Jantung-Dewi Ayu Sri Handayani
Jantung-Dewi Ayu Sri Handayani
Jantung-Dewi Ayu Sri Handayani
Original article
Dental College and Hospital, Hyderabad, India; 3Department of Cardiology, Yashoda Hospital, Hyderabad, India
Summary. Background: There is well documented scientific evidence supporting the association between
Coronary Heart Disease (CHD) and periodontitis. It is however, uncertain if this association is causal or is
mediated by the common inflammatory pathways. Hence, the study assessed and compared the Periodontal
Health Status among CHD patients with age and gender matched controls. Methods: A total of 808 medi-
cally confirmed CHD patients were compared with 808 age and gender matched controls. Oral examination
was conducted using Simplified Oral Hygiene Index (OHI-S) and modified World Health Organization
(WHO) Oral Health Assessment form, 1997. Mean scores were compared using Mann- Whitney-U test
and Analysis of Variance (ANOVA). Logistic regression analysed the association between the risk factors
and CHD. Results: Cases had significantly higher mean sextants with pockets and attachment loss ≥4mm
compared to controls (p≤0.05). The cases also had significantly poor oral hygiene mean scores compared to
controls (p=0.0001*). There was a lower and insignificant association between age (p=0.99), gender (p=0.84)
and CHD. Risk factors education (p=0.001), lesser frequency of dental visit (p=0.001) also showed a lower,
yet significant association. Risk of CHD was higher among tobacco (Odds ratio (OR) - 2.26) and alcohol
(OR-1.83) users. Presence of poor oral hygiene (OR-5.20), pocket of ≥6 mm (6.70) and attachment loss of
≥9 mm (OR-11.31) also showed higher risk of CHD. Conclusion: The study results support the association
between periodontal disease and CHD. To halt the epidemic of CHD, emphasis on screening of wide age
range, reinforcement of public health systems and early detection is recommended. (www.actabiomedica.it)
Key words: Coronary Heart Disease, periodontal disease, India, epidemiology, oral hygiene
women by 2020 (10). Few studies on morbidity trends vascular events. On the other hand, a follow up study
also divulge that CHD mortality is higher in South (23), did not support the assumption of a significant
Indian States both among men and women compared correlation between periodontitis and CHD. Similarly,
to central Indian states (10, 11). another cohort study by Hujoel PP et al (24), also did
This escalating burden of CHD in India can be not report convincing evidence of a causal association
attributed to the disturbing increase in the risk factors between periodontal disease and CHD. This could be
(genetic and environmental) like diabetes, hyperten- due to variations in the study design, difference in cri-
sion, abnormal serum lipids, age, smoking, socio-eco- teria used, and lack of accurate criteria for periodonti-
nomic status, gender etc. (12, 13). Apart from its mul- tis, assessment of the association without medical con-
tifactorial pathophysiology, bacterial and viral agents firmation and presence of other confounding factors.
are suggested to be contributory in both initiation (12, 14).
and progression of thromboembolic events leading to Hence, to clear this ambiguity, the present study
CHD (14). Growing literature has also implicated the was conducted with an aim to assess and compare the
role of oral infections, particularly periodontitis in the Periodontal Health Status among CHD patients with
pathogenesis of atherosclerosis (15, 16). The associa- age and gender matched controls.
tion between periodontitis and CHD was first given
by Mackenzie and Millard in 1963 (17). Since then,
evidence from various studies stated that there is a Materials and method
monotonic increasing gradient of risk for CHD due
to periodontal pathogens (largely due to gram negative The present study was approved by the Institution-
pathogens) (15, 16). al Review Board of the institution (PMVIDS&RC/
Periodontal gram negative bacteria along with IECPHD/DN/0038-15) and the study was conducted
their endotoxins enter the bloodstream and as a con- in accordance with the Declaration of Helsinki. Writ-
sequence, an increase in the plasma levels of inflam- ten informed consent was obtained from all the sub-
matory mediators like Interleukin-6 (IL-6) and tumor jects. The study fulfilled the STROBE guidelines for
necrosis factor (TNF) is observed. These inflammatory case-control study design.
mediators in turn induce secretion of C-reactive pro- Based on sample size calculation, it was estimated
tein (CRP) and trigger a cascade of biological and bio- to include a minimum of 804 subjects in each case and
chemical reactions leading to atherosclerosis and vas- control group. Therefore, a total of 808 cases and 808
cular thrombotic events, thereby exacerbating CHD. controls, fulfilling the inclusion criteria were included
It is also presumed that direct action of gram negative in the study.
pathogens causes platelet aggregation, alteration in the The present case-control study was conducted
host response and alter lipid metabolism thus promot- among patients with CHD and a healthy control
ing atherogenesis and thrombo-embolism leading to group. The study participants were recruited from the
ischemia (18-20). Cardiology Outpatient Department, Aarogyasri ward
Periodontal and coronary heart diseases are uni- of Yashoda Hospital, Malakpet, Hyderabad between
versal with a significant public health importance June 2016-December 2016. Permission to conduct
and relationship between the two has been identi- the study was obtained from authorities of the hospi-
fied in several studies (12, 14, 21), their association is tal. All patients aged ≥30 years; medically diagnosed
still debatable. For instance, Parker SM et al (20), in and confirmed of having CHD by a cardiologist were
their case control study concluded that patients with included in the case group. While the control group
myocardial infarction exhibited higher severity of peri- comprised of age and gender matched healthy attend-
odontitis and Simplified-Oral Hygiene Status scores ants of the patients, diagnosed to be free of the disease
compared to the control group. Likewise, Yu YH et al by a cardiologist. Other inclusion criteria for cases and
(22), also underlined that cases with periodontal dis- controls are- having minimum of 20 functional teeth
eases are at significantly higher risk for future cardio- with no history of systemic diseases affecting perio-
Acta Biomed 2021; Vol. 92, N. 1: e2021030 3
dontal status (diabetes, chronic obstructive pulmonary ble number of cases (533; 65.9%) and controls (536;
disease etc) and history of antibiotic or prophylaxis in 66.3%) had fair rating but poor score was more among
the last one month were included. Subjects not willing cases (213; 26.4%) (p=0.0001*) compared to controls
to give written informed consent were excluded from (45; 5.6%) (Table 2).
the study. Based on CPI codes, none of the subjects had
A structured questionnaire gathered information code 0, code X and code 9. A larger proportion of them
on demographics, deleterious habits and oral hygiene had a code of 3 (560; 34.7%) and code 4 (800; 49.5%).
practices. A trained calibrated single examiner per- Furthermore, it was observed that only code 4 was re-
formed oral examination using a plane mouth mirror, corded higher among cases (597; 73.9%) than controls
no. 5 Shepard’s Crook and CPI probe. Oral hygiene (203; 25.1%) and it was significant (p=0.0001*).
status was assessed using Simplified-Oral Hygiene In- On the contrary, for LOA, significantly higher
dex (OHI-S) by John C. Greene and Jack R. Vermil- number of cases had code 2 (236; 29%), code 3 (202;
lion, 1964. Community Periodontal Index (CPI) and 25%) and code 4 (50; 6.2%) compared to controls
Loss of Attachment (LOA) indices as per codes and (p=0.0001*) (Table 2).
criteria of World Health Organisation (WHO) pro- Age-wise comparison of mean DI-S scores among
forma, 1997 evaluated the periodontal status. cases and controls reported that all age groups among
cases (35-44 years=1.06±0.60, 45-54 years=1.29±0.58
Statistical analysis and 55-65 years=1.46±0.58) had significantly higher
mean scores compared to controls (p=0.0001*) for
Statistical analyses were done using Statistical the same age group. A similar situation, was noted for
Package for Social Sciences Software (SPSS version mean CI-S scores also (cases- 35-44 years=1.72±1.07,
21.0). Descriptive statistics were carried out for the 45-54 years=2.13±1.96 and 55-65 years=2.37±1.20)
demographic variables. Chi-square test, Mann- Whit- (p=0.0001*). Likewise, the mean OHI-S scores were also
ney-U test, Analysis of Variance (ANOVA) and re- significantly higher among cases compared to controls
gression analysis determined the association and com- (p=0.0001*). Higher scores among cases indicate a poor
pared the mean scores based on variables. Statistical oral hygiene status among them compared to controls.
significance was set at p≤0.05. When periodontal health status of the study pop-
ulation was considered, cases of all age groups reported
a poor periodontal health with significantly high CPI
Results and LOA scores compared to controls (p=0.0001*).
Intragroup comparison within cases and controls
The demographic details of the study population revealed that, the mean scores of all oral parameters
is described in table 1. increased significantly with increase in age. Therefore,
The majority of study population had fair Debris subjects aged 55-65 years reported significantly higher
Index- Simplified (DI-S) scores (1069; 66.1%), how- mean scores for all oral parameters in both case and
ever, higher percentage of study population had poor control group, indicating a poor oral health and peri-
scores for Calculus Index- Simplified (CI-S) (952; odontal status among them. (Table 3)
58.9%) and Simplified- Oral Hygiene Index (OHI-S) Both males and females in case group had signifi-
(905; 56%). cantly higher scores for all the oral parameters compared
Comparison among cases and controls demon- to controls (DI-S- p=0.0001*, CI-S- p=0.0001*, OHI-
strated that, a larger proportion of cases had poor scores S- p=0.0001*, CPI- p=0.0001* and LOA- p=0.0001*).
for CI-S (617; 76.4%), OHI-S (610; 75.5%) whereas Comparison based on gender within the case and
more number of controls had fair scores for the same control group demonstrated that males in each group
(CI-S=363; 44.9% and OHI-S=417; 51.6%). These had significantly higher scores for all the parameters
differences were statistically significant (p=0.0001 and except CI-S (cases- p= 0.37 and controls p=0.06) com-
p=0.0001* respectively). For DI-S scores, compara- pared to females (Table 4).
4 Acta Biomed 2021; Vol. 92, N. 1: e2021030
Tooth brush and toothpaste 678 (84) 710 (87.9) 1388 (86)
Method of cleaning
Any other 130 (16) 98 (12.1) 228 (14)
n=number of people
Acta Biomed 2021; Vol. 92, N. 1: e2021030 5
Table 2. Distribution of study population based on Simplified-Oral Hygiene Index (OHI-S), Community Periodontal Index (CPI)
and Loss of Attachment (LOA) coding criteria
n (%)
Variables Total
Cases Controls p-value
On the whole, cases reported poor oral hygiene tants with pocket depth of 4-5mm (cases- 2.36±1.38
(DI-S=1.50±0.59, CI-S=2.35±1.41 and OHI-S= and controls- 2.00±1.63; p=0.001*) and 6mm or more
3.90±2.39) and periodontal status (CPI= 3.69±0.57 (cases- 2.24±1.84 and controls- 0.51±1.09; p=0.001*)
and LOA=1.82±1.15) compared to controls (Table 5). were significantly higher among cases compared to
Based on total mean sextants scores of CPI, com- controls.
parable number of cases and controls had mean num- Contrary to the CPI mean sextant scores, cases
ber of sextants with code 1 (p=0.36). Furthermore, had significantly higher number of sextants affected
controls had significantly higher number of sextants with majority of codes (code 1=0.001*, code 2=0.001*,
affected with code 2 (cases- 0.89±1.33 and controls- code 3=0.001* and code 4=0.001*) compared to con-
2.48±1.72) (p=0.001*) whereas mean number of sex- trols. Conversely, mean number of sextants with code
6 Acta Biomed 2021; Vol. 92, N. 1: e2021030
Table 3. Comparison of mean Simplified-Oral Hygiene Index (OHI-S), Community Periodontal Index (CPI) and Loss of Attach-
ment (LOA) scores among cases and controls based on age
Mean ±S.D.
Variables p-value
Cases Controls
35-44 years 1.06±0.60 0.81±0.47 0.0001*
45-54 years 1.29±0.58 1.03±0.45 0.0001*
DI-S
55-65 years 1.46±0.58 1.28±0.53 0.0001*
p-value 0.0001* 0.0001*
35-44 years 1.72±1.07 1.29±0.75 0.0001*
45-54 years 2.13±1.96 1.89±2.33 0.0001*
CI-S
55-65 years 2.37±1.20 2.14±0.59 0.0001*
p-value 0.0001* 0.0001*
35-44 years 2.79±1.47 2.10±1.12 0.0001*
45-54 years 3.64±3.95 3.17±4.45 0.0001*
OHI-S
55-65 years 3.77±1.04 3.42±0.99 0.0001*
p-value 0.0001* 0.0001*
35-44 years 3.02±0.83 2.58±0.71 0.0001*
45-54 years 3.38±0.71 3.01±0.68 0.0001*
CPI
55-65 years 3.66±0.52 3.47±0.57 0.0001*
p-value 0.0001* 0.0001*
35-44 years 0.80±1.03 0.30±0.57 0.0001*
45-54 years 1.28±1.15 0.58±0.72 0.0001*
LOA
55-65 years 1.71±1.13 1.18±0.94 0.0001*
p-value 0.0001* 0.0001*
*statistically significant (p≤0.05)
DI-S- Debris Index- Simplified; CI-S- Calculus Index-Simplified; OHI-S- Simplified- Oral Hygiene Index;
CPI- Community Periodontal Index; LOA-Loss of Attachment; S.D.-Standard Deviation
0 was higher among controls compared to cases (cases- the disease compared to females, but after adjusting, a
2.36±218 and controls- 4.74±1.69; p=0.001*). lower association was noted (OR=0.82; p=0.84).
Risk factors education (p=0.001*), dental visit Subjects with primary (crude OR=0.60; adjust-
(0.001*), last dental visit (0.001*), history of tobac- ed OR=0.71) and high (crude OR- 0.32; adjusted
co (p=0.001*) and alcohol use (p=0.001*), method OR=0.45) school education showed significantly lesser
of cleaning (p=0.02*) and frequency of cleaning association with CHD.
(p=0.001*) showed a significant association with CHD. Considering the dental visit, subjects with no his-
In the present study, subjects aged 55-65 years tory of dental visit were at 1.63 times higher risk for
were at 1.01 times higher risk for developing CHD developing CHD compared to those with history of
compared to other age groups. However, after adjust- dental visit. This finding was persistent even after ad-
ing for other variables, age group 55-65 years reported justing for other variables, wherein, subjects without
to have lower and insignificant association (Odds Ra- history of dental visit were at higher odds (OR=1.62)
tio (OR)=0.28; p=0.99). of developing CHD.
A similar situation was observed when associa- However, of last dental visit reported to have a
tion between gender and CHD was evaluated, wherein lower association with CHD (OR= 0.54 and adjusted
males were at higher odds (OR=1.02) of developing OR=0.59).
Acta Biomed 2021; Vol. 92, N. 1: e2021030 7
Table 4. Comparison of mean Simplified-Oral Hygiene Index (OHI-S), Community Periodontal Index (CPI) and Loss of Attach-
ment (LOA) scores among cases and controls based on gender
Mean ±S.D.
Variables p-value
Cases Controls
Males 1.60±0.61 1.09±0.53 0.0001*
DI-S Females 1.33±0.53 0.89±0.44 0.0001*
p-value 0.0001* 0.0001*
Males 2.38±1.56 1.78±1.77 0.0001*
CI-S Females 2.30±1.11 1.70±1.37 0.0001*
p-value 0.37 0.06
Males 3.98±2.25 2.92±2.44 0.0001*
OHI-S Females 3.78±2.62 2.79±3.93 0.0001*
p-value 0.0001* 0.0007*
Males 3.73±0.53 3.04±0.77 0.0001*
CPI Females 3.60±0.62 2.85±0.69 0.0001*
p-value 0.01* 0.0006*
Males 1.95±1.17 0.72±0.86 0.0001*
LOA Females 1.59±1.09 0.47±0.66 0.0001*
p-value 0.0001* 0.0003*
*statistically significant (p≤0.05)
DI-S- Debris Index- Simplified; CI-S- Calculus Index-Simplified; OHI-S- Simplified- Oral Hygiene Index
CPI- Community Periodontal Index; LOA-Loss of Attachment; S.D.- Standard Deviation
Table 5. Comparison of total mean scores of Simplified-Oral Subjects with habit of tobacco and alcohol use
Hygiene Index (OHI-S), Community Periodontal Index (CPI)
and Loss of Attachment (LOA) among cases and controls
were at 2.26 times and 1.83 times respectively, higher
risk of developing CHD compared to non tobacco and
Mean ±S.D. alcohol users. Conversely, after adjusting for other var-
Variables p-value
Cases Controls iables, both the risk factors showed lower association
(tobacco user- adjusted OR=0.89 and alcohol user-
DI-S 1.50±0.59 1.01±0.51 0.0001*
adjusted OR=0.97) compared to non-users.
Cleansing of teeth using other hygiene aids (like
CI-S 2.35±1.41 1.75±1.64 0.0001*
neem sticks, miswak etc) showed lower risk of devel-
oping CHD (OR=0.71), however upon adjusting, it
OHI-S 3.90±2.39 2.87±3.07 0.0001* showed a 1.15 times higher risk for CHD.
Lower frequency of teeth cleaning among sub-
CPI 3.69±0.57 2.97±0.74 0.0001* jects was associated with 3.38 times higher risk for
CHD (OR=3.38; adjusted OR=2.54).
LOA 1.82±1.15 0.63±0.80 0.0001* Taking oral hygiene into account, poor oral hy-
giene showed significantly higher risk of developing
*statistically significant (p≤0.05)
CHD compared to those with good, fair oral hygiene
DI-S- Debris Index- Simplified; CI-S- Calculus Index-Sim-
plified; OHI-S- Simplified- Oral Hygiene Index; CPI- Com- (OR=5.2). Even after adjusting for other variables,
munity Periodontal Index; LOA-Loss of Attachment; subjects with poor oral hygiene were at higher odds of
S.D.- Standard Deviation developing the disease (adjusted OR=2.30) (p=0.001*).
Similarly, significant association was found be-
8 Acta Biomed 2021; Vol. 92, N. 1: e2021030
Table 6 - Logistic regression analysis of variables with Coronary Heart Disease (CHD)
Education High school 0.32 (0.24 – 0.45) 0.45 (0.30- 0.67) 0.001*
University Ref. Ref.
Yes Ref. Ref.
Dental visit 0.001*
No 1.63 (1.31 – 2.02) 1.62 (1.22-2.16)
6 months- 1 year Ref. Ref.
Last Dental visit 0.001*
>1 year 0.54 (0.37 – 0.78) 0.59 (0.36- 0.97)
No Ref. Ref.
History of tobacco use 0.001*
Yes 2.26 (1.78 – 2.86) 0.89 (0.62- 1.30)
No Ref. Ref.
History of alcohol use 0.001*
Yes 1.83 (1.40 – 2.41) 0.97 (0.64- 1.47)
However, after adjusting the risk of association re- of hospital stay which additionally could hamper their
duced (adjusted OR=6.46) (p=0.001*) (Table 6). oral hygiene practices (31). The overall higher sig-
nificant mean scores of DI-S (1.50±0.59; p=0.0001*),
Discussion CI-S (2.35±1.41; p=0.0001*) and OHI-S (3.90±2.39;
p=0.0001*) among cases also support the aforemen-
A significant role of periodontal diseases in the tioned results.
CHD is evident from the findings of the present study. A remarkable observation of the study was that
In order to fulfil the aim of the present study, OHI-S pocket depth of ≥6 mm was observed more among
Index by John C Greene and Jack R Vermillion, was cases, while significantly higher percentage of con-
used since the criteria are clear and examinations can trols had bleeding, calculus and pocket depth of 4-6
be carried out quickly (25). The periodontal status mm (p=0.0001*). In addition, significant percentage
was assessed using CPI and LOA index as per WHO of cases had LOA of ≥6 mm, compared to controls
codes and criteria (1997) as it is simple, reproducible (p=0.001*). These results further rationalize the sig-
and shows international uniformity (26). nificant difference in the CPI (p=0.0001*) and LOA
A total of 1616 (808-cases and 808-controls) sub- (p=0.0001*) mean scores among cases (3.69±0.57 and
jects matched for age and gender were included in the 1.82±1.15, respectively) and controls (2.97±0.74 and
study. Similar studies in Karnataka (19), (54.97±7.97 0.63±0.80, respectively), with cases showing poor peri-
years) and Gujarat (20), (54.3±11.01 years) reported odontal status. On the other hand, research by Johans-
higher mean age compared to the cases in the present son SC et al among Swedish population, reported a
study (48.30±7.73 years). This shows a change in the significantly higher percentage of sites with bleeding
disease pattern and emphasizes the need to screen in- on probing (p=0.009*) and periodontal pockets with
dividuals of different and younger age groups to detect 4-6mm probing depth (p=0.007*) among patients with
disease at an early stage. In this group of Indian popu- CHD compared to controls (32). Conversely, results
lation, both periodontitis and CHD showed male pre- of a similar Indian study were in accordance with the
ponderance. Similar findings were reported by Greets present study wherein cases had significantly (p≤0.05*)
et al (27), among Hongkong population (cases-85.2% higher mean CPI and LOA scores indicating a poor
males). periodontal status among them (19). Another nota-
An important determinant of CHD and poor ble finding of the study was, the cases had significant
oral health is socioeconomic status (SES), with greater more number of mean sextants with pocket and LOA
morbidity and mortality among people of lower SES of ≥4mm (p≤0.05). In congruence were the results of a
(28). Hence, to minimise this difference, attempt was study by Parker et al, where cases had significant poor
made to include both cases and controls from the Aar- oral hygiene scores and higher mean sextants with CPI
ogyasri ward (lower SES) of the hospital. Presence of code 3,4 and LOA code 2,3 (20).
traditional risk factors like lower frequency of dental Prevalence of debris, calculus, deeper pockets and
visit, tobacco and alcohol use, non-usage of tooth brush severe loss of attachment among cases is indicative of a
and toothpaste and lower frequency of tooth brushing long standing and established form of periodontal dis-
was higher among cases compared to controls which ease, validating its role as a risk factor for CHD (20).
was akin to other studies conducted in other parts of These pockets act as ideal niche for bacterial lodge-
India (19, 27), Finland (29), and Scotland (30). ment, resulting in bacteraemia and inflammation. This
Mackenzie et al reported that presence of cal- proves that, severe periodontitis is associated with
culus can lead to alveolar bone loss and arterioscle- greater thickness of carotid arterial lining, support-
rosis (17). Poor oral hygiene among cases was seen ing its role in formation of atheromas and consequent
compared to controls in this study (p=0.0001*). This coronary heart diseases (20, 30, 31, 33).
could be because of lower frequency of dental visit When strength of association between oral risk
(>1 year- cases=25.5%) and tooth cleaning (brushing factors and occurrence of CHD was accounted (i.e.,
once a day- cases= 98.6%) or due to longer duration among cases), poor oral hygiene and periodontal health
10 Acta Biomed 2021; Vol. 92, N. 1: e2021030
showed a significantly (p≤0.05) higher risk for CHD. the population is suffering with periodontitis. Hence,
Zanella et al, reported that age and gender were asso- suitable preventive and treatment strategies are recom-
ciated with the presence of CHD (14). On the con- mended to combat the epidemic of CHD.
trary, the present study did not confirm these findings, Conflict of interest: Each author declares that he or she has no
commercial associations (e.g. consultancies, stock ownership, equity
which could be due to variation in the inclusion crite- interest, patent/licensing arrangement etc.) that might pose a con-
ria. Further, the multivariate logistic regression analyses flict of interest in connection with the submitted article
confirmed the cumulative effect of other potential risk
factors like lower frequency of dental visit and brush-
ing, tobacco and alcohol habits on the incidence of the References
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