ISSN 0103-6440

Brazilian Dental Journal (2015) 26(1): 33-38

http://dx.doi.org/10.1590/0103-6440201300117

Is There a Relationship Between

Periodontal Disease and Causes of
Death? A Cross Sectional Study
Zuhair S. Natto1,2, Majdi Aladmawy1, Mohammed Alasqah1, Athena Papas3

The aim of this study was to evaluate whether there is any correlation between
periodontal disease and mortality contributing factors, such as cardiovascular disease
and diabetes mellitus in the elderly population. A dental evaluation was performed by a
single examiner at Tufts University dental clinics for 284 patients. Periodontal assessments
were performed by probing with a manual UNC-15 periodontal probe to measure pocket
depth and clinical attachment level (CAL) at 6 sites. Causes of death abstracted from
death certificate. Statistical analysis involved ANOVA, chi-square and multivariate logistic
regression analysis. The demographics of the population sample indicated that, most were
females (except for diabetes mellitus), white, married, completed 13 years of education
and were 83 years old on average. CAL (continuous or dichotomous) and marital status
attained statistical significance (p<0.05) in contingency table analysis (Chi-square for
independence). Individuals with increased CAL were 2.16 times more likely (OR=2.16,
95% CI=1.473.17) to die due to CVD and this effect persisted even after control for
age, marital status, gender, race, years of education (OR=2.03, 95% CI=1.35-3.03). CAL
(continuous or dichotomous) was much higher among those who died due to diabetes
mellitus or out of state of Massachusetts. However, these results were not statistically
significant. The same pattern was observed with pocket depth (continuous or dichotomous),
but these results were not statistically significant either. CAL seems to be more sensitive
to chronic diseases than pocket depth. Among those conditions, cardiovascular disease
has the strongest effect.

Introduction

Periodontal diseases contains multiple infectious

pathogens that can induce inflammation to the surrounding
soft or/and hard tissues, a bacterial niche combines mixed
gram positive (early colonizers) and negative (late colonizers)
bacteria. When the bacterial infection is combined with a
susceptible host the periodontal breakdown is initiated (1).
Factors that induce inflammation include the bacterial
biofilm, bacterial by products, e.g. lipopolysaccharides, and
host immune interactions with the bacterial products. The
host immune cell receptors (pattern recognition receptors,
PRR) can recognize the presence of bacterial pathogens
by pathogen-associated molecular patterns (PAMP),
which bind to the host receptors. When this interaction
between PAMPs and PRRs occurs, immune cells produce
pro-inflammatory cytokines to the site associated with
the presence of bacteria (2). The host immune system is
mainly activated for a protective function, but sometimescollateral damage to non-pathologic cells does occur.
The severity of the periodontal breakdown caused by
inflammation depends on the balance between the bacterial
virulence and the host immune reaction (2).
The host and the microbial challenge interaction can be
further influenced by a variety of systemic conditions one
of this conditions is cardiovascular disease (CVD). A previous

1Department

of Periodontology,
Tufts University School of Dental
Medicine, Boston, MA, USA
2Department of Dental Public Health,
King Abdualziz University, School
of Dentistry , Jeddah ,Saudi Arabia
3Division of Dental Public Health
Research and Oral Medicine,
Tufts University School of Dental
Medicine, Boston, MA, USA
Correspondence: Dr. Zuhair Natto,
One Kneeland Street, Boston, MA
02111, USA. Tel: +1-909-702-4119.
e-mail: zuhair.natto@tufts.edu

Key Words: periodontal

disease, mortality, diabetes,
cardiovascular disease, elderly.

study indicated an association between periodontitis and

CVD, but the observed association was modest. People
with periodontitis were at a greater risk of coronary heart
disease, when compared with healthy controls. The number
of remaining teeth was reported to have an association
with coronary heart disease. It was stated that subjects with
less than 10 remaining teeth had a high risk of coronary
heart disease when compared to subjects that had more
remaining teeth.
A cross-sectional study for patients with periodontitis
found that coronary heart disease had a high prevalence
with periodontitis patients when compared to healthy
subjects (4). Periodontitis can be considered as a risk
factor for coronary heart disease, but prospective studies
are needed to determine if there a causation between
both diseases.
Diabetes mellitus should be considered as a systemic
condition that interferes with relationship between
the virulent microbial invasion and the host response.
Diabetes mellitus is a metabolic disorder having a reduced
function, or lack of function from the beta cells in the
islets of Langerhans present in the pancreas, this leads to
high concentrations of blood glucose levels in the blood
serum and presence of sugar in urine (5). Diabetes is one
of the prevalent diseases among the metabolic disorders,

Braz Dent J 26(1) 2015

the incidence of diabetes around the world continues

to increase (6). As people get older their susceptibility
to diabetes increases, which is a similar finding for
periodontitis and age (7).
Some reports termed periodontitis as the Sixth
Complication of diabetes (8). There is no conscience
relating diabetes to the initiation of periodontitis. Different
opinions debating the correlation between diabetes and
periodontitis are still ongoing.
The earliest report of an association between
periodontitis and different causes of mortality was done
by DeStefano et al. (9) After 14 years of follow-up in
the NHANES 1 study, they reported that subjects with
periodontitis had a 50% increase in mortality risk (9).
The aim of the current study was to evaluate if there
is any relationship between periodontal disease and major
causes of death such as hypertension and diabetes mellitus
in the studies population.

Z.S. Natto et al.

Material and Methods

This study recruited volunteers from the Boston and its

is surrounding areas (57% from Tufts Geriatric Outreach
program and 43% from Tufts dental clinics). The Tufts
Geriatric Outreach program was conducted at 30 sites in
the greater Boston area, and included: dental screening,
nutritional screening and educational sessions for elderly
people.
Selection criteria for enrollment in the study included
being a local Boston area resident, presence of six or
more teeth, being free from terminal illness, endocrine
disease that would affect nutrition; recent unexplained
weight loss; and active alcoholism, and being willing and
able to complete a 3-day food diary in a predetermined
manner. Each participant signed a consent form agreeing
to participate in the study. The Human Investigation Review
Committee of Tufts University approved conduction of
the study
Clinical oral examinations were done at Tufts University
School of Dental Medicine by a single examiner using
artificial light, explorer, mirror and air syringe. The teeth
were dried before examination to assess the dental
decay. The coronal and root caries and periodontal
measurements were made on all subjects according to
the diagnostic criteria used in the US adult survey. Third
molars were excluded from examination. Training and
calibration sessions to standardize caries and periodontal
measurements were held semi-annually. Questionnaires
on health knowledge, attitudes and behavior, and general
and medication history were also administered. Causes of
death abstracted from death certificate.
It was expected to have 90% power based on: OR of
2.14 for CVD group compared with the group still living,
34

a sample size of 284, and =0.05. The sample size was

calculated using G*power software, version 3.1 (University
Kiel, Germany).
Descriptive statistics were expressed as meanSD or
N(%). The values of each variable were compared between
groups, according to the cause of death (cardiovascular,
diabetes, unknown cause of death) or still living. The
Shapiro-Wilk test was used to evaluate normality. Analysis
of variance and chi-square were applied.
The odds ratios of developing recession (continuous or
categorical) or pocket depth (continuous or categorical)
adjusting for significant variables in reduced model or all
variables in full model, comparing CVD, diabetic or unknown
cause of death to still living group, were estimated by the
use of logistic regression. Analyses were performed using
SAS software v. 9.3 (SAS Institute, Cary, NC, USA).

Results

This study compared the demographics and different

causes of death (Table 1). The demographics of the study
population indicated that, most of the sample was female
(except for diabetes mellitus), white, married, with 13
years of education, and 83 years old on average. They
had deeper CAL (3 mm) and shallower pocket depth (<3
mm). CAL (continuous or dichotomous) and marital status
attained statistical significance (p<0.05) in contingency
table analysis (chi-square test for independent samples).

Clinical Attachment Level (CAL) and Cause of Death

In a logistic regression model with cause of death (CVD,
diabetes mellitus, or died out of state) versus still living
group as the outcome variable and with marital status
and CAL (continuous in the first model and categorical in
the second one) as covariates, we found that individuals
with increased CAL were 2.16 times more likely (OR 2.16,
95% CI 1.473.17) to have mortality due to CVD when
compared to individuals that had normal CAL. This effect
persisted even after control for age, marital status, gender,
race, and years of education. We have the same results
with dichotomous CAL, which was 2.7 times for marital
status adjusted (OR 2.70, 95% 1.32-5.53) and 3.25 times
for multivariable adjusted model (OR 3.25, 95%1.44-7.30).
CAL (continuous or dichotomous) was much higher among
those who died due to diabetes mellitus or out of state.
However, these results were not statistical significant.

Pocket Depth and Cause of Death

In further analyses of logistic regression model (Table
3) with the same outcome variable with marital status
and pocket depth (PD) (continuous in the first model and
categorical in the second one) as covariates, we found
that pocket depth (continuous or dichotomous) was much

Braz Dent J 26(1) 2015

higher among those who died due to CVD, diabetes mellitus

or out of state compared with still living. However, these
results were not statistically significant.

Discussion

The main finding of the present study was that

83-year-old individuals showed an association between

increased CAL and CVD morbidity by 2.16 times compared

with individuals with CVD without CAL and are still alive,
when adjusted for age, marital status, gender, race, year
of education. The same findings were present for diabetic
patients but the statistical analysis showed that it was not
significant, probably due to the small sample size of diabetic
patients. Probing depth showed results that were higher

Table 1. Descriptive statistics of the study sample

Variable

CVD mortality
N= 60

Diabetes
mortality N=50

Out of the state

mortality N=26

Individuals that
are alive N=148

p value

Age (mean SD)

82.9010.74

81.997.54

85.147.78

82.6414.70

0.758

Male

27(47.4)

28(57.1)

12(46.2)

54(38.9)

0.159

Female

32(52.6)

21(42.9)

14(53.8)

85(61.1)

48(90.6)

43(87.8)

26(100)

123(89.8)

5(9.4)

6(12.2)

0 (0.0)

14(10.2)

Single

9(15.8)

6(12.2)

4(15.4)

39(28.5)

Married

28(49.1)

25(51.1)

12(46.2)

74(54.0)

Others**

20(35.1)

18(36.7)

10(38.4)

24(17.5)

Buccal

3.761.29

3.501.21

3.350.88

3.200.95

0.007*

Lingual

3.521.07

3.301.17

3.030.73

2.920.91

0.001*

Distal

3.881.04

3.671.06

3.540.82

3.320.97

0.002*

Mesial

3.871.08

3.500.81

3.500.73

3.320.83

0.001*

Total

3.791.07

3.500.85

3.350.72

3.190.82

0.000*

3 mm

45(75.0)

31(62.0)

17(65.4)

79(53.4)

0.033*

< 3 mm

15(25.0)

19(38.0)

9(34.6)

69(46.6)

Buccal

1.630.36

1.600.55

1.500.33

1.590.38

0.604

Lingual

1.770.54

2.260.57

1.680.40

1.730.45

0.387

Distal

2.410.58

2.280.64

2.380.63

2.340.58

0.608

Mesial

2.410.56

1.850.48

2.290.49

2.410.59

0.466

Total

2.060.42

2.010.45

1.960.42

2.020.43

0.758

3 mm

1(1.7)

1(2.0)

1(3.9)

6(4.1)

0.802

<3 mm

59(98.3)

49(98.0)

25(96.1)

142(95.9)

12.952.74

12.902.75

13.802.60

13.6814.70

Gender, n(%)

Race, n(%)

African American

0.334

Marital status, n(%)

0.015*

Clinical attachment level (CAL) (mean SD)

Clinical attachment level (CAL) n(%)

Pocket depth (mean SD)

Pocket depth (mean SD)

Year of education (meanSD)

0.104

*p value <0.05. p value obtained from either analysis of variance (ANOVA) for continuous variables, and chi-square for categorical variables. ** other
includes: divorced and widow.
35

Periodontal disease and causes of death

White

Braz Dent J 26(1) 2015

Z.S. Natto et al.

for individuals that had mortality with CVD or diabetes

in comparison with patients that are still alive, but as
mentioned it was not statistically significant.
Death was the final endpoint, causes of death were
taken from the death certificate. The classification of the
different categories was made before obtaining information
on the patients. Population sample had both males and
females (whites and African Americans). The analysis was
adjusted for a wide range of relevant factors; however, we
cannot exclude residual confounding factors as a possible
explanation for the association observed in this study.
This study is unique in that it looked into the relationship
between different periodontal parameters and the cause
of death for diabetic and CVD patients. Strippoli et al (10),
reported the association between periodontitis (in patients
on hemodialysis), and mortality as an outcome, they found,
that periodontitis might be associated with mortality in
dialysis patients. The reviewed for well-designed, larger
studies to look into the association between oral health
and mortality (10), which is in agreement with the results
of the present study.

Reports of an association between periodontitis

and mortality was investigated by Linden et al (11) in a
prospective study having a group of senior West European
men from Belfast, Northern Ireland. During a 9-year follow
up period that out of the 152 patients that died, 37 of them
had CAL less than 1.8 mm while 73 had CAL of more than
2.6 mm, they concluded that the group with severe loss of
periodontal attachment were at an increased risk of death
compared with individuals with lower loss of periodontal
attachment (11).
A prospective study in China reported an association
between periodontitis and CVD (12). However, they used PD
as the main variable and found that there is an association
between PD and CVD and all-cause mortality in men with
ages between 30-64 years. Another observation found,
was subjects that were older than 64 years did not show
statistical significance between periodontitis and CVD (12).
Periodontitis, which affects tooth structures if not
treated, would ultimately lead to tooth loss and a decrease
in health quality due to inadequate chewing of food (13).
Aida et al. (14) evaluated the oral health in old Japanese

Table 2. Association of clinical attachment level (CAL, continuous in model 1 and categorical in model 2) in several systemic diseases compared with
individuals that are still living using multivariable adjusted models
OR (95% CI) CVD mortality vs.
individuals that are still living

OR (95% CI) DM mortality vs.

individuals that are still living

OR (95% CI) Out of state mortality

vs. individuals that are still living

Married

2.74(0.88-8.51)

2.24(0.74-6.76)

1.40(0.39-5.04)

Others**

5.77(1.64-20.32)*

5.56(1.61-19.19)*

3.60(0.88-14.77)

0.99(0.95-1.02)

0.98(0.95-1.01)

1.00(0.96-1.05)

0.73(0.34-1.56)

0.44(0.20-0.98)*

0.63(0.25-1.59)

African American

0.73(0.20-2.68)

1.23(0.38-3.98)

Year of education

0.94(0.80-1.10)

0.91(0.77-1.07)

1.02(0.83-1.25)

2.03(1.35-3.03)*

1.46(0.93-2.31)

1.24(0.70-2.21)

3 mm

3.25(1.44-7.30)*

1.15(0.54-2.46)

1.37(0.54-3.52)

< 3 mm

Variable
Marital status
Single

Age
Gender
Male
Female
Race
White

CAL
Model 1
Total
Model 2

OR=odds ratio; CI=confidence interval. Adjusted for Age, Marital status, gender, race, year of education. In addition to the main exposure which is
clinical attachment level as a continuous or categorical. *p value <0.05. ** other includes: divorced and widow.
36

patients and mortality relationship, and found that CVD

and respiratory disease mortality were significant (14),
which agrees with the current study.
Thorstensson et al. (15) studied oral health relation to
survival in old population of >80 year-old Swedish patients,
which corresponds to the same age group in our study.
The authors reported that oral health was significantly
associated with subsequent survival in a sample of 80-yearold individuals (15).
Oliveira et al. (16) examined a population younger than
50 years of age in Scotland and reported on the oral hygiene
maintenance association with risk of CVD. The authors
found that inadequate oral hygiene was associated with a
high risk of developing CVD, and mild inflammation (16).
There are some limitations associated with our study;
this is a convenience sample and the sample distribution
is not representative for the United States population,
the sample is not chosen at random, the inherent bias in
convenience sampling means that inability to generalize
our results to the US population. Population size is small
for such epidemiological studies. The present research was

cross-sectional study, this gives a limitation on applying

causality between the variables being tested. We plan to
report on a longitudinal study having a larger sample size
representing the area in the future.
Literature has shown several studies that support our
results in that higher mortality rates were associated
with subjects that have CAL with CVD when compared
with periodontally healthy patients with CVD (17,18).
Our findings indicate that treatment should be given
to the elderly population to prevent attachment loss
around the teeth, as it is observed to increase mortality
rates among individuals with CVD. Attachment loss is
associated with bacterial deposition on both hard and soft
tissues surrounding the tooth. Bacterial virulence can be
controlled with regular maintenance visits to the dentist or
hygienist. Patient should be educated on the importance of
maintaining their CAL, as it can be of valuable information
for them to increase their quality and longevity in life.
There should be further research in this topic to identify
how CVD is associated with periodontitis.
People that had mortality due to CVD have a higher CAL

Table 3. Association of pocket depth (PD, continuous in model 1 and categorical in model 2) in several systemic diseases compared with individuals
that have the same disease but are still living using multivariable adjusted models
OR (95% CI) CVD mortality vs.
individuals that are still living

OR (95% CI DM mortality vs.

individuals that are still living

OR (95% CI) Out of state mortality

vs. individuals that are still living

Married

1.98(0.72-5.43)

2.29(0.79-6.62)

1.33(0.37-4.78)

Others**

4.83(1.56-14.94)*

6.69(2.00-22.30)*

3.66(0.90-14.93)

0.99(0.96-1.02)

0.98(0.95-1.01)

1.01(0.97-1.05)

0.58(0.28-1.18)

0.36(0.17-0.76)*

0.62(0.25-1.55)

African American

0.80(0.24-2.68)

1.39(0.43-4.50)

Year of education

0.89(0.77-1.03)

0.88(0.76-1.02)

1.01(0.83-1.24)

1.15(0.51-2.59)

0.81(0.36-1.82)

1.11(0.35-3.58)

3 mm

0.36(0.04-3.24)

1.79(0.17-18.97)

<3 mm

Variable
Marital status
Single

Age
Gender
Male
Female
Race
White

PD
Model 1
Total
Model 2

OR, odds ratio; CI, confidence interval. Adjusted for Age, Marital status, gender, race, year of education. In addition to the main exposure which is
clinical attachment level as a continuous or categorical. *p value < 0.05. ** other includes: divorced and widow.
37

Periodontal disease and causes of death

Braz Dent J 26(1) 2015

Braz Dent J 26(1) 2015

loss compared with people who are still living with CVD.
PD, in contrast, did not change between the two groups.
In addition, subjects with Diabetes mellitus and people
that died out of Massachusetts had the same pattern of
attachment lose but the results were not significant.

Z.S. Natto et al.

Resumo
O objetivo deste estudo foi avaliar se existe relao entre doena periodontal
e fatores de mortalidade como, por ex., doenas cardiovasculares e diabetes
melitus, numa amostra de pessoas idosas. Um nico examinador fez
avaliao dentria em 284 pacientes. As avaliaes periodontais foram
feitas com sonda manual UNC-15 para medir profundidade da bolsa
e nvel de insero clnica em 6 pontos. As causas dos bitos foram
obtidas das certides. Para anlise estatstica utilizou-se ANOVA, teste
do qui-quadrado e anlise de regresso logstica multivariada. Os dados
demogrficos indicaram que a maioria era constituda de mulheres (exceto
para diabetes melitus), leucodermas, casadas, completaram 13 anos de
escolaridade e mdia de 83 anos de idade. O nvel de insero clnica
(contnuo ou dicotomizado) e estado civil tiveram significncia estatstica
(p<0,05) na anlise das tabelas de contingncia (qui-quadrado para
independentes). O nvel de insero clnica foi 2,16 vezes mais provvel
causa de bito (OR=2,16; 95%CI 1,473,17) por doena cardiovascular
que o grupo dos sobreviventes e este efeito persistiu mesmo depois de
controlados idade, estado civil, sexo, raa e anos de escolaridade (OR=2,03,
95%CI 1.35-3.03). O nvel de insero clnica (contnuo ou dicotomizado)
foi muito maior entre os que morreram por diabetes melitus ou fora do
estado de Massachusetts, mas estes resultados no foram estatisticamente
significantes. O mesmo ocorreu com a profundidade da bolsa gengival
(contnua ou dicotomizada), mas estes resultados tambm no foram
estatisticamente significantes. Aparentemente a insero clnica mais
afetada pelas doenas crnicas em comparao com a profundidade da
bolsa. Entre estas doenas, as cardiovasculares tm efeito mais forte.

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Received June 6, 2014

Accepted December 13, 2014