Oral health status, C-reactive protein and mortality

– a 10 year follow-up study

S. Ajwani1, K. J. Mattila2, T. O. Närhi3, R. S. Tilvis4 and A. Ainamo1
1
Institute of Dentistry, University of Helsinki; 2Department of Medicine, Division of Infectious Diseases; 3Department of Prosthetic Dentistry,
Institute of Dentistry, University of Turku, Finland; 4Clinic of Geriatrics, Helsinki University Central Hospital, Helsinki

Abstract

Background: Epidemiological studies have reported a strong association between C-reactive protein
(CRP) and cardiovascular diseases (CVD). Elevated CRP levels have been observed both in dentate
individuals with chronic dental infections like periodontal disease and in those edentulous. The mechanisms
behind these observations, especially the reasons for the elevation of CRP in the edentulous, are poorly
understood. The comparative data on the importance of these inflammatory conditions in the oral cavity
as causes of elevated CRP levels and CVD risk factors are also limited. Objective: To determine if
edentulism is associated with increased levels of CRP and investigate the possible mechanism for this
association; and to study the influence of periodontal disease and edentulism on 10-year mortality.
Subjects: Of the 364 subjects aged 76, 81, and 86 years in 1990, 196 were dentate and 168 edentulous. By
December 1999, 179 had died, almost half (n=87) of them due to cardiovascular disease. Results:
Significantly more of the edentulous subjects had elevated (>3 mg/L) CRP levels as compared to those
with at least 20 teeth (p<0.01). They also had high salivary microbial counts (p<0.05), and more mucosal
lesions (p<0.0001) than those with at least 20 teeth. In multivariate analysis, high microbial counts (OR
2.3, CI 1.06-5.05) and mucosal lesions (OR 2.18, CI 1.03-4.61) were significantly associated with elevated
CRP levels. The risk for all-cause mortality was non-significantly elevated among the edentulous (RR
1.48, CI 0.95 – 2.31) and dentate with periodontal disease (RR 1.58, CI 0.96 – 2.61). CVD mortality was
significantly higher among the dentate with periodontal disease (RR 1.97, CI 1.01 – 3.85) when compared
with dentate without periodontal disease. Conclusion: Among the edentulous, chronic infections like
denture-related mucosal lesions are important determinants of elevated CRP, comparable to periodontal
disease in the dentate. Elevated CRP per se and edentulism were not significantly associated with increased
mortality. Periodontal disease was, however, still associated with a two-fold CVD mortality in this very
old population.

Key words: Oral health, elderly, CRP, mortality

Introduction infections, especially periodontitis possibly explain

C-reactive protein (CRP), a sensitive systemic the linkage between dental infections and
marker of inflammation, has been shown to predict cardiovascular diseases (CVD)7-10. Increased CVD
cardiovascular events among middle-aged and mortality and elevated CRP have also been
elderly subjects 1-6 . Elevated levels of CRP observed among the dentate elderly with
observed in dentate subjects with chronic dental periodontitis11.

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 Oral health status, C-reactive protein and mortality – a 10 year follow-up study 33

Data on the risk for CVD and mortality in died during the 10-year period and the primary
edentulous subjects and CRP levels in these cause of death for 49% of the decedents (n = 87)
individuals are sparse. Among the participants of was CVD (Figure 1). The information about the
The Health Professionals Follow-up Study (HPFS), death (cause and date) was obtained from the
a weak association was observed between tooth Finnish Death Register.
loss and increased CVD12. On the other hand, Data collection
National Health and Nutrition Examination Study The details of the medical examination have been
I, its epidemiological Follow-up Study (NHEFS)13 reported previously11,21. At baseline, blood samples
and The First National Health and Nutrition were collected, after an overnight fast, from all
Examination Survey (NHANES I)14, showed that participants for routine laboratory investigations.
CVD risk in the edentulous was similar to that in In 1998, these frozen (-20°C) serum samples were
individuals with periodontitis. The NHANES III15 used to measure the CRP using a sensitive
reported significantly higher levels of CRP among immunoenzymometric assay which made use of
the edentulous, as compared to dentate subjects two monoclonal antibodies (sensitivity =0.3 mg/l,
without periodontal disease; the reason for this is Medix Diacor)6. The range of this assay was 0.3 to
poorly understood. Factors like systemic diseases, 30 mg/l. The median normal circulating
ill-fitting dentures, inability to maintain good oral concentration of CRP is 0.8 mg/l and in 90% of
hygiene, and hyposalivation can result in the
growth of many oral microorganisms, and change
the oral microflora of the elderly 16-18. In the
edentulous, the denture plaque may cause chronic
oral diseases like denture-associated stomatitis and
other mucosal lesions, with systemic
consequences19.
The aim of this study was to determine if
edentulism was associated with increased levels
of CRP and to evaluate the relationship between
edentulism, denture-related chronic mucosal
diseases, salivary microorganisms and CRP levels.
Furthermore, the influence of these factors as well
as periodontal disease on 10-year all-cause and
CVD mortality among the dentate and edentulous
elderly was also studied. On the basis of the above
observations, we wanted to test the hypothesis that
like periodontitis, chronic mucosal diseases in the
edentulous elderly can cause inflammatory changes
in the oral cavity, reflected in elevated CRP levels.
Accordingly, both conditions can increase CVD
risk via this common inflammatory pathway.

Subjects and Methods

Subject sample
Details of the design and sampling of the Helsinki
Aging Study (HAS) have been published earlier20.
Briefly, 651 subjects aged 75 (n=239), 80 (n=212),
and 85 (n=200) years underwent medical
examination in 1989 and 600 elderly who were
alive one year later were invited for an oral
examination at the University Dental Clinic. Of
these, 364 subjects (196 dentate, 168 edentulous)
underwent baseline examination, and 121
participated in the follow-up examination, five
years later. The subjects were followed until
December 1999. Altogether, 179 participants had Figure 1. Participants of the denal study

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34 S Ajwani, K J Mattila, R S Tilvis, A Ainamo

the apparently healthy people the serum The growth densities of SM, and number of
concentration is less than 3 mg/l22. In our study, as colonies of salivary yeast were classified into 4
in some of the previous studies 23,24 , CRP categories (0 to III) from no growth to >106 CFUs/
concentration of 3 mg/l was the cut off level. mL, and no colonies to >50 colonies/side of the
Participant’s social class was judged on the basis slide, respectively28,29. In this study, we took the
on their occupation and level of education (class I average of SM and yeast categories for each
= upper, class IV = lower). The subjects were asked individual to determine their total microbial count.
about their smoking history and alcohol Those whose average category was less than 2 were
consumption during the interview and in the said to have ‘low’ microbial count and the rest as
questionnaire. They were accordingly categorized having ‘high’ microbial count.
into current smoker, ex-smoker, or non-smoker; Informed consent was obtained form all subjects
and taken once a week or more, less than once a prior to the study. The Ethics committee of the
week, or not taken at all respectively. History of Helsinki University Central Hospital, and the
CVD was based on a previous history of Institute of Dentistry, University of Helsinki,
myocardial infarction or angina or stroke. Finland approved the protocol of the study.
Four faculty members carried out the dental and Statistical analysis
oral examinations using a mouth mirror, a dental Statistical analyses were performed using the SPSS
explorer, and a periodontal probe. Among the for MS Windows (Version 9.0, SPSS Inc., Chicago,
edentulous, tongue, corners of the mouth, and oral USA). Chi-square test was used to compare
mucosa under and around the dentures were proportions and continuous variables were
examined using a modified scheme recommended analysed with ANOVA or non-parametric tests (if
by the WHO25. The diagnosis was based on clinical the distribution was not normal despite logarithmic
examination only26. All the signs in the mucosa transformation). No adjustments were made for
indicating a disease caused by yeast, such as multiple comparisons. Logistic regression was
angular chelitis, plaque-like lesion (hyperplastic used to investigate the associations of the number
or pseudomembranous), and erythematous lesions of teeth, mucosal lesions, and microbial count with
on tongue, mucosa, or hard palate, were termed as the risk of elevated CRP level and high microbial
“oral candidosis”. “Denture stomatitis”, on the count. The known elevators of CRP like history of
other hand, included localized or generalized smoking, alcohol use, blood pressure, and history
erythema and/or granular type hyperplasia under of chronic inflammatory diseases like chronic
a denture. Any and all inflammatory conditions of bronchitis, emphysema, asthma, and muscle and
the mouth, including mucosal lesions and denture joint diseases were adjusted for. Cox proportional
stomatitis, were broadly categorized under hazards model was used to study the predictors of
“Inflammation of the mouth”. mortality. Age and gender were forced in as
The dentate participants underwent clinical covariates. The survival data were also controlled
examination that included examination for dental for smoking, hypertension, cholesterol, body mass
caries, periodontal status and prosthetic evaluation. index, history of CVD and social class. p-value <
Community Periodontal Index for Treatment 0.05 was considered statistically significant.
Needs (CPITN) method was used for recording the
periodontal status. The details of the examination Results
have been reported earlier27. Periodontal status was The association of baseline demographic
dichotomized and those with CPITN codes 3 and characteristics and CV risk factors with periodontal
4 (periodontal pockets >4 mm) were categorised status of the participants and their status in 1999 is
as having periodontitis. However, as CPITN does shown in Table 1. Participants who had died within
not measure alveolar bone loss or recession, these the 10 year period were significantly older, of lower
could not be taken into account. social class, more often diabetic, had a lower BMI,
Salivary microbial (mutans streptococci and systolic and diastolic blood pressures and serum
yeast) counts were analyzed using commercial kits. cholesterol levels (Table 1). After adjusting for age
The methods of collecting saliva and assessing the and sex, diabetes and lower serum cholesterol
microbial counts have been reported elsewhere28. significantly predicted death (data not shown). As
Briefly, estimation of salivary mutans streptococci compared with dentate subjects, the edentulous
(SM) was done by the Dentocult-SM strip mutans® were of older age, predominantly females, of lower
method and salivary yeast was done by the Oricult- social class, and were more likely to be current
N® method (Orion Diagnostica, Espoo, Finland). smokers (Table 1). The only statistically significant

Gerodontology
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 Oral health status, C-reactive protein and mortality – a 10 year follow-up study 35

difference between dentate subjects with and were significantly higher in the edentulous, and
without periodontal disease was that the latter had those with denture stomatitis, oral candidosis or
significantly higher mean diastolic blood pressure inflammation in the mouth.
(Table 1). There was a non-significant trend for those with
CRP levels and edentulism at least 20 teeth and those dentate without
periodontitis to be more often alive at 10 years.
Edentulous subjects had more often elevated CRP
Factors showing independent association with
levels (>3 mg/L) than those with 20 or more teeth
elevated CRP were the presence of mucosal lesion
or dentate without periodontal disease or dentate
(RR 2.18, CI 1.03-4.61) and high salivary
without dentures (Table 2). Denture stomatitis was
microbial count (RR 2.31, CI 1.06-5.05) (Table 3).
associated with elevated CRP but this relationship
Mucosal lesion was also significantly associated
was affected by denture status. More subjects with
with high salivary microbial count (Table 3).
complete dentures and denture stomatitis had
elevated CRP levels than those without complete Periodontal status, edentulism and mortality
dentures and not having stomatitis. Among the Unadjusted, edentulism was significantly
edentulous, those with mucosal lesions or any associated with increased total and CVD mortality,
inflammation in the mouth had significantly more as it was with total mortality when adjusted for
often elevated CRP levels (p=0.007 and p=0.04 age and sex. After adjusting for all confounders
respectively, data not shown). This relationship was (age, sex, history of CVD, blood pressure, body
not significant among the dentate. A similar trend mass index, cholesterol, social class and smoking),
was observed for salivary microbial counts, which these associations lost statistical significance.

Table 1. Relationship of baseline characteristics with status in 1999, and baseline periodontal (PD) status
(percentage in parentheses)

Baseline characteristics Status in 1999 Periodontal (PD) status

Dead Alive PD – PD + Edentulous†
n = 179 n = 185 p n = 95 n = 80 n = 189 p

Age:
76 years 54 (33) 111 (67) 53 (32) 41 (25) 71 (43)
81 years 57 (54) 49 (46) 23 (22) 25 (24) 58 (54)
86 years 68 (73) 25 (27) <0.0001 19 (20) 14 (15) 60 (65) 0.01
Women 125 (48) 137 (52) 0.37 71 (27) 49 (19) 142 (54) 0.05
Social class:
Class I 15 (39) 24 (61) 12 (31) 12 (31) 15 (38)
Class II 30 (38) 49 (62) 30 (38) 18 (29) 31 (39)
Class III 68 (48) 74 (52) 36 (25) 35 (25) 71 (50)
Class IV 43 (61) 27 (39) 0.02 14 (20) 10 (14) 46 (66) 0.02
Current smoker 17 (53) 15 (47) 0.43 3 (9) 5 (16) 24 (75) 0.01
Alcohol (> once a week) 23 (51) 22 (49) 0.55 9 (20) 10 (22) 26 (58) 0.39
Diabetics 36 (66) 19 (34) 0.03 15 (27) 11 (20) 29 (53) 0.56
Hypertensives 64 (52) 63 (48) 0.94 36 (28) 24 (19) 67 (53) 0.28
BMI (kg/m_) 25.2+3.6 26.1+3.8 0.03 25.6+3.7 25.5+3.5 25.8+3.8 0.88
Systolic blood pressure (mm Hg) 154+26.0 159+24.9 0.04 160+24.8 155+24.9 155+26.1 0.38
Diastolic blood pressure (mm Hg) 81+11.6 83+11.9 0.05 85+13.9 80+12.1 81+11.6 <0.01
Serum cholesterol (mmol/L) 6.3+1.2 6.7+1.3 0.001 6.6+1.3 6.3+1.2 6.6+1.2 0.28
Serum HDL (mmol/L) 1.5+0.5 1.5+0.5 0.36 1.5+0.5 1.5+0.4 1.5+0.4 0.94
Serum triglyceride (mmol/L)* 1.4+0.8 1.4+0.8 0.62 1.5+0.9 1.2+0.6 1.4+0.7 0.05

† Edentulous also includes few of those who did not meet the CPITN criteria (i.e. had < 2 teeth per sextant)
Values are mean+SD.
Statistical evaluation by Chi square test and ANOVA
* Statistical evaluation by Kruskal-Wallis Test

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36 S Ajwani, K J Mattila, R S Tilvis, A Ainamo

After adjusting for confounders, periodontitis with total mortality fell short from being
was associated with almost a two-fold CVD statistically significant (Table 4).
mortality (RR 1.97, CI 1.01-3.85); the association

Table 2. Dental factors associated with elevated CRP levels, high microbial (Streptococcus mutans and
yeast) count and 10-year survival (Percentage in parentheses)

Oral status CRP value* Microbial count* Alive at 10 years*

Low Elevated p Low High p n=185 p
n = 188 n = 69 n = 93 n = 132

No.of teeth: 77 (64) 43 (36) 47 (34) 91 (66) 80 (48)

1-9 teeth 46 (75) 15 (25) 35 (48) 38 (52) a 37 (46)
10-19 teeth 31 (82) 7 (18) 17 (31) 38 (69) 31 (50)
20-32 teeth 34 (90) 4 (10) b 0.02 25 (53) 22 (47) a 0.02 37 (70) b 0.08

Periodontal (PD) status:

PD –ve 53 (81) 13 (19) c 40 (46) 46 (54) 61 (64) d
PD +ve 45 (82) 10 (18) c 30 (40) 45 (60) 41 (51)
Edentulous† 88 (66) 46 (34) 0.03 54(35) 98 (65) ns 83 (44) 0.05

Denture status:
Dentate without dentures 38 (86) 6 (14) f 31 (55) 25 (45) f 42 (65) e
Dentate with dentures 66 (77) 20 (23) 44 (39) 69 (61) 62 (50) e
Edentulous with CD 82 (66) 43 (34) 0.03 46 (33) 94 (67) 0.03 80 (46) 0.09

Denture stomatitis:
No 130 (77) 39 (23) 103 (48) 112 (52) 113 (54)
Yes 48 (64) 27 (36) 0.04 19 (22) 69 (78) <0.0001 50 (50) ns

Dentures and stomatitis:

No CD without stomatitis 57 (85) 10 (15) 45 (50) 45 (50) 61 (59)
No CD with stomatitis 8 (80) 2 (20) 1 (8) 11 (92) g 9 (64)
CD without stomatitis 74 (72) 29 (28) 59 (47) 67 (53) 72 (50)
CD with stomatitis 38 (60) 25 (40) h 0.02 17 (23) 57 (77) i <0.0001 40 (48) ns

Mucosal lesions:
No 110 (80) 28 (20) 90 (49) 95 (51) 113 (55)
Yes 68 (64) 38 (36) 0.01 31 (26) 86 (74) <0.0001 69 (49) ns

Inflammation of the mouth:

No 118 (78) 34 (22) 97 (48 104 (52) 123 (55)
Yes 60 (65) 32 (35) 0.05 25 (24) 77 (76) <0.0001 60 (49) ns

CRP value:
Low (< 3 mg/l) 76 (45) 93 (55) 98 (52)
High (>3 mg/l) 17 (30) 39 (70) 0.07 29 (42) ns

* Adjusted for age and sex

† Edentulous also includes few of those who did not meet the CPITN criteria (i.e. had < 2 teeth per sextant)
Statistical evaluation by Chi square test
a
Differs significantly from “No teeth group”, p<0.05; b Differs significantly from “No teeth group”, p<0.01.
c
Differs significantly from “Edentulous group”, p<0.05; d Differs significantly from “Edentulous group”, p<0.01.
e
Differs significantly from “Edentulous with CD group”, p<0.05; f Differs significantly from “Edentulous with CD group”, p<0.01.
g
Differs significantly from “No CD without stomatitis group”, p<0.05; h Differs significantly from “No CD without
stomatitis group”, p=0.005; i Differs significantly from “No CD without stomatitis group”, p=0.000

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 Oral health status, C-reactive protein and mortality – a 10 year follow-up study 37

Table 3. Adjusted odds ratios for elevated baseline CRP levels and high salivary microbial counts associated
with oral infections

Dependent Independent variables Odds 95% CI Odds 95% CI

variables ratio* ratio**
Elevated CRP Teeth 0.95 (0.91 – 1.00) 0.95 (0.90– 1.00)
Mucosal lesions (0=No, 1=yes) 2.10 (1.02 – 4.36) 2.18 (1.03 – 4.61)
Microbial count (0=low, 1=high) 2.13 (1.00 – 4.53) 2.31 (1.06 – 5.05)
Elevated Teeth 0.99 (0.96 – 1.03) 0.99 (0.96– 1.04)
microbial count Mucosal lesions (0=No, 1=yes) 2.15 (1.34 – 4.07) 2.13 (1.11 – 4.11)

Logistic regression model used

* Adjusted for age and sex
** Adjusted for age, sex, history of smoking, alcohol consumption, blood pressure, social class [and presence of
established risk factors for elevated CRP like emphysema or chronic bronchitis or asthma or muscle and joint disease
(only for high CRP)]
(None of these variables were significant in the model)

Table 4. Periodontal status and risk of all-cause and cardiovascular mortality

Unadjusted Adjusted for age and sex Adjusted for other confounder
Hazards 95% CI Hazards 95% CI Hazards 95% CI
ratio ratio ratio
All-cause mortality*
Periodontal disease
0=No 1.00 1.00 1.00
1=Yes 1.58 (0.97 – 2.59) 1.59 (0.97 – 2.61) 1.58 (0.96 – 2.61)
2=Edentulous† 1.85 (1.21 – 2.82) 1.57 (1.03 – 2.41) 1.48 (0.95 – 2.31)
CV mortality**
Periodontal disease
0=No 1.00 1.00 1.00
1=Yes 1.86 (0.96 – 3.58) 1.94 (1.00 – 3.75) 1.97 (1.01 – 3.85)
2=Edentulous† 1.90 (1.06 – 3.39) 1.52 (0.85 – 2.74) 1.40 (0.76 – 2.59)

† Edentulous also includes few of those who did not meet the CPITN criteria (i.e. had <2 teeth per sextant)
* Cox regression model adjusted for confounders like age, sex, social class, body mass index, smoking status, blood
pressure and serum cholesterol level
** Cox regression model adjusted for confounders like age, sex, history of cardiovascular disease, social class, body
mass index, smoking status, blood pressure and serum cholesterol level

Discussion The mechanism behind elevated CRP and

Our study identified mucosal lesions in the increased CVD risk is unclear. Recent data suggest
edentulous as an important factor associated with that elevated CRP levels may at least partly reflect
elevated CRP levels among individuals aged 75 extravascular infections, including periodontitis,
or more. Furthermore, periodontal disease was which are among the causes of endothelial
associated with a two-fold CVD mortality even in dysfunction linked with CVD30,31. CRP is elevated
this age group. in periodontitis and this may be one of the reasons
Participants of this study are representative of for the association between periodontitis and
the home-dwelling elderly of Helsinki. They CVD7-10. Corresponding data in edentulous elderly
underwent a series of in-depth medical and dental are very few or missing. In the NHANES III15, the
examinations during the10-year study period. Such age standardised prevalence of elevated CRP was
a dental study on subjects aged over 75 years, has significantly higher among the edentulous than in
not been undertaken before. those with no pockets, but did not differ

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38 S Ajwani, K J Mattila, R S Tilvis, A Ainamo

significantly from those with extensive periodontal “remnant” of the joint effect of chronic infection
pockets. In our study, after adjusting for age and and elevated CRP.
sex, a higher percentage of edentulous subjects had In conclusion, our study in these very old subjects
elevated CRP level, as compared with the dentate showed that edentulism is associated with elevated
with or without periodontal disease. CRP levels, suggesting that loss of teeth does not
The reasons for CRP being elevated in mean absence of infectious conditions in the oral
edentulous individuals are not well understood. cavity. Mucosal lesions and high microbial count
However, it is well known that with ageing, oral commonly found among the elderly may be equally
mucosa becomes more vulnerable to mechanical important risk factors for elevated CRP levels as
damage32. Dentures, inability to maintain optimal periodontal disease. Another important finding of
oral hygiene, hyposalivation and various the study was that periodontal disease carried a
medications create an environment that favours two-fold CVD mortality during a 10-year follow-
microbial growth and make the elderly subjects up even in this age group.
highly prone to mucosal changes15,33. Earlier studies Increasing attention should be paid to denture
have shown that Gram-positive cocci like mutans hygiene habits of the elderly. Further research is
streptococci may act as adherence bacteria for needed to study the denture-related micro flora and
yeasts and helping them to attach to the mucosal its local and systemic effects.
surface34, resulting in chronic oral candidiasis. Co-
aggregation with mutans streptococci has also been Acknowledgements
found to increase the adhesion of C.albicans on Financial support from Ragnar Ekberg Foundation,
acrylic surfaces35. The candida proteinase acts as Center for International Mobility, Päivikki and
a keratinase-like enzyme in vitro and may damage Sakari Sohlberg Foundation, Ella and Georg
the keratinized palatal mucosa36. In our study Ehrnrooth Foundation, and Helsinki City Council
population, mucosal lesions and high salivary is gratefully acknowledged.
microbial counts were significantly associated with
elevated CRP levels. Both these conditions were
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40 S Ajwani, K J Mattila, R S Tilvis, A Ainamo

34. Bagg J, Silverwood R W. Coagglutination Address for correspondence:

reactions between Candida albicans and oral bacteria.
J Med Microbiol 1986; 22: 165-169. Dr Shilpi Ajwani
Department of Oral Rehabilitation
35. Branting C, Sund M L, Linder L E. The
School of Dentistry, University of Otago
influence of Streptococcus mutans on adhesion of
Candida albicans to acrylic surfaces in vitro. Archs PO Box 647, Dunedin
Oral Biol 1989; 34: 347-353. New Zealand

36. Ruechel R. Virulence factors of Candida Phone: +64 3 4797061

species. In: Samaranayake L P, MacFarlane T W, eds. Fax: +64 3 4795079
Oral Candidosis. Kent: Wright, 1990; pp.47-65 e-mail: shilpi.ajwani@stonebow.otago.ac.nz

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