association between low bone mineral density and clinical attachment loss in japanese postmenopausal...

Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120613

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Association Between Low Bone Mineral Density and Clinical

Attachment Loss in Japanese Postmenopausal Women

Masanori Iwasaki*, PhD, George W. Taylor

†, DMD, DrPH, Kazutoshi Nakamura

‡, MD,

Akihiro Yoshihara§, PhD, Hideo Miyazaki

*, PhD

*Division of Preventive Dentistry, Department of Oral Health Science, Niigata University

Graduate School of Medical and Dental Sciences, Niigata City, Japan.

†Department of Preventive and Restorative Dental Sciences, University of California San

Francisco, San Francisco, CA, U.S.

‡Department of Preventive Medicine, Niigata University Graduate School of Medical and

Dental Sciences, Niigata City, Japan.

§Division of Oral Science for Health Promotion, Department of Oral Health and Welfare,

Niigata University Graduate School of Medical and Dental Sciences, Niigata City, Japan.

Background: Previous studies have shown conflicting results as to whether low bone mineral

density (BMD) is associated with severe clinical attachment loss (CA loss). The effect of dental restoration

on CA loss was not considered in most studies. In addition, studies of this association in Japanese subjects

are limited. The aim of this cross-sectional study was to evaluate the possible association between BMD

and CA loss with dental restoration information in Japanese community-dwelling postmenopausal women.

Methods: The subjects were 397 women (average age, 68.2 years). BMDs of the lumbar spine and

right proximal femur were measured by the dual-energy X-ray absorptiometry method. Based on lower

BMD/young adult mean (YAM) among the two sites measured, subjects were classified into three groups:

(1) Normal: BMD = 80% YAM or higher (n = 161); (2) Osteopenia: BMD = 70%–80% YAM (n = 136);

and (3) Osteoporosis: BMD = less than 70% YAM (n = 100). Multivariable analyses of the differences in

CA loss values among three BMD groups was conducted using general linear models. Adjustments for the

percentage of teeth restored and other covariates were considered.

Results: Individuals with osteopenia had significantly higher average CA loss than individuals

with normal BMD (p = 0.022). Additionally, the osteoporosis group displayed significantly higher average

CA loss (p = 0.003) and higher percentages of sites with CA loss ≥4mm (p = 0.007).

Conclusion: The results of the present study indicate that low systemic BMD was associated with

severe CA loss in Japanese community-dwelling postmenopausal women.


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KEY WORDS:

Epidemiology, Osteoporosis, Periodontitis

Osteoporosis and osteopenia are diseases that affect women primarily and are the most

common metabolic bone disease among the elderly.1 They are characterized by a loss of

bone mineral density (BMD), with osteoporosis being the more severe form. They often

culminate in a fracture of the hip, wrist, and/or vertebrae. Fractures related to such

diseases have become a major health and economic burden in Japan,2 just as they have in

North America and Europe.3, 4

Periodontal disease is characterized by the resorption of

alveolar bone as well as by loss of the soft-tissue attachment to teeth. It is common, with

an estimated world prevalence of 10 to 15%,5 and is one of the leading causes of tooth

loss in the elderly.6

A possible association between osteoporosis/osteopenia and periodontal disease has

been suggested. Bone loss is a common feature of osteoporosis and periodontal disease.

Both diseases share common etiologic factors such as smoking, nutritional deficiencies,

increasing age, corticosteroid use and immune dysfunction.7 Previous studies

8-10 that

evaluated this association used differing periodontal measures, including clinical

attachment loss (CA loss), loss of alveolar crestal height (ACH) and tooth loss. Studies

have shown low BMD to be independently and consistently associated with loss of ACH7,

8, 11, 12 and tooth loss.

9, 13-18 Wactawski-Wende and colleagues

8 investigated the

association between systemic BMD and ACH in a cohort of 1,341 postmenopausal

women aged 53 to 85 and demonstrated that women with osteoporosis had greater odds of

having loss of ACH than those with normal BMD. We observed a significant relationship

between a change in BMD and the number of lost teeth in a 5-year cohort;9 however,

findings of studies that focused on the relation of osteoporosis to CA loss have not been as

consistent. Some studies found significant negative relationship between BMD and CA

loss10, 19-23

while others reported no relationship.24-28

Overall, no clear association

between osteoporosis and CA loss was found, requiring further investigations.

Small sample sizes and/or a lack of adequate control of potential confounding

variables are major limitations of most studies conducted to date.29

Dental restorations

have been demonstrated to be a risk factor for CA loss;30, 31

however, most studies on the

relationship between CA loss and BMD did not control for the effect of dental

restorations, which may partly explain the inconsistent results in previous studies of CA

loss. Furthermore, many have evaluated the association between BMD and CA loss in

Caucasians, while sparse research has been conducted among the Japanese population.


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Differing genetic backgrounds and lifestyles among populations may affect this

association. As increasing age is an important risk factor for both osteoporosis and

periodontal disease,7 a well-controlled, large-scale study is needed to clarify the

association between osteoporosis and CA loss in the Japanese, one of the fastest aging

populations in the world. If an association between low systemic BMD and severe CA

loss were found, it might be possible to identify patients at risk for oral bone loss and pay

extra attention to their periodontal care.

The aim of this cross-sectional study was to evaluate the association between

systemic BMD and CA loss with dental restoration information, using a large cohort of

Japanese community-dwelling postmenopausal women. Specifically, we hypothesize

that more severe CA loss is found in women with low systemic BMD than in women with

normal BMD.

MATERIALS AND METHODS

Study Design, Setting, and Participants

The population for this study was drawn from the Yokogoshi study, an epidemiologic,

community-based investigation of bone health for postmenopausal women. The original

sample consists of 674 women (55–74 years old) who lived in Yokogoshi (Niigata City,

Japan). The baseline examination was conducted in 2005. Details of sampling

methodology and selection were published previously.32

Five years after the Yokogoshi

study was initiated, 544 postmenopausal women were enrolled in the current study. All

subjects were non-institutionalized, ambulatory, and independent. They underwent BMD

measurement, dental examination, interview, and biochemical analyses of blood. The

following women were excluded: (1) women who had known systemic endocrine,

metabolic or skeletal bone disorders (n = 59), (2) women who had received any

medications that would influence bone remodeling (e.g., hormone replacement therapy or

bisphosphonates) (n = 46), (3) women who were edentulous (n = 22) and (4) women who

did not submit complete data (n = 20). Data were therefore analyzed for 397 participants

aged 60 to 80 years (average age 68.2 years).

This study was conducted according to the guidelines laid down in the Declaration of

Helsinki (version 2002) and all procedures involving human subjects were approved by

the Ethics Committee of Niigata University School of Medicine. Written informed

consent was obtained from all study participants.


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BMD Measurement

BMDs of the lumbar spine (L2–4) and right proximal femur were measured using the

dual-energy X-ray absorptiometry device|| by a single, trained X-ray technician, as

previously reported.9 The in vivo coefficients of variation of the BMD measurements

were 0.2% for the lumbar spine and 0.1% for the proximal femur. BMDs were expressed

as a percentage of the young adult (20–44 years old) mean (YAM).

Dental Examination

The dental examination was conducted under sufficient illumination using artificial light

by two calibrated dentists [MI & AY],9 who assessed the following parameters:

(1) CA loss: Pressure-sensitive probe¶ was used to measure to the nearest millimeter

the distance from the cemento-enamel junction (CEJ) to the base of the pocket, at two

sites (mesio-buccal and mid-buccal) of all remaining natural teeth. In sites where the CEJ

was unclear because it was concealed by the margin of the crown restoration, the position

of the CEJ was estimated using adjacent landmarks and dental anatomy. When the CEJ

could not be estimated, the site was excluded from the examination.

(2) Probing depth (PD): The distance from the gingival margin to the base of the

pocket was measured to the nearest millimeter at two sites per tooth, as for CA loss.

(3) Percentage of sites with bleeding on probing (BOP): The presence or absence of

bleeding within 15 seconds following removal of the probe was observed at two sites per

tooth, as for CA loss.

Using PD and BOP scores, dichotomous periodontitis variable was defined. Women

who presented with one or more sites with PD of ≥4mm and BOP of >10 % were defined

as having periodontitis.33

(4) The number and the status of teeth (including the third molar):34

The number of

teeth was counted and the status of teeth (decayed, missing and filled teeth [DMFT]) was

assessed. The percentage of teeth restored (F/number of teeth percent) for each

participant was calculated.35, 36

Interview and Evaluation of Handgrip Strength and Anthropometric

Characteristics

Demographic and lifestyle information was obtained at interview. Age, menopausal age

and health behavior (smoking status [never/previous/current smoker], status of visits to a


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dentist [regularly/episodically] and use of devices for interdental cleaning [yes/no]) were

recorded. Early menopause was defined as women who reached menopause before age

45. Handgrip strength was measured once in the dominant hand with a digital hand

dynamometer. #

No one reported a musculoskeletal problem and preferred not to undergo

testing on the day of the physical performance examination or reported difficulties

managing their own oral care due to musculoskeletal problems.

Biochemical Analyses of Blood

Biochemical values, including serum hemoglobin A1c (HbA1c) and high sensitivity

C-reactive protein (hs-CRP) were evaluated. Hyperglycemia was defined as HbA1c

≥6.2% and elevated hs-CRP was defined as hs-CRP ≥0.1mg/dl. The value for HbA1c (%)

is estimated as the National Glycohemoglobin Standardization Program (NGSP)

equivalent value (%) calculated by the formula HbA1c (%) = HbA1c (Japan Diabetes

Society [JDS]) (%) + 0.4%，considering the relational expression of HbA1c (JDS) (%)

measured by the previous Japanese standard substance and measurement methods and

HbA1c (NGSP).37

Description of Outcome Variables

The two primary outcome variables for the analyses were the severity and extent of

periodontal disease, which were represented as average CA loss and the percentage of

sites with CA loss ≥4mm, respectively.38, 39

Average PD, the percentage of sites with PD

≥5mm and BOP (%) were included as secondary outcome variables.

Description of Principal Exposure Variable

The principal exposure variable included BMDs of the lumbar spine and right proximal

femur. Among the two sites measured for each participant, lower BMD/YAM was used

for the principal exposure variable definition.22

Based on participants’ BMD/YAM, three

categories were derived from the diagnostic criteria for primary osteoporosis (year 2000

revision) established by the Japanese Society for Bone and Mineral Research.40

The three

categories used to specify the exposure variables for this study were: (1) Normal: BMD =

80% YAM or higher; (2) Osteopenia: BMD = 70%–80% YAM; and (3) Osteoporosis:

BMD = less than 70% YAM.


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Statistical Analyses

Initially, analysis of variance for continuous variables and Chi-Square test for categorical

variables was used to test differences in means and percentages of selected characteristics

among three BMD groups (normal, osteopenia, and osteoporosis).

Before the main analyses, outcome variables (average CA loss and the percentage of

sites with CA loss ≥4mm) were assessed for normality. While the distributions of the

outcome variables were right skewed, transformation of data yielded similar results and

we elected to use the untransformed data to ease interpretation.

Univariable and multivariable analysis of the differences in CA loss values (average

CA loss and the percentage of sites with CA loss ≥4mm) among three BMD groups was

conducted using general linear models to test the hypothesis that individuals with low

BMD had more severe CA loss. For each outcome variable, the final multivariable model

was selected after backward-elimination modeling assessment using a significance level

for retention at α = 0.2. The candidate covariates for multivariable modeling included the

following variables potentially related to CA loss: age, smoking status, percentage of

teeth restored, status of visits to a dentist, use of devices for interdental cleaning, handgrip

strength, hyperglycemia and elevated hs-CRP. In addition, BOP was included as a

potential confounder when the outcome variable was CA loss or PD. Effect modification

by age was evaluated using interaction terms. Statistical significance was set at α = 0.05.

All calculations and statistical analyses were performed using the statistical software

package. **

RESULTS

Study Participants’ Characteristics

Table 1 shows study participants’ characteristics by BMD status. The distribution of

participants’ BMD status was: (1) Normal, 161 individuals (40.5%); (2) Osteopenia, 136

individuals (34.3%) and (3) Osteoporosis, 100 individuals (25.2%). There were

significant differences in BMD status (p <0.001), the number of teeth present (p = 0.031)

and age (p <0.001). No significant differences were found in other characteristics.

Teeth Status and CA Loss

Table 2 shows Pearson correlation coefficients between CA loss and dental variables.

Number of teeth was inversely associated with the average CA loss or the percentage of

sites with CA loss ≥4mm (r = -0.46; p <0.001 and r = -0.44; p <0.001, respectively). In


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contrast, the percentage of teeth restored was positively associated with the average CA

loss or the percentage of sites with CA loss ≥4mm (r = 0.18; p <0.001 and r = 0.18; p

<0.001, respectively).

BMD Status and CA Loss

The results from general linear models of CA loss values are shown in Table 3. The first

row shows a regression models that include only BMD status as a predictor. The second

row shows multivariable regression models created using backward elimination. Same

set of covariates was selected for both the average CA loss and the percentage of sites

with CA loss ≥ 4mm; age, BOP, percentage of teeth restored, status of visits to a dentist,

smoking status, hyperglycemia and elevated hs-CRP. There were no interactions of

systemic BMDs with age. Analyses stratified by age group (≥ 65, < 65 years) did not

change the results appreciably (data not shown).

In unadjusted analyses, the osteopenia/osteoporosis group displayed more severe

(higher average CA loss, p = 0.005 for osteopenia and p = 0.004 for osteoporosis) and

extensive (higher percentages of sites with CA loss ≥ 4mm, p = 0.011 for osteopenia and

p = 0.010 for osteoporosis) periodontal disease than the group with normal BMD (Table

3). This remained significant after adjustment for confounders. The difference in the

adjusted means between women with osteopenia and with normal BMD was 0.18mm (p =

0.022) for average CA loss and 3.68% (p = 0.053) for the percentage of sites with CA loss

≥4mm. The difference in the adjusted means between women with osteoporosis and with

normal BMD was 0.26 (p = 0.003) for average CA loss and 5.72% (p = 0.007) for the

percentage of sites with CA loss ≥4mm (Table 3). In multivariable models, older age,

higher BOP, higher percentage of teeth restored, current smoking, hyperglycemia and

elevated hs-CRP were also associated with more severe and extensive periodontal

disease, whereas a regular dental checkup was associated with lower average CA loss

(Table 3).

BMD Status and PD/BOP

The prevalence of periodontitis based on PD and BOP is presented in Table 2.

Periodontitis prevalence did not differ significantly among the three BMD groups (p =

0.448). The results from general linear models of PD and BOP are shown in Table 4. The

first column shows a regression model that includes only the BMD status as a predictor.

The second column shows adjusted regression model results created using backward

elimination. In unadjusted analyses, osteopenia was associated significantly with average

PD (p = 0.031); however, this significant association disappeared after adjustment for


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confounders. There were no associations of BMD groups with the percentage of sites

with PD ≥5mm and BOP.

DISCUSSION

We observed a significant association between low systemic BMD and severe CA loss

after controlling for other important health characteristics in the multivariable general

linear model. Individuals with osteopenia/osteoporosis were more likely to have higher

average CA loss than individuals with normal BMD. In addition, individuals with

osteoporosis were more likely to have a higher percentage of sites with CA loss ≥4mm.

This finding concurs with a recent study from Greece, which examined the associations

between systemic BMD and periodontal conditions. Pepelassi and colleagues22

demonstrated that low systemic BMD was significantly associated with greater CA loss

in a cohort of 45-70-year-old women.

Dental restorations appear to be associated with CA loss.30, 31

In our study, the

percentage of teeth restored was positively associated with the average CA loss or the

percentage of sites with CA loss ≥4mm. Women with more teeth restored were likely to

have more severe CA loss. As the type and material of the restoration or surface of the

teeth restored was not considered during the dental examination, we do not believe that

this variable entirely explains individuals’ dental health status; however, the percentage

of teeth restored can explain, on some level, the risk of attachment loss as well as the

cumulative lifetime experience of dental caries, which can be associated with individuals’

oral health behavior. The percentage of teeth restored did not differ significantly among

the three BMD groups. The association between low systemic BMD and severe CA loss

remained even after controlling for the percentage of teeth restored. These results suggest

that the association found between BMD and CA loss is not the result of dental

restorations.

In addition to the dental restoration variable, we added BOP as a potential

confounder, when the outcome variable was CA loss or PD. Checchi and colleagues41

demonstrated a direct relationship between BOP and the presence/amount of subgingival

deposits. Low systemic BMD was significantly associated with severe CA loss after

controlling for BOP.

Systemic BMDs were not associated with PD and BOP. Similar to the results from

other studies,26, 28

the severe CA loss among osteopenia/osteoporosis women was mainly

associated with gingival recession rather than with deepening of the periodontal pockets.


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No significant difference in gingival inflammation assessed by BOP was observed

between women with osteopenia/osteoporosis and with normal BMD.

Because bone loss is a common feature of periodontal disease and osteoporosis, both

diseases may share common etiologic factors which may either affect or modulate the

process of both diseases.7 Although periodontal disease is thought to be the result of an

insult by an infectious agent within dental plaque, the underlying host susceptibility may

play an important role in the onset and progression of oral bone loss. Considering these

facts, it is reasonable that our study showed a significant relationship between BMD and

CA loss. Systemic factors in systemic bone loss might also modify the local tissue

response to a periodontal pathogen, which leads to the loss of tooth-supporting tissues,

including alveolar bone, and eventual tooth loss. Various researchers have proposed

several plausible findings. Brennan and colleagues19

studied 1,329 postmenopausal

women and revealed an inverse association between systemic BMD and CA loss. This

association was strongest among women without subgingival calculus.

Another possible explanation for the relationship between BMD and CA loss in this

cohort of post-menopausal women is estrogen deficiency, which plays a pathogenic role

in women with post-menopausal osteoporosis and may also lead to the progression of

mandibular bone loss through inflammation-induced bone resorption.42

Estrogen

suppresses the expression of several cytokines including interleukin-1 (IL-1), IL-6 and

tumor necrosis factor-α, which are suggested to be responsible for osteoclast stimulation

in inflammatory conditions.43

In fact, it has been demonstrated that estrogen replacement

therapy is associated with protection against alveolar bone loss26

and tooth loss.44

Although several potential mechanisms have been proposed, in fact, there have been

conflicting results on the association between the two diseases.10, 19-28

This may not only

be because the studies have small sample sizes, limited control of potential confounders,

or varying definitions of diseases. Both osteoporosis and periodontal disease are complex

disorders with various underlying cellular and metabolic pathologies. Systemic BMD

might not influence alveolar bone loss directly in some cases. The skeleton is heterogenic,

and bone density, bone turnover rate and bone remolding ability differ in some parts of

the skeleton, suggesting that those regions, although related to each other, have some

degree of independence.10, 45-47

The strengths of this study include a homogenous group of Japanese postmenopausal

women, which eliminated the influences of variations in race and gender on our results.

On the other hand, there were several limitations in our study. First, it had a

cross-sectional design, which prevented us from establishing the temporal sequence of


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the association between low systemic BMD and severe CA loss. Second, we could not

identify the CA loss of all 6 sites, but only 2 sites (mesio-buccal and mid-buccal) per

tooth. Some researchers have expressed concern over the discrepancy between a partial

mouth examination and the “gold standard” full mouth examination.48-50

Since we

examined only 2 sites per tooth, it is likely that we underestimated the prevalence of

periodontal disease; however, this possible underestimation of periodontal disease

prevalence determined by the partial mouth examination would probably bias the results

towards the null hypothesis and not lead to overestimation of the observed associations.

Third, because other information regarding participants’ socioeconomic status (e.g.

income and educational status) and oral health status (e.g., dental plaque scores,

subgingival biofilm, and history of dental treatment) was not collected, a number of other

potentially important confounders could not be included in the analyses. Residual

confounding remains a risk.

In summary, within the limitations of the reported study, an independent relationship

between low systemic BMD and severe CA loss in Japanese community-dwelling

postmenopausal women was found. Additional longitudinal epidemiologic studies with

larger, more diversified samples and more complete periodontal information are needed

to further evaluate the relationship between these two diseases.

ACKNOWLEDGEMENTS

We wish to thank the staff of the Health Promotion Division, Niigata City Yokogoshi Branch Office for

their help with data collection. This study was supported by a Grant-in-Aid for Scientific Research (B)

No.21390558 and (C) No.40339958 from the Japanese Ministry of Education, Culture, Sports, Science and

Technology, Tokyo, Japan.

ACKNOWLEDGEMENTS:

This study was supported by a Grant-in-Aid for Scientific Research (B) No.21390558 and (C)

No.40339958 from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

Conflicts of Interest:

The authors have no conflicts of interest to report.


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bisphosphonate treatment. J Oral Maxillofac Surg 2008;66:987-994.

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prevalence and severity of various. Community Dent Oral 1993;21:354-359.

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examination protocols. J Dent Res 2010;89:1208-1213.

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Corresponding author:, Masanori Iwasaki, Division of Preventive Dentistry,

Department of Oral Health Science, Niigata University Graduate School of Medical and

Dental Sciences, 2-5274 Gakkocho-Dori, Chuo-Ku, Niigata City 951-8514, Japan, Tel.:

+81 25 227 2858; Fax: +81 25 227 0807; E-mail: [email protected]

Submitted October 10, 2012; accepted for publication January 19, 2013.


15

Table 1. Selected characteristics by bone mineral density

All participants

Normal Osteopenia Osteoporosis

BMD: more than

80% of YAM

BMD: 70% - 80%

of YAM

BMD: less than

70% of YAM

Variables n = 397 n = 161 n = 136 n = 100 p*

BMD status

BMD of the lumbar spine (g/cm2) 0.83 ± 0.14 0.95 ± 0.10 0.80 ± 0.08 0.67 ± 0.09 <0.001

BMD of the right proximal femur (g/cm2) 0.71 ± 0.11 0.80 ± 0.08 0.69 ± 0.06 0.60 ± 0.07 <0.001

BMD/YAM of the lumbar spine (%) 82.1 ± 14.0 93.8 ± 10.1 79.4 ± 8.1 67.2 ± 8.5 <0.001

BMD/YAM of the right proximal femur (%) 82.6 ± 12.3 92.5 ± 9.2 80.2 ± 6.9 70.0 ± 8.5 <0.001

Lower BMD/YAM (%)† 77.8 ± 11.8 89.1 ± 7.3 74.8 ± 2.8 63.8 ± 6.2 <0.001

Periodontal condition

Periodontitis 142 (35.8) 56 (34.8) 54 (39.7) 32 (32.0) 0.448

Dental condition

No. of teeth 21.7 ± 6.6 22.4 ± 6.2 21.7 ± 6.3 20.3 ± 7.5 0.031

Percentage of teeth restored 68.7 ± 21.4 67.6 ± 21.1 69.6 ± 19.9 69.4 ± 24.0 0.686

Demographic and Socioeconomic status

Age ≥65 years 255 (64.2) 83 (51.6) 93 (68.4) 79 (79.0) <0.001

Health behavior

Cigarette smoking

Never smoker 358 (90.2) 144 (89.4) 123 (90.4) 91 (91.0) 0.603

Previous smoker 27 (6.8) 14 (8.7) 8 (5.9) 5 (5.0)

Current smoker 12 (3.0) 3 (1.9) 5 (3.7) 4 (4.0)

Visit dentist regularly 167 (42.1) 66 (41.0) 59 (43.4) 42 (42.0) 0.917

Use devices for interdental cleaning 196 (49.4) 73 (45.3) 72 (52.9) 51 (51.0) 0.397

Health status

Early menopause 35 (8.8) 17 (10.6) 9 (6.6) 9 (9.0) 0.489

Hyperglycemia 28 (7.1) 13 (8.1) 10 (7.4) 5 (5.0) 0.632

Elevated hs-CRP 62 (15.6) 32 (19.9) 21 (15.4) 9 (9.0) 0.063

Physical status

Dominant hand grip strength (kg) 24.3 ± 4.3 24.7 ± 5.0 24.0 ± 3.9 24.0 ± 3.4 0.253

Continuous variables (BMD status and no. of teeth) expressed as mean ± standard deviation; categorical variables (age group, health behavior and

health status), as n (percentage).

Bold text highlights statistically significant findings (p <0.05).


16

*P value for the comparison of selected characteristics by bone mineral density. Analysis of variance for continuous variable, Chi-Square test for

categorical variables.

†Lower BMD/YAM of the lumbar spine and the right proximal femur (used for the determination of the presence or not of osteopenia or

osteoporosis).

BMD, bone mineral density; YAM, young adult mean (20–44 years old); hs-CRP, high sensitivity C-reactive protein.

Periodontitis = one or more sites with PD of ≥4mm and BOP of >10 %; Early menopause = menopausal age <45years; Hyperglycemia = HbA1c

≥6.2%; Elevated hs-CRP = hs-CRP ≥0.1mg/dl.


17

Table 2. Correlation coefficient between CA loss and dental variables

CA loss variables

Average CA loss Percentage of sites with CA loss ≥4mm

Dental variables r p r p

Number of teeth -0.46 <0.001 -0.44 <0.001

Percentage of teeth restored 0.18 <0.001 0.18 <0.001

CA loss, clinical attachment loss; r, correlation coefficient.



18

Table 3. General linear model of the effect of BMD on the CA loss

Unadjusted


Variables B SE p B SE p

low BMD (versus normal)

Osteopenia 0.25 0.09 0.005 5.29 2.07 0.011

Osteoporosis 0.28 0.10 0.004 5.90 2.27 0.010

Multiple adjustment


Variables B SE p B SE P

low BMD (versus normal)

Osteopenia 0.18 0.08 0.022 3.68 1.90 0.053

Osteoporosis 0.26 0.09 0.003 5.72 2.11 0.007

Age ( ≥65 versus <65 years) 0.18 0.08 0.019 2.52 1.79 0.160

BOP 0.02 0.003 <0.001 0.52 0.08 <0.001

Percentage of teeth restored 0.004 0.002 0.015 0.09 0.04 0.018

Visit dentist regularly (yes versus no) -0.14 0.07 0.046 -2.56 1.66 0.123

Cigarette smoking (versus never smoker)

Previous smoker 0.22 0.14 0.107 3.83 3.21 0.233

Current smoker 0.70 0.20 0.001 13.6 4.75 0.004

Hyperglycemia (yes versus no) 0.43 0.14 0.002 8.47 3.22 0.009

Elevated hs-CRP (yes versus no) 0.32 0.10 0.001 5.06 2.28 0.027

B, the difference in the adjusted means of periodontal parameters between one group and the reference group; SE, the standard error of the estimate

(B).


BMD, bone mineral density; CAL, clinical attachment level; BOP, bleeding on probing; CRP, C-reactive protein; YAM, young adult mean (20–44

years old).

Osteopenia = BMD: 70%-80% of YAM; Osteoporosis = BMD <70% of YAM; Hyperglycemia = HbA1c ≥6.2%; Elevated hs-CRP = hs-CRP

≥0.1mg/dl.


19

Table 4. General linear models of the effect of BMD on the PD and BOP

Crude Adjusted*

Variables B SE p B SE p

Outcome: Average PD

BMD/YAM Group (versus normal)

Osteopenia 0.12 0.05 0.031 0.07 0.05 0.128

Osteoporosis 0.10 0.06 0.083 0.09 0.05 0.097

Outcome: Percentage of sites with PD ≥5mm


Osteopenia 1.09 0.79 0.166 0.69 0.70 0.324

Osteoporosis 1.04 0.86 0.224 1.17 0.77 0.131

Outcome: BOP


Osteopenia 2.02 1.29 0.118 1.91 1.27 0.133

Osteoporosis 0.48 1.41 0.732 0.35 1.39 0.801

B, coefficient for the difference in the adjusted means of periodontal parameters between one group and the reference group; SE,

standard error of the estimate (B).


*Adjusted for following covariates:

Outcome: Average PD; age, BOP, percentage of teeth restored, status of visits to a dentist, use of devices for interdental cleaning, and

elevated high sensitivity C-reactive protein.

Outcome: Percentage of sites with PD ≥5mm; BOP, percentage of teeth restored, smoking status, status of visits to a dentist,

hyperglycemia, and elevated high sensitivity C-reactive protein.

Outcome: BOP; percentage of teeth restored and status of visits to a dentist.

BMD, bone mineral density; PD, probing depth; BOP, bleeding on probing; YAM, young adult mean (20–44 years old).

Osteopenia = BMD: 70%-80% of YAM; Osteoporosis = BMD <70% of YAM

‖ QDR4500a, Hologic Inc., Bedford, MA, USA

¶ Vivacare TPS probe, Vivadent Co., Schaan, Liechtenstein

# T.K.K. 5401, Takei Scientific Instruments Co. Ltd., Niigata, Japan

** STATA (version 12), Stata Corp., TX, USA

association between low bone mineral density and clinical attachment loss in japanese postmenopausal...

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