Journal of Dental Sciences (2017) 12, 368e374

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Original Article

C-reactive protein in patients with

aggressive periodontitis
Jaroslav Mysak a*, Stepan Podzimek b, Jana Vasakova c,
Jiri Mazanek d, Alex Vinsu b, Jana Duskova b

a
Department of Periodontology, Institute of Dental Medicine, First Faculty of Medicine and General
University Hospital, Charles University, Karlovo Namesti 32 and Katerinska 32, 121 11 Prague, Czech
Republic
b
Department of Oral Biology, Institute of Dental Medicine, First Faculty of Medicine and General
University Hospital, Charles University, Karlovo Namesti 32 and Katerinska 32, 121 11 Prague, Czech
Republic
c
Department of Paediatric Dentistry, Institute of Dental Medicine, First Faculty of Medicine and
General University Hospital, Charles University, Karlovo Namesti 32 and Katerinska 32, 121 11
Prague, Czech Republic
d
Department of Maxillofacial Surgery, Institute of Dental Medicine, First Faculty of Medicine and
General University Hospital, Charles University, Karlovo Namesti 32 and Katerinska 32, 121 11
Prague, Czech Republic

Received 12 February 2017; Final revision received 6 April 2017

Available online 31 July 2017

KEYWORDS Abstract Background/purpose: The aim of this study was to evaluate and compare the sys-
aggressive temic levels of C-reactive protein (CRP) in peripheral blood samples of patients with aggressive
periodontitis; periodontitis during the first twelve months of periodontal treatment, at exactly six month in-
C-reactive protein; terval measurements, and compare them with clinical periodontal parameters.
periodontal index; Materials and methods: All patients (N Z 45) were examined prior to the initiation of peri-
cardiovascular odontal treatment. Patients were divided into two groups GAgP (Generalised form of aggres-
diseases sive periodontitis, N Z 23) and group LAgP (Localised form of aggressive periodontitis,
N Z 22). Control group (CON) included 60 individuals with healthy periodontium. The levels
of CRP were determined in both groups GAgP and LAgP three times in 6 month intervals during
the periodontal treatment.
Results: CRP is a plasma protein that reflects the extent of the acute phase response to inflam-
mation and is one of the markers of choice for monitoring this response. In our study, CRP
levels decreased in course of periodontal treatment in both groups (GAgP and LAgP) in a similar
way as bleeding on probing (BOP) and probing pocket depth (PPD) indices.

* Corresponding author. Institute of Dental Medicine, First Faculty of Medicine and General University Hospital, Charles University,
Katerinska 32, 121 11 Prague 2, Czech Republic.
E-mail address: [Link]@[Link] (J. Mysak).

[Link]
1991-7902/ª 2017 Association for Dental Sciences of the Republic of China. Publishing services by Elsevier B.V. This is an open access article under
the CC BY-NC-ND license ([Link]
C-reactive protein in patients with aggressive periodontitis 369

Conclusion: Our study results showed that CRP levels, as well as bleeding on probing (BOP) and
probing pocket depth (PPD), indices decreased in course of periodontal treatment in patients
with generalised and localised aggressive periodontitis. Therefore this marker might be
exploitable as a means to evaluate periodontal health in patients with aggressive periodontitis.
ª 2017 Association for Dental Sciences of the Republic of China. Publishing services by Elsevier
B.V. This is an open access article under the CC BY-NC-ND license ([Link]
org/licenses/by-nc-nd/4.0/).

Introduction other than periodontitis, such as other infections, trauma

and hypoxia, and it is regulated by diverse cytokines. CRP
Periodontal disease is an inflammatory disease that affects levels have an association with smoking, obesity, tri-
the soft and hard structures that support the teeth.1 In glycerides, diabetes, and periodontal disease.7 Changes in
gingivitis, inflammation localised to the supracrestal region peripheral blood cellular and molecular components can be
of the periodontium leads to ulceration of the junctional found in patients with periodontitis due to inflammatory
epithelium. Although this is technically a loss of clinical changes of the periodontal tissues.8 Positive correlation
attachment (because in healthy tissue the epithelium at- between CRP and periodontal disease severity was proved
taches to the surface of the tooth), clinical attachment loss by many studies,9e11 and levels of CRP decrease after
(CAL) is used almost exclusively to refer to connective tis- nonsurgical periodontal therapy,12 but most studies have
sue attachment loss. Sites with periodontitis exhibit clinical focused on CRP levels in chronic periodontitis, and very few
signs of gingival inflammation and loss of connective tissue are conducted on patients with aggressive periodonti-
attachment. Connective tissue attachment loss refers to tis.13,14 The link between inflammation and systemic dis-
the pathological detachment of collagen fibres from the eases, e.g. cardiovascular disease (CVD), appears to be
cemental surface with the concomitant apical migration of firmly established.15 Epidemiological associations between
the junctional or pocket epithelium on the root surface.2 periodontitis and CVD have been reported.16,17 Among the
Diagnosis of aggressive periodontitis is made on clinical, several biomarkers that have been proposed for cardio-
radiographic and historical findings which show rapid vascular risk stratification, high-sensitivity C-reactive pro-
attachment loss and bone destruction, and possible familial tein (hs-CRP) appears to contribute to the identification of
aggregation of disease. The disease often occurs in people people at risk of developing CVD18; however, the evaluation
under 35 years of age, but it may also affect older patients. of hs-CRP has not yet been widely recommended in guide-
Except for periodontal disease, patients are systemically lines.19 Wohlfeil et al. compared systemic inflammatory
healthy. Other features that may be present are peri- mediators in patients with untreated aggressive and chronic
odontal tissue destruction that is greater than would be periodontitis and in periodontally healthy controls. Patients
expected given the level of local factors, elevated levels of with aggressive periodontitis have statistically significant
Aggregatibacter actinomycetemcomitans or Porphyr- elevations in serum CRP levels compared to subjects with
omonas gingivalis, phagocyte abnormalities and increased healthy periodontium.20,21
production of prostaglandin E2 and interleukin-1b.3 Early Thus, the aim of this study was to evaluate and compare
onset (aggressive) forms of periodontal diseases are the systemic levels of CRP in peripheral blood samples of 45
detectable in all age and ethnic groups.4 This disease is patients with aggressive periodontitis in course of peri-
divided into localised and generalised form by classification odontal treatment and of 60 healthy controls and their
of periodontal diseases from 1999. It can be further clas- correlation with periodontal clinical parameters.
sified on the basis of extent and severity. Aggressive peri-
odontitis is subcategorised into localised (
30% of the teeth
are affected) and generalised form (>30% of the teeth are Materials and methods
affected). Severity is based on the amount of clinical
attachment loss (CAL) and is designated as slight (1e2 mm Study population
CAL), moderate (3e4 mm CAL) or severe (>5 mm CAL).3
Bacterial aetiology of aggressive forms of periodontitis is All patients (N Z 45) were recruited from the patient pool
confirmed by the studies which have demonstrated the of the Department of Periodontology, Institute of Dental
presence of a layer of bacterial deposits on the root surface Medicine, First Faculty of Medicine and General University
of advanced aggressive periodontitis lesions.5 A rapid rate Hospital, Charles University, Prague, Czech Republic, from
of destruction of the periodontium is a major criterion for 2014 to 2016, and all patients were examined prior to the
the diagnosis of aggressive periodontitis.6 Diagnostic diffi- initiation of periodontal treatment. In our study, the pa-
culty is related to the fact that periodontal destruction is tients were treated by conservative treatment e deep
often diagnosed when the attachment loss is already fairly scaling and root planing, surgical techniques were not used.
advanced. In general, distinct alterations in the morphology Deep scaling and root planing were performed three
of the periodontium and substantial tissue damage are months after the first collection of CRP samples (appoint-
necessary for establishing a clear diagnosis. CRP (C-reactive ment I). We examined the periodontal parameters and
protein) is produced in response to many forms of injury measured the CRP levels in each patient every six months
370 J. Mysak et al

(appointment I e before beginning periodontal treatment, CRP determination

appointment II e six months after beginning periodontal
treatment, appointment III e twelve months after begin- CRP levels (mg/L) were measured in capillary blood using
ning periodontal treatment). Inclusion criteria were good QuikRead go CRP þ Hb (Orion Diagnostica Oy, Finland),
general health, no medication, diagnosis of aggressive which works on the principle of photometry and turbidim-
periodontitis according to the ADA AAP Classification,22 and etry. Capillary blood from the middle finger was collected
patient’s agreement with CRP level determination from from the patients before the clinical periodontal exami-
peripheral blood. Exclusion criteria included history of any nation using a thin glass capillary. The samples were
systemic disease or any other disease manifested locally in immediately processed and the established values were
the oral cavity, current pregnancy or lactation, high blood recorded.
pressure, sleep disturbances, depression, excessive alcohol
use, and smoking recently or in the past 10 years. All pa-
tients were of Caucasian origin. Diagnosis of aggressive Statistical analysis
periodontitis was based on a detailed clinical examination,
medical and dental history, tooth mobility, and radio- For calculations descriptive statistics were used e mean,
graphic assessment of intraoral x-ray status and panoramic standard deviation, frequencies and standard error. This
x-ray performed in each patient. A group of 60 students method was used to describe different groups in terms of
(23.4  1.3 years; mean age  SD) from the third year of age, CRP and other indices present in groups. For evalua-
our Institute of Dental Medicine was elected as a control tion of the differences between groups, Student’s t-test
group CON. The clinical condition of periodontium was and Fisher test were used. Significance level of 0.05 was
examined in each individual from the control group iden- used in all tests. MS Excel 2016 and Data analysis ToolPak
tically as in the group of patients with aggressive peri- add-in statistical software were used (Microsoft Office
odontitis. The study was performed with the approval of Professional Plus 2016, Microsoft, Redmont, WA, USA).
the Ethics Committee of the First Faculty of Medicine and
General University Hospital, Charles University, Prague,
Czech Republic. Written informed consent was obtained Results
from all participants in line with the Helsinki declaration
before inclusion in the study. This study was performed as a All results are summarised in Table 1.
cross-sectional study.
CRP levels in patient groups GAgP and LAgP in mea-
surements during periodontal treatment and in control
Periodontal evaluation group CON (Fig. 1):

Patients with aggressive periodontitis had to have at least In both groups (GAgP and LAgP), CRP levels decreased
one tooth with positive bleeding on probing (BOP) and a during periodontal treatment, in GAgP group from
probing pocket depth (PPD) of >5 mm in all quadrants 4.1  4.1 mg/L to 3.1  3.3 mg/L, in LAgP group from
(excluding third molars). Probing pocket depth was 2.6  2.4 mg/L to 1.3  1.7 mg/L, CRP level in control
assessed by WHO periodontal probe with a cut-off of group CON was 1.9  2.3 mg/L. In both groups (GAgP and
11.5 mm from six sites on every tooth present. Clinical LAgP), BOP index decreased during periodontal treatment,
attachment loss (CAL) is a sign of destructive periodontal in GAgP group from 36.8  32.4% to 6.8  11.9%, in LAgP
disease. In our study, we measured CAL vestibulary for each group from 30.4  25.4% to 10.0  18.2%, BOP index in
tooth with a calibrated University of North Carolina probe control group CON was 4.6  8.1% (Fig. 2). No statistically
with a cut-off of 15 mm. For the statistical evaluation, we significant differences were found between all measure-
used the highest value from the upper and lower jaw. All ments during periodontal treatment in CRP levels.
patients were examined at regular intervals of 6 months.
The resorption process of alveolar bone was assessed in all CRP levels and PPD index in patient groups GAgP and
patients radiographically at the beginning of periodontal LAgP in measurements during periodontal treatment and
treatment. In our study, we divided our patients into two in control group CON (Fig. 3):
groups e GAgP and LAgP. Group GAgP included 23 patients
with generalised aggressive periodontitis (36.9  6.2 years; In both groups (GAgP and LAgP), PPD index decreased
mean age  SD) and group LAgP included 22 patients with during periodontal treatment, in GAgP group from
localised aggressive periodontitis (33.5  7.7 years; mean 6.9  2.4 mms to 4.2  2.7 mms, in LAgP group from
age  SD). Whether it is a localised or generalised aggres- 7.5  3.1 mms to 4.4  2.1 mms, PPD index in control group
sive periodontitis was decided based on the classification of CON was 1.5  0.7 mms.
the American Association of Periodontology from 1999.21
We used panoramic x-ray and x-ray status which included CRP levels and CAL index in patient groups GAgP and
12e14 x-ray pictures. We performed control intraoral x- LAgP in measurements during periodontal treatment and
rays after the third measurement of CRP, i.e. 12 months in control group CON (Fig. 4):
after the treatment began. We evaluated the presence or
absence of lamina corticalis and the shape of the bone CAL index increased during periodontal treatment in
defects. All determined evaluation indices were assessed GAgP group from 8.9  2.3 mms to 9.7  2.7 mms, in LAgP
according to WHO oral health surveys.23 group this index decreased during periodontal treatment
C-reactive protein in patients with aggressive periodontitis 371

Table 1 Levels of CRP and clinical periodontal parameters in all tested groups.
AGE CRP I. CRP II. CRP III. BOP I. BOP II. BOP III. PPD I. PPD II. PPD III. CAL I. CAL II. CAL III.
(mg/L) (mg/L) (mg/L) (%) (%) (%) (mms) (mms) (mms) (mms) (mms) (mms)
GAgP Mean 36.9 4.1 4.2 3.1 36.8 19.8 6.8 6.9 5.1 4.2 8.9 9.0 9.7
SD 6.2 4.1 4.6 3.3 32.4 26.4 11.9 2.4 3.1 2.7 2.3 2.4 2.7
LAgP Mean 33.5 2.6 1.7 1.3 30.4 16.5 10.0 7.5 5.4 4.4 8.4 7.4 7.7
SD 7.7 2.4 1.4 1.7 25.4 17.0 18.2 3.1 2.1 2.1 3.4 3.6 3.9
CON Mean 23.4 1.9 4.6 1.5 2.0
SD 1.3 2.3 8.1 0.7 1.2
BOP: bleeding on probing, CAL: clinical attachment loss, CON: control group, CRP: C-reactive protein, GAgP: group of patients with
generalised aggressive periodontitis, LAgP: group of patients with localised aggressive periodontitis, PPD: probing pocket depth, SD:
standard deviation.

Figure 1 Levels of CRP (mean  SE, mg/L). CRP levels in patient groups GAgP and LAgP in stages of periodontal treatment and in
control group CON (*statistically significant differences).

Figure 2 CRP levels and BOP index in stages of periodontal treatment (mean  SE, mg/L). CRP levels and BOP index in patient
groups GAgP and LAgP in stages of periodontal treatment and in control group CON (*statistically significant differences).
372 J. Mysak et al

Figure 3 CRP levels and PPD index in stages of periodontal treatment (mean  SE, mg/L). CRP levels and PPD index in patient
groups GAgP and LAgP in stages of periodontal treatment and in control group CON (*statistically significant differences).

Figure 4 CRP levels and CAL index in stages of periodontal treatment (mean  SE, mg/L). CRP levels and CAL index in patient
groups GAgP and LAgP in stages of periodontal treatment and in control group CON (*statistically significant differences).

from 8.4  3.4 mms to 7.7  3.9 mms, CAL index in control Statistically significant differences (p
0.05) were found
group CON was 2.0  1.2 mms. between all measurements during periodontal treatment in
BOP and PPD indices and I. vs. II. and I. vs. III. in CRP levels.
Statistical comparisons of CRP levels and clinical peri- This corresponds to the healing of periodontium with severe
odontal parameters in patient group GAgP between process of destruction of periodontium.
measurements during periodontal treatment (Table 2):
Statistical comparisons of CRP levels and clinical peri-
Statistically significant differences (p
0.05) were odontal parameters in all patients (groups GAgP and
found between all measurements during periodontal LAgP together) between measurements during peri-
treatment in BOP and PPD indices and in CAL index to II. vs. odontal treatment (Table 2):
III. and I. vs. III.
Statistically significant differences (p
0.05) were
Statistical comparisons of CRP levels and clinical peri- found between all measurements during periodontal
odontal parameters in patient group LAgP between treatment in BOP and PPD indices, II. vs. III. in CAL index
measurements during periodontal treatment (Table 2): and II. vs. III. and I. vs. III. in CRP levels.
C-reactive protein in patients with aggressive periodontitis 373

control group CON in measurements during periodontal

Table 2 Statistical comparison of CRP levels and clinical
treatment (Table 3):
periodontal parameters in patient groups GAgP, LAgP and
GAgP þ LAgP between stages of periodontal treatment.
Statistically significant differences (p
0.05) were
Group I vs. II (p) II vs. III (p) I vs. III (p) found between values in all measurements during peri-
CRP GAgP 0.922 0.071 0.216 odontal treatment in LAgP and CON groups in values of PPD
LAgP 0.043* 0.140 0.024* and CAL indices, between values of BOP index I. vs. II.
GAgP þ LAgP 0.389 0.023* 0.022* during periodontal treatment in LAgP and CON groups and
BOP GAgP 0.017* 0.005* 0.000* between CRP levels in measurement II. in LAgP and CON
LAgP 0.002* 0.030* 0.001* groups.
GAgP þ LAgP 0.000* 0.000* 0.000* Statistical comparisons of CRP levels and clinical peri-
PPD GAgP 0.000* 0.018* 0.000* odontal parameters between a group of all patients (groups
LAgP 0.001* 0.035* 0.000* GAgP and LAgP together) and control group CON in mea-
GAgP þ LAgP 0.000* 0.001* 0.000* surements during periodontal treatment (Table 3): Statis-
CAL GAgP 0.840 0.002* 0.022* tically significant differences (p
0.05) were found
LAgP 0.090 0.248 0.287 between values in all measurements during periodontal
GAgP þ LAgP 0.130 0.002* 0.862 treatment in the group of all patients (groups GAgP and
LAgP together) and CON group in values of PPD and CAL
*Statistically significant differences (p
0.05).
indices, between values of BOP index in measurements I.
BOP: bleeding on probing, CAL: clinical attachment loss, CRP:
C-reactive protein, PPD: probing pocket depth. vs. II. during periodontal treatment in the group of all pa-
tients (groups GAgP and LAgP together) and CON group and
between CRP levels I. vs. II. during periodontal treatment in
Statistical comparisons of CRP levels and clinical peri- the group of all patients (groups GAgP and LAgP together)
odontal parameters between patient group GAgP and and CON group.
control group CON in measurements during periodontal
treatment (Table 3):
Discussion
Statistically significant differences (p
0.05) were
found between values in all measurements during peri- The treatment of aggressive periodontitis should be timely,
odontal treatment in GAgP and CON groups in CRP levels with absolute compliance to the treatment plan, and with
and in values of PPD and CAL indices and between values of perfect cooperation between patient, dentist and dental
BOP index I. vs. II. in GAgP and CON groups. These results hygienist. CRP as an inflammatory protein could contribute
show the gradual healing of periodontium which also cor- to more complete understanding of the condition of peri-
responded to the decrease in CRP levels approaching those odontal tissues during periodontal therapy and after its
of healthy periodontal tissues in group CON. completion, i.e. during the recall. CRP could indicate
exacerbation of inflammatory process before the onset of
Statistical comparisons of CRP levels and clinical peri- its own clinical features e increase in bleeding on probing24
odontal parameters between patient group LAgP and and deepening of periodontal pockets. In our study, we
found BOP and PPD indices significantly decreased after
precise execution of deep scaling and root planing in the
Table 3 Statistical comparison of CRP levels and clinical initial phase of periodontal treatment.
periodontal parameters between patient group GAgP, LAgP, Bleeding on probing is a sign of inflammation and in-
GAgP þ LAgP and control group CON in stages of periodontal dicates some sort of destruction and erosion to the lining of
treatment. the sulcus or the ulceration of sulcular epithelium. The
Group I vs. CON II vs. CON III vs. CON blood comes from the lamina propria after the ulceration of
(p) (p) (p) the lining.2
CRP GAgP 0.018* 0.000* 0.030* Bokhari et al. confirmed that the BOP index is the only
LAgP 0.239 0.000* 0.610 periodontal parameter which shows significant relationship
GAgP þ LAgP 0.014* 0.000* 0.092 to systemic parameters such as CRP and fibrinogen levels,
BOP GAgP 0.000* 0.012* 0.416 and white blood cell count.25 In our study in patients with
LAgP 0.000* 0.004* 0.194 aggressive periodontitis we demonstrated statistically sig-
GAgP þ LAgP 0.000* 0.000* 0.137 nificant differences in BOP development between mea-
PPD GAgP 0.000* 0.000* 0.000* surement I. vs. CON and between measurement II. (i.e.
LAgP 0.000* 0.000* 0.000* after subgingival treatment) vs. CON.
GAgP þ LAgP 0.000* 0.000* 0.000* Patients with aggressive periodontitis have statistically
CAL GAgP 0.000* 0.000* 0.000* significant elevations in serum CRP levels compared to
LAgP 0.000* 0.000* 0.000* subjects with healthy periodontium. Elevated CRP in these
GAgP þ LAgP 0.000* 0.000* 0.000* subjects might represent a contribution of periodontal
infection to systemic inflammation in relatively young in-
*Statistically significant differences (p
0.05).
dividuals.21 In patients with aggressive periodontitis
BOP: bleeding on probing, CAL: clinical attachment loss, CRP:
increased levels of CRP could be a united indicator of both
C-reactive protein, PPD: probing pocket depth.
the condition of periodontal tissues and the risk of systemic
374 J. Mysak et al

diseases, such as cardiovascular diseases. In the study of 10. Jayaprakash D, Aghanashini S, Chatterjee A, Bharwani A,
Goyal et al., significantly higher levels of CRP were Vijayendra R, Rosh R. Effect of periodontal therapy on C-
demonstrated in patients with generalised aggressive reactive protein levels in gingival crevicular fluid of patients
periodontitis.13 In our study statistically significant differ- with gingivitis and chronic periodontitis: a clinical and
biochemical study. J Indian Soc Periodontol 2014;18:456e60.
ences in CRP levels were found between I. vs. II. and I. vs.
11. Pradeep AR, Manjunath RG, Kathariya R. Progressive peri-
III. measurements in group LAgP. On the contrary, in group odontal disease has a simultaneous incremental elevation of
GAgP, no statistically significant differences were found in gingival crevicular fluid and serum CRP levels. J Investig Clin
CRP levels between all three measurements during the Dent 2010;1:133e8.
initial phase of periodontal treatment. This could show that 12. Marcaccini AM, Meschiari CA, Sorgl CA, et al. Circulating
conservative (non-surgical) therapy might have been interleukin-6 and high sensitivity C-reactive protein decrease
insufficient in patients with generalised aggressive peri- after periodontal therapy in otherwise healthy subjects. J
odontitis for the reduction of inflammatory process in Periodontol 2009;80:594e602.
periodontal tissues. Nevertheless, the results in our study 13. Goyal L, Bey A, Gupta ND, Sharma VK. Comparative evaluation
could also indicate that using BOP index in the clinical ex- of serum C-reactive protein levels in chronic and aggressive
periodontitis patients and association with periodontal disease
amination might be more pertinent than measuring CRP
severity. Contemp Clin Dent 2014;5:484e8.
levels to evaluate healing of periodontal tissues. 14. Shi D, Liu YY, Li W, et al. Association between plasma leptin
level and systemic inflammatory markers in patients with
Conflict of interest aggressive periodontitis. Chin Med J Engl 2015;128:528e32.
15. Dutta P, Courties G, Wei Y, et al. Myocardial infarction accel-
erates atherosclerosis. Nature 2012;487:325e9.
The authors declare that they have no conflict of interests
16. Janket SJ, Baird AE, Chuang SK, Jones JA. Meta-analysis of
associated with this work. periodontal disease and risk of coronary heart disease and
stroke. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;
Acknowledgements 95:559e69.
17. Meurman JH, Sanz M, Janket SJ. Oral health, atherosclerosis,
and cardiovascular disease. Crit Rev Oral Biol Med 2004;15:
The study was supported by PROGRES Q29 (Charles Uni- 403e13.
versity of Prague, Czech Republic), by project 14-37368G 18. Ridker PM, MacFadyen JG, Fonseca FA, et al. Number needed
(Grant Agency, Czech Republic) and by project 17-30753A to treat with rosuvastatin to prevent first cardiovascular events
(Czech health research council, Czech Republic). and death among men and women with low low-density lipo-
protein cholesterol and elevated high-sensitivity C-reactive
protein: justification for the use of statins in prevention: an
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