beikler and flemmig proofs 2010

Oral biofilm-associated diseases:trends and implications forquality of life, systemic healthand expenditures

THOMAS BEIKLER & THOMAS F. FLEMMIG

Biofilms are surface-associated communities of

microorganisms embedded in an extracellular poly-

meric substance, which upon contact with the host

may affect tissue hemostasis and result in disease

(61). It is estimated that approximately 80% of the

world�s microbial biomass resides in a biofilm state

and that microbial biofilms cause more than 75% of

all microbial infections found in humans (35). The

oral cavity is replete with biofilms colonizing mucous

membranes, dental materials and teeth (57, 110, 120,

121, 123). Oral biofilms are strongly associated with

the etiology of periodontal diseases, dental caries,

pulpal diseases, apical periodontitis, peri-implant

diseases and candidosis (39, 48, 58, 80, 89, 94, 95, 105,

115, 137, 153) (Table 1).

Risk factors for oral biofilm-associated diseases

The presence of a biofilm alone1 is often not sufficient

to cause disease because most oral biofilm-associ-

ated diseases are complex with a multifactorial eti-

ology. Additional factors that benefit the microbial

community, or make the host more susceptible, are

often required for a disease to develop and progress.

Visible plaque on teeth confers an elevated risk for

dental caries (odds ratio = 2.75) and the presence of

additional factors, such as snacking more than three

times daily between meals2 (odds ratio = 1.91), deep

pits and fissures (odds ratio = 1.93), inadequate saliva

flow (odds ratio = 1.37) and recreational drug use

(odds ratio = 2.03) can further increase the risk (39,

46).

For periodontitis, both endogenous risk factors

(such as genetics and diabetes mellitus) and exoge-

nous risk factors (e.g. cigarette smoking and

psychological stress) have been identified. Approxi-

mately 50% of the variance in clinical attachment

loss in a population may be attributable to heredity,

as indicated by the results of studies on twins 3(96). It

is estimated that at least 10–20 modifying genes are

involved in the onset and progression of chronic or

aggressive periodontitis, although attempts to iden-

tify these genes have shown controversial results (84,

131). Single gene mutations that are strongly associ-

ated with periodontitis, as reported for the CTSC gene 4

in the Papillon-Lefevre syndrome, are extremely rare

(84, 138). Diabetes mellitus type 1 and type 2, par-

ticularly in patients with poor glycemic control, have

been shown to increase the risk for periodontitis

(odds ratio = 2 to 3) (44, 56, 71, 92, 93, 122, 132, 141).

Probably the greatest exogenous risk factor for

periodontitis, with a dose-dependent relative risk of

5–6, is cigarette smoking (21). More than half of

all periodontitis cases in adults in the USA have been

attributed to smoking (135).

Trends in dental caries andperiodontal diseases

Oral biofilm-associated diseases may be as old as

mankind itself, as evidenced by signs of alveolar bone

loss in a 3-million-year-old hominid and other hu-

man remains from later time-periods (74). One of the

earliest descriptions of periodontal disease recorded

was in the army of the Greek general Xenophon,

P R D 3 6 0 B Dispatch: 11.3.10 Journal: PRD CE: Janaki Rekha

Journal Name Manuscript No. Author Received: No. of pages: 18 PE: Raymond 1

Periodontology 2000, Vol. 53, 2010, 1–18

Printed in Singapore. All rights reserved

� 2010 John Wiley & Sons A/S

PERIODONTOLOGY 2000

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dating back to 400 BC (74). Dental caries can be

traced back to the upper Palaeolithic area (70,000–

35,000 BC). However, compared with modern times,

dental caries may have been rare in those days (49,

79). The prevalence of caries and pulpal diseases rose

dramatically, however, when the widening availabil-

Table 1. Oral biofilm-associated diseases and their consequences 17

References

Oral biofilm-associated diseases

Gingivitis Mariotti 1999 (89)

Periodontitis (chronic, aggressive) Flemmig 1999 (48), Tonetti & Mombelli 1999 (137)

Necrotizing periodontal diseases Novak 1999 (105)

Abscesses of the periodontium Meng 1999 (94)

Periodontitis associated with endodontic lesions Meng 1999 (95)

Dental caries Domejean-Orliaguet et al. 2006 (39)

Pulpitits Levin et al. 2009 (80)

Apical periodontitis Gutmann et al. 2009 (58)

Peri-implant diseases Zitzmann et al. 2008 (153)

Candidosis Ramage et al. 2009 (115)

Diseases and conditions that may result from oral biofilm-associated diseases

Tooth loss See Table 3

Implant failure Pjetursson et al. 2007

Noma Enwonwu et al. 2000 (45)

Deep neck infections* Vieira et al. 2008 (143)

Osteomyelitis of the jaw* Sharkawy 2007 (125)

Maxillary sinusitis* Bomeli et al. 2009 (23)

Ludwig�s angina* Parahitiyawa et al. 2009 (111)

Orbital cellulitis* Parahitiyawa et al. 2009 (111)

Cervicofacial actinomycosis* Sharkawy 2007 (125)

Septicemia* Parahitiyawa et al. 2009 (111)

Death* Robertson and Smith 2009 (119)

Diseases that may be associated with hematogenous spreading of oral biofilm bacteria

Infective endocarditis Wilson et al. 2007 (149)

Acute bacterial myocarditis Parahitiyawa et al. 2009 (111)

Brain abscess Mueller et al. 2009 (99)

Liver abscess Wagner et al. 2006 (144)

Lung abscess Parahitiyawa et al. 2009 (111)

Cavernous sinus thrombosis Parahitiyawa et al. 2009 (111)

Prosthetic joint infection Bartzokas et al. 1994 (19)

Diseases and conditions for which periodontal inflammation is considered as a risk factor

Cardiovascular disease Persson and Persson 2008 (112)

Cerebrovascular disease Dorfer et al. 2004 (40)

Diabetes mellitus with poor glycemic control Lim et al. 2007 (82)

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ity and subsequent consumption of fermentable

carbohydrates in developed countries increased (75,

133).

Preventive efforts over the past decades have

markedly decreased caries experience in children,

adolescent and young adults, in most, but not all,

countries of the world (24, 147) (Fig. 1). Globally, the

mean decayed, missing, filled teeth index value in 12-

year-old children5 decreased from 1.74 in 2001 to 1.64

in 2004 (24, 146), but in some developing countries

(e.g. India and China), where traditional dietary pat-

terns and lifestyles have changed with increasing

economic wealth, caries experience has risen (24,

113). Among 12-year-old children6 , the dental caries

experience varies considerably in different parts of

the world. It is relatively high in the Americas (de-

cayed, missing, filled teeth index value = 2.76) and in

Europe (decayed, missing, filled teeth index va-

lue = 2.56), whereas the caries experience is lowest in

most of Africa (decayed, missing, filled teeth index

value = 1.15) and Asia (decayed, missing, filled teeth

index value = 1.12) (147) (Fig. 2). Caries experience in

adults remains high, with a prevalence approaching

100% in developed countries (41). The decrease in

caries prevalence in young age groups seen in

developed countries has been paralleled by a pro-

nounced increase in tooth retention among the

middle aged and elderly (16). As risk factors for caries

become more prevalent with increasing age (60, 66,

77), it is not surprising that tooth retention is asso-

ciated with higher mean decayed, missing, filled teeth

scores and an increased rate of root canal treatments

(62, 63).

The prevalence of periodontal diseases has shown

heterogeneous trends throughout the world over re-

cent years. The Community Periodontal Index of

Treatment Needs has improved in some parts of

Africa and Asia, whereas the prevalence of peri-

odontitis has remained unchanged, or even in-

creased, in other parts of Asia, America and Europe

(Figs 3 and 4). In most countries the periodontal

disease burden remains high, with approximately 5–

20% of adults and 2% of youths affected by severe

periodontitis (Fig. 5) (5, 113, 145). Although the

widely used Community Periodontal Index of Treat-

ment Needs allows some comparison between

countries, the information needs to be interpreted

with caution owing to a categorical and partial-

mouth assessment, which may underestimate the

true prevalence of periodontal disease (15). The lack

of a universally accepted definition of what consti-

tutes a periodontitis case makes assessment of the

true prevalence of periodontitis in various popula-

tions elusive (30).

Epidemiological surveys that have been conducted

in detail in developed countries with ready access to

professional dental care provide more insight

regarding the trends of periodontitis prevalence in

these populations. In Oslo, Norway, the proportion of

35-year-old subjects with detectable alveolar bone

loss showed a significant decrease from 54%, in 1973,

to 24%, in 2003. Furthermore, the percentage of

subjects with advanced periodontal destruction was

found to be reduced from 21.8%, in 1984, to 8.1%, in

2003 (127). Similar findings were reported in 20- to

80-year-old subjects in Jonkoping, Sweden. The pro-

portion of individuals with healthy gingivae increased

from 8 to 44%, whereas the proportion of individuals

DMFT decreased

DMFT increased or unchanged

No data available

Fig. 1. Changes in decayed, missing, filled teeth (DMFT)

scores in various regions of the world. Decayed, missing,

filled teeth scores have been considered as increased or

decreased when the most recent decayed, missing, filled

teeth values weremore than 0.3 different from the previous

decayed, missing, filled teeth value. Observation periods

ranged from 3 to 68 years in the various regions (148).

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1.4

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DM

FT

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8

0

3

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1

WHO-regions

Fig. 2. Weighted means of decayed, missing, filled teeth

(DMFT) scores in 12-year-old children in the World Health

Organization (WHO) regions in 2004 (147).

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with severe periodontitis remained largely un-

changed over a 30-year observation period (64). Sig-

nificantly improved oral hygiene scores accompanied

the improved periodontal health in the aforemen-

tioned populations.

The most dramatic improvement in periodontal

health has been reported in the USA where the esti-

mated prevalence of periodontitis decreased from

87% (in 1955) to 4.2% in 2002–2004 (30). Although

these numbers need to be interpreted with caution

given that different periodontal assessment parame-

ters were used and periodontitis case definitions were

not uniform throughout the years, the improvement

in periodontal health seen in the USA is most

remarkable. Improved oral hygiene (52) and reduced

smoking habits (65) have been associated with the

decrease in periodontitis prevalence. Little attention,

however, has been given to the fact that there are

approximately 130,000 active dental hygienists in the

USA, by far the greatest number of dental hygienist

per capita in the world. In 1996, 42.9% of Americans

(115 million) had at least one dental visit and, of

these, approximately 75% (86 million Americans) had

at least one dental visit for preventive care (54). Of all

procedures performed in US dental offices in 2004,

more than 30% were preventive in nature (87). From

1990 to 1999 alone, the number of prophylaxes per-

formed increased from 178.5 million to 191 million,

and the number of periodontal maintenance proce-

dures increased from 9.8 million to 12.7 million. Over

the same time-period, scaling and root planing pro-

cedures decreased from 14.1 million to 10.8 million,

supporting the notion of a reduced periodontal

treatment need in the USA (26).

Impact of oral biofilm-associateddiseases on quality of life

Oral biofilm-associated diseases may impact an

individual�s ability to function as well as affect the

perception of well-being in physical, mental and so-

CPITN 3 decreased

CPITN 3 increased or unchanged

No data available

Fig. 3. Prevalence trends of mild to moderate periodon-

titis in various regions of the world. The prevalence of

Community Periodontal Index of Treatment Needs

(CPITN) three values have been considered to be de-

creased or increased when there was a difference of ‡ 5%

between the most recently and previously reported CPITN

values. Changes cover observation periods ranging from 3

to 22 years (145). Note that the increased periodontitis

prevalence in the USA reported by the World Health

Organization is contradicted by national data showing a

reduction in periodontitis prevalence (30).

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60

70

80

90

0 1 2 3 4

15–19 years

35–44 years>65 years

% g

lob

al p

op

ula

tio

n

CPITN

Fig. 5. Estimated global periodontal disease prevalence.

Mean Community Periodontal Index of Treatment Needs

(CPITN) scores were shown for the following age groups:

15–19 years (89 countries); 35–44 years (89 countries);

and 65–74 years (28 countries). Error bars indicate stan-

dard deviation (145).

CPITN 4 decreased

CPITN 4 increased/stable

No data available

Fig. 4. Trends in severe periodontitis prevalence in

countries around the world. The prevalence of Commu-

nity Periodontal Index of Treatment Needs (CPITN) four

values have been considered as decreased or increased

when there was a difference of ‡ 5% between the most

recently and previously reported CPITN values. Changes

cover observation periods ranging from 3 to 22 years

(145). Note that the increased periodontitis prevalence in

the USA, reported by the World Health Organization, is

contradicted by national data showing a reduction in

periodontitis prevalence (30).

COLOR

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cial domains of life (32). Specific instruments to as-

sess oral health-related quality of life have been

developed (59). Most of the assessments capture

attributes ranging from the domains of symptoms

(e.g. pain, comfort), physical aspects (eating, speech,

appearance), psychological aspects (confidence,

mood, personality), to social aspects, such as social

life, work and finances.

A recent systematic review indicated that dental

caries in children is associated with reduced oral

health-related quality of life (18). In adolescents and

adults, the impact of dental caries on oral health-

related quality of life is less clear and appears to be

most pronounced in populations exhibiting high

dental caries prevalence. Among Brazilian adoles-

cents with a high prevalence of caries (88.3%), a

positive correlation was found between Oral Health

Impact Profile scores, where higher scores indicate

impairment of oral health-related quality of life, and

decayed teeth (22). However, in a Swedish population

with an overall low prevalence and low incidence of

caries, oral health-related quality of life measures

were unable to discriminate between individuals with

high or no caries experience (108). Similarly, among

adults, coronal decayed surfaces and the Root Caries

Index were associated with patient-based scores only

in a cohort exhibiting high disease prevalence

(1.6 ± 3.0; 0.1 ± 0.2, respectively), but not in a cohort

having a low disease prevalence (0.9 ± 2.3; 0.02 ± 0.1,

respectively) (68). Other findings, showing decayed

teeth to be negatively associated with almost all

dimensions of the Dental Impact of Daily Living and

positively associated with Oral Health Impact Profile

14 scores, support the notion that untreated teeth

with caries have a negative impact on perceived oral

health-related quality of life (76, 78). Restorative

treatment in young children with severe dental caries

experience was shown to substantially improve oral

health-related quality of life and positively impact

families (86). Information regarding the impact of

restorative measures on oral health-related quality of

life in other populations and age groups is sparse.

Caries, trauma and dental restorationsmay result in

pulpal and apical diseases. Although pain is recog-

nized as a cardinal symptom of reversible and irre-

versible pulpitis, symptomatic apical periodontitis

and acute apical abscess (58, 80), there is a paucity of

information regarding the impact of these diseases on

other oral health-related quality of life attributes.

Arguably, the greatest and most immediate impact on

patient-centered outcomes may be relieving acute

pain resulting from root canal treatment of pulpal and

apical diseases. Given the favorable long-term success

rates of root canal treatment, the reoccurrence of

symptoms that may impact oral health-related quality

of life appears to be rare (139). A comprehensive

assessment of the impact of root canal treatment on

oral health-related quality of life, however, is lacking.

Chronic forms of periodontal diseases have long

been viewed as silent diseases that are not noticed by

affected patients. However, recent findings indicating

a considerable impact of periodontitis on oral health-

related quality of life measures have challenged this

concept (68, 69, 76, 78). A negative impact across a

wide range of physical, social and psychological as-

pects of quality of life were found among individuals

with periodontitis. UK oral health-related quality of

life (oral health-related quality of life-UK) scores,

ranging from 16 (poorest) to 80 (best), were negatively

associated with patient�s self-reported periodontal

health experiences of swollen gums, sore gums,

receding gums, loose teeth, drifting teeth, bad breath

and toothache. A significant, negative correlation be-

tween the number of teeth with pocket probing depth

of ‡ 5 mm and oral health-related quality of life-UK

was found (103). In another study, having more than

eight teeth with pocket probing depths of > 5 mm

compared to having fewer than three teeth with

pocket probing depths of > 5 mm was associated

with worse perceived oral health (odds ratio = 1.45

and odds ratio = 2.83, respectively) (34). Using the

EuroQoL 7assessment, pain or discomfort were found

among 6.1% of those with gingivitis, 11.1% of those

with gingival recessions and 25.8% of individuals with

pocket probing depths of ‡ 6 mm (25). With the

exception of pain and eating restriction, gingival

bleeding, calculus and periodontal pockets were

found to be negatively associated with all Dental

Impact of Daily Living measures. When gingival

bleeding, calculus and number of periodontal

pockets increased, respondents� satisfaction regarding

appearance, performance, comfort and the total

Dental Impact of Daily Living score decreased (78).

Among adolescents, both attachment loss (odds ra-

tio = 2.0) and necrotizing ulcerative gingivitis (odds

ratio = 1.6) were significantly associated with negative

impact on oral health-related quality of life (85). In

children, more than one-fifth perceived bleeding and

swollen gums to impact on their lives (51).

Patients receiving regular periodontal supportive

therapy have reported significantly better average oral

health-related quality of life-UK scores (55.7) than

patients with untreated periodontitis (47.7), indicating

the positive effect that periodontal therapy has on oral

health-related quality of life (103). These cross-

sectional observations have been further substanti-

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ated by longitudinal clinical trials demonstrating that

nonsurgical periodontal therapy improves oral health-

related quality of life in patients with periodontitis (13,

69, 109). Improvements in oral health-related quality

of life measures resulting from nonsurgical perio-

dontal therapy were detected within 1 week after

therapy, whereas oral health-related quality of life

scores were found to deteriorate in the first few days

following periodontal flap surgery and returned to

baseline levels within 1 week (109). The long-term

effect of surgical periodontal therapy on oral health-

related quality of life has not been assessed.

Oral biofilm-associated diseases remain the major

cause for tooth loss in the developed world. Generally,

caries caused by periodontal diseases were the reason

for 76% (ranging from 48 to 97%) of all tooth

extractions (1, 2, 4, 9, 27, 29, 70, 73, 91, 100, 107, 114,

117, 118, 130, 140) (Table 2). The number of teeth

present was positively correlated with perceived

satisfaction of an individuals� oral condition. The

presence of anterior teeth was the most significant

predictor for satisfaction, whereas the presence of

molar pairs added little value to satisfaction (42). The

presence of teeth is important for daily activities,

including opportunity for conversation with family

members or others8 , regular physical activities and

attending meetings or group outings (152). Oral Im-

pacts on Daily Performances scores were found to be

highest among dentate seniors with the lowest num-

ber of teeth (126). A minimum of 20 teeth, with 9–10

pairs of contacting units (including anterior teeth), is

generally associated with adequate masticatory effi-

ciency, as assessed by comminution efficiency and

self-reported masticatory ability. However, there is

marked variation in subjective measures of esthetics

and psychosocial comfort among age groups, social

classes, cultures, regions and countries (3, 55).

Restoring edentulous jaws with conventional

complete dentures has resulted in an improvement in

oral health-related quality of life, as measured using

Oral Health Impact Profile scores (6, 7). Compelling

evidence has been presented in a recently published

systematic review that edentulous patients are more

satisfied with implant-supported overdentures than

conventional complete dentures, particularly in the

mandible. Furthermore, implant-supported over-

dentures may significantly improve oral health-

related quality of life (134). Evidence to support an

impact of mandibular implant-supported overden-

ture on perceived general health, however, is lacking

(43). For the edentulous maxilla, implant-supported

prostheses were generally rated as not different from

conventional completed maxillary dentures (134).

In partially edentulous patients (Kennedy Class I),

the replacement of at least the first molars using a

removable dental prosthesis has been shown to im-

prove Oral Health Impact Profile scores. It, however,

did not show any advantage over a fixed premolar

occlusion in terms of oral health-related quality of life

measures (151). The quality of removable partial

dentures, as assessed by denture stability and

esthetics, is directly associated with the perceived

quality of life in partially edentulous patients (67).

Information regarding oral health-related quality of

life or satisfaction outcomes for the majority of other

forms of prosthetic dentistry is sparse.

Systemic implications of oralbiofilm-associated diseases

Oral biofilm-associated diseases may affect systemic

health by (i) spreading infections to adjacent tissues

and spaces, (ii) hematogenous dissemination of

oral biofilm bacteria, or (iii 9) through inflammatory

mechanisms.

Acute forms of odontogenic infections may spread

into the adjacent tissues, causing osteomyelitis of the

jaws, maxillary sinusitis, noma, deep neck infections,

Ludwig�s angina, orbital cellulitis, skin ulcers, cervi-

cofacial actinomycosis, septicemia and, in rare cases,

even death (23, 45, 111, 119, 125, 143) (Table 1).

Odontogenic infections can be life threatening. Mor-

tality rates of descending necrotizing mediastinitis,

resulting fromodontogenic infections and noma, have

been reported to range from 50 to 80% when no ade-

quate therapy was rendered (88). It is therefore not

surprising that in medieval Europe, dental caries and

periodontal diseases were associated with an in-

creased risk of death (37). According to church regis-

tries from the 18th and 19th centuries, �dental fever�

was given as the cause of death in 30% of infants (8).

Although medical advances and improved access to

care formanypopulationshavedrastically reduced the

mortality rate resulting from dental infections, there

are still approximately 21,000 hospital admissions and

at least 150deaths causedby odontogenic infections in

the USA every year (53) and approximately 770,000

cases of life-threatening noma worldwide (17, 98).

Oral biofilms represent an abundant reservoir of

microorganisms that may spread via transient bac-

teremia, as demonstrated by the types of oral bio-

films isolated from infections remote from the oral

cavity (81). Shedding and subsequent hematogenous

dissemination of oral biofilm bacteria have been

associated with some forms of infective endocarditis,

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acute bacterial myocarditis, brain abscess, liver ab-

scess, lung abscess, cavernous sinus thrombosis and

prosthetic joint infections (19, 99, 102, 111, 142, 144,

149) (Table 1). The incidence of organ infections

associated with oral biofilm bacteria appears to be

extremely low as the supporting evidence is mostly

based on case reports (99, 102, 111, 142, 144). The

incidence of infective endocarditis caused by viridans

group streptococci is estimated to be 1.7–6.2 cases

per 100,000 patient years. Men are twice as often af-

fected as women, and the incidence of infective

endocarditis increases with age (101). In Finland, the

number of septicemias in adults caused by viridans

group streptococci has almost doubled over the past

decade. Interestingly, this number is directly pro-

portional to the number of individuals remaining

dentate throughout their lives (116). One can only

speculate whether the increased retention of teeth in

seniors, together with an increased life expectancy in

many parts of the world, may lead to a rise in infec-

tive endocarditis.

The notion that oral biofilms may impact systemic

health by inflammatory mechanisms is supported by

cross-sectional studies reporting elevated systemic

inflammatory markers in patients with periodontitis

(28, 33, 36, 83, 128). Strong evidence supports the oral–

Table 2. Reasons presented for tooth extraction related to oral biofilm-associated diseases in various geographicregions

Author Year Country Extracted teeth

(n)

Dental caries (%) Periodontal

disease (%)

Total (%)

Cahen et al.

(27)

1985 France 14621 49 32 81

Kay and Blink-

horn (70)

1986 Scotland 2190 50 21 71

Agerholm and

Sidi (1)

1988 Enland ⁄ Wales 5274 48 27 75

Chauncey et al.

(29)

1989 US 1142 33 19 52

Klock et al. (73) 1991 Norway 985 35 19 54

Stephens et al.

(130)

1991 Canada 2510 63 34 97

Reich and Hiller

(117)

1993 Germany 1215 21 27 48

Phipps and

Stevens (114)

1995 US 1877 51 35 86

Ong et al. (107) 1996 Singapore 272 35 36 71

Angelillo et al.

(9)

1996 Italy 1056 34 33 68

Murray et al.

(100)

1997 Canada 1710 29 26 55

McCaul et al.

(91)

2001 Scotland 2558 55 17 72

Trovik et al.

(140)

2001 Norway 1495 40 24 64

Richards et al.

(118)

2005 South Wales 558 59 29 88

Aida et al. (2) 2006 Japan 9115 33 42 75

Al-Shammari

et al. (4)

2006 Kuwait 2783 44 37 81

Weighted mean 76

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systemic link between periodontitis and cardiovascu-

lar diseases, cerebrovascular diseases and diabetes

mellitus, all of which have an inflammatory etiology. A

number of cross-sectional and cohort studies have

demonstrated consistent associations between peri-

odontitis and cardiovascular disease, irrespective of

common underlying risk factors or confounders such

as smoking, age, education, body mass index and

lifestyle factors (112). Hazard ratios and relative risk

ratios for fatal and nonfatal coronary events have been

reported to range from 1.5 to 2.0 in individuals with

periodontitis (20, 38); the adjusted risk ratio for cere-

bral ischemia is 7.4 (31, 40). In diabetic patients, peri-

odontitis has been identified as a risk factor for poor

glycemic control (31, 82, 104, 132). The association of

periodontitis with adverse pregnancy outcomes,

osteoporosis, cancer and chronic obstructive pulmo-

nary diseases remains controversial (14, 47, 72, 150).

There is some evidence to support that treatment

of periodontitis may improve glycemic control in

diabetic patients (50). Periodontal therapy also has

been shown to reduce inflammatory biomarkers,

improve surrogate measures of vascular endothelial

function (136) and thereby possibly exert an effect on

inflammatory vascular diseases. However, direct

evidence that periodontal therapy may reduce the

risk for cardiovascular or cerebrovascular diseases is

lacking. With regard to adverse pregnancy outcomes,

an intervention trial with more than 800 enrolled

patients demonstrated that treatment of periodontal

disease improved periodontal conditions, but did not

significantly reduce the risk of adverse pregnancy

outcomes (97).

Financial expenditures for dentalservices related to oral biofilm-associated diseases

In order to estimate the costs of managing oral bio-

film-associated diseases, the national expenditures

for professional dental services related to these dis-

eases were calculated. For this purpose, the 500 +

10 dental procedures listed in the Current Dental Ter-

minology 2009 ⁄ 2010 of the American Dental Asso-

ciation (11) were categorized based on whether they

are used primarily for the prevention (A), diagnosis,

or treatment of oral biofilm-associated diseases and

their sequelae, primarily for conditions unrelated to

oral biofilm-associated diseases (B) or for oral bio-

film-associated diseases as well as other oral condi-

tions (C). Although there may be instances in which

procedures that were assigned to category A or cat-

egory B are used for other purposes, the frequency of

this occurrence was considered to be negligible.

Where reliable data were available, the proportions of

category C procedures used for oral biofilm-associ-

ated diseases or other oral conditions were deter-

mined. For example, 86% of tooth extractions in the

USA are the result of caries (114), while 14% of

extractions were considered to be related to condi-

tions other than oral biofilm-associated diseases. The

same proportions (i.e. 86–14%) were applied to res-

torations, such as fixed prostheses or implant-sup-

ported restorations, aimed at replacing lost teeth. For

other procedures where no reliable data were avail-

able, the proportion of each procedure used for the

management of biofilm-associated diseases was

estimated using expert opinion (Table 3). Using the

ADA 112005–06 Survey of Dental Services Rendered

(10), and the 50th percentile of the national fees for

dental procedures (12), it was estimated that 87% of

all dental procedures rendered were related to the

prevention, diagnosis and management of oral bio-

film-associated diseases in dental offices; the cost of

these dental procedures corresponded to 90% of the

national expenditures for dental services, amounting

to $81 billion in 2006 (124). These figures do not

include the approximately $9 billion in expendi-

tures for oral hygiene products sold in the USA in

2006 (90).

Oral biofilm-associated diseasesare among the most costly medicalconditions

The estimated national expenditures for oral biofilm-

associated diseases in the USA have almost doubled

from 1997 to 2006. In 2006, the estimated national

expenditures for oral biofilm-associated diseases to-

taled $81 billion and were greater than for any one of

the five most expensive medical conditions reported

by the Medical Expenditure Panel Survey: heart

conditions ($78.0 billion); trauma-related disorders

($68.1 billion); cancer ($57.5 billion); mental disor-

ders ($57.2 billion); and pulmonary conditions ($51.3

billion) (Fig. 6) (106, 124, 129).

Concluding remarks

Oral biofilm-associated diseases, and their sub-

sequent diseases and conditions, have broad impli-

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Flemmig

Inserted Text

or periodontal disease

Table 3. Procedures assumed to be performed that are unrelated to oral biofilm-associated diseases 18

CDT code Description

Estimated percentage

unrelated to oral

biofilm-associated

diseases (%)

Diagnostic

D0120 Periodic oral evaluation* 10

D0140 Limited oral evaluation* 10

D0150 Comprehensive oral

evaluation*

10

D0160 Detailed and extensive oral

evaluation*

10

D0170 Re-evaluation* 10

D0180 Comprehensive periodontal

evaluation*

10

D0210–D0230 Intra-oral radiographs,

peri-apical radiographs*

10

D0270–D0274 Bitewing radiographs* 10

D0330 Panoramic film* 23

D0340

Cephalometric film

100

D0350 Oral ⁄ facial photographic

images

100

D0431

Adjunctive test for mucosal

abnormalities

100

D0460 Pulp vitality tests* 10

D0470 Diagnostic casts* 10

Preventive

D1510 ⁄ 1515 Space maintainer – fixed 100

D1520 ⁄ 1525

Space maintainer – removable

100

Restorative

D2330 Resin-based composite – one

surface, anterior�20

D2391

Resin-based composite – one

surface, posterior�

20

D2710–2794 Crown – single restoration� 10

D2950

Core buildup�

10

D2952–2954, 2957 Post and core� 10

D2960–2962

Labial veneer

100

Endodontics

D3351–3353 Apexification ⁄ recalcification 100

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Table 3. (Continued) 18



unrelated to oral

biofilm-associated

diseases (%)

Periodontics

D4270,4271

Free soft tissue graft,

subepithelial connective

tissue graft

100

Maxillofacial prosthetics

D5982 ⁄ 5988 Surgical stent, surgical splint 100

Implant services

D6010 Surgical placement of implant

body§14

D6053 ⁄ 6054

Implant ⁄ abutment-supported

removable denture§

14

D6056 Prefabricated abutment§ 14

D6057

Custom abutment§14

D6058–6067, 6094

Abutment- or implant-

supported supported crown§

14

D6068–6077, 6194 Abutment- or implant-

supported retainer§14

Prosthodontics (fixed)

D6205–6252 Pontic§ 24

D6710–6792, 6794 Crown§ 24

Oral and maxillofacial surgery

D7111, 7140 Extraction– 14

D7210, 7210 Surgical extraction– 14

D7220 Removal of impacted tooth –

soft tissue

100

D7230–7241 Removal of impacted tooth –

bony

100

D7261 Primary closure of a sinus

perforation

100

D7280 Surgical access of an

unerupted tooth

100

D7283 Placement of device to

facilitate eruption

100

D7340 ⁄ 7350 Vestibuloplasty – ridge

extension

100

D7410-7411 Excision of benign lesion 100

D7412 Excision of benign lesion,

complicated

100

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unrelated to oral

biofilm-associated

diseases (%)

D7413–7415 Excision of malignant lesion 100

D7450 ⁄ 7460 Removal of benign

odontogenic cyst or tumor

100

D7451 ⁄ 7461 Removal of benign

odontogenic cyst or tumor

100

D7471 ⁄ 7485 Removal of lateral exostosis 100

D7472 ⁄ 7473 Removal of torus palatinus or

torus mandibularis

100

D7610 ⁄ 7620 Simple fracture maxilla 100

D7630 ⁄ 7640 Simple fracture mandible 100

D7670 ⁄ 7671 Alveolus – simple 100

D7680 Facial bones – simple –

complicated reduction

100

D7710 ⁄ 7720 Compound facture maxilla 100

D7730 ⁄ 7740 Compound fracture mandible 100

D7780 Facial bones – compound –

complicated reduction

100

D7820 Closed reduction of dislocation 100

D7865 Arthroplasty 100

D7870 Arthrocentesis 100

D7872–7877 Arthroscopy – surgical 100

D7880 Occlusal orthotic device 100

D7941 ⁄ 7943 Osteotomy – mandibular rami 100

D7945 Osteotomy – body of mandible 100

D7950 Osseous, osteoperiosteal, or

cartilage graft

100

D7955 Repair of maxillofacial soft

and ⁄ or hard tissue defect

100

D7960 ⁄ 7963 Frenulectomy or frenotomy 100

Orthodontics

D8010 Limited orthodontic treatment

– primary dentition

100


– transitional dentition

100


– adolescent dentition

100


– adult dentition

100

D8050 Interceptive orthodontic treat-

ment of the primary dentition

100

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unrelated to oral

biofilm-associated

diseases (%)

D8060 Interceptive orthodontic

treatment of the transitional

dentition

100

D8070 Comprehensive orthodontic

treatment of the transitional

dentition

100


treatment of the adolescent

dentition

100


treatment of the adult denti-

tion

100

D8210 Removable appliance therapy 100

D8220 Fixed appliance therapy 100

D8660 Pre-orthodontic treatment visit 100

D8670 Periodic orthodontic treatment

visit

100

D8680 Orthodontic retention 100

D8690 Orthodontic treatment

(alternative billing)

100

D8691 Repair of orthodontic

appliance

100

D8692 Replacement of lost or broken

retainer

100

D8999 Unspecified orthodontic

procedure

100

Adjunctive general services

D9220 Deep sedation ⁄ general anes-

thesia – first 30 minutes

100

D9221 Deep sedation ⁄ general

anesthesia – each additional

15 minutes

100

D9230 Analgesia, anxiolysis,

inhalation of nitrous oxide

100

D9241 ⁄ 9242 Intravenous conscious

sedation ⁄ analgesia

100

D9248 Nonintravenous conscious

sedation

100

D9610 Therapeutic parenteral drug 100

D9910 ⁄ 9911 Desensitizing

medicament ⁄ resin

100

D9920 Behavior management 100

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cations on systemic health and oral health-related

quality of life, and pose a significant cost burden on

societies. Considerable strides have been made in the

prevention and management of oral biofilm-associ-

ated diseases and their sequelae. Caries is a formida-

ble example of the success of preventive measures, as

shown by the substantial decline in its prevalence

reported by many developed countries. With respect

to the prevention of periodontitis, however, success of

prevention is less apparent and varies greatly between

populations. Despite the great progress that has been

made, large portions of the world�s population remain

affected by oral biofilm-associated diseases. If the

disease burden is to be further reduced, new andmore

cost-effective prevention and treatment strategies are

needed that result in sustained oral health with min-

imal reliance on patients� compliance and regular

access to professional dental care.

The following assumptions were made with regard

to the proportion of procedures that may be em-

ployed for both oral biofilm-associated and other

conditions.

• as 10% of all therapeutic procedures were found to

be unrelated to oral biofilm-associated diseases, the

same proportion of all diagnostic procedures was

assumed to be unrelated to oral biofilm-associated

diseases. Panoramic films include those taken by

orthodontists.

• 20% of all resin-based composites are used for

noncarious cervical lesions.

• 10% of all crowns, core buildup, post and core are

performed for esthetic reasons.

• as 14% of all teeth are extracted for reasons other

than caries or periodontal disease, the same pro-

portion of procedures aimed at replacing lost teeth




unrelated to oral

biofilm-associated

diseases (%)

D9940 ⁄ 9941 Occlusal guard ⁄ athletic

mouthguard

100

D9942 Repair and ⁄ or reline of

occlusal guard

100

D9951 ⁄ 9952 Occlusal adjustment 100

D9970 Enamel microabrasion 100

D9972 ⁄ 9973 External bleaching 100

D9974 Internal bleaching 100

0

10

20

30

40

50

60

70

80

90

1997 2002 2006

$ b

illi

on

s

Year

Oral biofilm-associated diseasesHeart conditions

Trauma-related disorders

Cancer

Mental disorders

Pulmonary conditions

Fig. 6. National expenditures for the most costly

medical conditions and oral biofilm-associated diseases

in the USA in 1997, 2002 and 2006. Expenditures are

defined as the sum of direct payments for care provided

during the year, including out-of-pocket payments and

payments by private insurance, Medicaid, Medicare and

other sources. International Classification of Diseases,

Ninth Revision (ICD-9) condition codes are aggregated

into clinically meaningful categories that group similar

conditions using Clinical Classification System (CCS)

software. Cancer includes CCS codes 11–45; heart con-

ditions, CCS codes 96, 97 and 100–108; pulmonary

conditions (COPD16 , asthma), CCS codes 127–134; trauma,

CCS codes 225–236, 239, 240 and 244; and mental

disorders, CCS codes 650–663. Expenditures for oral

biofilm-associated diseases are estimates corresponding

to 90% of the national expenditures for dental services

(106, 124, 129).

COLOR

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was assumed to be unrelated to oral biofilm-asso-

ciated diseases. Fixed prosthodontics procedures

include 10% performed for esthetic reasons.

• average percentage of extractions performed for

reasons other than caries or periodontal disease

based on the data presented in Table 2.

References

1. Agerholm DM, Sidi AD. Reasons given for extraction of

permanent teeth by general dental practitioners in England

and Wales. Br Dent J 1988: 164: 345–348.

2. Aida J, Ando Y, Akhter R, Aoyama H, Masui M, Morita M.

Reasons for permanent tooth extractions in Japan. J Epi-

demiol 2006: 16: 214–219.

3. Akifusa S, Soh I, Ansai T, Hamasaki T, Takata Y, Yohida A,

Fukuhara M, Sonoki K, Takehara T. Relationship of

number of remaining teeth to health-related quality of life

in community-dwelling elderly. Gerodontology 2005: 22:

91–97.

4. Al-Shammari KF, Al-Ansari JM, Al-Melh MA, Al-Khabbaz

AK. Reasons for tooth extraction in Kuwait.Med Princ Pract

2006: 15: 417–422.

5. Albandar JM, Brown LJ, Loe H. Clinical features of

early-onset periodontitis. J Am Dent Assoc 1997: 128: 1393–

1399.

6. Allen F, Locker D. A modified short version of the oral

health impact profile for assessing health-related quality of

life in edentulous adults. Int J Prosthodont 2002: 15: 446–

450.

7. Allen PF, Thomason JM, Jepson NJ, Nohl F, Smith DG, Ellis

J. A randomized controlled trial of implant-retained man-

dibular overdentures. J Dent Res 2006: 85: 547–551.

8. Alt KW NN, Held P, Meyer C, Roßbach A, Burwinkel M

Zahne als Gesundheits- und Mortalitatsrisiko Rahden.

Westfalia, Germany: Marie Leidorf Verlag 2006: 25–42.12

9. Angelillo IF, Nobile CG, Pavia M. Survey of reasons for

extraction of permanent teeth in Italy. Community Dent

Oral Epidemiol 1996: 24: 336–340.

10. Anonymous. 2005–06 Survey of dental services rendered.

Chicago, IL: American Dental Association, 2007.

11. Anonymous. Current Dental Terminology 2009–2010. Chi-

cago, IL: American Dental Association, 2008.

12. Anonymous. National dental advisory service comprehen-

sive fee report 2007. In, 2007.

13. Aslund M, Suvan J, Moles DR, D�Aiuto F, Tonetti MS. Ef-

fects of two different methods of non-surgical periodontal

therapy on patient perception of pain and quality of life: a

randomized controlled clinical trial. J Periodontol 2008: 79:

1031–1040.

14. Azarpazhooh A, Leake JL. Systematic review of the associ-

ation between respiratory diseases and oral health.

J Periodontol 2006: 77: 1465–1482.

15. Baelum V, Fejerskov O, Manji F, Wanzala P. Influence of

CPITN partial recordings on estimates of prevalence and

severity of various periodontal conditions in adults.

Community Dent Oral Epidemiol 1993: 21: 354–359.

16. Baelum V, van Palenstein Helderman W, Hugoson A, Yee R,

Fejerskov O. A global perspective on changes in the burden

of caries and periodontitis: implications for dentistry.

J Oral Rehabil 2007: 34: 872–906; discussion 940.

17. Baratti-Mayer D, Pittet B, Montandon D, Bolivar I, Bornand

JE, Hugonnet S, Jaquinet A, Schrenzel J, Pittet D; Geneva

Study Group on Noma. Noma: an ‘‘infectious’’ disease of

unknown aetiology. Lancet Infect Dis 2003: 3: 419–431.

18. Barbosa TS, Gaviao MB. Oral health-related quality of life

in children: part II. Effects of clinical oral health status. A

systematic review. Int J Dent Hyg 2008: 6: 100–107.

19. Bartzokas CA, Johnson R, Jane M, Martin MV, Pearce PK,

Saw Y. Relation between mouth and haematogenous

infection in total joint replacements. BMJ 1994: 309: 506–

508.

20. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S.

Periodontal disease and cardiovascular disease. J Period-

ontol 1996: 67: 1123–1137.

21. Bergstrom J. Tobacco smoking and chronic destructive

periodontal disease. Odontology 2004: 92: 1–8.

22. Biazevic MG, Rissotto RR, Michel-Crosato E, Mendes LA,

Mendes MO. Relationship between oral health and its

impact on quality of life among adolescents. Braz Oral Res

2008: 22: 36–42.

23. Bomeli SR, Branstetter BFt, Ferguson BJ. Frequency of a

dental source for acute maxillary sinusitis. Laryngoscope

2009: 119: 580–584.

24. Bratthall D. Estimation of global DMFT for 12-year-olds in

2004. Int Dent J 2005: 55: 370–372.

25. Brennan DS, Spencer AJ, Roberts-Thomson KF. Quality of

life and disability weights associated with periodontal

disease. J Dent Res 2007: 86: 713–717.

26. Brown LJ, Johns BA, Wall TP. The economics of periodontal

diseases. Periodontol 2000 2002: 29: 223–234.

27. Cahen PM, Frank RM, Turlot JC. A survey of the reasons for

dental extractions in France. J Dent Res 1985: 64: 1087–

1093.

28. Chapple IL. The impact of oral disease upon systemic

health – symposium overview. J Dent 2009: 37: S568–S571.

29. Chauncey HH, Glass RL, Alman JE. Dental caries. Principal

cause of tooth extraction in a sample of US male adults.

Caries Res 1989: 23: 200–205.

30. Cobb CM, Williams KB, Gerkovitch MM. Is the prevalence

of periodontitis in the USA in decline? Periodontol 2000

2009: 50: 13–24.

31. Collin HL, Uusitupa M, Niskanen L, Kontturi-Narhi V,

Markkanen H, Koivisto AM, Meurman JH. Periodontal

findings in elderly patients with non-insulin dependent

diabetes mellitus. J Periodontol 1998: 69: 962–966.

32. Coons SJ, Rao S, Keininger DL, Hays RD. A comparative

review of generic quality-of-life instruments. Pharmaco-

economics 2000: 17: 13–35.

33. Craig RG, Yip JK, So MK, Boylan RJ, Socransky SS,

Haffajee AD. Relationship of destructive periodontal

disease to the acute-phase response. J Periodontol 2003: 74:

1007–1016.

34. Cunha-Cruz J, Hujoel PP, Kressin NR. Oral health-related

quality of life of periodontal patients. J Periodontal Res

2007: 42: 169–176.

35. Davies D. Understanding biofilm resistance to antibacterial

agents. Nat Rev Drug Discov 2003: 2: 114–122.

36. Deliargyris EN, Madianos PN, Kadoma W, Marron I, Smith

SC Jr, Beck JD, Offenbacher S. Periodontal disease in pa-

tients with acute myocardial infarction: prevalence and

14

Beikler & Flemmig

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

27

28

29

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

47

48

49

50

51

52

53

contribution to elevated C-reactive protein levels. Am

Heart J 2004: 147: 1005–1009.

37. Dewitte SN, Bekvalac J. Oral health and frailty in the

medieval English cemetery of St Mary Graces. Am J Phys

Anthropol 2009: ???: ???–???.13

38. Dietrich T, Jimenez M, Krall Kaye EA, Vokonas PS, Garcia

RI. Age-dependent associations between chronic perio-

dontitis ⁄ edentulism and risk of coronary heart disease.

Circulation 2008: 117: 1668–1674.

39. Domejean-Orliaguet S, Gansky SA, Featherstone JD. Caries

risk assessment in an educational environment. J Dent

Educ 2006: 70: 1346–1354.

40. Dorfer CE, Becher H, Ziegler CM, Kaiser C, Lutz R, Jorss D,

Lichy C, Buggle F, Bultmann S, Preusch M, Grau AJ. The

association of gingivitis and periodontitis with ischemic

stroke. J Clin Periodontol 2004: 31: 396–401.

41. Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-

Evans G, Eke PI, Beltran-Aguilar ED, Horowitz AM, Li CH.

Trends in oral health status: United States, 1988–1994 and

1999–2004. Vital Health Stat 2007: 11: 1–92.

42. Elias AC, Sheiham A. The relationship between satisfaction

with mouth and number, position and condition of teeth:

studies in Brazilian adults. J Oral Rehabil 1999: 26: 53–71.

43. Emami E, Heydecke G, Rompre PH, de Grandmont P, Feine

JS. Impact of implant support for mandibular dentures on

satisfaction, oral and general health-related quality of life: a

meta-analysis of randomized-controlled trials. Clin Oral

Implants Res 2009: 20: 533–544.

44. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in

non-insulin-dependent diabetes mellitus. J Periodontol

1991: 62: 123–131.

45. Enwonwu CO, Falkler WA, Idigbe EO. Oro-facial gangrene

(noma ⁄ cancrum oris): pathogenetic mechanisms. Crit Rev

Oral Biol Med 2000: 11: 159–171.

46. Featherstone JD, Domejean-Orliaguet S, Jenson L, Wolff M,

Young DA Caries risk assessment in practice for age 6

through adult. J Calif Dent Assoc 2007: 35: 703–707, 710–

703.

47. Fitzpatrick SG, Katz J. The Association Between Periodontal

Disease and Cancer: a Review of the Literature. J Dent 2010:

38: 83–95.

48. Flemmig TF. Periodontitis. Ann Periodontol 1999: 4: 32–38.

49. Forshaw RJ. Dental health and disease in ancient Egypt. Br

Dent J 2009: 206: 421–424.

50. Garcia R. Periodontal treatment could improve glycaemic

control in diabetic patients. Evid BasedDent 2009: 10: 20–21.

51. Gherunpong S, Tsakos G, Sheiham A. The prevalence and

severity of oral impacts on daily performances in Thai

primary school children. Health Qual Life Outcomes 2004:

2: 57.

52. Gjermo PE. Impact of periodontal preventive programmes

on the data from epidemiologic studies. J Clin Periodontol

2005: 32 (Suppl. 6): 294–300.

53. Goldberg MTR. Oral and Maxillofacial Infections, 4th edn.:

Elsevier Health Sciences, 2002: 158-188.

54. Goodman HS, Manski MC, Williams JN, Manski RJ. An

analysis of preventive dental visits by provider type, 1996.

J Am Dent Assoc 2005: 136: 221–228.

55. Gotfredsen K, Walls AW. What dentition assures oral

function? Clin Oral Implants Res 2007: 18 (Suppl. 3): 34–45.

56. Grossi SG. Assessment of risk for periodontal disease. I. Risk

indicators for attachment loss. J Periodontol 1994: 65: 260.

57. Grossner-Schreiber B, Teichmann J, Hannig M, Dorfer C,

Wenderoth DF, Ott SJ. Modified implant surfaces show

different biofilm compositions under in vivo conditions.

Clin Oral Implants Res 2009: 20: 817–826.

58. Gutmann JL, Baumgartner JC, Gluskin AH, Hartwell GR,

Walton RE. Identify and define all diagnostic terms for

periapical ⁄ periradicular health and disease States. J Endod

2009: 35: 1658–1674.

59. Hebling E, Pereira AC. Oral health-related quality of life: a

critical appraisal of assessment tools used in elderly peo-

ple. Gerodontology 2007: 24: 151–161.

60. Hintao J, Teanpaisan R, Chongsuvivatwong V, Ratarasan C,

Dahlen G. The microbiological profiles of saliva, supra-

gingival and subgingival plaque and dental caries in adults

with and without type 2 diabetes mellitus. Oral Microbiol

Immunol 2007: 22: 175–181.

61. Hojo K, Nagaoka S, Ohshima T, Maeda N. Bacterial inter-

actions in dental biofilm development. J Dent Res 2009: 88:

982–990.

62. Hugoson A, Koch G, Gothberg C, Helkimo AN, Lundin SA,

Norderyd O, Sjodin B, Sondell K. Oral health of individuals

aged 3–80 years in Jonkoping, Sweden during 30 years

(1973-2003). I. Review of findings on dental care habits and

knowledge of oral health. Swed Dent J 2005: 29: 125–138.

63. Hugoson A, Koch G, Gothberg C, Helkimo AN, Lundin SA,

Norderyd O, Sjodin B, Sondell K. Oral health of individuals

aged 3–80 years in Jonkoping, Sweden during 30 years

(1973-2003). II. Review of clinical and radiographic find-

ings. Swed Dent J 2005: 29: 139–155.

64. Hugoson A, Sjodin B, Norderyd O. Trends over 30 years,

1973-2003, in the prevalence and severity of periodontal

disease. J Clin Periodontol 2008: 35: 405–414.

65. Hujoel PP, del Aguila MA, DeRouen TA, Bergstrom J. A

hidden periodontitis epidemic during the 20th century?


66. Imazato S, Ikebe K, Nokubi T, Ebisu S, Walls AW. Preva-

lence of root caries in a selected population of older adults

in Japan. J Oral Rehabil 2006: 33: 137–143.

67. Inukai M, Baba K, John MT, Igarashi Y. Does removable

partial denture quality affect individuals� oral health? J Dent

Res 2008: 87: 736–739.

68. Jones JA, Kressin NR, Miller DR, Orner MB, Garcia RI, Spiro

A III. Comparison of patient-based oral health outcome

measures. Qual Life Res 2004: 13: 975–985.

69. Jowett AK, Orr MT, Rawlinson A, Robinson PG. Psychoso-

cial impact of periodontal disease and its treatment with

24-h root surface debridement. J Clin Periodontol 2009: 36:

413–418.

70. Kay EJ, Blinkhorn AS. The reasons underlying the extrac-

tion of teeth in Scotland. Br Dent J 1986: 160: 287–290.

71. Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha

WQ. Periodontal status of diabetics compared with non-

diabetics: a meta-analysis. J Diabetes Complications 2006:

20: 59–68.

72. Kim J, Amar S. Periodontal disease and systemic condi-

tions: a bidirectional relationship. Odontology 2006: 94:

10–21.

73. Klock KS, Haugejorden O. Primary reasons for extraction of

permanent teeth in Norway: changes from 1968 to 1988.


74. Langsjoen O, ed. Diseases of the dentition. Cambridge:

Cambridge University Press: 1998: 393–412.

15


1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

27

28

29

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

47

48

49

50

51

52

53

75. Larsen CS. Biological changes in human populations with

agriculture. Annual Review of Anthropology 1995: 24: 185–

213.

76. Lawrence HP, Thomson WM, Broadbent JM, Poulton R.

Oral health-related quality of life in a birth cohort of

32-year olds. Community Dent Oral Epidemiol 2008: 36:

305–316.

77. Le Pera AF, Mahevich RA, Silverstein H. Xerostomia and its

effects on the dentition. J N J Dent Assoc 2005: 76: 19–21.

78. Leao A, Sheiham A. Relation between clinical dental status

and subjective impacts on daily living. J Dent Res 1995: 74:

1408–1413.

79. Leek FF. Observations on the Dental Pathology Seen in

Ancient Egyptian Skulls. The Journal of Egyptian Archae-

ology 1966: 52: 59–64.

80. Levin LG, Law AS, Holland GR, Abbott PV, Roda RS. Iden-

tify and define all diagnostic terms for pulpal health and

disease States. J Endod 2009: 35: 1645–1657.

81. Li X, Kolltveit KM, Tronstad L, Olsen I. Systemic diseases

caused by oral infection. Clin Microbiol Rev 2000: 13: 547–

558.

82. Lim LP, Tay FB, Sum CF, Thai AC. Relationship between

markers of metabolic control and inflammation on severity

of periodontal disease in patients with diabetes mellitus.

J Clin Periodontol 2007: 34: 118–123.

83. Linden GJ, McClean K, Young I, Evans A, Kee F. Persistently

raised C-reactive protein levels are associated with ad-

vanced periodontal disease. J Clin Periodontol 2008: 35:

741–747.

84. Loos BG, John RP, Laine ML. Identification of genetic risk

factors for periodontitis and possible mechanisms of ac-

tion. J Clin Periodontol 2005: 32: 159.

85. Lopez R, Baelum V. Oral health impact of periodontal

diseases in adolescents. J Dent Res 2007: 86: 1105–1109.

86. Malden PE, Thomson WM, Jokovic A, Locker D. Changes in

parent-assessed oral health-related quality of life among

young children following dental treatment under general

anaesthetic. Community Dent Oral Epidemiol 2008: 36:

108–117.

87. Manski RJBE. Dental use, expenses, private dental cover-

age, and changes, 1996 and 2004. In: MEPS Chartbook No

17. Rockville, MD: Agency for Healthcare Research and

Quality, 2007.14

88. Marck KW. A history of noma, the ‘‘Face of Poverty’’. Plast

Reconstr Surg 2003: 111: 1702–1707.

89. Mariotti A. Dental plaque-induced gingival diseases. Ann

Periodontol 1999: 4: 7–19.

90. Markets Ra. Oral Hygiene: Global industry guide. In, 2009.

91. McCaul LK, Jenkins WM, Kay EJ. The reasons for extraction

of permanent teeth in Scotland: a 15-year follow-up study.

Br Dent J 2001: 190: 658–662.

92. Mealey B. American Academy of Periodontology Position

Paper - Diabetes and periodontal diseases. J Periodontol

2000: 71: 664.

93. Mealey BL, Oates TW. Diabetes mellitus and periodontal

diseases. J Periodontol 2006: 77: 1289–1303.

94. Meng HX. Periodontal abscess. Ann Periodontol 1999: 4:

79–83.

95. Meng HX. Periodontic-endodontic lesions. Ann Periodontol

1999: 4: 84–90.

96. Michalowicz BS, Diehl SR, Gunsolley JC, Sparks BS, Brooks

CN, Koertge TE, Califano JV, Burmeister JA, Schenkein HA.

Evidence of a substantial genetic basis for risk of adult

periodontitis. J Periodontol 2000: 71: 1699–1707.

97. Michalowicz BS, Hodges JS, DiAngelis AJ, Lupo VR, Novak

MJ, Ferguson JE, Buchanan W, Bofill J, Papapanou PN,

Mitchell DA, Matseoane S, Tschida PA; OPT Study. Treat-

ment of periodontal disease and the risk of preterm birth.

N Engl J Med 2006: 355: 1885–1894.

98. Mignogna MD, Fedele S. The neglected global burden of

chronic oral diseases. J Dent Res 2006: 85: 390–391.

99. Mueller AA, Saldamli B, Stubinger S, Walter C, Fluckiger U,

Merlo A, Schwenzer-Zimmerer K, Zeilhofer HF, Zimmerer

S. Oral bacterial cultures in nontraumatic brain abscesses:

results of a first-line study. Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2009: 107: 469–476.

100. Murray H, Clarke M, Locker D, Kay EJ. Reasons for tooth

extractions in dental practices in Ontario, Canada accord-

ing to tooth type. Int Dent J 1997: 47: 3–8.

101. Mylonakis E, Calderwood SB. Infective endocarditis in

adults. N Engl J Med 2001: 345: 1318–1330.

102. Mylonas AI, Tzerbos FH, Mihalaki M, Rologis D, Boutsi-

kakis I. Cerebral abscess of odontogenic origin. J Cranio-

maxillofac Surg 2007: 35: 63–67.

103. Needleman I, McGrath C, Floyd P, Biddle A. Impact of oral

health on the life quality of periodontal patients. J Clin

Periodontol 2004: 31: 454–457.

104. Nelson RG, Shlossman M, Budding LM, Pettitt DJ, Saad

MF, Genco RJ, Knowler WC. Periodontal disease and

NIDDM in Pima Indians. Diabetes Care 1990: 13: 836–840.

105. Novak MJ. Necrotizing ulcerative periodontitis. Ann


106. Olin GLRJ. The five most costly medical conditions, 1997

and 2002: Estimates for the U.S. civilian noninstitutional-

ized population. In: Medical Expenditure Panel Survey.

Rockville, MD: Agency for Healthcare Research and Qual-

ity, 2005. 15

107. Ong G, Yeo JF, Bhole S. A survey of reasons for extraction of

permanent teeth in Singapore. Community Dent Oral

Epidemiol 1996: 24: 124–127.

108. Oscarson N, Kallestal C, Lindholm L. A pilot study of the

use of oral health-related quality of life measures as an

outcome for analysing the impact of caries disease among

Swedish 19-year-olds. Caries Res 2007: 41: 85–92.

109. Ozcelik O, Haytac MC, Seydaoglu G. Immediate post-

operative effects of different periodontal treatment

modalities on oral health-related quality of life: a ran-

domized clinical trial. J Clin Periodontol 2007: 34: 788–796.

110. Palmer RJ. Oral bacterial biofilms – history in progress.

Microbiology 2009: 155: 2113–2114.

111. Parahitiyawa NB, Jin LJ, Leung WK, Yam WC, Samarana-

yake LP Microbiology of odontogenic bacteremia: beyond

endocarditis. Clin Microbiol Rev 2009: 22: 46–64, Table of

Contents.

112. Persson GR, Persson RE. Cardiovascular disease and peri-

odontitis: an update on the associations and risk. J Clin

Periodontol 2008: 35: 362–379.

113. Petersen PE, Bourgeois D, Ogawa H, Estupinan-Day S,

Ndiaye C. The global burden of oral diseases and risks to

oral health. Bull World Health Organ 2005: 83: 661–669.

114. Phipps KR, Stevens VJ. Relative contribution of caries and

periodontal disease in adult tooth loss for an HMO

dental population. J Public Health Dent 1995: 55: 250–

252.

16

Beikler & Flemmig

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

27

28

29

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

47

48

49

50

51

52

53

115. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J.

Our current understanding of fungal biofilms. Crit Rev

Microbiol 2009: 35: 340–355.

116. Rautemaa R, Lauhio A, Cullinan MP, Seymour GJ. Oral

infections and systemic disease–an emerging problem in

medicine. Clin Microbiol Infect 2007: 13: 1041–1047.

117. Reich E, Hiller KA. Reasons for tooth extraction in the

western states of Germany. Community Dent Oral

Epidemiol 1993: 21: 379–383.

118. Richards W, Ameen J, Coll AM, Higgs G. Reasons for tooth

extraction in four general dental practices in South Wales.

Br Dent J 2005: 198: 275–278.

119. Robertson D, Smith AJ. The microbiology of the acute

dental abscess. J Med Microbiol 2009: 58: 155–162.

120. Rocha CT, Rossi MA, Leonardo MR, Rocha LB, Nelson-

Filho P, Silva LA. Biofilm on the apical region of roots in

primary teeth with vital and necrotic pulps with or without

radiographically evident apical pathosis. Int Endod J 2008:

41: 664–669.

121. Sachdeo A, Haffajee AD, Socransky SS. Biofilms in the

edentulous oral cavity. J Prosthodont 2008: 17: 348–356.

122. Salvi GE, Carollo-Bittel B, Lang NP. Effects of diabetes

mellitus on periodontal and peri-implant conditions: up-

date on associations and risks. J Clin Periodontol 2008: 35:

398–409.

123. Schaudinn C, Gorur A, Keller D, Sedghizadeh PP, Costerton

JW. Periodontitis: an archetypical biofilm disease. J Am

Dent Assoc 2009: 140: 978–986.

124. Services CfMM. National health expenditure data. In, 2009.

125. Sharkawy AA Cervicofacial actinomycosis and mandibular

osteomyelitis. Infect Dis Clin North Am 2007: 21: 543–556,

viii.

126. Sheiham A, Steele JG, Marcenes W, Tsakos G, Finch S,

Walls AW. Prevalence of impacts of dental and oral disor-

ders and their effects on eating among older people; a

national survey in Great Britain. Community Dent Oral

Epidemiol 2001: 29: 195–203.

127. Skudutyte-Rysstad R, Eriksen HM, Hansen BF. Trends in

periodontal health among 35-year-olds in Oslo, 1973–2003.

J Clin Periodontol 2007: 34: 867–872.

128. Slade GD, Offenbacher S, Beck JD, Heiss G, Pankow JS.

Acute-phase inflammatory response to periodontal disease

in the US population. J Dent Res 2000: 79: 49–57.

129. Soni A The five most costly conditions, 1996 and 2006:

Estimates for the U.S. civilian noninstitutionalized popu-

lation. in: Medical Expenditure Panel Survey. Rockville,

MD: Agency for Healthcare Reasearch and Quality, 2009.

130. Stephens RG, Kogon SL, Jarvis AM. A study of the reasons

for tooth extraction in a Canadian population sample.

J Can Dent Assoc 1991: 57: 501–504.

131. Tabor HK, Risch NJ, Myers RM. Candidate-gene

approaches for studying complex genetic traits: practical

considerations. Nat Rev Genet 2002: 3: 391–397.

132. Taylor GW. Glycaemic control and alveolar bone loss pro-

gression in type 2 diabetes. Ann Periodontol 1998: 3: 30.

133. Temple DH, Larsen CS. Dental caries prevalence as evi-

dence for agriculture and subsistence variation during the

Yayoi period in prehistoric Japan: biocultural interpreta-

tions of an economy in transition. Am J Phys Anthropol

2007: 134: 501–512.

134. Thomason JM, Heydecke G, Feine JS, Ellis JS. How do

patients perceive the benefit of reconstructive dentistry

with regard to oral health-related quality of life and patient

satisfaction? A systematic review Clin Oral Implants Res

2007: 18 (Suppl. 3): 168–188.

135. Tomar SL, Asma S. Smoking-attributable periodontitis in

the United States: findings from NHANES III. National

Health and Nutrition Examination Survey. J Periodontol

2000: 71: 743–751.

136. Tonetti MS. Periodontitis and risk for atherosclerosis: an

update on intervention trials. J Clin Periodontol 2009:

36(Suppl 10): 15–19.

137. Tonetti MS, Mombelli A. Early-onset periodontitis. Ann


138. Toomes C, James J, Wood AJ, Wu CL, McCormick D, Lench

N, Hewitt C, Moynihan L, Roberts E, Woods CG, Markham

A, Wong M, Widmer R, Ghaffar KA, Pemberton M, Hussein

IR, Temtamy SA, Davies R, Read AP, Sloan P, Dixon MJ,

Thakker NS. Loss-of-function mutations in the cathepsin C

gene result in periodontal disease and palmoplantar kera-

tosis. Nat Genet 1999: 23: 421–424.

139. Torabinejad M, Anderson P, Bader J, Brown LJ, Chen LH,

Goodacre CJ, Kattadiyil MT, Kutsenko D, Lozada J, Patel R,

Petersen F, Puterman I, White SN. Outcomes of root canal

treatment and restoration, implant-supported single

crowns, fixed partial dentures, and extraction without

replacement: a systematic review. J Prosthet Dent 2007: 98:

285–311.

140. Trovik TA, Klock KS, Haugejorden O. Trends in reasons for

tooth extractions in Norway from 1968 to 1998. Acta Od-

ontol Scand 2000: 58: 89–96.

141. Tsai C, Hayes C, Taylor GW. Glycemic control of type 2

diabetes and severe periodontal disease in the US adult

population. Community Dent Oral Epidemiol 2002: 30:

182–192.

142. Ulivieri S, Oliveri G, Filosomi G. Brain abscess following

dental procedures. Case report.Minerva Stomatol 2007: 56:

303–305.

143. Vieira F, Allen SM, Stocks RM, Thompson JW. Deep neck

infection. Otolaryngol Clin North Am 2008: 41: 459–483, vii.

144. Wagner KW, Schon R, Schumacher M, Schmelzeisen R,

Schulze D. Case report: brain and liver abscesses caused by

oral infection with Streptococcus intermedius. Oral Surg

OralMedOral Pathol Oral Radiol Endod 2006: 102: e21–e23.

145. WHO. http://www.dent.niigata-u.ac.jp/prevent/perio/

contents.html. 2009.

146. WHO. http://www.whocollab.od.mah.se/countriesalphab.

html. Geneva 2009

147. WHO. http://www.whocollab.od.mah.se/expl/globalcar1.

html. 2009.

148. WHO. http://www.whocollab.od.mah.se/expl/regions.html.

2009.

149. Wilson W, Taubert KA, Gewitz M, Lockhart PB, Baddour

LM, Levison M, Bolger A, Cabell CH, Takahashi M, Balti-

more RS, Newburger JW, Strom BL, Tani LY, Gerber M,

Bonow RO, Pallasch T, Shulman ST, Rowley AH, Burns JC,

Ferrieri P, Gardner T, Goff D, Durack DTAmerican Heart

Association Rheumatic Fever, Endocarditis, and Kawasaki

Disease Committee; American Heart Association Council

on Cardiovascular Disease in the Young; American Heart

Association Council on Clinical Cardiology; American

Heart Association Council on Cardiovascular Surgery and

Anesthesia; Quality of Care and Outcomes Research

Interdisciplinary Working Group. Prevention of infective

17


1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

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endocarditis: guidelines from the American Heart Associ-

ation: a guideline from the American Heart Association

Rheumatic Fever, Endocarditis, and Kawasaki Disease

Committee, Council on Cardiovascular Disease in the

Young, and the Council on Clinical Cardiology, Council on

Cardiovascular Surgery and Anesthesia, and the Quality of

Care and Outcomes Research Interdisciplinary Working

Group. Circulation 2007: 116: 1736–1754.

150. Wimmer G, Pihlstrom BL. A critical assessment of adverse

pregnancy outcome and periodontal disease. J Clin Peri-

odontol 2008: 35: 380–397.

151. Wolfart S, Heydecke G, Luthardt RG, Marre B, Freesmeyer

WB, Stark H, Wostmann B, Mundt T, Pospiech P, Jahn F,

Gitt I, Schadler M, Aggstaller H, Talebpur F, Busche E, Bell

M. Effects of prosthetic treatment for shortened dental

arches on oral health-related quality of life, self-reports of

pain and jaw disability: results from the pilot-phase of a

randomized multicentre trial. J Oral Rehabil 2005: 32: 815–

822.

152. Yoshida Y, Hatanaka Y, Imaki M, Ogawa Y, Miyatani S,

Tanada S. Epidemiological study on improving the QOL

and oral conditions of the aged – Part 1: the relationship

between the status of tooth preservation and QOL. J Physiol

Anthropol Appl Human Sci 2001: 20: 363–368.

153. Zitzmann NU, Berglundh T. Definition and prevalence of

peri-implant diseases. J Clin Periodontol 2008: 35: 286–291.

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