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Journal of Dental Research
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Clinical

Association between Serum Albumin and Root Caries in Community-dwelling Older Adults

A. Yoshihara1,*, N. Hanada2 and H. Miyazaki1

1 Division of Preventive Dentistry, Department of Oral Health Science, Graduate School of Medical and Dental Sciences, Niigata University, 2-5274, Gakkocho-Dori, Niigata, 951-8514, Japan; and
2 Department of Oral Science, National Institute of Public Health;

Correspondence: *corresponding author, akihiro{at}dent.niigata-u.ac.jp


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 RESULTS
 DISCUSSION
 REFERENCES
 
Recently, associations between dental diseases and the general health condition have been reported. The purpose of this study was to evaluate, by serum albumin concentrations, the relationship between the general health condition and root caries. We randomly selected 763 individuals (600 70-year-olds and 163 80-year-olds) living in Niigata City, Japan. The variables body composition, blood measurements, daily nutrient intakes, and root caries were measured. The relationship between root caries and serum albumin concentration was evaluated. The differences in serum albumin concentrations between subjects with untreated root caries (DT = 0 and DT > 3) were 75.56 mg/dL in 70-year-olds and 202.97 mg/dL in 80-year-olds (p < 0.05, ANOVA). The findings of the present study indicated that a relationship between root caries and serum albumin concentration in these elderly subjects is highly possible.

Key Words: serum albumin • root caries • elderly people


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 RESULTS
 DISCUSSION
 REFERENCES
 
Disabilities in daily living occur frequently in elderly people because of inflammatory states or disorders. Regarding oral health, elderly people have few remaining teeth. Dental caries, including root caries, has been shown to be significantly associated with the incidence of tooth loss (Hand et al., 1991; Locker et al., 1996).

Recently, associations between dental diseases such as periodontitis or dental caries and the general health condition have been reported. The possible role of periodontal infections as risk factors for systemic diseases such as coronary heart disease has attracted special attention (Genco, 1996; Papapanou, 1996). The composite dental index—combining caries, periodontitis, periapical lesions, pericoronitis, and edentulousness—was linked to ischemic events in patients with coronary heart disease (Mattila et al., 1995). Furthermore, it has been shown that dental caries may be associated with immune response (Tenovuo et al., 1990). Dental caries might be a risk marker or factor for the general health condition. However, the relationship between a dental disease such as root caries and the general health condition, including nutrient intake, infections, or anthropometry, is still unknown in elderly people.

The purpose of this study was to evaluate the relationship between the so-called general health condition and root caries. In particular, we adopted the serum albumin concentration as a criterion which shows us the general health condition. Serum albumin levels may be an index of the severity of an underlying disease. In addition, a strong association between albumin level and mortality has been reported (Phillips et al., 1989; Darnes and Ducimetiere, 1990). Many conditions, such as malnutrition, inflammatory states, liver diseases, and renal diseases, reduce serum albumin levels (Herrmann et al., 1992). We evaluated the relationship between the serum albumin level and root caries.

MATERIALS & METHODS
Initially, questionnaires were sent to all 6629 inhabitants aged 70 and 80 yrs old according to a registry of residents in Niigata City in Japan, and they were informed of the purpose of this survey. The response rate was 79.5% (3695 70-year-olds; 1578 80-year-olds; six, age indistinct). Among them, we randomly selected 763 (600 70-year-olds; 163 80-year-olds) individuals to have approximately the same number per gender in each age. We evaluated, in the people who were examined in this study compared with all other residents, the differences in the general health condition, such as the number of cases of disease (heart disease, blood disease, liver disease, kidney disease, diabetes mellitus, high blood pressure, rheumatism, respiratory disease, lumbago, allergies, digestive disease, cerebral apoplexy) from which the subjects had suffered, the percentage of smokers, and the percentage of people with trouble chewing. Written informed consent was obtained from all subjects. The protocol for this study was approved by the Ethics Committee of Niigata University School of Dentistry.

Root Caries
Four trained dentists assessed the oral health conditions. Dental clinical examinations were done by means of dental mirrors and WHO ball-pointed periodontal probes under artificial light, without bite-wing radiographs. Root caries was diagnosed according to WHO criteria (World Health Organization, 1997), except for unerupted/unexposed roots and arrested lesions. Root decay was defined when a lesion was detected on an exposed root surface and felt soft or leathery when probed. For a single incidence of decay or for a filling affecting both the crown and the root, the likely site of origin of the lesion was recorded as decayed or filled. The examiners were calibrated by 18 volunteer patients in the University Hospital before and during the survey. Interexaminer reliability for surfaces was assessed for the four examiners. We calculated a kappa score using 5 codes (Sound, Filled, Decayed, Filled [with decay], and Bridge abutment: Special crown or Veneer/implant). The kappa values between each pair of examiners were 0.84-0.97.

Body Composition and Blood Measurements
Anthropometric evaluation included measurements of weight and height for the calculation of Body Mass Index. In addition, determinations of serum albumin, IgG and IgA concentration were also made. The serum albumin concentration was measured by a BCG method (Doumas et al., 1971).

Food Intake
Dieticians instructed participants on recording their own dietary intake for one day. The interviewer provided each person with written directions and food models for recording food intake and reviewed the completed records with each subject. Total daily nutrient intakes of sugar, fat, and protein from food were computed for those subjects.

Statistical Analysis
For descriptive data (serum albumin, anthropometric measurements, food intake, biochemical measurements, and root caries), statistical differences between age and gender were evaluated by an analysis of variance. In addition, the relationship between serum albumin concentration and the presence of untreated and treated root caries, missing teeth, Body Mass Index, nutrient intakes, and biochemical values was evaluated by an analysis of variance adjusted for age and gender. For evaluation of the relationship between root caries and serum albumin concentration, linear multiple-regression analysis was performed. As a dependent variable, serum albumin concentration was used. As independent variables, we selected the independent variables, which had p-values less than 0.05 according to the analysis of variance adjusted by gender and age for each variable.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 RESULTS
 DISCUSSION
 REFERENCES
 
We evaluated the differences in general health condition between the people who were examined in this study (EX) and all other residents (RE). The numbers of cases of disease which EX and RE had had previously were 1.50 (SD = 1.13) and 1.16 (SD = 1.16) for 70-year-olds, and 1.86 (SD = 1.39) and 1.32 (SD = 1.32) for 80-year-olds, respectively. The percentages of smokers in EX and in RE were 19.5% and 22.3% for 70-year-olds, and 13.2% and 13.0% for 80-year-olds, respectively. The percentages of people with trouble chewing in EX and in RE were 16.4% and 18.8% for 70-year-olds, and 16.6% and 25.1% for 80-year-olds, respectively. There were no significant differences in the numbers of cases of disease, the percentages of smokers, and the percentages of people with trouble chewing between EX and RE by gender, except the numbers of cases of disease in males aged 80 yrs (2.52 [SD = 1.41] for EX vs. 2.04 [SD = 1.34] for RE, p < 0.05 by t test) and the percentages of people with trouble chewing in females aged 80 yrs (11.9% for EX vs. 27.3% for RE, p < 0.01 by chi-square test).

In addition, we compared the descriptive variables of subjects (Table 1Go). There were significant differences in IgA, Body Mass Index, sugar intake, protein intake, the presence of untreated root caries, and the presence of treated root caries by gender by an analysis of variance. All significant parameter levels except Body Mass Index were higher in males. In addition, serum albumin, fat intake, number of missing teeth, and the presence of treated root caries were significantly associated with age by an analysis of variance. All significant parameter levels except number of missing teeth were lower in 80-year-olds.


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Table 1. Mean of the Number of Instances of Root Caries, Biochemical Values, Body Mass Index, and Nutrient Intakes by Sex and Age
 
The Fig.Go shows the differences in the distributions of serum albumin concentrations according to the presence of untreated root caries (DT) in subjects who were divided into 3 categories (DT = 0, DT = 1 or 2, DT > 3). The subjects with many instances of DT had a significantly lower serum albumin concentration by an analysis of variance adjusted for gender and age (p < 0.05). The differences in the serum albumin concentrations between subjects with DT = 0 and those with DT > 3 were 75.56 mg/dL in 70-year-olds and 202.97 mg/dL in 80-year-olds. The maximum number of instances of DT was 7 for 70-year-olds (n = 2) and 6 for 80-year-olds (n = 3). The differences in the serum albumin concentrations between subjects with DT = 0 and subjects with the highest levels of DT were 173.38 mg/dL for 70-year-olds and 298.17 mg/dL for 80-year-olds. In addition, the subjects with a low Body Mass Index and a high IgG concentration had a significantly lower level of serum albumin by an analysis of variance adjusted for gender and age (p < 0.05, Table 2Go). In contrast, the subjects with a large number of instances of treated root caries and a high level of serum IgG concentration had a significantly greater number of instances of untreated root caries (p < 0.01, p < 0.05, Table 2Go), even if there was no increase in the number of missing teeth. In particular, the serum IgG concentration was significantly associated with both the serum albumin concentration and the number of instances of untreated root caries. The level of the serum IgG concentration and the number of instances of untreated root caries increased, while the level of the serum albumin concentration decreased.


Figure F
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Figure. Serum albumin concentrations according to number of instances of untreated root caries by age. The subjects with more than 3 instances of untreated root caries had significantly lower serum albumin concentrations by an analysis of variance adjusted for age and gender (p < 0.05). DT = number of instances of untreated root caries. The n for each cell of data was DT = 0 (n = 484 for 70-year-olds, n = 131 for 80-year-olds), DT = 1 or 2 (n = 92 for 70-year-olds, n = 24 for 80-year-olds), and DT > 3 (n = 24 for 70-year-olds, n = 8 for 80-year-olds).

 

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Table 2. The Relation between Serum Albumin Concentration or Untreated Root Caries and Treated Root Caries, Missing Teeth, Body Mass Index, Biochemical Values, and Nutrient Intake
 
For evaluation of the relationship between root caries and serum albumin concentration, 4 variables (number of instances of untreated root caries, age, Body Mass Index, and concentration of IgG) were selected for the independent variables of the final model. The result of linear multiple-regression analysis by the final model is presented in Table 3Go. The number of instances of untreated root caries was significantly associated with the concentration of serum albumin adjusted for age, Body Mass Index, and concentration of IgG (p < 0.05).


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Table 3. Multiple Linear Regression and Associated P-values
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 RESULTS
 DISCUSSION
 REFERENCES
 
According to the results of our study of the differences in general health condition between EX and RE, there was a small difference in the number of cases of disease, the percentage of smokers, and the percentage of people with trouble chewing. Therefore, we thought that the subjects in this study were representative of the community. In contrast, the R2 by the multiple-regression analysis is low (Table 3Go). This means that the amount of variance explained by the multiple-regression analysis is low, which indicates that although the 4 independent variables had significant probability, there are other explanatory factors. We should keep in mind the limitations of the present study.

In this study, the number of untreated teeth (DT) was a significant factor associated with serum albumin concentration. The differences in the serum albumin concentrations between subjects with DT = 0 and those with DT > 3 were 75.56 mg/dL in 70-year-olds and 202.97 mg/dL in 80-year-olds (p < 0.05). Furthermore, there was a big difference in the serum albumin concentrations between those with DT = 0 and those with DT = maximum: 173.38 mg/dL for 70-year-olds and 298.17 mg/dL for 80-year-olds.

Hypoalbuminemia may be directly linked to adverse effects. A strong association between albumin levels and mortality has been reported. Especially, Shibata et al. (1991) investigated the relationship between serum albumin and mortality in a 10-year longitudinal study of 421 community residents aged 69-71 yrs. In that report, subjects who were divided into four groups according to the quartile of serum albumin levels (-4.1, 4.2-4.3, 4.4-4.5, 4.6+, g/dl) had significantly different survival rates. There was even an evident difference in survival rates between the first and second quartiles. Our study indicates that the difference in serum albumin levels between the number of instances of untreated root caries shown in the subjects might have a meaningful influence on the subjects’ general health status. However, we could not find a significant relationship between the number of instances of treated root surfaces and the serum albumin concentration. Regarding root surface filling, a previous study reported that 45% of restorations were placed because of decay, while 55% were done for cervical wear/sensitivity (Walls et al., 2000). Because it is unclear what rate is due to untreated root caries vs. cervical wear, it might be difficult to evaluate the relationship between the treated teeth and the serum albumin concentration. Furthermore, we could not find any significant relationship between the number of missing teeth and the serum albumin concentration. There are many studies that evaluated the factors for tooth loss, which indicated that not only caries but also periodontitis was a major factor for tooth loss. Many other local factors, such as abutment teeth for removable partial dentures, increased the tooth loss risk (Hirotomi et al., 2002). It might be difficult to evaluate the relationship between missing teeth and the serum albumin concentration, especially in elderly people.

The background of the effect of serum albumin value on mortality is not well-understood. We thought of two conceivable possibilities about that relationship: One is the influence of a chronic disease; the other is the influence of nutrient intake. In this study, the serum IgG concentration was significantly associated with both the serum albumin concentration and number of instances of untreated root caries. The level of the serum IgG concentration and the number of instances of untreated root caries increased, while the level of the serum albumin concentration decreased. If a decrease of the serum albumin concentration was influenced by the subject’s malnourished state, the serum IgG concentration might, conversely, show a tendency to decrease. The significant relationship between the serum albumin concentration and number of instances of untreated root caries in this study might be influenced by chronic infectional disease rather than by nutritional condition.

The serum IgG level increased with the presence of caries (Parkash et al., 1994). The nature of the human immune response to dental caries suggests that Streptococcus mutans amd serum antibodies may play a major role in pathogenesis. Furthermore, there was a significant relation between the serum albumin and the serum IgG concentrations (Goubran Botros et al., 1996). The serum albumin concentration may fall due to a variety of infections, including root caries, with an increase of the serum IgG concentration. However, it is difficult to discuss this causality by only this study. Further studies should be conducted to find the relationship between root caries and serum albumin, taking into consideration not only root caries but also systemic infectional diseases.

In contrast, serum albumin value might be a good guideline for a subject’s nutritional condition. Certainly, some reports have indicated that dietary intake influences serum albumin (Magagnotti et al., 2000; Giordano et al., 2001). However, correcting the malnourished state might be more difficult in elderly people than in younger ones. The rate of albumin synthesis in elderly subjects might not be sensitive to changes in protein intake (Walrand et al., 2000). There was a report that synthesis speed of albumin in the liver in elderly people is not influenced by the ingestion of protein, and that serum albumin might be influenced by aging itself (Shibata et al., 1991). However, there was a significant relationship between serum albumin concentration and Body Mass Index in this study. It has been reported that low Body Mass Index becomes a risk factor for all-cause mortality (Shirasaki, 1996; Ishii et al., 1998; Landi et al., 1999), and the risk of daily activity limitation (Allison et al., 1997). Because of a good relationship between Body Mass Index and nutrient intake, we could not completely deny the relationship between serum albumin concentration and nutrient intake. We could not find any significant relation between nutrient intake and both the serum albumin concentration and the number of instances of untreated root caries in this study.


    ACKNOWLEDGMENTS
 
This work was supported by a grant-in-aid from the Ministry of Health and Welfare of Japan (H10-Iryo-001).

Received for publication March 25, 2002. Revision received November 14, 2002. Accepted for publication November 26, 2002.


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 REFERENCES
 

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Journal of Dental Research, Vol. 82, No. 3, 218-222 (2003)
DOI: 10.1177/154405910308200313


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