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Objective To analyze the subgingival microflora and S. mutans compared with controls both at gingivitis
composition of inflammatory bowel disease (IBD) patients and at periodontitis sites (P < 0.05). UC patients harbored
with untreated chronic periodontitis and compare them higher levels of S. aureus (P = 0.01) and P. anaerobius
with systemically healthy controls also having untreated (P = 0.05) than controls only in gingivitis sites.
chronic periodontitis.
Conclusion Our study showed that even with similar
Method Thirty IBD patients [15 with Crohn’s disease (CD) clinical periodontal parameters, IBD patients harbor higher
and 15 with ulcerative colitis (UC)] and 15 control levels of bacteria that are related to opportunistic
individuals participated in the study. All patients had been infections in inflamed subgingival sites that might be
diagnosed with untreated chronic periodontitis. From every harmful for the crucial microbe–host interaction. Eur J
patient, subgingival plaque was collected from four Gastroenterol Hepatol 25:239–245
c 2013 Wolters Kluwer
gingivitis and four periodontitis sites with paper points. Health | Lippincott Williams & Wilkins.
Samples from the same category (gingivitis or European Journal of Gastroenterology & Hepatology 2013, 25:239–245
periodontitis) in each patient were pooled together
and stored at – 708C until analysis using a checkerboard Keywords: checkerboard DNA–DNA hybridization, inflammatory bowel
disease, periodontal disease, subgingival plaque
DNA–DNA hybridization technique for 74 bacterial species.
a
Departament of Periodontology, Faculty of Odontology, bDepartment
Results Multiple-comparison analysis showed that the of Gastroenterology, Faculty of Medicine, Rio de Janeiro State University,
c
Department of Gastroenterology, Faculty of Medicine, Federal University of Rio
groups differed in bacterial counts for Bacteroides de Janeiro, Rio de Janeiro, Brazil, dDepartment of Periodontology, School of
ureolyticus, Campylobacter gracilis, Parvimonas micra, Dental Medicine, University of Bern, Bern, Switzerland, eDepartment of Oral
Medicine, School of Dentistry, University of Washington, Seattle, Washington,
Prevotella melaninogenica, Peptostreptococcus anaerobius, USA and fDepartment of Dental Medicine, Division of Perisodontology, Karolinska
Staphylococcus aureus, Streptococcus anginosus, Institutet, Stockholm, Sweden
Streptococcus intermedius, Streptococcus mitis, Correspondence to Carlos M.S. Figueredo, PhD, Departament of Periodontology,
Streptococcus mutans, and Treponema denticola Faculty of Odontology, Rio de Janeiro State University, Boulevard 28
de Setembro 157, Pavilhão de Pesquisa, Vila Isabel, Rio de Janeiro
(P < 0.001). CD patients had significantly higher levels 20551-030, Brazil
of these bacteria than UC patients either in gingivitis Tel/fax: + 55 212 868 8642; e-mail: cmfigueredo@hotmail.com
or in periodontitis sites (P < 0.05). CD patients harbored
Received 12 July 2012 Accepted 5 September 2012
higher levels of P. melaninogenica, S. aureus, S. anginosus,
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
240 European Journal of Gastroenterology & Hepatology 2013, Vol 25 No 2
ecological niches for hosting microorganisms that could Rio de Janeiro State University and at the Clementino
act as opportunistic pathogens [10]. Guidelines for the Fraga Filho University Hospital of Federal University of
prevention of opportunistic infections in IBD patients Rio de Janeiro, both in Rio de Janeiro, Brazil. Employees
mention that the dental status needs to be evaluated and at both University Hospitals, and who did not show any
appropriate dental care has to be performed. However, no clinical signs of present systemic disease other than
special mention is made of the periodontal condition periodontitis, and who had not taken antibiotics, or anti-
of these patients [11]. inflammatory drugs for at least 6 months before the study,
were included in the control group. The smoking habit
Some attempts to identify the oral IBD microflora have
was registered as current smokers (those who currently
been made through the years. van Dyke et al. [12] studied
smoke cigarettes daily) and nonsmokers (those who had
the periodontal flora of IBD patients with and without
never smoked cigarettes or former smokers who had quit
periodontitis and found a unique microflora composed
smoking for >5 years).
predominantly of small, motile, Gram-negative rods that
were most consistent with the genus Wolinella. Sundh The diagnosis of CD or UC had been established
et al. [13] reported that CD patients had higher counts of previously by clinical, radiological, endoscopic, and
Streptococcus mutans than controls. More recently, Docktor histological analyses. Crohn’s Disease Activity Index [15]
et al. [14] found a significant decrease in overall diversity was used to assess disease activity in CD patients,
in the oral microbiome of pediatric CD. According to the whereas Truelove and Witts’ index [16] was used to
authors, further studies of the oral microbiome in IBD assess disease activity in UC patients. CD patients were
may be of potential diagnostic and prognostic value. taking immunomodulators (n = 7), aminosalicylates (n = 4),
and immunomodulators + aminosalicylates (n = 2). Two
The host–microbe interaction has been implicated in the
CD patients were not taking any medication. In the UC
pathogenesis of IBD in genetically susceptible hosts, but
group, the disease was active in three patients and was in
limited information exists about oral microbes in such
remission in 12 of the patients. In the UC group, patients
patients. Our hypothesis is that the presence of
were taking immunomodulators (n = 1), aminosalicylates
pathogenic bacteria in the inflamed subgingival area
(n = 9), and immunomodulators + aminosalicylates (n = 5).
might be harmful for the crucial microbe–host interaction
None of the individuals in the control group used any
in IBD patients. Therefore, our aim was to analyze the
prescribed medications.
subgingival microflora composition of IBD patients with
untreated chronic periodontitis and to compare with
systemically healthy controls also having untreated Clinical examination
chronic periodontitis. Clinical parameters were evaluated at six sites in all
teeth, excluding third molars. The parameters included
Materials and methods PPD, CAL, presence of plaque, and presence of bleeding
Selection of participants on probing (BOP). PPD, CAL, and BOP were measured
The Committee on Ethics and Research of the University using a conventional periodontal probe (Hu-Friedy,
Hospitals Pedro Ernesto and Clementino Fraga Filho, and Chicago, Illinois, USA). After the diagnosis of chronic
at the Karolinska Institutet (Stockholm, Sweden), periodontitis was made, the sites to be sampled were
approved the study. All the selected patients signed an selected. All the patients had moderate to severe chronic
informed consent. periodontitis [17].
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Subgingival flora in IBD patients Brito et al. 241
Table 1 Bacterial species and subspecies included in the DNA–DNA checkerboard kit
Species panel 1 Collection Species panel 2 Collectiona
1a. Aggregatibacter actinomycetemcomitans (strain a) ATCC 29523 1. Actinomyces neuii GUH 550898
1b. Aggregatibacter actinomycetemcomitans (Y4) ATCC 43718 2. Aerococcus christensenii GUH 070938
2. Actinomyces israelii ATCC 12102 3. Anaerococcus vaginalis GUH 290486
3. Actinomyces naeslundii (type I + II) ATCC 43146 4. Atopobium parvulum GUH 160323
4. Actinomyces odontolyticus ATCC 17929 5. Atopobium vaginae GUH 010535
5. Campylobacter gracilis ATCC 33236 6. Bacteroides ureolyticus GUH 080189
6. Campylobacter rectus ATCC 33238 7. Bifidobacterium biavati GUH 071026
7. Campylobacter showae ATCC 51146 8. Bifidobacterium bifidum GUH 070962
8. Capnocytophaga gingivalis ATCC 33612 9. Bifidobacterium breve GUH 080484
9. Capnocytophaga ochracea ATCC 33596 10. Bifidobacterium longum GUH 180689
10. Capnocytophaga sputigena ATCC 33612 11. Corynebacterium nigricans GUH 450453
11. Eikenella corrodens ATCC 23834 12. Corynebacterium aurimucosum pseudogenitalium GUH 071035
12. Eubacterium saburreum ATCC 33271 13. Dialister spp. GUH071045
13a. Fusobacterium nucleatum nucleatum ATCC 25586 14a. Enterococcus faecalis GUH170812
13b. Fusobacterium nucleatum polymorphum ATCC 10953 14b. Enterococcus faecalis ATCC 29212
13c. Fusobacterium nucleatum naviforme ATCC 49256 15. Escherichia coli GUH 070903
14. Fusobacterium periodonticum ATCC 33693 16. Gardnerella vaginalis GUH 080585
15. Lactobacillus acidophilus ATCC 11975 17. Haemophilus influenzae ATCC 49247
16. Leptotrichia buccalis ATCC 14201 18. Helicobacter pylori ATCC 43504
17. Parvimonas micra ATCC 19696 19. Lactobacillus crispatus GUH 160342
18. Neisseria mucosa ATCC 33270 20. Lactobacillus gasseri GUH 170856
19. Prevotella intermedia ATCC 25611 21. Lactobacillus iners GUH 160334
20. Prevotella melaninogenica ATCC 25845 22. Lactobacillus jensenii GUH 160339
21. Prevotella nigrescens ATCC 33563 23. Lactobacillus vaginalis GUH 0780928
22. Porphyromonas gingivalis ATCC 33277 24. Mobiluncus curtisii GUH 070927
23. Propionibacterium acnes (type I + II) ATCC11827/28 25. Mobiluncus mulieris GUH 070926
24. Selenomonasnoxia ATCC 43541 26. Peptoniphilus spp. GUH 550970
25. Staphylococcus aureus ATCC 25923 27. Porphyromonas endodontalis ATCC35406
26. Streptococcus anginosus ATCC 33397 28. Peptostreptococcus anaerobius GUH 160362
27. Streptococcus constellatus ATCC 27823 (M32b) 29. Prevotella bivia GUH 450429
28. Streptococcus gordonii ATCC 10558 30. Prevotella disiens GUH 190184
29. Streptococcus intermedius ATCC 27335 31. Prevotella mirabilis GUH 070918
30. Streptococcus mitis ATCC 49456 32. Pseudomonas aeruginosa ATCC 33467
31. Streptococcus oralis ATCC 35037 33a. Staphylococcus aureus (yellow) GUH 070921
32. Streptococcus sanguinis ATCC 10556 33b. Staphylococcus aureus (white) GUH 070922
33. Streptococcus mutans ATCC 25175 34. Staphylococcus epidermidis GUH 130381
34. Tannerella forsythia ATCC 43037 (338) 35. Staphylococcus haemolyticus GUH071047
35. Treponema denticola ATCC 35405 36. Streptococcus agalactiae GUH 230282
36. Treponema socranskii D40DR2 37. Varibaculum cambriense GUH 070917
37. Veillonella parvula ATCC 10790
ATCC, American Type Culture Collection; D, sample from Forsyth Institute (Boston, Massachusetts); GUH, Ghent University Hospital Collection (Ghent, Belgium).
a
Strain a bacteria evaluated.
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242 European Journal of Gastroenterology & Hepatology 2013, Vol 25 No 2
Table 2 Clinical characteristics of patients with Crohn’s disease, ulcerative colitis, and control individuals
Crohn’s disease Ulcerative colitis Controls
ANOVA, analysis of variance; BOP, bleeding on probing; IBD, inflammatory bowel disease.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Subgingival flora in IBD patients Brito et al. 243
Table 3 Distributions of bacteria with differences in bacterial counts and significance levels, Crohn disease, ulcerative colitis, and control
groups in sites with gingivitis or periodontitis
Bacteria Patient group 25th 50th 75th Comparisons Significance
Gingivitis
Parvimonas micra Control 0.00 0.87 1.12 CD vs. UC 0.001
CD 0.98 1.36 2.53 CD vs. control 0.01
UC 0.00 0.47 0.85 UC vs. control 0.01
Prevotella melaninogenica Control 0.14 0.29 0.79 CD vs. UC 0.01
CD 0.80 1.26 2.01 CD vs. control 0.001
UC 0.22 0.30 0.89 UC vs. Control NS
Peptostreptococcus anaerobius Control 0.15 0.26 0.43 CD vs. UC 0.05
CD 0.31 0.62 1.04 CD vs. control 0.05
UC 0.14 0.21 0.54 UC vs. control 0.05
Staphylococcus aureus Control 0.28 0.36 0.71 CD vs. UC 0.01
CD 0.82 1.76 2.40 CD vs. control 0.001
UC 0.22 0.46 1.55 UC vs. control 0.01
Streptococcus anginosus Control 0.14 0.29 0.43 CD vs. UC 0.01
CD 0.53 0.97 1.82 CD vs. control 0.001
UC 0.12 0.19 0.41 UC vs. control 0.01
Streptococcus mitis Control 0.14 0.40 0.63 CD vs. UC 0.01
CD 0.24 0.74 1.25 CD vs. control NS
UC 0.10 0.21 0.25 UC vs. control 0.01
Streptococcus mutans Control 0.00 0.29 0.57 CD vs. UC 0.023
CD 0.00 0.78 1.66 CD vs. control 0.039
UC 0.00 0.18 0.33 UC vs. control NS
Treponema denticola Control 0.00 0.15 0.44 CD vs. UC 0.013
CD 0.20 0.54 1.39 CD vs. control NS
UC 0.00 0.17 0.22 UC vs. control NS
Periodontitis
Bacteroides ureolyticus Control 0.12 0.18 0.28 CD vs. UC 0.03
CD 0.30 0.48 0.62 CD vs. control 0.02
UC 0.14 0.21 0.28 UC vs. control NS
Campylobacter gracilis Control 0.14 0.38 0.71 CD vs. UC 0.001
CD 0.55 0.82 1.29 CD vs. control 0.05
UC 0.19 0.37 0.71 UC vs. control NS
P. melaninogenica Control 0.27 0.48 0.93 CD vs. UC 0.001
CD 0.74 1.34 2.32 CD vs. control 0.01
UC 0.25 0.46 0.69 UC vs. control NS
S. aureus Control 0.18 0.51 1.05 CD vs. UC 0.001
CD 0.78 1.34 2.33 CD vs. control 0.05
UC 0.28 0.47 0.63 UC vs. control NS
S. anginosus Control 0.14 0.32 0.54 CD vs. UC 0.001
CD 0.74 1.09 1.75 CD vs. control 0.001
UC 0.15 0.25 0.43 UC vs. control NS
S. intermedius Control 0.21 0.35 0.55 CD vs. UC 0.001
CD 0.55 0.78 1.25 CD vs. control 0.01
UC 0.20 0.34 0.49 UC vs. control NS
S. mitis Control 0.24 0.32 0.68 CD vs. UC 0.001
CD 0.44 0.66 1.00 CD vs. control NS
UC 0.12 0.29 0.41 UC vs. control NS
S. mutans Control 0.00 0.32 0.66 CD vs. UC 0.001
CD 0.34 0.86 1.49 CD vs. control 0.006
UC 0.19 0.22 0.48 UC vs. control NS
compared with controls and UC patients. As S. anginosus is ontitis. Specifically, N. mucosa and Prevotella intermedia
an opportunistic bacterium that has been associated with were included among the 10 species in the control group
endocarditis [33–34], the diagnosis of periodontal dis- but not in CD or UC patients. Both S. aureus and
eases and consequently the elimination of inflamed sites S. haemolyticus were included in CD patients, and
through periodontal treatment is an important approach S. haemolyticus was found among the four highest-ranking
to eradicate an important reservoir of opportunistic species both in CD and in UC patients but were not
bacteria in IBD patients. included in the HC patients. Moreover, Firmicutes,
Bacteroidetes, and Proteobacteria identified as prevalent
Although the distribution of the 10 most dominating species in CD [35] were found in subgingival samples
species in CD, UC, and control individuals included more from our patients with CD and untreated periodontitis.
or less the same species, the ranking order differed. Large This may indicate a disturbed microbiota in CD patients
differences in bacterial counts were not expected because even presenting periodontal characteristics similar to
of the fact that the participants had untreated period- those of UC patients and controls.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
244 European Journal of Gastroenterology & Hepatology 2013, Vol 25 No 2
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