Clinical and microbiologic effect of nonsurgical periodontal therapy on ...

Q U I N T E S S E N C E I N T E R N AT I O N A L

PERIODONTOLOGY Clinical and microbiologic effect of nonsurgical periodontal therapy on patients with chronic or aggressive periodontitis Jingbo Liu, PhD, DMD1/Jian Zhao, PhD, DMD2/Chen Li, PhD, DMD1/ Ning Yu, DDS3/Dongmei Zhang, PhD, DMD2/Yaping Pan, PhD, DMD4

Objective: To evaluate the changes in the clinical parameters, and the prevalence and quantities of three major periodontopathic bacteria, namely Porphyromonas gingivalis, Aggregatibacter actinomycetemcomitans, and Tannerella forsythia, in subgingival plaque collected from patients with generalized chronic periodontitis (GCP) or generalized aggressive periodontitis (GAgP) in response to nonsurgical periodontal therapy. Method and Materials: 73 GCP patients and 57 GAgP patients were enrolled in this study. Clinical parameters, including probing depth (PD), clinical attachment loss (CAL), and Sulcus Bleeding Index (SBI) were measured. The prevalence and quantities of the three bacteria collected from the subgingival plaque were detected by real-time PCR. Both clinical and microbiologic parameters were evaluated at baseline, 4, and 12 weeks after the nonsurgical periodontal treatment. Results: PD, CAL, and SBI were significantly improved in GCP and GAgP groups at 4 and 12 weeks after nonsurgical periodontal therapy, compared to the baseline levels. The prevalence and quantities of P gingivalis in GCP at baseline (82.19% and 3.35E+5) were statistically higher than those found in GAgP (66.67% and 1.08E+5; P < .05). After therapy, the prevalence and quantities of the three bacteria were sufficiently reduced in both groups at 4 and 12 weeks. There was no significant difference in improvement of clinical and microbiologic parameters between the GCP and GAgP patients after treatment. Conclusion: There was a difference in P gingivalis prevalence and quantity between the GCP and GAgP patients at baseline. In addition, nonsurgical periodontal therapy was effective in the treatment of clinical symptoms and the major periodontopathic bacterial control between GCP and GAgP patients. (Quintessence Int 2013;44:575–583; doi: 10.3290/j.qi.a29752)

Key words: aggressive periodontitis, chronic periodontitis, nonsurgical periodontal therapy

Periodontitis is an infectious disease initi-

tooth surface at the gingival margin and

ated by plaque, which accumulates on the

induces an inflammatory reaction. Porphyromonas gingivalis, Aggregatibacter actino-

1

Lecturer, Department of Periodontics, School of Stomatology, China Medical University, Shenyang, Liaoning, P.R. China.

2

3

Associate Professor, Department of Periodontics, School of

have been considered putative pathogens, and they are closely related to the progres-

Stomatology, China Medical University, Shenyang, Liaoning,

sion of periodontitis.1,2 P gingivalis and T

P.R. China.

forsythia are the major bacteria in the “red

Postgraduate Student, Department of Periodontics, School of

complex,” which is strongly associated with

Stomatology, China Medical University, Shenyang, Liaoning,

the severity of periodontitis.3 A actinomy-

P.R. China; and Department of Oral Biology, School of Dentistry, Center for Oral and Systemic Diseases, University of North Caro-

4

mycetemcomitans, and Tannerella forsythia

cetemcomitans has been considered as a

lina at Chapel Hill, Chapel Hill, NC, USA.

major dominant bacterium in patients with

Professor, Department of Periodontology and Oral Biology,

aggressive periodontitis (AgP),4,5 which is

School of Stomatology, China Medical University, Shenyang,

also present in the subgingival plaque of

Liaoning, P.R. China.

patients with chronic periodontitis (CP).6

Correspondence: Dr Yaping Pan, Department of Periodontics

The prevalence and quantity of A actinomy-

and Department of Oral Biology, School of Stomatology, China

cetemcomitans is much lower than that of

Medical University, Nanjing North St. No.117, Heping district, Shenyang, Liaoning 110002, P.R. China. Email: [email protected].

the predominant periodontopathic bacteria.

edu.cn

However, even at low levels, this species is

VOLUME 44 • NUMBER 8 • SEPTEMBER 2013

575

Q U I N T E S S E N C E I N T E R N AT I O N A L Liu et al

harmful to periodontal tissues.7 Prevalence

basis of the amount of clinical attachment

of putative periodontal pathogens such as

loss (CAL) as follows10:

P gingivalis, A actinomycetemcomitans,

•

slight, 1 or 2 mm CAL

and T forsythia should influence the choice

•

moderate, 3 or 4 mm CAL

of therapy. Monitoring changes in bacteria

•

severe, ≥ 5 mm CAL.

in the subgingival plaque may be useful to guide more effective and accurate peri-

Exclusion criteria included pregnancy, use

odontal therapy.8

of antibiotics, use of hormonal or nonhor-

Wang et al9 suggested that gingivitis

monal anti-inflammatory drugs during the

and periodontitis were common findings in

past 3 months, periodontal therapy in the

China, which may be attributed to the lack

past 6 months, any systemic conditions that

of common knowledge of periodontal pre-

could affect the course of periodontal dis-

vention and treatment in most Chinese peo-

ease, patients with fewer than 14 natural

ple. Moreover, few reports have examined

teeth,

the differences in the changes in clinical

trauma, and smokers.

parameters

and

subgingival

patients

with

primary

occlusal

bacteria

Informed consent was obtained from all

between CP and AgP patients in the Chi-

subjects to permit the collection of subgin-

nese population.

gival plaque samples and the use of clinical

The aim of the present study was to

and microbiologic data. The study was

investigate the presence and quantities of

approved by the Institutional Review Board

the aforementioned bacteria, and the clin-

of the School of Stomatology of China Medi-

ical parameters, in patients of different peri-

cal University.

odontal status (generalized CP [GCP] or generalized

AgP

[GAgP])

before

and

Periodontal treatment protocol

shortly after nonsurgical periodontal ther-

Nonsurgical periodontal therapy consisted

apy. The purpose was to compare the char-

of oral hygiene instruction, and supragin-

acteristic

Chinese

gival and subgingival scaling and root plan-

patients with GCP and GAgP, and to evalu-

ing was applied on all affected teeth of

ate the treatment effect of nonsurgical peri-

every patient with GCP or GAgP. The

odontal therapy.

patients were monitored clinically and

features

between

microbiologically at baseline, 4 weeks, and 12 weeks after nonsurgical periodontal ther-

METHOD AND MATERIALS

apy. All patients were treated by the same operator.

Subjects In total, 130 subjects referred to the Depart-

Clinical measurement

ment of Periodontics of the School of Sto-

At baseline, 4, and 12 weeks after nonsurgi-

matology of China Medical University

cal periodontal therapy, a periodontal

between February 2006 and November

probe (PCPUNC 15, Hu-Friedy) was used

2010 were recruited into the study. These

to record the probing depth (PD) and CAL

subjects were classified into one of two

of six sites (mesiobuccal, midbuccal, disto-

groups (GCP or GAgP) according to the cri-

buccal, mesiolingual, midlingual, and disto-

teria defined at the workshop sponsored by

lingual) of every involved tooth, except the

the American Academy of Periodontology

third molars. The probes were wiped with

(AAP) in 1999. 10,11 GCP was defined as

70% isopropyl alcohol wipes between mea-

extension of periodontal destruction (> 30%

surements to reduce bacterial cross-con-

of sites affected),10 while GAgP was charac-

tamination to the collected subgingival

terized

interproximal

plaque samples. Sulcus Bleeding Index

attachment loss affecting at least three per-

(SBI, scores 0 to 5) was estimated simulta-

manent teeth other than first molars and

neously with the pocket measurements.13

by

incisors”.

12

“generalized

In total, 73 subjects were

Two calibrated examiners performed all

assigned to the GCP group, and the

measurements. In both groups, digitalized

remaining 57 subjects to the GAgP group

orthopantomographs were performed at

(see Table 1). Severity was defined on the

baseline and 12 weeks after nonsurgical

576



periodontal therapy. All orthopantomo-

utes at 50°C, 10 minutes at 95°C, followed

graphs were assessed under optimal view-

by 40 cycles of 15 seconds at 95°C, and 1

ing conditions where the surrounding

minute at 60°C. Absolute quantities of tar-

(environmental) lighting was controllable to

get bacteria in subgingival samples were

achieve the maximum radiographic con-

calculated based on standard curves

trast.

obtained from P gingivalis ATCC 33277, A actinomycetemcomitans FDC Y4, and T for-

Subgingival plaque samples

sythia ATCC 43037, as described previ-

A pooled subgingival plaque sample was

ously.15

collected from the mesiobuccal sites of each involved tooth, except the third

Statistical analysis

molars. After the supragingival plaque was

In total, 390 subgingival samples were col-

carefully cleaned, the sample area was iso-

lected from 73 GCP patients, and 57 GAgP

lated with cotton rolls and dried with an air

patients. The individual subject was used

syringe to reduce cross-contamination from

as the experimental unit for analysis. Data

saliva or supragingival plaque. Samples of

were processed using SPSS version 13.0

subgingival plaque were then collected by

for Windows (SPSS). Mantel-Haenszel test

inserting three sterile paper points into the

was used for the comparison of frequencies

pockets for 20 seconds until mild resistance

of the prevalence of the three bacteria,

was felt. Samples contaminated by blood

Mann-Whitney U test was used for the com-

were discarded. The paper points were

parison of the quantities of three bacteria,

stored in Eppendorf vials filled with 0.5 ml

and unpaired t test was used for the com-

sterile phosphate-buffered saline (PBS)

parison of PD, CAL, SBI, and age. A P

solution and stored at −70°C for real-time

value less than .05 was considered statisti-

PCR detection.

cally significant.

Quantitative PCR DNA was isolated using DNeasy Tissue kit

RESULTS

(Qiagen), according to the manufacturer’s of P gingivalis, A actinomycetemcomitans,

Demographic details of subjects

and T forsythia were analyzed by the SYBR

Table 1 shows the demographic character-

Green-based real-time PCR. The corre-

istics of study subjects. Both groups pre-

sponding primers were based on the study

sented a female majority (71.23% in GCP

by Lau et al.14 Negative control (sterile ultra-

group and 68.42% in GAgP group). The

pure water) was tested in each PCR run.

mean

The amplification was carried out in ABI

27.14 ± 5.68 years, which was statistically

Prism 7500 system (Applied Biosystems)

younger

using Fast-Start DNA Master SYBR Green I

(42.75 ± 10.85 years, P < .05). The GCP

kit (Roche Diagnostics). In brief, this took

group consisted of 73 patients (10 mild

place under the following conditions: 2 min-

periodontitis, 44 moderate periodontitis,

instructions. The prevalence and quantities

Table 1

age

of

than

GAgP that

of

patients GCP

was

patients

Demographic details of GCP and GAgP groups

Characteristic

GCP (N = 73)

Age (years, mean ± SD)

GAgP (N = 57)

42.75 ± 10.85

27.14 ± 5.68

Male (n)

21

18

Female (n)

52

39

Mild periodontitis (n)

10

8

Moderate periodontitis (n)

44

36

Severe periodontitis (n)

19

13

Gender

Severity


577


a

b

c

d

Fig 1 Photographs and radiographs of a patient with GCP before and 12 weeks after nonsurgical periodontal treatment. (a) Pretreatment photograph. (b) 12-week follow-up photograph. (c) Pretreatment radiograph. (d) 12-week follow-up radiograph.

and 19 severe periodontitis), and GAgP

significant difference in the orthopantomo-

included 57 patients (8 mild periodontitis,

graphs was detected between baseline and

36 moderate periodontitis, and 13 severe

12 weeks after treatment.

periodontitis). There were no significant dif-

periodontitis patients between GCP and

Changes in microbiologic variables in GCP and GAgP patients

GAgP groups.

After the therapy, the prevalence and quan-

ferences in the numbers of mild periodontitis, moderate periodontitis, and severe

tities of these bacteria were significantly

Changes in clinical variables in GCP and GAgP patients

reduced in both groups at 4 and 12 weeks,

Figures 1 and 2 show the photographs and

(Table 3). The prevalence and quantity of P

radiographs of the patients with GCP (Fig 1)

gingivalis in GCP at baseline were 82.19%

and GAgP (Fig 2) before treatment and 12

and 3.35E+5 respectively, which were sta-

weeks after treatment. The treatment dis-

tistically higher than those found in GAgP

played effective benefits on periodontal

(66.67%

health, which was indicated by significant

P < .05). With regard to A actinomycetem-

improvement of PD, CAL, and SBI in both

comitans, the GAgP patients presented

GCP and GAgP patients after treatment

higher detection rates in these parameters

(Table 2). The magnitude of reductions in

compared to the GCP patients at baseline

PD and CAL were higher in patients with

(31.58% vs 20.55%), but this difference was

GCP than those in patients with GAgP at 4

not statistically significant.

when compared to the baseline levels

and

1.08E+5

respectively;

weeks (PD, 2.09 ± 0.93 vs 1.80 ± 1.02; CAL, 1.00 ± 1.02 vs 0.86 ± 0.88) and 12 weeks (PD, 2.17 ± 0.86 vs 2.01 ± 1.14;

DISCUSSION

CAL, 0.99 ± 1.01 vs 0.79 ± 1.03). However, no significant difference was detected

CP and AgP are two major subclasses of

between the two groups with respect to the

periodontitis. While CP is an infectious dis-

degree of reduction of PD, SBI, or CAL at 4

ease leading to slowly or moderately pro-

and 12 weeks after therapy. In addition, no

gressive loss of attachment and bone, AgP

578



a

b

c

d

Fig 2 Photographs and radiographs of a patient with GAgP before and 12 weeks after nonsurgical periodontal treatment. (a) Pretreatment photograph. (b) 12-week follow-up photograph. (c) Pretreatment radiograph. (d) 12-week follow-up radiograph.

Table 2

Changes in clinical variables of the subjects

Group

GCP

GAgP

Time (weeks)

PD (mm, mean ± SD)

CAL (mm, mean ± SD)

SBI (mean ± SD)

0

4.32 ± 0.73

3.61 ± 1.15

2.89 ± 1.14

4

2.28 ± 0.88*

2.61 ± 1.24*

0.59 ± 0.68*

12

2.19 ± 0.79*

2.62 ± 1.31*

1.02 ± 0.94*

0

4.23 ± 1.12

3.42 ± 1.21

3.08 ± 0.94

4

2.46 ± 1.12*

2.64 ± 1.15*

0.65 ± 0.89*

12

2.31 ± 1.06*

2.65 ± 1.17*

1.15 ± 1.17*

*Statistical significance compared to the values in the same group at baseline (0 weeks) (P < .05). Significant changes in PD, CAL, and SBI were found between baseline vs 4-week group, and baseline vs 12-week group, within both the GCP and GAgP groups.

Table 3

Group

GCP

GAgP

Changes in microbiologic variables of the subjects Cell counts (CFU ml-1, median)

Prevalence (% of positive sites)

Time (weeks)

Pg

Aa

Tf

Pg

Aa

Tf

0

82.19†

20.55

64.38

3.35E+5†

6.52E+4

2.13E+6

4

35.61*

6.85*

13.70*

6.24E+3*

6.77E+2*

2.34E+3*

12

47.95*

10.96*

23.29*

9.13E+4*

1.16E+3*

4.73E+4*

0

66.67

31.58

63.16

1.08E+5

6.29E+4

1.69E+6

4

31.58*

3.51*

7.02*

5.22E+3*

6.53E+2*

1.26E+3*

12

45.61*

15.79*

22.81*

6.14E+4*

1.83E+3*

3.41E+4*

†

*Statistical significance compared to the values in the same group at baseline (0 weeks) (P < .05). Statistical significance compared to the values in GAgP group (P < .05). Significant changes in prevalence and cell counts of P gingivalis (Pg), A actinomycetemcomitans (Aa), and T forsythia (Tf) were found between baseline vs 4-week group, and baseline vs 12-week group, within both the GCP and GAgP groups.


579


is defined as a specific type of periodontitis

found relatively low prevalence of A actino-

that is characterized by its early-adult onset

mycetemcomitans in both groups, with a

and

bone

higher rate in GAgP than in GCP. These

destruction.10,11 The role of oral microbiota

findings indicate that the subgingival micro-

in the etiology of various inflammatory peri-

biota differs between untreated Chinese

odontal diseases has been well estab-

patients with GCP and GAgP, which might

lished, and specificity might exist between

be one of the factors contributing to the dif-

certain bacterial species or groups and

ferential clinical symptoms in patients. How-

some forms of periodontal diseases. Many

ever, the potential differences in the sero-

studies have putatively demonstrated the

and genetic types of P gingivalis, A

role of P gingivalis, A actinomycetemcomi-

actinomycetemcomitans, and T forsythia

tans, and T forsythia as periodontal patho-

between Chinese GCP and GAgP patients

gens. 16-18 Furthermore, the existence of

are still unknown, which warrants further

interplay between these species has also

investigation.

rapid

attachment

loss

and

been revealed. For instance, it has been

Nonsurgical periodontal therapy is one

reported that P gingivalis can enhance the

of the most commonly utilized procedures

attachment and invasion of T forsythia to

for patients with periodontitis, and its aim is

host epithelial cells and thus facilitates the

to remove the microbiologically contami-

development of periodontitis.19

nated cementum layer, and eliminate or

The prevalence of P gingivalis, A actino-

reduce the number of pathogenic microor-

mycetemcomitans, and T forsythia reported

ganisms in periodontal pockets, thus affect-

in periodontitis varies among ethnic groups.

ing the subgingival microflora, clinical par-

For P gingivalis, the prevalence was 68% in

ameters, and oral health-related quality of

CP patients and 80% in AgP patients from

life in patients.25-28 Several studies have

Brazil, 76.47% in CP patients and 91.6% in

showed

AgP patients from Colombia, 81.1% in peri-

patients receiving nonsurgical treatment

odontal patients from Korea, and 81.8% in

might not be favorable.29,30 In contrast, the

periodontal patients from Germany.20-22 For

present study showed that nonsurgical peri-

A actinomycetemcomitans, the prevalence

odontal therapy resulted in significant clin-

was 41.6% in CP patients and 72% in AgP

ical improvement and reductions in the fre-

patients from Brazil, 33.62% in CP patients

quency, prevalence and quantity of P

from southwestern China, and 17.5% in

gingivalis, A actinomycetemcomitans, and

GAgP patients and 8.6% in CP patients

T forsythia in Chinese GCP and GAgP

from Japan. 20,23,24 For T forsythia, the

groups. No significant difference was

reported prevalence was 45.5% in CP

detected between the two groups with

patients and 56% in AgP patients from Bra-

respect to the degree of reduction in PD,

zil, 50% in CP patients and 50% in AgP

SBI, or CAL at 4 and 12 weeks after ther-

patients from Colombia, 88.9% in periodon-

apy.

tal patients from Korea, and 95.5% in peri-

changes in response to nonsurgical peri-

odontal patients from Germany.20-22

odontal

that

The

the

clinical

treatment

prognosis

and were

of

GAgP

microbiologic no

different

In the present study, the prevalence of P

between the GCP and GAgP groups, which


was consistent with the findings by Rosa-

T forsythia was 82.19%, 20.55%, and

lem et al.31 This controversial finding might

64.38% in untreated GCP patients, and

be attributed to differences in ethnicity of

66.67%, 31.58%, and 63.16% in untreated

subjects, the host’s individual susceptibility

GAgP patients, respectively. Methods of

to the bacteria, the time of research, or the

bacterial sampling and identification, ethni-

skills and efforts of patients in maintaining

city, geographic location, and the periodon-

oral hygiene after treatment. In the present

tal condition of the population samples

short-term study, no significant difference

could influence the results of bacterial anal-

was

ysis. P gingivalis and T forsythia were prev-

before and after treatment.

detected

in

orthopantomographs

alent microorganisms in GCP and GAgP,

Shortly after treatment, beneficial and

and the detection rate of P gingivalis was

pathogenic species can recolonize in the

higher in GCP than that in GAgP. We also

subgingival area. Teles et al32 found that the

580



redevelopment of subgingival plaque varies

hygiene, and if necessary perform appro-

between the condition of healthy periodon-

priate reinforcing treatment for periodontal

tium and periodontitis, and is slower than

patients. In addition, controlling the peri-

and very different from the redevelopment

odontal disease and improving oral hygiene

of supragingival plaque. Subjects with peri-

are essential in the prevention and manage-

odontitis treated under maintenance dis-

ment of these systemic conditions. Paying

played more rapid attachment loss than

attention

periodontally healthy subjects in a preven-

patients with systemic diseases is important

tive regimen, and this greater tendency of

for treatment of these diseases in general

disease progression may be related to an

practice.

to

the

periodontal

health

of

elevated exposure to periodontal pathogens.33 During the periodontal maintenance period, clinicians’ timely evaluation and

CONCLUSION

monitoring of periodontitis patients is necessary.

The present short-term study revealed that

Evidence for the association between

nonsurgical periodontal therapy resulted in

periodontal disease and several systemic

sufficient clinical improvement and reduc-

diseases including cardiovascular dis-

tions in the prevalence and quantities of P

eases, diabetes mellitus, respiratory dis-


eases, rheumatoid arthritis, osteoporosis,

T forsythia in Chinese GCP and GAgP

adverse pregnancy outcomes, and anemia

patients, and no significant difference

is growing rapidly.34-40 As the periodontal

existed in clinical and microbiologic effect

tissues mount an immune inflammatory

of nonsurgical periodontal therapy between

response to bacteria and their products, the

patients with GCP and GAgP. Besides the

systemic challenge with these agents also

bacteria in the present study, Prevotella

can lead to these systemic diseases. It has

intermedia/nigrescens,

become increasingly clear in recent years

nucleatum, Treponema denticola, and Veil-

that periodontal disease can cause a dra-

lonella parvula are also putative periodontal

matic increase in the levels of markers of

pathogens. To further understand the role

systemic inflammation, and that periodontal

of P gingivalis, A actinomycetemcomitans,

therapy can result in reduction in the levels

T Forsythia, and other putative periodontal

of these markers. Several studies demon-

pathogens in subgingival plaque in contrib-

strate the beneficial effect of periodontal

uting to periodontitis in the long term, fur-

treatment on the metabolic control of type 2

ther follow-up observation is warranted.

Fusobacterium

diabetic patients, the signs and symptoms of rheumatoid arthritis, and improvement of anemic status of patients with periodontitis.40-42 In addition, periodontal treatment lowered serum inflammatory markers in patients with coronary artery disease.

43,44

ACKNOWLEDGMENTS This work was supported by a research grant from the Natural Science Projects of China (81271153).

This may result in a decreased risk for coronary artery disease in the treated patients. Improving periodontal health and oral

REFERENCES

hygiene may be a potentially preventive

1. Genco R, Kornman K, Williams R, et al. Consensus

strategy against chronic obstructive pulmo-

report periodontal diseases: pathogenesis and microbial factors. Ann Periodontol 1996;1:926–932.

nary disease exacerbations.45 It can be concluded from the present

2. Nishihara T, Koseki T. Microbial etiology of periodontitis. Periodontol 2000 2004;36:14–26.

study that clinicians can apply nonsurgical periodontal therapy for effective treatment

3. Wara-aswapati N, Pitiphat W, Chanchaimongkon L,

of GCP and GAgP patients. In the early period after nonsurgical periodontal therapy, clinicians should regularly monitor the

Taweechaisupapong S, Boch JA, Ishikawa I. Red bacterial complex is associated with the severity of chronic periodontitis in a Thai population. Oral Dis 2009;15:354–359.

patient’s clinical and microbiologic parameters,

urge

patients

to

maintain

oral


581


4. Schacher B, Baron F, Rossberg M, Wohlfeil M, Arndt

18. Johansson A. Aggregatibacter actinomycetemcomi-

R, Eickholz P. Aggregatibacter actinomycetemcomi-

tans leukotoxin: a powerful tool with capacity to

tans as indicator for aggressive periodontitis by two

cause imbalance in the host inflammatory response.

analysing strategies. J Clin Periodontol 2007;34: 566–573.

Toxins (Basel) 2011;3:242–259. 19. Inagaki S, Onishi S, Kuramitsu HK, Sharma A. Porphy-

5. Casarin RC, Ribeiro Edel P, Mariano FS, Casati MZ,

romonas gingivalis vesicles enhance attachment,

Gonçalves RB. Levels of Aggregatibacter actinomy-

and the leucine-rich repeat BspA protein is required

cetemcomitans, Porphyromonas gingivalis, inflam-

for invasion of epithelial cells by “Tannerella for-

matory cytokines and species-specific immuno-

sythia”. Infect Immun 2006;74:5023–5028.

globulin G in generalized aggressive and chronic

20. Cortelli JR, Cortelli SC, Jordan S, Haraszthy VI, Zam-

periodontitis. J Periodontal Res 2010;45:635–642.

bon JJ. Prevalence of periodontal pathogens in

6. Nogueira Moreira A, Chiappe V, Fernández Caniggia

Brazilians with aggressive or chronic periodontitis. J

L, Alonso C, Piovano S. Clinical and microbiological associations in chronic periodontitis. Acta Odontol Latinoam 2004;17:15–21.

Clin Periodontol 2005;32:860–866. 21. Botero JE, Contreras A, Lafaurie G, Jaramillo A, Betancourt M, Arce RM. Occurrence of periodonto-

7. Rams TE, Listgarten MA, Slots J. Utility of 5 major

pathic and superinfecting bacteria in chronic and

putative periodontal pathogens and selected clinic-

aggressive periodontitis subjects in a Colombian

al parameters to predict periodontal breakdown in patients on maintenance care. J Clin Periodontol 1996;23:346–354.

population. J Periodontol 2007;78:696–704. 22. Kim TS, Kang NW, Lee SB, Eickholz P, Pretzl B, Kim CK. Differences in subgingival microflora of Korean

8. Takamatsu N, Yano K, He T, Umeda M, Ishikawa I. Effect of initial periodontal therapy on the frequen-

and German periodontal patients. Arch Oral Biol 2009;54:223–229.

cy of detecting Bacteroides forsythus, Porphyromon-

23. Meng S, Zhao L, Yang H, Wu Y, Ouyang Y. Preva-

as gingivalis, and Actinobacillus actinomycetemcomi-

lence of Actinobacillus actinomycetemcomitans in

tans. J Periodontol 1999;70:574–580.

Chinese chronic periodontitis patients and peri-

9. Wang QT, Wu ZF, Wu YF, Shu R, Pan YP, Xia JL. Epidemiology and preventive direction of periodontology in China. J Clin Periodontol 2007;34:946–951.

odontally

healthy

adults.

Quintessence

Int

2009;40:53–60. 24. Takeuchi Y, Umeda M, Ishizuka M, Huang Y, Ishika-

10. Armitage GC. Development of a classification sys-

wa I. Prevalence of periodontopathic bacteria in

tem for periodontal diseases and conditions. Ann

aggressive periodontitis patients in a Japanese

Periodontol 1999;4:1–6.

population. J Periodontol 2003;74:1460–1469.

11. Tonetti MS, Mombelli A. Early-onset periodontitis. Ann Periodontol 1999;4:39–53.

25. Doungudomdacha S, Rawlinson A, Walsh TF, Douglas CW. Effect of non-surgical periodontal treatment

12. Lang N, Bartold PM, Cullinan M, et al. Consensus

on clinical parameters and the numbers of Porphy-

report: aggressive periodontitis. Ann Peridontol

romonas gingivalis, Prevotella intermedia and Actino-

1999;4:53.

bacillus actinomycetemcomitans at adult periodon-

13. Mühlemann HR, Son S. Gingival sulcus bleeding: a leading symptom in initial gingivitis. Helv Odontol

titis sites. J Clin Periodontol 2001;28:437–445. 26. Cobb CM. Non-surgical pocket therapy: mechanical. Ann Periodontol 1996;1:443–490.

Acta 1971;15:107–113. 14. Lau L, Sanz M, Herrera D, Morillo JM, Martín C, Silva

27. Darby IB, Hodge PJ, Riggio MP, Kinane DF. Clinical

A. Quantitative real-time polymerase chain reaction

and microbiological effect of scaling and root plan-

versus culture: a comparison between two methods

ing in smoker and non-smoker chronic and aggres-

for the detection and quantification of Actinobacillus

sive periodontitis patients. J Clin Periodontol

actinomycetemcomitans, Porphyromonas gingivalis and Tannerella forsythensis in subgingival plaque

2005;32:200–206. 28. Saito A, Hosaka Y, Kikuchi M, et al. Effect of initial

samples. J Clin Periodontol 2004;31:1061–1069.

periodontal therapy on oral health-related quality

15. Kirakodu SS, Govindaswami M, Novak MJ, Ebersole

of life in patients with periodontitis in Japan. J Peri-

JL, Novak KF. Optimizing qPCR for the quantification of periodontal pathogens in a complex plaque biofilm. Open Dent J 2008;2:49–55.

odontol 2010;81:1001–1009. 29. Mestnik MJ, Feres M, Figueiredo LC, Duarte PM, Lira EA, Faveri M. Short-term benefits of the adjunctive

16. Socransky SS, Smith C, Haffajee AD. Subgingival

use of metronidazole plus amoxicillin in the micro-

microbial profiles in refractory periodontal disease.

bial profile and in the clinical parameters of subjects

J Clin Periodontol 2002;29:260–268.

with generalized aggressive periodontitis. J Clin

17. Grenier D, La VD. Proteases of Porphyromonas gingi-

Periodontol 2010;37:353–365.

valis as important virulence factors in periodontal

30. Haas AN, de Castro GD, Moreno T, et al. Azithromy-

disease and potential targets for plant-derived

cin as an adjunctive treatment of aggressive peri-

compounds: a review article. Curr Drug Targets

odontitis: 12-months randomized clinical trial. J Clin

2011;12:322–331.

Periodontol 2008;35:696–704.

582



31. Rosalem W, Rescala B, Teles RP, Fischer RG, Gustafs-

39. Sert T, Kırzıoğlu FY, Fentoğlu O, Aylak F, Mungan T.

son A, Figueredo CM. Effect of non-surgical treat-

Serum placental growth factor, vascular endothelial

ment on chronic and aggressive periodontitis: clin-

growth factor, soluble vascular endothelial growth

ical, immunologic, and microbiologic findings. J

factor receptor-1 and -2 levels in periodontal dis-

Periodontol 2011;82:979–989.

ease, and adverse pregnancy outcomes. J Periodontol 2011;82:1735–1748.

32. Teles FR, Teles RP, Uzel NG, et al. Early microbial succession in redeveloping dental biofilms in peri-

40. Pradeep AR, Anuj S. Anemia of chronic disease and

odontal health and disease. J Periodont Res

chronic periodontitis: does periodontal therapy

2012;47:95–104.

have an effect on anemic status? J Periodontol 2011;82:388–394.

33. Teles RP, Patel M, Socransky SS, Haffajee AD. Disease progression in periodontally healthy and mainte-

41. Gonçalves D, Correa FO, Khalil NM, de Faria Oliveira

nance subjects. J Periodontol 2008;79:784–794.

OM, Orrico SR. The effect of non-surgical periodon-

34. Shrihari TG. Potential correlation between peri-

tal therapy on peroxidase activity in diabetic

odontitis and coronary heart disease: an overview.

patients: a case-control pilot study. J Clin Periodontol 2008;35:799–806.

Gen Dent 2012;60:20–24. 35. Preshaw PM, Alba AL, Herrera D, et al. Periodontitis

42. Ortiz P, Bissada NF, Palomo L, et al. Periodontal

and diabetes: a two-way relationship. Diabetologia

therapy reduces the severity of active rheumatoid

2012;55:21–31.

arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol 2009;80:

36. Ogrendik M. Does periodontopathic bacterial infec-

535–540.

tion contribute to the etiopathogenesis of the autoimmune disease rheumatoid arthritis? Discov

43. Hussain Bokhari SA, Khan AA, Tatakis DN, Azhar M, Hanif M, Izhar M. Non-surgical periodontal therapy

Med 2012;13:349–355.

lowers serum inflammatory markers: a pilot study. J

37. Detert J, Pischon N, Burmester GR, Buttgereit F. The

Periodontol 2009;80:1574–1580.

association between rheumatoid arthritis and periodontal disease. Arthritis Res Ther 2010;12:218.

44. Rastogi P, Singhal R, Sethi A, Agarwal A, Singh VK, Sethi R. Assessment of the effect of periodontal

38. Martínez-Maestre MÁ, González-Cejudo C, Machuca

treatment in patients with coronary artery disease:

G, Torrejón R, Castelo-Branco C. Periodontitis and

A pilot survey. J Cardiovasc Dis Res 2012;3:124–127.

osteoporosis: a systematic review. Climacteric 2010;13:523–529.

45. Si Y, Fan H, Song Y, Zhou X, Zhang J, Wang Z. Association between periodontitis and chronic obstructive pulmonary disease (COPD) in a Chinese population. J Periodontol 2012;83:1288–1296.


583

Copyright of Quintessence International is the property of Quintessence Publishing Company Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.

Copyright of Quintessence International is the property of Quintessence Publishing Company Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.