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J Clin Periodontol 2015; 42: 998–1005 doi: 10.1111/jcpe.

12471

The association of hypertension Yoo-Been Ahn1,*, Myung-Seop


Shin1,*, Jong-Seok Byun2 and
Hyun-Duck Kim1,3

with periodontitis is highlighted in 1


Department of Preventive and Social
Dentistry, School of Dentistry, Seoul National
University, Seoul, Korea; 2Department of

female adults: results from the Applied Statistics, College of IT, Hanshin
University, Osan-Si, Gyeonggi-Do, Korea;
3
Dental Research Institute, School of

Fourth Korea National Health Dentistry, Seoul National University, Seoul,


Korea

*Dr Ahn and Dr Shin are co-first authors who

and Nutrition Examination contributed equally to this work.

Survey
Ahn Y-B, Shin M-S, Byun J-S, Kim H-D. The association of hypertension
with periodontitis is highlighted in female adults: results from the Fourth Korea
National Health and Nutrition Examination Survey. J Clin Periodontol 2015; 42:
998–1005. doi: 10.1111/jcpe.12471.

Abstract
Aim: To evaluate the association of hypertension and high systolic and diastolic
blood pressure (SBP and DBP) with periodontitis in a nationally representative
Korean adult population.
Materials and Methods: Total of 14,625 participants of Fourth Korea National
Health and Nutrition Examination Survey (KNHANES IV) aged over 19 years
were cross-sectionally surveyed. Periodontitis was defined as CPI score of 3 or 4.
Hypertension was categorized as: normotensive (SBP < 120 mmHg and
DBP < 80 mmHg), pre-hypertensive (120 < SBP < 140 mmHg or
80 < DBP < 90 mmHg) and hypertensive (SBP ≥ 140 mmHg or
DBP ≥ 90 mmHg or taking antihypertensive medication). Multivariate Poisson
regression analyses were performed controlling for age, sex, household income,
drinking, smoking, physical activity, obesity, hypercholesterolaemia and diabetes
mellitus. Stratified analyses were performed to identify specific risk groups.
Results: Hypertension showed a significant positive association with periodontitis
in the fully adjusted model in female adults with a dose–response relationship.
This association was highlighted in females aged 30–59 years (prevalence
Key words: epidemiology; females;
ratio = 1.25; 95% confidence interval: 1.11–1.40). The strength of the association
hypertension; KNHANES; periodontitis
was highest in females aged 30–39 years and decreased with increasing age.
Among females aged 30–59 years, high-risk groups of this link were lower middle Accepted for publication 8 October 2015

Conflict of interest and source of funding statement


The authors declare no conflicts of interest. The data from the Fourth Korea National Health and Nutrition Examination Sur-
vey were provided by the Korea Centers for Disease Control and Prevention. This work was supported by a grant from the
Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Edu-
cation, Science and Technology (No. 2013-062881) and the NRF Grant through the Oromaxillofacial Dysfunction Research
Center for the Elderly (No. 2014-050477) at Seoul National University of Korea. Dr Ahn was supported by the Brain Korea
21 grant from Seoul National University, School of Dentistry of Korea.

998 © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hypertension and periodontitis 999

income quartile, never drinker and non-diabetes groups for both pre-hypertension
and hypertension.
Conclusion: Our data showed that hypertension was associated with periodontitis
in Korean female adults independent of known confounders.

Periodontal disease has drawn and diastolic pressure (SBP and surements were taken by trained
increasing attention for its associa- DBP) with periodontitis (Franek staff members. Face-to-face inter-
tion with cardiovascular disease et al. 2009). In a subsequent study views were conducted with a struc-
(CVD), as a chronic multifactorial of 155 type 2 diabetes individuals, tured questionnaire by trained
condition linked with systemic central SBP and DBP were reported interviewers. Out of the 24,871 par-
inflammatory markers and endothe- to be associated with periodontitis ticipants of this survey, only those
lial dysfunction. In 2013, a consen- severity (Franek et al. 2010). In individuals aged over 19 who had
sus report of the joint EFP/AAP another cross-sectional study of 79 complete datasets were included in
Workshop was published to address Brazilians, DBP was associated with the analysis, which constituted a
that the current state of the evidence severe periodontitis among individu- total of 14,625 participants (6247
supports a positive and significant als with heterozygous familial hyper- males and 8378 females) (Table 1).
association between periodontitis cholesterolaemia, after adjusting for
and atherosclerotic CVD (Tonetti traditional risk factors for Assessment of hypertension
et al. 2013). Known as a major risk atherosclerosis (Vieira et al. 2011).
factor for CVD, hypertension is also To date, however, no nationally rep- A standard mercury sphygmo-
considered to play a role as a risk resentative epidemiological study has manometer (Baumanometer, W.A.
factor for periodontitis. World reported on the role of high blood Baum, Copiague, NY, USA) was
Health Organization (WHO) reports pressure on periodontitis pathogene- used to measure SBP and DBP on the
that periodontitis and hypertension sis. participants’ right arm in a seated
affect approximately one third of the In the lack of evidence on the position after at least 5 min. of rest
world’s adult population, the latter association of hypertension with before the initial measurement. The
of which accounts for 51% of deaths periodontitis in Koreans, the authors blood pressure measurements were
from stroke and 45% of CVD mor- explored this potential link in a taken twice at a 5-min. interval and
tality (WHO, 2014). Similarly, peri- nationally representative sample of the average values were used for the
odontitis and hypertension are Korean population, using the Fourth analysis. For our analyses, pre-hyper-
highly prevalent in Korea, affecting Korea National Health and Nutri- tension was defined as having either
one third of adults aged over 30 tion Examination Survey 120 ≤ SBP < 140 mmHg or 80 ≤
(KCDC, 2014). As such, hyperten- (KNHANES IV) data. The aim of DBP < 90 mmHg and hypertension
sion and periodontitis are major this study was to test the hypothesis was defined as having an average SBP
health problems and the elucidation that hypertension is associated with over 140 mmHg or DBP over
of their association is of public periodontitis. 90 mmHg or medicated for hyperten-
health concern. sion. This classification was based on
Several potential mechanisms of the SBP and DBP cut-off points sug-
Materials and Methods
hypertension-induced periodontal gested by the JNC7 report (Choba-
deterioration have been proposed. nian et al. 2003).
Study design and subjects
Endothelial dysfunction of small
arterioles and the subsequent gingi- To test the hypothesis that hyperten- Assessment of periodontitis
val arteriolar wall thickening and sion is associated with periodontitis,
microcirculatory dysfunction caused cross-sectional analyses were per- Periodontal status of the participants
by high blood pressure have been formed using a dataset of nationally was assessed by dentists using the
suggested as possible mechanisms representative Korean population. Community Periodontal Index of
(Tsioufis et al. 2011). In an experi- The data were derived from the Treatment Needs (CPITN). Accord-
mental study, heightened levels of KNHANES IV, conducted between ing to the WHO guidelines, a CPI
inflammatory mediators were found 2007 and 2009 by the Korea Centers probe with a 0.5-mm ball tip was
in the gingival tissue of sponta- for Disease Control and Prevention used with an approximately 20 g
neously hypertensive rats, suggesting (KCDC). A detailed description of probing force. Periodontal pocket
that hypertensive condition favours the sampling methods and survey depths (PD) were measured at six
the inflammatory process which can contents is described in previous sites (mesio-buccal, mid-buccal,
affect the periodontium peripherally publications (Lee et al. 2013, Kim disto-buccal, disto-lingual, mid-
(Bonato et al. 2012). Several epi- et al. 2014), and in the KNHANES lingual and mesio-lingual) per tooth.
demiological data have suggested a IV report (KCDC, 2009). In the Ten index teeth selected for the
positive association of hypertension KNHANES, physical and dental examination were: the first and sec-
with periodontitis. A cross-sectional examinations and blood sampling ond molars in each posterior sextant,
study of 99 Polanders found a crude were performed at a mobile exami- the upper right incisor in upper
association of elevated aortic systolic nation centre and all clinical mea- middle sextant and the lower left
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
1000 Ahn et al.

Table 1. Characteristics of the participants by periodontitis (CPI 3–4) (n = 14,625) ing on probing), 2 (presence of cal-
Variable N Periodontitis (CPI 3–4) p Value* culus), 3 (PD ≥ 3.5 mm) and 4
(PD ≥ 5.5 mm). Training and cali-
No Yes bration procedure preceded each
annual survey in accordance with
Age (years), n (%) the KNHANES standards. The
19–29 2010 1871 (19.8) 139 (2.7) <0.001 Kappa value means for inter-exami-
30–39 3107 2489 (26.3) 618 (11.9) ner reliability were 0.71 (0.69–0.77)
40–49 3048 1914 (20.2) 1134 (21.9)
in 2007, 0.89 (0.55–1.00) in 2008 and
50–59 2557 1291 (13.7) 1266 (24.5)
≥60 3903 1887 (20.0) 2016 (39.0)
0.75 (0.53–0.94) in 2009 (KCDC,
Sex, n (%) 2009). For the analysis, periodontal
Female 8378 5889 (62.3) 2489 (48.1) <0.001 status was dichotomized into peri-
Male 6247 3563 (37.7) 2684 (51.9) odontitis negative (CPI score of 0–2,
Household income, n (%) including normal and gingivitis) and
Lowest quartile 2811 1528 (16.2) 1283 (24.8) <0.001 periodontitis positive (CPI score of
Lower middle quartile 3645 2250 (23.8) 1395 (27.0) 3–4).
Upper middle quartile 4032 2701 (28.6) 1331 (25.7)
Highest quartile 4137 2973 (31.5) 1164 (22.5)
Drinking, n (%) Assessment of potential confounders
Never 2003 1203 (12.7) 800 (15.5) <0.001
Ever in lifetime 12,622 8249 (87.3) 4373 (84.5)
The authors considered the following
Smoking, n (%) as potential confounders: (1) age, (2)
Never 8626 6046 (64.0) 2580 (49.9) <0.001 sex, (3) household income, (4)
Ever in lifetime 5999 3406 (36.0) 2593 (50.1) drinking, (5) smoking, (6) physical
Physical activity, n (%) activity, (7) obesity, (8) hypercholes-
None 9699 6142 (65.0) 3557 (68.8) <0.001 terolaemia and (9) diabetes mellitus
≥1 day/week 4926 3310 (35.0) 1616 (31.2) (Tsioufis et al. 2011).
Obesity†, n (%) Information on age, sex, income
Non-obese 9954 6662 (70.5) 3292 (63.6) <0.001 and such lifestyle variables as smok-
Obese 4671 2790 (29.5) 1881 (36.4)
ing and drinking habits, and physical
Hypercholesterolaemia‡, n (%)
No 13,037 8567 (90.6) 4470 (86.4) <0.001
activity was collected from the par-
Yes 1588 885 (9.4) 703 (13.6) ticipants’ responses to a standardized
Diabetes§, n (%) questionnaire through in-person
Non-diabetic 13,293 8824 (93.4) 4469 (86.4) <0.001 interviews. Participants were catego-
Diabetic 1332 628 (6.6) 704 (13.6) rized into five age groups: 19–29,
Hypertension¶, n (%) 30–39, 40–49, 50–59 and over
Normal 6942 5122 (54.2) 1820 (35.2) <0.001 60 years. Income status was mea-
Pre-hypertension 3573 2204 (23.3) 1369 (26.5) sured by the household income and
Hypertension 4110 2126 (22.5) 1984 (38.4) was categorized into quartiles. Self-
Systolic blood pressure (SBP), n (%)
<120 mmHg 8552 6193 (65.6) 2359 (45.6) <0.001
reported alcohol consumption was
120 ≤ SBP < 140 mmHg 2834 1663 (17.6) 1171 (22.6) dichotomized into none or ever in
≥140 mmHg†† 3239 1596 (16.9) 1643 (31.8) lifetime. Self-reported smoking status
Diastolic blood pressure (DBP), n (%) was similarly dichotomized into
<80 mmHg 8829 6245 (66.1) 2584 (50.0) <0.001 never smokers or ever a smoker in
80 ≤ DBP < 90 mmHg 2389 1477 (15.6) 912 (17.6) lifetime. Information on physical
≥90 mmHg†† 3407 1730 (18.3) 1677 (32.4) activity was assessed by the number
*Obtained from chi-square test.
of days per week strenuous activities

Obesity is defined as body mass index (BMI, kg/m2) ≥ 25. are conducted and grouped as none

Hypercholesterolaemia: total cholesterol in blood (TC) ≥ 240 mg/dl or medicated for or more than 1 day per week. Body
hypercholesterolaemia; normal: TC < 240 mg/dl. weight and height were measured to
§
Diabetes: fasting plasma glucose (FPG) ≥ 126 mg/dl or medicated for diabetes; pre-dia- the nearest 0.1 kg and 0.1 cm,
betes: 100 ≤ FPG < 126 mg/dl; normal: FPG < 100 mg/dl. respectively, with the participants in
Hypertension: SBP ≥ 140 mmHg or DBP ≥ 90 mmHg or medicated for hypertension; light in-door clothing without shoes.
pre-hypertension: 120 ≤ SBP < 140 mmHg or 80 ≤ DBP < 90 mmHg; normal: SBP < 120 Body mass index (BMI: kg/m2) was
mmHg and DBP < 80 mmHg. calculated using the formula weight/
††
Includes individuals medicated for hypertension.
height2 (kg/m2). Obesity was defined
as having BMI over 25 kg/m2. Blood
samples were collected from the
central incisor in lower middle sex- examined. If no adjacent tooth was antecubital vein of each participant
tant. A sextant was examined only if present, all remaining teeth were after at least 8 h of fasting and anal-
there were two or more teeth present examined and the highest score was ysed within 24 h of collection. Con-
that were not scheduled for extrac- recorded as the score for that sex- centrations of total cholesterol (TC)
tion. If the index tooth was absent tant. CPI was scored from 0 to 4: 0 and fasting plasma glucose (FPG)
in a sextant, the adjacent tooth was (normal), 1 (gingivitis with bleed- were measured in an automatic
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hypertension and periodontitis 1001

analyser using commercially avail- In sequential analyses, the hyperten- hypertensive criteria respectively.
able enzymatic assay kits (1470 sion variable of Model III was sub- The hypertensive SBP and DBP cat-
Wizard; PerkinElmer, Wallac: stituted with ternary SBP and DBP egories included those individuals
Waltham, Massachusetts, USA). variables to test for the association medicated for hypertension.
Hypercholesterolaemia was defined of these components with periodon- Evaluation of the interaction
as having TC over 240 mg/dl or titis individually in SBP and DBP effects between hypertension and
medicated for hypercholesterolaemia. models. The ternary SBP and DBP confounders on the association of
Diabetes was defined as FPG over variables adopted the diagnostic cri- hypertension with periodontitis were
126 mg/dl or medicated for diabetes, teria as suggested by the JNC7 performed for drinking, smoking,
according to the WHO criteria report (Chobanian et al. 2003): SBP exercise, obesity and diabetes vari-
(WHO, 2006). cut-offs were 120 and 140 mmHg ables.
while those of DBP were 80 and Finally, to investigate high-
Statistical analyses
90 mmHg for pre-hypertensive and risk group of the link between

In the analysis, the outcome variable


was periodontitis and the main
explanatory variable was hyperten- Table 2. Adjusted association of hypertension with periodontitis (CPI 3–4) in multiple
sion status. Summary statistics of models (n = 14,625)
the population characteristics were Variable N Prevalence ratio (95% confidence interval)
calculated as frequencies and per-
centages. Any statistically significant Model I Model II Model III
differences between the periodontitis
Hypertension
positive and negative groups, in
Normal 6942 1 1 1
terms of the socio-economic, beha- Pre-hypertension 3573 1.10 (1.04–1.16) 1.10 (1.04–1.16) 1.09 (1.03–1.15)
vioural and health-related factors, Hypertension 4110 1.12 (1.07–1.18) 1.13 (1.07–1.19) 1.10 (1.04–1.16)
were examined using chi-square test. Trend-p < 0.001 Trend-p < 0.001 Trend-p = 0.001
Multiple multivariate Poisson Age (years)
regression models were applied to 19–29 2010 1 1 1
evaluate the adjusted prevalence 30–39 3107 2.90 (2.43–3.45) 2.85 (2.39–3.39) 2.84 (2.38–3.38)
ratios (PRs) of the association of 40–49 3048 5.32 (4.50–6.28) 5.26 (4.45–6.22) 5.22 (4.42–6.16)
hypertension with periodontitis while 50–59 2557 6.87 (5.82–8.11) 6.82 (5.77–8.05) 6.72 (5.69–7.93)
adjusting for potential confounders. ≥60 3903 6.71 (5.68–7.93) 6.62 (5.60–7.82) 6.53 (5.52–7.72)
Trend-p < 0.001 Trend-p < 0.001 Trend-p < 0.001
Model I was adjusted for socio-
Sex
economic variables including age Female 8378 1 1 1
group, sex and household income. Male 6247 1.43 (1.38–1.50) 1.13 (1.15–1.30) 1.23 (1.15–1.30)
Model II was adjusted for socio-eco- Household income
nomic variables and health-related Lowest quartile 2811 1 1 1
behavioural variables including Lower middle quartile 3645 1.00 (0.94–1.06) 1.01 (0.95–1.07) 1.01 (0.95–1.06)
drinking, smoking and physical Upper middle quartile 4032 0.95 (0.90–1.01) 0.96 (0.91–1.02) 0.96 (0.91–1.02)
activity. Model III and the final Highest quartile 4137 0.80 (0.75–0.86) 0.82 (0.77–0.88) 0.82 (0.77–0.88)
model, was adjusted for all the Trend-p < 0.001 Trend-p < 0.001 Trend-p < 0.001
Drinking
aforementioned variables and sys-
Never 2003 1 1
temic health-related variables includ- Ever in lifetime 12,622 0.99 (0.93–1.05) 0.99 (0.93–1.05)
ing obesity, hypercholesterolaemia Smoking
and diabetes. For each model, the Never 8626 1 1
adjusted PRs, confidence intervals Ever in lifetime 5999 1.25 (1.18–1.33) 1.25 (1.18–1.33)
(CI) and the trend p-values for mul- Physical activity
ti-category variables were calculated. None 9699 1 1
In accordance with the age group ≥1 day/week 4926 0.96 (0.92–1.01) 0.96 (0.92–1.01)
and sex-stratified design of Obesity
KNHANES sampling (KCDC, Non-obese 9954 1
Obese 4671 1.05 (1.01–1.10)
2009), age group (five groups: 19–29,
Hypercholesterolaemia
30–39, 40–49, 50–59 or over No 13,037 1
60 years) and sex-stratified analyses Yes 1588 1.03 (0.97–1.09)
were performed both individually Diabetes
and in combination to adjust for the Non-diabetic 13,293 1
residual decrease in p-value due to Diabetic 1332 1.10 (1.04–1.16)
the big sample size of over 10,000.
Model I: adjusted for socio-economic factors including age group, sex and household
For the age and sex groups in income. Model II: adjusted for all variables in Model I and behavioural factors including
which the association of hyperten- drinking, smoking and physical activity. Model III: adjusted for all variables in Model II
sion with periodontitis was found and systemic health-related factors including obesity, hypercholesterolaemia and diabetes
significant, PRs for periodontitis was mellitus.
estimated using the same Model III. Bold denotes statistical significance at p < 0.05.

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
1002 Ahn et al.

hypertension and periodontitis, Age group and sex-stratified association p < 0.001). Increasing SBP and DBP
stratified analyses by economic, of hypertension with periodontitis also showed independent association
behavioural and systemic factors The link of hypertension on peri- with periodontitis (PR: 1.24; 95%
were performed using the Model odontitis was highlighted in the fol- CI: 1.10–1.39 for hypertensive SBP
III in the subgroup of females aged lowing age and sex groups (Table 3): and PR: 1.25; 95% CI: 1.11–1.40 for
30–59 years in which significant 40–49 years group (PR = 1.13; 95% hypertensive DBP) with a dose–
association was found. Stratification CI: 1.00–1.28) and females (PR = response relationship (trend p < 0.001)
groups were as follows: (1) income 1.19; 95% CI: 1.09–1.29). The asso- for both models.
quartiles, (2) physical activity (two ciation was strongest in the 30–39
groups: none or ≥1 day per week), years group (PR = 1.64; 95% CI: Effect of interaction terms between
(3) drinking (two groups: never or 1.08–2.48), which gradually hypertension and confounders in females
ever in lifetime), (4) smoking (two decreased with increasing age to aged 30–59 years
groups: never or ever in lifetime), reach the null in the over 60 years
(5) obesity (two groups: non-obese The interaction effect between
group (PR = 1.10; 95% CI: 0.97–
or obese), (6) hypercholesterolaemia hypertension and confounders on
1.24). For the 19–29 years female
(two groups: normal or hyperc- the association of hypertension with
group, the PR of hypertension could
holesterolemia) and (7) diabetes periodontitis was not significant for
not be estimated due to the small
mellitus (two groups: normal or drinking, smoking, physical activity,
sample size of 19.
diabetic). obesity or diabetes in females aged
For the analyses, statistical signif- 30–59 years. However, the fully
icance was set at p-values < 0.05. Relationship between hypertension, high adjusted PR was increased from
SBP and high DBP and periodontitis in 1.25 (95% CI: 1.11–1.40) to 1.40
females aged 30–59 years (95% CI: 1.11–1.77) for interaction
Results with drinking and 1.34 (95% CI:
In females aged 30–59 years
(n = 5010), the association of hyper- 1.16–1.55) for interaction with
General characteristics obesity.
tension with periodontitis was stron-
Compared to the participants with- ger than that of total population
out periodontitis, those with peri- (Fig. 1). The fully adjusted PR was Stratified association of hypertension with
odontitis were significantly older 1.13 (95% CI: 1.01–1.26) for pre- periodontitis in females aged 30–59 years
and more represented by males, hypertension and 1.25 (95% CI:
smokers, never drinkers and indi- 1.11–1.40) for hypertension with a In terms of socio-economic and
viduals with lower household dose–response relationship (trend health-related factors, the link of
income (Table 1). Higher prevalence
of obesity, hypercholesterolaemia, Table 3. Age and sex-stratified adjusted association of hypertension with periodontitis (CPI
diabetes, pre-hypertension, hyper- 3–4) (n = 14,625)
tension and higher SBP and DBP Stratum N Prevalence ratio (95% confidence interval)
was observed among individuals
with periodontitis. Normal Pre-hypertension Hypertension†

Age (years)
Relationship between hypertension and 19–29 2010 1 1.30 (0.85–1.97) 0.76 (0.30–1.94)
periodontitis 30–39 3107 1 0.89 (0.74–1.06) 1.00 (0.79–1.26)
Hypertension was consistently asso- 40–49 3048 1 1.14 (1.02–1.27) 1.13 (1.00–1.28)
50–59 2557 1 1.10 (1.00–1.22) 1.09 (0.99–1.20)
ciated with periodontitis throughout
≥60 3903 1 1.05 (0.96–1.15) 1.08 (0.99–1.17)
the adjustment process in Models I, Sex
II and III with a dose–response rela- Female 8378 1 1.15 (1.05–1.25) 1.19 (1.09–1.29)
tionship (Table 2). The positive asso- Male 6247 1 1.01 (0.94–1.08) 1.00 (0.93–1.07)
ciation of pre-hypertension and Age and sex
hypertension with periodontitis 19- to 29-year-old female 1142 1 2.19 (1.25–3.84) –
found in the age-, sex- and income- 30- to 39-year-old female 1813 1 0.94 (0.68–1.31) 1.64 (1.08–2.48)
adjusted Model I was consistent in 40- to 49-year-old female 1735 1 1.10 (0.91–1.32) 1.34 (1.10–1.63)
Model II, which was further 50- to 59-year-old female 1462 1 1.17 (1.00–1.36) 1.18 (1.02–1.36)
≥60-year-old female 2226 1 1.08 (0.94–1.25) 1.10 (0.97–1.24)
adjusted for lifestyle variables. In the
19- to 29-year-old male 868 1 0.95 (0.57–1.59) 0.89 (0.34–2.33)
final Model III, after the inclusion of 30- to 39-year-old male 1294 1 0.84 (0.68–1.03) 0.87 (0.67–1.13)
obesity, hypercholesterolaemia and 40- to 49-year-old male 1313 1 1.12 (0.98–1.28) 1.02 (0.88–1.18)
diabetes variables, the strength of 50- to 59-year-old male 1095 1 1.04 (0.91–1.18) 1.00 (0.88–1.13)
the association of hypertension with ≥60-year-old male 1677 1 1.03 (0.91–1.16) 1.05 (0.94–1.17)
periodontitis was slightly attenuated,
nonetheless, remained significant Prevalence ratios are adjusted for age groups, sex, household income, drinking, smoking,
physical activity, obesity, hypercholesterolaemia and diabetes except the stratum.
(PR = 1.09; 95% CI: 1.03–1.15 for †
Hypertension: either SBP ≥ 140 mmHg or DBP ≥ 90 mmHg or medicated for hyperten-
pre-hypertension; PR = 1.10; 95% sion; pre-hypertension: 120 ≤ SBP < 140 mmHg or 80 ≤ DBP < 90 mmHg; normal:
CI: 1.04–1.16 for hypertension; SBP < 120 mmHg and DBP < 80 mmHg.
trend-p = 0.001). Bold denotes statistical significance at p < 0.05.

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hypertension and periodontitis 1003

Fig. 1. Adjusted association of hypertension, systolic and diastolic blood pressure (SBP and DBP) with periodontitis (CPI 3–4) in
females aged 30–59 years (n = 5010): (a) prevalence ratio (PR) of hypertension on periodontitis; (b) PR of SBP on periodontitis; (c)
PR of DBP on periodontitis. Adjusted PRs are controlled for age group, sex, household income, drinking, smoking, physical activ-
ity, obesity, hypercholesterolaemia and diabetes mellitus. Diamond denotes PR and bar denotes 95% confidence interval. Diamond
with value 1 represents the reference. Bold denotes statistical significance at p < 0.05.

hypertension on periodontitis in physical activity, obesity, hyperc- effect as a result of the decreased
females aged 30–59 years was high- holesterolaemia and diabetes, based standard error due to the large sam-
lighted in the following subgroups on a Korean national data. To the ple greater than 10,000.
(Table 4): lower middle income best of our knowledge, this study The findings of our study high-
quartile (PR = 1.71; 95% CI: 1.25– presents the first evidence that light the importance of female sex in
2.33), highest income quartile hypertension is associated with high the relationship between hyperten-
(PR = 1.29 (1.01–1.65; 95% CI: prevalence of periodontitis in mid- sion and periodontal disease.
1.01–1.65), never drinker (PR = 1.51; dle-aged females. Females have higher risk of develop-
95% CI: 1.16–1.98), never smoker The major strengths of our study ing CVD than males (Appelman
(PR = 1.27; 95% CI: 1.12–1.43), are fourfold. First, the KNHANES et al. 2015). Females may have lower
physically active (PR = 1.33; 95% data used for this study are a large- threshold blood pressure for devel-
CI: 1.06–1.66), non-obese (PR = scale national survey of representa- oping peripheral vascular diseases,
1.32; 95% CI: 1.14–1.53), hyperc- tive Korean population. Second, we possibly due to the female-specific
holesterolaemia (PR = 1.68; 95% CI: used the Poisson model and higher prevalence of arterial stiffness
1.23–2.29) and non-diabetes (PR = reported PRs instead of odds ratio. (Coutinho 2014). The higher suscep-
1.28; 95% CI: 1.13–1.44). Also, the The frequently used odds ratios tibility of females to peripheral vas-
link of pre-hypertension on peri- from logistic regression analysis cular disease at lower blood pressure
odontitis was highlighted in the fol- overestimate the PR. PRs are the could contribute to the higher preva-
lowing subgroups: lower middle measure of choice in the analysis of lence of hypertension-related peri-
income quartile (PR = 1.30; 95% CI: cross-sectional survey data and pro- odontal disease in females. Further
1.07–1.58), never drinker (PR = 1.31; vide more robust results (Barros & studies are needed to clarify the
95% CI: 1.02–1.70) and non-diabetes Hirakata 2003). Third, currently underlying mechanisms of this phe-
(PR = 1.14; 95% CI: 1.02–1.28). known confounders of periodontitis nomenon.
have shown statistically significant Interestingly, the association of
independent association with peri- hypertension with periodontitis in
Discussion
odontitis in our data, hence corrob- females was highlighted in younger
Our results demonstrated that hyper- orating our data reliable. Finally, age group. The chronic nature of
tension is associated with periodonti- the association of hypertension with periodontitis and hypertension
tis among Korean female adults, periodontitis was assessed by age means that a period of time is
independent of the effects of age, group and sex-stratified analyses to required for the risk factors to con-
sex, income, drinking, smoking, minimize the residual false-positive tribute to the development of these
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
1004 Ahn et al.

Table 4. Stratified association of hypertension with periodontitis (CPI 3–4) in females aged reduced blood supply to periodontal
30–59 years (n = 5010) tissues could lead to increased sus-
Variable N Prevalence ratio (95% confidence interval) ceptibility to periodontal inflamma-
tion (Higashi et al. 2008). In
Category Normal Pre-hypertension Hypertension† addition, hypertension contributes to
systemic diseases such as metabolic
Household income syndrome which are risk factors for
Lowest quartile 501 1 1.25 (0.95–1.63) 1.10 (0.83–1.45) periodontitis (Kim et al. 2010, Han
Lower middle quartile 1217 1 1.30 (1.07–1.58) 1.48 (1.22–1.80)
et al. 2012a).
Upper middle quartile 1628 1 0.94 (0.76–1.17) 1.13 (0.90–1.41)
Highest quartile 1664 1 1.10 (0.88–1.37) 1.29 (1.01–1.65)
In the stratified analyses, those
Drinking with hypercholesterolaemia, lower
Never 710 1 1.31 (1.02–1.70) 1.51 (1.16–1.98) middle income, highest income and
Ever in lifetime 4300 1 1.09 (0.97–1.23) 1.20 (1.05–1.36) never drinking, never smoking, phys-
Smoking ically active, non-obese and non-dia-
Never 4510 1 1.13 (1.01–1.27) 1.27 (1.12–1.43) betic showed highlighted association
Ever in lifetime 500 1 1.13 (0.83–1.54) 1.11 (0.81–1.52) between hypertension and periodon-
Physical activity titis. Alcohol drinking, smoking,
None 3485 1 1.09 (0.96–1.24) 1.22 (1.07–1.39) non-exercise, obesity and diabetes
≥1 day/week 1525 1 1.22 (0.99–1.50) 1.33 (1.06–1.66)
Obesity
are well-known confounders (Tsiou-
Non-obese 3653 1 1.09 (0.95–1.25) 1.32 (1.14–1.53) fis et al. 2011) of the relationship
Obese 1357 1 1.16 (0.97–1.40) 1.18 (0.99–1.41) between hypertension and periodon-
Hypercholesterolaemia titis. Since periodontitis is a multi-
No 4532 1 1.12 (0.99–1.26) 1.19 (1.04–1.35) factorial disease, when the
Yes 478 1 1.37 (0.96–1.95) 1.68 (1.23–2.29) confounding effects of the risk fac-
Diabetes tors are removed, the link between
No 4761 1 1.14 (1.02–1.28) 1.28 (1.13–1.44) hypertension and periodontitis
Yes 249 1 0.85 (0.58–1.26) 1.04 (0.74–1.46) becomes highlighted. Since highest
Prevalence ratios are adjusted for age group, household income, drinking, smoking, physical income group are usually less
activity, obesity, hypercholesterolaemia and diabetes except the stratum. exposed to common risk factors, the

Hypertension: either SBP ≥ 140 mmHg or DBP ≥ 90 mmHg or medicated for hyperten- effect of hypertension on periodonti-
sion; pre-hypertension: 120 ≤ SBP < 140 mmHg or 80 ≤ DBP < 90 mmHg; normal: tis would be emphasized in this
SBP < 120 mmHg and DBP < 80 mmHg. group. The link of association
Bold denotes statistical significance at p < 0.05 and prevalence ratios greater than 1.13 for between hypertension and periodon-
pre-hypertension or 1.25 for hypertension. titis was also highlighted in females
with lower middle income. Consider-
ing that prevalence of hypertension
chronic diseases. The exposure time 2012). Therefore, the relatively lower in Korean female adults is highest in
to the risk factors in younger indi- level of female sex hormones in old the lower middle income group
viduals is considerably shorter than women could mean highlighted (26.3%) (KCDC, 2014), further
that in the older. As such, the longer effect of common risk factors of studies are needed to clarify the link.
exposure time to the common risk periodontitis and hypertension. Fur- Moreover, our data support the
factors for periodontitis and hyper- ther studies including sex hormones previous report that high blood
tension in older women means that and immune functions will clarify pressure is associated with high
the contribution of hypertension on the link. prevalence of periodontitis among
the development of periodontitis The mechanism of how hyperten- individuals with hypercholestero-
could be masked by the influence of sion induces periodontitis remains laemia (Franek et al. 2009, 2010,
these common risk factors. There- largely unknown. A possible linkage Vieira et al. 2011).
fore, high blood pressure in younger between hypertension and periodon- Our study has some limitations.
women may have played a more sig- titis is inflammation (Bonato et al. Owing to the limitations of the
nificant role in developing periodon- 2012). Both diseases are chronic cross-sectional design of the survey,
titis than that in older women. inflammatory diseases and are asso- no inference on the causality could
Similarly, the association of hyper- ciated with oxidative stress and pro- be made. Also, as the KNHANES
tension with periodontitis was gener- inflammatory cytokines (Han et al. employs CPITN index as a peri-
ally highlighted in never drinkers, 2012b, 2013). Systemic circulation of odontal assessment tool, our
never smokers and physically active, theses inflammatory products could periodontitis cases could have been
non-obese and non-diabetic individu- play a part in the link between underestimated. This could be a
als who were less exposed to these hypertension and periodontitis. non-differential bias and could have
common risk factors. Moreover, sev- Increased peripheral resistance, mea- diluted the estimated association.
eral female sex hormones including sured by pulse wave velocity was Notwithstanding these limitations,
oestrogen, progesterone and pro- also associated with periodontitis the results of our study are reliable
lactin influence the development of T (Shanker et al. 2013). Endothelial enough to test the hypothesis that
and B cells, the major players of cel- dysfunction caused by elevated high blood pressure is associated
lular immune response (Pennell et al. blood pressure and the subsequent with periodontitis.
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hypertension and periodontitis 1005

Overall, hypertension was associ- treated patients with essential hypertension. Health and Nutrition Examination Survey.
American Journal of Hypertension 22, 203–207. Journal of Clinical Periodontology 40, 437–442.
ated with higher prevalence of peri-
Franek, E., Napora, M., Blach, A., Budlewski, Pennell, L. M., Galligan, C. L. & Fish, E. N.
odontitis among middle-aged T., Gozdowski, D., Jedynasty, K., Krajewski, (2012) Sex affects immunity. Journal of Autoim-
Korean females independent of J. & Gorska, R. (2010) Blood pressure and left munity 38, J282–J291.
known confounders. Dentists should ventricular mass in subjects with type 2 dia- Shanker, J., Setty, P., Arvind, P., Nair, J., Bhas-
take precautions for individuals with betes and gingivitis or chronic periodontitis. ker, D., Balakrishna, G. & Kakkar, V. V.
Journal of Clinical Periodontology 37, 875–880. (2013) Relationship between periodontal dis-
hypertension to prevent and control Han, D. H., Kim, M. S., Shin, H. S., Park, K. P. ease, Porphyromonas gingivalis, peripheral vas-
for periodontitis. Further research is & Kim, H. D. (2013) Association between peri- cular resistance markers and coronary artery
indicated to confirm this association odontitis and salivary nitric oxide metabolites disease in Asian Indians. Thrombosis Research
in other ethnic population. Also, among community elderly Koreans. Journal of 132, e8–e14.
Periodontology 84, 776–784. Tonetti, M. S., Van Dyke, T. E. & Working
studies with prospective or experi- Han, D. H., Lim, S., Paek, D. & Kim, H. D. Group 1 of the Joint, EFP/AAP (2013) Peri-
mental design will aid the clarifica- (2012a) Periodontitis could be related factors odontitis and atherosclerotic cardiovascular
tion of the causality and mechanism on metabolic syndrome among Koreans: a disease: consensus report of the Joint EFP/
of this link. case-control study. Journal of Clinical Periodon- AAP Workshop on Periodontitis and Systemic
tology 39, 30–37. Diseases. Journal of Clinical Periodontology 40
Han, D. H., Shin, H. S., Kim, M. S., Paek, D. & (Suppl 14), S24–S29.
Kim, H. D. (2012b) Group of serum inflamma- Tsioufis, C., Kasiakogias, A., Thomopoulos, C. &
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Association of chronic periodontitis with left association between periodontitis and dyslipi- E-mail: hyundkim@snu.ac.kr
ventricular mass and central blood pressure in demia based on the Fourth Korea National

Clinical Relevance Principal findings: Hypertension was needs to be confirmed in different


Scientific rationale for the study: associated with periodontitis in a ethnic populations. Nonetheless,
Hypertension could be linked to representative Korean female adult periodontists may incorporate
periodontitis via systemic inflam- population. blood pressure screening into regu-
matory mediators, endothelial dys- Practical implications: Our data pre- lar dental checkups to help identify
function and common risk factors. sent the first evidence that hyperten- patients with higher risk of peri-
Yet, there is a lack of large-scale sion is associated with periodontitis odontitis.
epidemiological evidence on this in Korean females, based on a large-
association. scale national data. This association

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

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