abstract/Free Full Text]

  33. Suzuki M, Loesche WJ. Ceruloplasmin can substitute for rabbit serum in stimulating the growth of Treponema denticola. Infect Immun 1989;57(2):643–4.[Abstract/Free Full Text]

  34. Kornman KS, Loesche WJ. Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun 1982;35(1):256–63.[Abstract/Free Full Text]

  35. Bretz WA, Eklund SA, Radicchi R, et al. The use of a rapid enzymatic assay in the field for the detection of infections associated with adult periodontitis. J Public Health Dent 1993;53(4):235–40.[Medline]

  36. Hirsch DI, Kulbersh R, Kaczynski R. Assessment of pretreatment orthodontic patients using the BANA test. N-benzoyl-DL-argininenaphthylamide. Am J Orthod Dentofacial Orthop 1997;112(2):154–8.[Medline]

  37. Orrico SR, de Toledo BE, Fonseca L, Ito IY. Influence of age on the reactivity of the BANA test among Brazilian children. Braz Dent J 1992;2(2):115–22.[Medline]

  38. Pomes CE, Bretz WA, de Leon A, Aguirre R, Milian E, Chaves ES. Risk indicators for periodontal diseases in Guatemalan adolescents. Braz Dent J 2000;11(1):49–57.[Medline]

  39. Papapanou PN. Periodontal diseases: epidemiology. Ann Periodontol 1996;1(1):1–36.[Medline]

  40. Albandar JM, Brown LJ, Genco RJ, Loe H. Clinical classification of periodontitis in adolescents and young adults. J Periodontol 1997; 68(6):545–55.[Medline]

  41. Lopez NJ, Mellado JC, Giglio MS, Leighton GX. Occurrence of certain bacterial species and morphotypes in juvenile periodontitis in Chile. J Periodontol 1995;66(7):559–67.[Medline]

  42. Darby IB, Hodge PJ, Riggio MP, Kinane DF. Microbial comparison of smoker and non-smoker adult and early-onset periodontitis patients by polymerase chain reaction. J Clin Periodontol 2000;27(6): 417–24.[Medline]

  43. Loesche WJ. Periodontal infection a risk factor for cardiovascular disease? Postgrad Med 2000;107(5):

  44. Offenbacher S, Beck JD. A perspective on the potential cardioprotective benefits of periodontal therapy. Am Heart J 2005;149(6):950–4.[Medline]

  45. Beck JD, Koch GG, Rozier RG, Tudor GE. Prevalence and risk indicators for periodontal attachment loss in a population of older community-dwelling blacks and whites. J Periodontol 1990;61(8):521–8.[Medline]

  46. Elter JR, Beck JD, Slade GD, Offenbacher S. Etiologic models for incident periodontal attachment loss in older adults. J Clin Periodontol 1999;26(2):113–23.[Medline]

  47. Grossi SG, Zambon JJ, Ho AW, et al. Assessment of risk for periodontal disease, I: risk indicators for attachment loss. J Periodontol 1994;65(3):260–7.[Medline]

  48. Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev 2001;14(4):727–52.[Abstract/Free Full Text]





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lee, Y.
Right arrow Articles by Loesche, W. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lee, Y.
Right arrow Articles by Loesche, W. J.
Related Collections
Right arrow Periodontics

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS