J Clin Periodontol 2013; 40: 118124 doi: 10.1111/jcpe.

12033

Association of internal exposure

of cadmium and lead with
periodontal disease: a study of
the Fourth Korean National
Health and Nutrition Examination
Survey

Young-Soon Won1, Ji-Hyun Kim2,

Young-Soo Kim3 and
Kwang-Hak Bae4,5
1

Department of Dental Hygiene, Byuksung

College, Gimje, Korea; 2Department of
Preventive Medicine, College of Medicine,
Graduate School of Public Health, Korea
University, Seoul, Korea; 3Department of
Clinical Preventive Dentistry and Oral
Biostatistics, Dental department in Guro
Hospital, Korea University Medical Center,
Seoul, Korea; 4Department of Preventive and
Public Health Dentistry, School of Dentistry,
Seoul National University, Seoul, Korea;
5
Dental Research Institute, School of
Dentistry, Seoul National University, Seoul,
Korea

Won Y-S., Kim J-H., Kim Y-S., Bae K-H. Association of internal exposure of
cadmium and lead with periodontal disease: a study of the Fourth Korean National
Health and Nutrition Examination Survey. J Clin Periodontol 2013; 40: 118124.
doi: 10.1111/jcpe.12033.

Abstract
Aims: This study was performed to examine the association of the internal
exposure of cadmium and lead with periodontitis in a representative sample of
adults, who were involved in the Fourth Korea National Health and Nutrition
Examination Survey (KNHANES).
Materials and methods: One thousand nine hundred and sixty-six subjects over the
age of 19 who participated in KNHANES were examined. Cadmium (Cd) and lead
(Pb) exposure were grouped into three categories: low (<25th percentile), middle
(25th75th percentile) and high (  75th percentile). The periodontal status was
assessed by the Community Periodontal Index. The multivariate logistic regression
analysis was performed to get the adjusted odds ratio (OR), and subgroup analysis
was also performed. All analyses considered a complex sampling design.
Results: The multivariate logistic regression analysis revealed associations of Cd
with periodontitis. Subjects with a high Cd had a 1.57 (95% CI: 1.03-2.38) times
higher OR for periodontitis than those with a low Cd. In the subgroup analysis,
the association of Pb and Cd with periodontitis was different according to the
strata of gender and smoking.
Conclusions: High Cd could be associated with periodontitis in females and current smokers, and middle Pb showed associations in females and non-smokers
among a representative sample of adults in Korea.

Conflict of interest and source of funding statement

The authors declare no conflicts of interest related to this study. The study was
self-supported, but the Korea Center for Disease Control and Prevention provided
the data of the Fourth Korea National Health and Nutrition Examination Survey
to be used in the study.

118

Key words: association; cadmium; Korean

National Health and Nutrition Examination
Survey; lead; periodontal disease
Accepted for publication 13 October 2012

Cadmium (Cd) and lead (Pb) are

known to exist commonly in our
daily environment as hazardous
heavy metals, and to flow into the
human body occupationally and
environmentally, thereby influencing
2012 John Wiley & Sons A/S

Cadmium and lead with periodontitis

ones causing influence upon health. Cd
is being widely used in coating &
plating, battery making, dyes, polyvinyl
chloride stabilizers and cadmium alloys
(IARC 1993). Pb is often used as a
painting material. Both Cd and Pb are
extensively used in battery storage, lead
melting, lead casting, printing, soldering
and lead glass work (IARC 1980).
Cd and Pb can cause serious
adverse health effects, including kidney disease and poor bone remodelling (Dye & Dillon 2010). Most
importantly, the fact that exposure
to Cd drops bone density and leads
to osteoporosis has been clarified
and factualized by research (Alfven
et al. 2000, Akesson et al. 2006,
Gallagher et al. 2008).
Periodontitis is a chronic and
long-lasting low-grade inflammatory
disease (Li et al. 2009) that leads to
a breakdown of the connective tissue
and bone that anchors the teeth to
the jaws (Williams 1990). Periodontal disease is one of the most common chronic diseases in the world
and occurs in at least 35% of the
American population (Albander
et al. 1999). In Korea, the prevalence
of periodontal disease is 30.7%
among adults (Korea Center for Disease Control and Prevention & Ministry of Health and Welfare 2008).
As for the occurrence of periodontal disease, it is a disease that is
not caused by one risk element, but is
formed and developed by complex risk
factors (Van Dyke 2005). However,
some research has been reported
recently suggesting that Cd and Pb may
have an effect on the cause of periodontal disease among other diverse causes
(Dye et al. 2002, Saraiva et al. 2007,
Arora et al. 2009a, b).
A previous study concluded that
environmental exposure to Cd, which
was measured by the concentration
of Cd in urine, had a correlation with
periodontal disease in American
adults (Arora et al. 2009a). According to a study that was carried out in
America, there might be a relationship between Pb and periodontal
disease in men and women (Saraiva
et al. 2007). In addition, the study
reported that there was a strong
correlation between the loss of the
alveolar bone and a high concentration of Pb (Dye et al. 2002). Up to
now, however, related research is
lacking. There has not been a nationwide and representative study on the
2012 John Wiley & Sons A/S

association of Cd and Pb with periodontitis in Asia.

Therefore, this study was performed to examine the association of
the internal exposure of Cd and Pb
with periodontitis in a representative
sample of adults who were involved
in the fourth Korean National
Health and Nutrition Examination
Survey (KNHANES).

Materials and Methods

Study design and subject selection

The data include a subset of the

fourth KNHANES conducted in
2009 by the Korea Center for Disease Control and Prevention. The
sampling protocol for the KNHANES was designed to involve a
complex, stratified and multistage of
probability-cluster survey of a representative sample of the non-institutionalized civilian population of Korea.
The survey was performed by the
Korean Ministry of Health and
Welfare. The target population of the
survey included all non-institutionalized
civilian Korean individuals aged 1 year
or older. The survey employed multistage stratified probability sampling
units based on geographical area, gender and age, which were determined
based on the household registries of the
2005 National Census Registry, the
most recent 5-year national census in
Korea. Using the 2005 census data, 200
primary sampling units were selected
across Korea. The final sample set for
KNHANES included 4600 households.
In the Korean National Health and
Nutrition Examination Survey, there
were 10,533 participants. Among
these people, 7095 aged 19 years and
over have had a periodontal examination. Among them, the number of
the subjects who were measured Cd
and Pb in blood was 1966, which
was the number of the finally analytical subjects. A detailed description
of the sampling was described in the
KNHANES report (KCDC (Centers
for Disease Control) 2009). The
power of this study to detect the
association of periodontitis with Pb
and Cd was 0.87 and 0.79, respectively, using the equation of power
estimation with 1.5 of odds ratio
and 1.56 of design effect of complex
sampling (Wang et al. 2002, Lohr
2010).

119

Clinical variables

Cadmium and Lead

Cd and Pb exposure was measured
by the whole blood level (lg/dL, lg/
L), which was analysed with 1 ml
sample of blood from the subject
based on the standard addition method
using the flameless atomic absorption
spectrometer-graphite furnace (Korea
Center for Disease Control &
Prevention 2010a, b). The plasma
concentration of Cd and Pb is
divided into three categories: low
(<25th percentile, 1.7289 lg/dl and
0.6689 lg/l), middle (25th-75th percentile) and high (  75th percentile,
3.04 lg/dl and 1.467 lg/l).
Periodontitis
The WHO community periodontal
index (CPI) was used to assess periodontitis. Periodontitis was defined
as a CPI greater than or equal to
code 3, which indicates that at
least one site had a > 3.5 mm (code
4 >5.5 mm) pocket. The index
tooth numbers were 11, 16, 17, 26,
27, 31, 36, 37, 46 and 47.
A CPI probe that met the WHO
guidelines was used (World Health
Organization 1997). The mouth was
divided into sextants. Approximately,
20 g probing force was used. In 2009
KNHANES, 13 trained dentists examined the periodontal status of the
subjects. The inter-examiner mean of
Kappa value was 0.75 (0.530.94)
(Korea Center for Disease Control &
Prevention 2010a, b).
Covariates
The socio-demographic variables
included gender, age, household
income and educational level. Household income was the family income
adjusting for the number of family
members. The educational level was
assessed by highest diploma.
The oral health behaviours
included use of dental floss and
inter-proximal toothbrush. As health
behaviours, alcohol consumption
experience, current smoking status,
environmental tobacco smoke in
workplace and in home were
included. According to the current
smoking status, the subjects were
divided to three groups (Non-smokers: those who had never smoked or
had smoked fewer than 100 cigarettes in their life, current smokers:
those who were currently smoking

120

Won et al.

and had smoked 100 cigarettes or

more in their whole life, past smokers: those who had smoked in the
past but they stopped smoking at
that time).
The systemic health behaviours
included diabetes and hypertension.
The oral health status included the
number of decayed, missing or filled
permanent teeth.
Statistical analysis

The individual weighted factors were

used and the complex sampling
design of the survey was considered
to obtain the variances. Multivariate
logistic regression analyses were
applied to examine the associations
of Cd and Pb with periodontitis. The
odds ratios (OR) of Cd and Pb for
periodontitis were adjusted for
above-mentioned covariates in logistic model. As the interaction terms of
periodontitis with age, gender and
smoking were significant, subgroup
analyses were performed to determine
estimates stratified according to the
effect modifiers. Each effect modifier
was excluded from its multivariate
model of the subgroup except age.
Statistical analyses were performed
using PASW version 18.0 software
(PASW, Chicago, IL, USA).
Results

Periodontitis defined as a CPI code

 3 was 32.3%. Tables 1, 2 and 3
list the characteristics of the study
subjects categorized by their periodontal status.
Table 4 shows the significant
associations between Cd and periodontitis in the multivariate logistic
regression models. Compared with
subjects with low Cd, those with
high Cd had a 1.57 (95% CI: 1.03
2.38) times significantly higher odds
ratio (OR) for periodontitis. Higher
Pb exposure might be associated
with periodontitis, but the strength
of the association was marginal. The
results of the subgroup analyses are
also presented in Table 4. The association was different according to
the strata of gender and smoking.
Periodontitis showed moderate or
slight associations with high Cd in
females (OR: 1.99; 95% CI: 1.03
2.38) and current smokers (OR:
1.64; 95% CI: 0.992.70). Middle Pb
also showed significant associations

Table 1. Univariate comparisons of the socio-demographic characteristics in subjects with

and without periodontitis
No periodontitis

Age (n = 1966)
Gender (n = 1966)
Male

%*
(95% CI)

%*
(95% CI)

1320

41.39
(40.5442.25)

646

53.12
(51.9154.33)

62.4
(58.866.0)
72.8
(69.176.2)

382

37.6
(34.041.2)
27.2
(23.830.9)

49.8
(43.756.0)
62.7
(55.269.7)
72.4
(68.076.3)
76.2
(71.979.9)

202

599

Female

721

Highest diploma (n = 1955)

Primary school

214

Middle school

135

High school

531

 University or College

437

Household income (n = 1950)

<25%

Periodontitis

193

2550%

293

5075%

398

>75%

426

56.1
(50.062.0)
62.6
(57.367.6)
70.2
(64.675.2)
75.7
(70.980.0)

264

88
205
143

156
175
167
142

50.2
(44.056.3)
37.3
(30.344.8)
27.6
(23.732.0)
23.8
(20.128.1)
43.9
(38.050.0)
37.4
(32.442.7)
29.8
(24.835.4)
24.3
(20.029.1)

*Weighted per cent and 95% confidence interval.

Weighted mean and 95% confidence interval.

Household income: monthly average family equivalent income.

(=monthly average household income/(the number of household members).

in females (OR: 1.61; 95% CI: 1.02

2.52) and non-smokers (OR: 1.57;
95% CI: 1.012.43).
Discussion

It was found that exposure to Cd

was associated with periodontitis
after adjusting for the socio-demographics, oral and systemic health
behaviour, systemic health and oral
health status among the overall subjects of this study, and that gender
and smoking could modify the effect
of Cd on periodontitis as the association was significant only in females
and smokers.
To the best of our knowledge,
this is the first study to report gender and smoking as effect modifying
factors of the association between
Cd and periodontitis. Women have a
higher body burden of cadmium
than that of men. Low iron stores
that are common during pregnancy
and before menopause lead to an
up-regulation of the duodenal metal
transporter, which has a high affinity

for cadmium (Vahter et al. 2007).

This may be one of the reasons for
the gender difference. As smoking is
a major source of Cd in adults
(Paschal et al. 2000) and is also
associated with an increased risk of
periodontal disease (Tomar & Asma
2000), effect modification according
to smoking habit could be inferred.
However, the effect modification
found in this study needs to be studied further.
This study is consistent with the
research by Arora et al. (2009a),
which reported the relationship
between Cd and periodontitis. But
follow-up research efforts should
be made to confirm the relationship as there are only few studies
which could be compared with this
study.
Environmental cadmium exposure promotes skeletal demineralization (Staessen et al. 1999). Furthermore,
there is a direct effect of Cd on bone
resorption (osteoclasts), resulting in
increased urine deoxypyridinoline
(Akesson et al. 2006).
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Cadmium and lead with periodontitis

Table 2. Univariate comparisons between
the subjects with and without periodontitis
in oral and general health status
No
periodontitis
n

%*
(95% CI)

%*
(95% CI)

Hypertension (n = 1965)
No
1170 71.6
483 28.4
(68.674.4)
(25.631.4)
Yes
150 46.0
163 54.0
(39.752.3)
(47.760.3)

Cd
<0.6689
lg/L
0.669
1.467
lg/L
 1.467
lg/L

Table 3. Univariate comparisons of the oral and general health behaviours in subjects with
and without periodontitis
No periodontitis

Periodontitis

Periodontitis

Diabetes (n = 1966)
No
1265 68.8
581 31.2
(65.871.6)
(28.434.2)
Yes
55 49.3
65 50.7
(39.059.6)
(40.461.0)

Pb
<1.7289
lg/dL
1.729
3.04
lg/dL
 3.04
lg/dL

121

384 80.8
107 19.2
(76.984.2)
(15.823.1)
657 66.7
327 33.3
(62.670.7)
(29.337.4)
279 56.2
212 43.8
(50.961.3)
(38.749.1)

387 81.3
102 18.7
(77.284.8)
(15.222.8)
651 66.2
331 33.8
(62.669.7)
(30.337.4)
282 56.3
213 43.7
(50.661.9)
(38.149.4)

*Weighted percent and 95% confidence

interval.
The plasma concentration of Pb and Cd is
divided into three categories: <25th (1.7289 lg/
dL and 0.6689 lg/L), 25th75th, and  75th
percentile and (3.04 lg/dL and 1.467 lg/L).
Cd, Cadmium; Pb, lead.

Oral health behaviours

Use of floss (n = 1963)
No
Yes

%*
(95% CI)

%*
(95% CI)

1104

65.3
(62.268.3)
81.7
(75.686.5)

587

34.7
(31.737.8)
18.3
(13.524.4)

214

Use of inter-proximal tooth brush (n = 1963)

No
1132
67.3
(64.270.3)
Yes
186
69.6
(62.975.5)
General health behaviours
Alcohol consumption experience in a lifetime (n = 1959)
No
145
61.6
(53.968.7)
Yes
1173
68.8
(65.971.5)
Present Smoking status (n = 1963)
Past smoker
232
60.9
(55.166.5)
Current smoker
303
60.3
(55.265.3)
Non-smoker
783
73.5
(69.876.8)
Environmental tobacco smoke in workplace(n = 1959)
Over one hour
359
71.5
(66.276.2)
One hour or less
98
69.6
(60.377.5)
Non-exposure
861
66.3
(62.869.5)
Environmental tobacco smoke in home (n = 1963)
Over one hour
120
74.8
(66.481.6)
One hour or less
33
70.2
(52.983.1)
Non-exposure
1165
66.8
(63.869.7)

58

561
84

91
550

155
206
284

145
48
448

47
13
585

32.7
(29.735.8)
30.4
(24.537.1)

38.4
(31.346.1)
31.2
(28.534.1)
39.1
(33.544.9)
39.7
(34.744.8)
26.5
(23.230.2)
28.5
(23.833.8)
30.4
(22.539.7)
33.7
(30.537.2)
25.2
(18.433.6)
29.8
(16.947.1)
33.2
(30.336.2)

*Weighted per cent and 95% confidence interval.

Secondhand adverse effects of

exposure to Cd upon bones due to
liver damage including lower vitamin
D activity, higher calcium output
and lower osteogenesis activity
(Kjellstrom 1992, Alfven et al. 2000).
Laboratory studies strongly support the epidemiologic evidence for a
direct osteotoxic effect from Cd
(Brzoska & Moniuszko-Jakoniuk
2004, Wilson et al. 1996).
It could be inferred that Cd affects
bone metabolism. Lately, many studies have been reporting that even
exposure to low levels of Cd may
have adverse effects on the skeletal
system, and as a result inducing osteopenia or osteoporosis (Alfven et al.
2000, Akesson et al. 2006, Gallagher
2012 John Wiley & Sons A/S

et al. 2008, Schutte et al. 2008).

Osteoporosis and periodontal disease
are similar in that they both involve
bone loss (Lai 2004, NicopoulouKarayianni et al. 2009).
The relationship between periodontal disease and osteoporosis is so
far uncertain, but they have had
significant correlation in a few studies
(Tezal et al. 2000, Geurs et al. 2003).
A finding that women affected by
osteoporosis were three times more
susceptible to loss of alveolar bone
than women without osteoporosis,
(Geurs et al. 2003), which implies
that internal bone conditions have
an independent influence on loss of
alveolar bone (Kaye 2007). Also,
Inagaki et al. (2001) found that

periodontitis and tooth loss may be a

useful indicator of metacarpal bone
mineral density loss in Japanese
women.
Furthermore, it is reported that
both osteoporosis and periodontitis
are associated with common risk
factors such as smoking, a poor
nutritional status, advanced age,
glucocorticoid therapy and immunological diseases (Mart nez-Maestre
et al. 2010).
Both diseases affect bone mass
and share common risk factors
(Machuca et al. 2005). In addition,
the pathological effects of Cd on
bones, including the ability to promote inflammation, are pertinent to
periodontal disease, where disruption

122

Won et al.

Table 4. Adjusted odds ratios and 95% confidence intervals of periodontitis (CPI  3) for MS and its components in total and each subgroup
Total

Pb*
<1.7289 lg/dl
1.7293.04 lg/dl
 3.04 lg/dl
Cd*
<0.669 lg/l
0.6691.467 lg/l
 1.467 lg/l

Age group

Gender

Current smoker

<40 age

 40 age

Male

Female

Yes

No

Reference
1.37
(0.971.93)
1.31
(0.881.96)

1.76
(0.833.74)
1.36
(0.503.66)

1.19
(0.781.80)
1.09
(0.681.74)

0.91
(0.551.53)
1.03
(0.611.74)

1.61
(1.022.52)
1.27
(0.702.30)

1.34
(0.752.40)
1.48
(0.802.73)

1.57
(1.012.43)
1.38
(0.762.53)

Reference
1.32
(0.951.83)
1.57
(1.032.38)

1.15
(0.642.07)
0.99
(0.452.17)

1.24
(0.781.96)
1.54
(0.932.54)

1.14
(0.731.79)
1.20
(0.672.15)

1.58
(0.912.74)
1.99
(1.073.71)

1.39
(0.912.12)
1.64
(0.992.70)

1.23
(0.742.04)
1.54
(0.872.74)

*The plasma concentration of Pb and Cd is divided into three levels based on the criteria of 25th (1.7289 lg/dl and 0.6689 lg/l) and 75th
percentile (3.04 lg/dl and 1.467 lg/l).
The multivariate logistic regression model was adjusted for the socio-demographic variables (age, gender, family income, educational level),
oral health behaviours (use of floss, use of inter-proximal toothbrush) and health behaviours (alcohol consumption experience in a lifetime,
present smoking status, environmental tobacco smoke in workplace, environmental tobacco smoke in home), general health status (diabetes,
hypertension) and oral health status (Decayed, missing or filled permanent teeth).
In subgroup, each effect modifier was excluded from its multivariate model except age.
Cd, Cadmium; and Pb, lead.

of the host inflammatory response is

considered a primary factor in disease
progression and subsequent alveolar
bone loss (Arora et al. 2009a). For these
reasons, it has been postulated that they
may be related.
The demonstration of a relationship
between osteoporosis and periodontitis
is complex because both are multifactorial diseases and both share common
mechanisms (Mart nez-Maestre et al.
2010). A biological plausibility exists
suggesting that at least part of the
periodontal destruction is influenced by
systemic bone loss.
In contrast to our findings on
Cd, there was only a marginal association with Pb and periodontitis
among the overall subjects of this
study, contrary to conventional relevant reports on various ethnic
groups (Dye et al. 2002, Saraiva
et al. 2007). However, a significant
association was found in females
and non-smokers.
As it appears that accelerated
bone turnover or mineral loss can
contribute to increased lead in the
blood, it seems biologically plausible
that bone loss from advanced periodontal disease would be associated
with increased levels of Pb in the
blood (Dye et al. 2002).
Dye et al. (2002) reported that
there is a significant association
between the Pb level and periodontitis among people with a history of

smoking. This result was contrary to

our study and there might be several
reasons for this.
The first reason could be the relationship between lead and periodontal
diseases might hinge on the definition
of periodontitis. During a different
study on periodontal health, periodontal pocket depth was not a significant
factor for higher levels of Pb in the
blood (Dye et al. 2002).
The second reason could be the
relationship between Pb and periodontitis might be different according
to race. This is because only Caucasians among several races showed a
relationship in a study that proved
the relationship between Pb and osteoporosis (Campbell & Auinger 2007).
The final reason could be the difference in the level of Pb exposure.
The Pb exposure level has been
dropping over time [CDC (Centers
for Disease Control and Prevention)
2009]. Studies on the relationship
between Pb and periodontal diseases
mostly examined the relationship
based on the data of the NHANES
III (19881994). However, we used
the Pb exposure level of Korean
adults, which was surveyed in 2009.
It seems to suggest that Pb is likely
to affect bones when the level of Pb
exposure is higher than the current
level.
As smoking is a major source of
blood Pb and associated with an

increased risk of periodontal disease

(Tomar & Asma 2000), the effect of
Pb might be masked in smokers.
Gender difference could be related
to smoking or biological differences
such as menstruation. Further studies will be necessary to elucidate the
effect modification of smoking and
gender found in this study.
This study had several limitations. The periodontal status was
assessed by CPI. Although CPI is an
easier way to assess the prevalence
of periodontitis in a population survey and has been adopted as an
index for periodontitis in epidemiological studies on the association
between systemic health and periodontal disease (Kwon et al. 2011),
the limitation of CPI should be
deliberately considered as it can overestimate or underestimate the prevalence of periodontitis due to the use of
representative teeth and pseudo pockets (Kingman & Albandar 2002).
Another important limitation of this
study is its cross-sectional design,
which makes it impossible to determine the direction of the causal
relationships of Cd and Pb with
periodontitis.
Nevertheless, this is the first epidemiologic study to report a significant association between Cd level in
the blood and periodontitis in a
nationally representative sample of
adults.
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Cadmium and lead with periodontitis

Conclusions

High exposure of Cd could be associated with periodontitis in females

and current smokers, and middle
exposure of Pb showed significant
associations in females and nonsmokers among a representative
sample of adults in Korea. The
underlying biological mechanisms
showing a causaleffect relationship
of Cd and Pb with periodontitis
remains to be determined through
prospective cohort studies.
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Address:
Kwang-Hak Bae
Department of Preventive and Public Health
Dentistry, School of Dentistry, Seoul
NationalUniversity, 28, Yeongeuon-dong,
Jongno-gu, Seoul, 110-749, Korea (South)
Tel: +82-2-740-8747
Fax: +82-2-765-1722
E-mail: baekh@snu.ac.kr

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Won et al.

Clinical Relevance

Scientific rationale for the study:

Although an association of Cd and
Pb with periodontitis has been
reported in some studies, more
studies are necessary to confirm
the association. In particular,
few studies have examined the
association of Cd and Pb with
periodontitis based on a compre-

hensive, nationwide, representative

survey in Asia.
Principle findings: Among a national
representative sample of Korean
adults, this study found that periodontitis is associated with Cd in
females and non-smokers, and with
Pb in females and current smokers.
Practical implications: The association of periodontitis with Cd and Pb

was different according to the

strata of gender and smoking in
Koreans over age 20. Further studies are necessary to determine if
there is a cause and effect relationship between these two conditions
taking into consideration effect
modification.

2012 John Wiley & Sons A/S