Journal of Indian Society of Periodontology - Vol 16, Issue 1, Jan-Mar 2012 65

Original Article
Address for
correspondence:
Prof. Carlos M. Ardila,
Ca lle 64 N
52-59 Medelln, Colombia.
E-mail: martinardila@
gmail.com
Submission: 27-05-2010
Accepted: 05-12-2011
Department of
Periodontology, School
of Dentistry, University
of Antioquia, Medelln,
Colombia
Relationship between Gram negative
enteric rods, Aggregatibacter
actinomycetemcomitans, and clinical
parameters in periodontal disease
Carlos M. Ardila, Juliana Alzate, Isabel C. Guzmn
Abstract:
Background: The association between Gram negative enteric rods and Aggregatibacter actinomycetemcomitans
in periodontal diseases has received little attention in the literature. The objective of this study was to explore
the relationship between these organisms and clinical parameters of periodontal disease. Materials and
Methods: Clinical parameters and occurrence of Gram-negative enteric rods and A. actinomycetemcomitans
were examined in 76 patients with chronic periodontitis. Chi-square and Mann-Whitney tests were used to
determine differences in clinical variables versus the presence or absence of both microorganisms. Correlation
among both organisms and clinical data were determined using Spearman rank correlation coeffcient.
Results: Gram-negative enteric rods and A. actinomycetemcomitans were detected in 20 (26.3%) and
18 (23.7%) individuals, respectively. A total of 14 (18.4%) patients harbored both microorganisms studied.
There were signifcantly positive correlations between enteric rods and presence of A. actinomycetemcomitans
(r=0.652, P<0.0001). Both microorganisms were signifcant and positively correlated with probing depth (PD),
clinical attachment level, and bleeding on probing (P<0.0001). The mean PD (mm) of the sampled sites was
signifcantly deeper in patients with presence of A. actinomycetemcomitans and Gram-negative enteric rods.
Conclusion: The results of the present study suggest a strong positive correlation between Gram-negative
enteric rods and A. actinomycetemcomitans in the population studied. This fnding must be taken into account
when considering the best therapeutic approach, including the utilization of antimicrobials. The adverse clinical
outcomes observed in presence of these microorganisms could have implications in the pathogenesis of
periodontal disease and a possible impact on outcomes after treatment.
Key words:
Aggregatibacter actinomycetemcomitans, gram negative enteric rods, periodontitis
INTRODUCTION
P
eriodontitis, a chronic inflammatory
disease, begins with a microbial infection,
followed by a host-mediated destruction of
soft tissue caused by hyperactivated or primed
leukocytes and the generation of cytokines,
eicosanoids, and matrix metalloproteinases
that cause clinically significant connective
tissue and bone destruction.
[1]
Aggregatibacter
actinomycetemcomitans is implicated in the
pathogenesis of periodontitis.
[2]
On the other
hand, the role of Gram-negative enteric rods in the
pathogenesis of periodontal disease is unknown,
but some investigators have suggested that these
organisms may have an impact on progression
and treatment of periodontal disease.
[3]
As
pointed out by Slots et al.
[3]
enteric rods have been
shown to persist after periodontal debridement
and surgery and have been implicated as key
pathogens in cases of refractory periodontitis.
[3-7]
These microorganisms were detected at higher
frequency and in higher proportions in patients
with failing implants.
[5]
These bacteria are
able to produce virulence factors and tissue
destruction.
[2,8]
Examples of virulence factors
include enterotoxins and endotoxins produced
by Gram negative enteric rods
[8]
and leukotoxins
produced by A. actinomycetemcomitans.
[2]
Enteric
rods have shown the capacity to invade human
tissue,
[8]
while A. actinomycetemcomitans has
demonstrated the ability to invade human oral
epithelial cells in cell culture.
[9]
Invasiveness
and ubiquitous intraoral distribution may be
the main reasons for the reported observation
of rather poor results after conventional,
merely mechanical treatment of periodontal
infections.
[10]
To our knowledge, there are no investigations
that study the interaction among enteric rods
and A. actinomycetemcomitans. Geographical
differences in the presence of these microorganisms
could impact clinical parameters and periodontal
treatment protocols, which may enable the
establishment of specifc therapeutic strategies.
The aim of this study was to investigate the
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DOI:
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66 Journal of Indian Society of Periodontology - Vol 16, Issue 1, Jan-Mar 2012
Ardila, et al.: Relationships between enteric and periodontopathogens and clinical parameters
relationships between these organisms and clinical parameters
of patients with chronic periodontitis.
MATERIALS AND METHODS
Subjects
Seventy-six systemically healthy Colombian subjects (45 women
and 31 men), aged 27 to 66 years (468.08 years), who attended
the dental clinics of the University of Antioquia were invited
to participate in this study between October 2008 and March
2009. Informed and written consent was obtained from each
participant. The study design was approved by the Ethical
Committee on Human Research of the University Investigation
Department of the University of Antioquia, according to the
Declaration of Helsinki on experimentation involving human
subjects. Patients with a diagnosis of chronic periodontitis
were considered candidates for the study. The diagnosis of
chronic periodontitis was made based on criteria defned
at the workshop sponsored by the American Academy of
Periodontology.
[11]
Exclusion criteria included diabetes,
cardiovascular disease, or any other systemic disease that
could alter the course of periodontal disease. Pregnancy,
recent (six months) consumption of systemic antimicrobials
or anti-infammatory drugs, periodontal therapy during the
last six months, and subjects regularly using chlorhexidine
mouthwash also served as exclusion criteria.
Clinical evaluation
Medical history and clinical examination were conducted
for each patient and a full-mouth periapical X-ray status was
performed. One of the authors (CA) performed all clinical
examinations. The presence or absence of bleeding on probing
(BOP), plaque, and suppuration were registered. The presence
of plaque was recorded dichotomously, as the presence or
absence of plaque according to detection of plaque deposits
determined by running the tip of a periodontal probe along
the tooth surface at the gingival margin of each site. BOP
was designated as positive if bleeding occurred within 20 s
after periodontal probing. Probing depth (PD) and clinical
attachment level (CAL) were measured at all approximal,
buccal, and lingual surfaces to the nearest millimeter by
a calibrated standard probe.
*
Location of gingival margin
(GM): The distance between the gingival margin and a fxed
reference point on the tooth (cement enamel junction (CEJ)
or the margin of a restoration). A negative value was given
when the gingival margin was located coronal to the CEJ. PD
was recorded from the GM to the base of the pocket. CAL was
calculated as PD+GM.
Microbial sampling
Microbial sampling on periodontitis patients was performed
on pockets 5 mm. The deepest six pockets were selected for
sampling. After removing supragingival plaque with curets
and isolating the area with cotton pellets, the paper points
were inserted into each periodontal pocket for 20 seconds. The
paper points

were transferred to a tube with Viability Medium

Gteborg Anaerobically (VMGA) III medium.
[12]
All samples
were labeled properly and processed within four hours after
sampling. The samples were analyzed using microbial culture
techniques for the presence of periodontopathic bacteria
according to slots.
[13]
Briefy, most samples were processed at
room temperature (25C) and incubated in CO
2
and anaerobic
culture systems. Brucella blood agar medium was incubated at
35C in an anaerobic jar for seven days. The Trypticicase Soy
Serum Bacitracin Vancomycin agar medium was incubated
in 10% CO
2
at 37C for four days. Presumptive identifcation
was performed according to the methods described
[13,14]
and
using a commercial identifcation micromethod system

for
A. actinomycetemcomitans. Total viable counts (TVC) were
defned as the total number of colony-forming units obtained
on non-selective media plates. Species found on selective
media were enumerated and their percentage of TVC was
calculated.
Isolation of Gram-negative enteric rods by culture: After
placement for 20 s, the paper points were pooled into a
vial containing 2.0 ml of VMGA III transport medium.
[12]

The sample vials were maintained at room temperature,
transferred to the laboratory, and processed within 4 h after
sampling. After the vials were placed in an incubator for
30 min at 37C, bacterial plaque was mechanically dispersed
with a test tube mixer at the maximal setting for 60 s. Serial
10-fold dilutions were prepared in pepton water, and aliquots
were plated on MacConkey agar. The plates were incubated
aerobically at 37C for 24 h. Each isolate was characterized
according to colonial and cellular morphology and Gram-stain
characteristics. Gram-negative enteric rods were speciated
using a standardized biochemical test.
#
Total viable counts were
defned as the total number of colony forming units obtained
on non selective media plates. Species found on selective media
were enumerated and presented as counts 10
5
.
Each patient provided a pooled subgingival plaque sample.
Equal numbers of isolates were used from each subject.
Statistical analysis
Data were entered into an Excel** database and were proofed for
entry errors. The database was subsequently locked, imported
into Statistical Package for Social Sciences (SPSS) for Windows,

formatted, and analyzed. Indicators of descriptive statistics were
used, such as frequencies, percentage, average, variance, and
standard deviation. The presence of A. actinomycetemcomitans
and Gram-negative enteric rods-positive individuals were
described as the percentage of individuals with at least one
infected pocket. The Chi-square test was used to assess
differences between BOP versus the presence or absence of
A. actinomycetemcomitans and Gram-negative enteric rods.
PD and CAL differences and the presence or absence of
A. actinomycetemcomitans and Gram-negative enteric rods were
determined by the Mann-Whitney test. Association among
A. actinomycetemcomitans and Gram-negative enteric rods was
expressed through a non-parametric correlation coeffcient
(Spearman rank). Only sites presenting concomitantly CAL
and PD of 4 mm or more at baseline were considered in the
analyses of CAL, PD, and BOP. The signifcance level was set
at 0.05 for all tests.

UNC-15, Hu-Friedy, Chicago, IL.

*
Maillefer, Ballaigues, Switzerland

RapID ANA, Remel, Norcross, GA

#
API 20E, BioMerieux, Marcy LEtoile, France
**Microsoft Offce 2007

SPSS Inc. version 15.0

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Journal of Indian Society of Periodontology - Vol 16, Issue 1, Jan-Mar 2012 67
Ardila, et al.: Relationships between enteric and periodontopathogens and clinical parameters
RESULTS
A total of 45 women (59.2%) and 31 men (40.8%) with chronic
periodontitis were studied (age: 468.08 years, of whom 21.05%
[16 subjects]) were current smokers. Table 1 describes the
clinical characteristics of the patients.
Among 76 patients examined, Gram-negative enteric rods,
and A. actinomycetemcomitans were detected in 20 (26.3%)
and 18 (23.7%) individuals, respectively. A total of 14 (18.4%)
patients harbored both microorganisms studied.
Gram-negative enteric rods in periodontal pockets was
highly signifcant and positively correlated with presence of
A. actinomycetemcomitans (r=0.652, P<0.0001) and also both
organisms were highly signifcant and positively correlated
with PD, CAL, and BOP [Table 2].
Patients with presence or absence of A. actinomycetemcomitans
and Gram-negative enteric rods showed signifcantly different
clinical conditions, as assessed by the clinical parameters
studied (P<0.001) [Table 3]. The mean PD (mm) of the sampled
sites was signifcantly deeper in patients with presence of
A. actinomycetemcomitans and Gram-negative enteric rods, when
compared with patients with absence of both microorganisms.
Similar results were found for the CAL data. The proportion of
sites with BOP was signifcantly higher in patients with presence
of A. actinomycetemcomitans and Gram-negative enteric rods,
when compared with patients without these bacteria.
DISCUSSION
In this study, we investigated the relationships between
A. actinomycetemcomitans and Gram-negative enteric rods
and clinical parameters from patients with untreated chronic
periodontitis. Information from the present study may have
therapeutic implications for the treatment of non-oral infections
caused by oral pathogens. Dissemination of periodontal
pathogens to other body sites frequently occurs and may cause
serious diseases.
[15,16]
This study identifed Gram negative enteric rods in 20 (26.31%)
of 76 patients. Our previous paper
[17]
reported four species
of Gram-negative enteric rods in subgingival plaque in
20 (26.31%) of 76 patients: K. pneumoniae occurred in twelve
patients, Pseudomonas aeruginosa in four patients, and three
other species were recovered with lower prevalence.
Their prevalence in the periodontal pocket varies around
the world, ranging from 14% in the United States to 92% in
Sudan.
[18,19]
In Latin America, similar frequencies to those
encountered in our study were reported among Brazilians
[20,21]

and Colombians.
[22,24]
These bacteria are often recovered
from the subgingival microbiota of patients considered
to be clinically refractory to mechanical and conventional
antibiotic periodontal therapies.
[3-8]
Additionally, they exhibit
less susceptibility to chlorhexidine
[25]
and in vitro resistance
to the majority of adjunctive antibiotics used to treat
periodontitis.
[7,17,23,26]
In the present investigation, A. actinomycetemcomitans was
observed in 18 (23.7%) individuals. Their frequency in chronic
periodontitis varied between 15% and 40% in America, Europe,
and Australia.
[27-29]
Our values are similar to the frequencies
reported, using culture techniques (26.6%; 26.3%) and
polymerase chain reaction (PCR) (23.6%) in South Americans
populations.
[24,30,31]
A. actinomycetemcomitans has ability to
survive and colonize periodontal pockets probably related to its
large scope of virulence factors that include proteolytic activity,
capacity of modulate immune response, evasion of phagocytosis,
ability to evade, and damage the immune system and produce
periodontal breakdown.
[32]
Some previously published
studies even demonstrated that A. actinomycetemcomitans is a
pathogen which is able to invade periodontal tissues, but evade
mechanical-chemical therapies.
[33,34]
To the best of our knowledge, there are no studies on the
association of periodontal Gram-negative enteric rods and
A. actinomycetemcomitans and relating these microorganisms
with clinical parameters. In this study, a significantly
positive correlation between Gram-negative enteric rods
and A. actinomycetemcomitans was observed (P<0.0001). Slots
et al.
[7]
found that A. actinomycetemcomitans was isolated
from approximately one-ffth of the patients, whose cultures
Table 3: Comparison of clinical data at sampled sites: PD, CAL, percentage of sites with BOP
Parameter Presence enteric and
A. actinomycetemcomitans
Absence enteric
A. actinomycetemcomitans
Statistics
PD (mmSD) 5.91.4 51.2 Mann Whitney P<0.001
CAL (mmSD) 6.442 5.361.6 Mann Whitney P<0.001
% BOP (%SD) 8513 6317
2
P<0.001
mm Millimeter; S Standard deviation; PD Probing depth; CAL Clinical attachment level; BOP Bleeding on probing
Table 1: Clinical data at sampled sites: Probing depth,
clinical attachment level, percentage (%) of sites with
bleeding on probing, percentage (%) of sites with
plaque, percentage (%) of sites with suppuration
Clinical parameter MeanSD
PD (mmSD) 5.141.33
CAL (mmSD) 5.611.83
% BOP (%SD) 7016
% PI (%SD) 5619
% SUP (%SD) 4.33.1
PD Probing depth; CAL Clinical attachment level; BOP Bleeding on
probing; PI plaque; SUP Suppuration; mm Millimeter; SD Standard
deviation
Table 2: Correlations among Gram negative enteric
rods and A. actinomycetemcomitans with probing
depth, clinical attachment level, percentage of sites with
bleeding on probing
Clinical
parameter
Presence enteric and
A. actinomycetemcomitans
Statistics
PD (mm; mean) r=0.662 Spearman P<0.0001
CAL (mm; mean) r=0.698 Spearman P<0.0001
BOP (% of sites) r=0.621 Spearman P<0.0001
PD Probing depth; CAL Clinical attachment level; BOP Bleeding on
probing
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68 Journal of Indian Society of Periodontology - Vol 16, Issue 1, Jan-Mar 2012
Ardila, et al.: Relationships between enteric and periodontopathogens and clinical parameters
were positive for subgingival Gram negative enteric rods.
In this regard, Botero et al.
[23]
noted that colonies of enteric
rods are bigger in size indicating that these organisms could
colonize the periodontal pockets in high proportions. On the
other hand, PCR detection does not take into consideration
whether the sample is viable, and thus may yield to a
higher frequency.
[23]
DErcole et al.,
[35]
recently compared
conventional culture methods and multiplex PCR for the
detection of periodontopathogenic bacteria and observed
that for both methods, there was a good degree of accuracy
in the determination of A. actinomycetemcomitans. As with
Botero et al.
[23]
the present study reports on the occurrence
of the microorganisms detected based on culture techniques
because it allows us later to work with the cultured
microorganisms.
Clinical parameters studied were signifcantly increased in
presence of A. actinomycetemcomitans and Gram-negative
enteric rods, when compared with patients with absence of
both microorganisms [Tables 2 and 3]. This evidence indicated
that A. actinomycetemcomitans and Gram-negative enteric
rods are closely associated with the process of periodontal
breakdown and both microorganisms may be involved in
the course of tissue destruction such as pocket deepening or
active attachment loss. However, the differences in disease
severity (probing PD) and smoking habits among the subjects,
detected in the present study, could have had an impact on
the microbiological results, because both factors have been
shown to have an infuence on the subgingival microfora,
[22]

but their particular impact on the present population could
not be assessed.
Enteric rods and A. actinomycetemcomitans share certain aspects
that could explain its biological plausibility associated with
adverse periodontal parameters. These bacteria produce
aggressive virulence factors and tissue destruction.
[2,8]

Invasiveness and ubiquitous intraoral distribution may be
the main reasons for the reported observation of deep pocket.
The present investigation confirms that the presence of
Gram negative enteric rods and A. actinomycetemcomitans
is related to adverse periodontal conditions. These results
could impact periodontal treatment and should be taken into
account in the mechanical and antimicrobial treatment of
periodontal disease in Latin American populations. The study
of the subgingival microbiota in a particular country becomes
pertinent to identify its possible impact on outcomes after
treatment.
[22]
A larger investigation would be more appropriate
to study correlations between Gram-negative enteric rods and
A. actinomycetemcomitans further. Differences in host response,
oral hygiene habits, oral health care access, and microbial
composition may help explain these differences in the clinical
expression of periodontitis in the population studied.
[36]
More
exhaustive investigations addressing the relationship between
periodontitis and environmental, economic, and genetic
variables are needed in Latin America.
[22]
ACKNOWLEDGMENTS
This study was supported, in part, by a grant from the National Public
Health School and Epidemiology Group of the University of Antioquia.
The authors report no conficts of interest related to this study.
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How to cite this article: Ardila CM, Alzate J, Guzmn IC.
Relationship between Gram negative enteric rods, Aggregatibacter
actinomycetemcomitans, and clinical parameters in periodontal
disease. J Indian Soc Periodontol 2012;16:65-9.
Source of Support: Grant from the National Public Health School
and Epidemiology Group of the University of Antioquia., Confict of
Interest: No conficts of interest related to this study.
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