Periodontology 2000, Vol. 53, 2010, 118 Printed in Singapore.

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2010 John Wiley & Sons A/S

PERIODONTOLOGY 2000

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Oral biolm-associated diseases: trends and implications for quality of life, systemic health and expenditures
T H O M A S B E I K L E R & T H O M A S F. F L E M M I G

Biolms are surface-associated communities of microorganisms embedded in an extracellular polymeric substance, which upon contact with the host may affect tissue hemostasis and result in disease (61). It is estimated that approximately 80% of the worlds microbial biomass resides in a biolm state and that microbial biolms cause more than 75% of all microbial infections found in humans (35). The oral cavity is replete with biolms colonizing mucous membranes, dental materials and teeth (57, 110, 120, 121, 123). Oral biolms 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 biolmassociated diseases

1 The presence of a biolm alone is often not sufcient to cause disease because most oral biolm-associated diseases are complex with a multifactorial etiology. Additional factors that benet 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 2 times daily between meals (odds ratio = 1.91), deep pits and ssures (odds ratio = 1.93), inadequate saliva ow (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 exogenous risk factors (e.g. cigarette smoking and psychological stress) have been identied. Approximately 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 (96). It 3 is estimated that at least 1020 modifying genes are involved in the onset and progression of chronic or aggressive periodontitis, although attempts to identify these genes have shown controversial results (84, 131). Single gene mutations that are strongly associated with periodontitis, as reported for the CTSC gene 4 ` vre syndrome, are extremely rare in the Papillon-Lefe (84, 138). Diabetes mellitus type 1 and type 2, particularly 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 56, 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 and periodontal diseases

Oral biolm-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 human remains from later time-periods (74). One of the earliest descriptions of periodontal disease recorded was in the army of the Greek general Xenophon,
Dispatch: 11.3.10 Author Received: Journal: PRD CE: Janaki Rekha No. of pages: 18 PE: Raymond

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Table 1. Oral biolm-associated diseases and their consequences

References Oral biolm-associated diseases Gingivitis Periodontitis (chronic, aggressive) Necrotizing periodontal diseases Abscesses of the periodontium Periodontitis associated with endodontic lesions Dental caries Pulpitits Apical periodontitis Peri-implant diseases Candidosis Diseases and conditions that may result from oral biolm-associated diseases Tooth loss Implant failure Noma Deep neck infections* Osteomyelitis of the jaw* Maxillary sinusitis* Ludwigs angina* Orbital cellulitis* Cervicofacial actinomycosis* Septicemia* Death* See Table 3 Pjetursson et al. 2007 Enwonwu et al. 2000 (45) Vieira et al. 2008 (143) Sharkawy 2007 (125) Bomeli et al. 2009 (23) Parahitiyawa et al. 2009 (111) Parahitiyawa et al. 2009 (111) Sharkawy 2007 (125) Parahitiyawa et al. 2009 (111) Robertson and Smith 2009 (119) Mariotti 1999 (89) Flemmig 1999 (48), Tonetti & Mombelli 1999 (137) Novak 1999 (105) Meng 1999 (94) Meng 1999 (95) Domejean-Orliaguet et al. 2006 (39) Levin et al. 2009 (80) Gutmann et al. 2009 (58) Zitzmann et al. 2008 (153) Ramage et al. 2009 (115)

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Diseases that may be associated with hematogenous spreading of oral biolm bacteria Infective endocarditis Acute bacterial myocarditis Brain abscess Liver abscess Lung abscess Cavernous sinus thrombosis Prosthetic joint infection Wilson et al. 2007 (149) Parahitiyawa et al. 2009 (111) Mueller et al. 2009 (99) Wagner et al. 2006 (144) Parahitiyawa et al. 2009 (111) Parahitiyawa et al. 2009 (111) Bartzokas et al. 1994 (19)

Diseases and conditions for which periodontal inammation is considered as a risk factor Cardiovascular disease Cerebrovascular disease Diabetes mellitus with poor glycemic control Persson and Persson 2008 (112) Dorfer et al. 2004 (40) Lim et al. 2007 (82)

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-

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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, lled teeth index value in 125 year-old children 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 patterns and lifestyles have changed with increasing economic wealth, caries experience has risen (24, 6 113). Among 12-year-old children, the dental caries experience varies considerably in different parts of the world. It is relatively high in the Americas (decayed, missing, lled teeth index value = 2.76) and in Europe (decayed, missing, lled teeth index value = 2.56), whereas the caries experience is lowest in most of Africa (decayed, missing, lled teeth index value = 1.15) and Asia (decayed, missing, lled 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 pronounced 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 associated with higher mean decayed, missing, lled teeth scores and an increased rate of root canal treatments (62, 63).

DMFT

2.76

2.57

1.15

1.58

1.12

WHO-regions

Fig. 2. Weighted means of decayed, missing, lled teeth (DMFT) scores in 12-year-old children in the World Health Organization (WHO) regions in 2004 (147).

DMFT decreased DMFT increased or unchanged No data available

Fig. 1. Changes in decayed, missing, lled teeth (DMFT) scores in various regions of the world. Decayed, missing, lled teeth scores have been considered as increased or decreased when the most recent decayed, missing, lled teeth values were more than 0.3 different from the previous decayed, missing, lled teeth value. Observation periods ranged from 3 to 68 years in the various regions (148).

The prevalence of periodontal diseases has shown heterogeneous trends throughout the world over recent years. The Community Periodontal Index of Treatment Needs has improved in some parts of Africa and Asia, whereas the prevalence of periodontitis has remained unchanged, or even increased, 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 Treatment Needs allows some comparison between countries, the information needs to be interpreted with caution owing to a categorical and partialmouth assessment, which may underestimate the true prevalence of periodontal disease (15). The lack of a universally accepted denition of what constitutes a periodontitis case makes assessment of the true prevalence of periodontitis in various populations 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 signicant 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 ndings were reported in 20- to ping, Sweden. The pro80-year-old subjects in Jonko portion of individuals with healthy gingivae increased from 8 to 44%, whereas the proportion of individuals

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% global population

80 70 60 50 40 30 20 10 0 0 1 2 3

1519 years 3544 years >65 years

CPITN 3 decreased CPITN 3 increased or unchanged No data available

Fig. 3. Prevalence trends of mild to moderate periodontitis in various regions of the world. The prevalence of Community Periodontal Index of Treatment Needs (CPITN) three values have been considered to be 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).

CPITN
Fig. 5. Estimated global periodontal disease prevalence. Mean Community Periodontal Index of Treatment Needs (CPITN) scores were shown for the following age groups: 1519 years (89 countries); 3544 years (89 countries); and 6574 years (28 countries). Error bars indicate standard 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 Community 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).

mated prevalence of periodontitis decreased from 87% (in 1955) to 4.2% in 20022004 (30). Although these numbers need to be interpreted with caution given that different periodontal assessment parameters were used and periodontitis case denitions 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 ofces in 2004, more than 30% were preventive in nature (87). From 1990 to 1999 alone, the number of prophylaxes performed increased from 178.5 million to 191 million, and the number of periodontal maintenance procedures increased from 9.8 million to 12.7 million. Over the same time-period, scaling and root planing procedures decreased from 14.1 million to 10.8 million, supporting the notion of a reduced periodontal treatment need in the USA (26).

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with severe periodontitis remained largely unchanged over a 30-year observation period (64). Signicantly improved oral hygiene scores accompanied the improved periodontal health in the aforementioned populations. The most dramatic improvement in periodontal health has been reported in the USA where the esti-

Impact of oral biolm-associated diseases on quality of life

Oral biolm-associated diseases may impact an individuals ability to function as well as affect the perception of well-being in physical, mental and so-

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cial domains of life (32). Specic instruments to assess 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 (condence, mood, personality), to social aspects, such as social life, work and nances. 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 healthrelated quality of life is less clear and appears to be most pronounced in populations exhibiting high dental caries prevalence. Among Brazilian adolescents with a high prevalence of caries (88.3%), a positive correlation was found between Oral Health Impact Prole 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 ndings, 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 Prole 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 restorations may result in pulpal and apical diseases. Although pain is recognized as a cardinal symptom of reversible and irreversible 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 ndings indicating a considerable impact of periodontitis on oral healthrelated quality of life measures have challenged this concept (68, 69, 76, 78). A negative impact across a wide range of physical, social and psychological aspects 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 patients self-reported periodontal health experiences of swollen gums, sore gums, receding gums, loose teeth, drifting teeth, bad breath and toothache. A signicant, negative correlation between 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 assessment, pain or discomfort were found 7 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 ratio = 2.0) and necrotizing ulcerative gingivitis (odds ratio = 1.6) were signicantly associated with negative impact on oral health-related quality of life (85). In children, more than one-fth perceived bleeding and swollen gums to impact on their lives (51). Patients receiving regular periodontal supportive therapy have reported signicantly 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 crosssectional observations have been further substanti-

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ated by longitudinal clinical trials demonstrating that nonsurgical periodontal therapy improves oral healthrelated quality of life in patients with periodontitis (13, 69, 109). Improvements in oral health-related quality of life measures resulting from nonsurgical periodontal therapy were detected within 1 week after therapy, whereas oral health-related quality of life scores were found to deteriorate in the rst few days following periodontal ap surgery and returned to baseline levels within 1 week (109). The long-term effect of surgical periodontal therapy on oral healthrelated quality of life has not been assessed. Oral biolm-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 signicant 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 8 members or others, regular physical activities and attending meetings or group outings (152). Oral Impacts on Daily Performances scores were found to be highest among dentate seniors with the lowest number of teeth (126). A minimum of 20 teeth, with 910 pairs of contacting units (including anterior teeth), is generally associated with adequate masticatory efciency, as assessed by comminution efciency 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 Prole scores (6, 7). Compelling evidence has been presented in a recently published systematic review that edentulous patients are more satised with implant-supported overdentures than conventional complete dentures, particularly in the mandible. Furthermore, implant-supported overdentures may signicantly improve oral healthrelated quality of life (134). Evidence to support an impact of mandibular implant-supported overdenture 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 rst molars using a removable dental prosthesis has been shown to improve Oral Health Impact Prole scores. It, however, did not show any advantage over a xed 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 oral biolm-associated diseases

Oral biolm-associated diseases may affect systemic health by (i) spreading infections to adjacent tissues and spaces, (ii) hematogenous dissemination of oral biolm bacteria, or (iii) through inammatory 9 mechanisms. Acute forms of odontogenic infections may spread into the adjacent tissues, causing osteomyelitis of the jaws, maxillary sinusitis, noma, deep neck infections, Ludwigs angina, orbital cellulitis, skin ulcers, cervicofacial actinomycosis, septicemia and, in rare cases, even death (23, 45, 111, 119, 125, 143) (Table 1). Odontogenic infections can be life threatening. Mortality rates of descending necrotizing mediastinitis, resulting from odontogenic infections and noma, have been reported to range from 50 to 80% when no adequate therapy was rendered (88). It is therefore not surprising that in medieval Europe, dental caries and periodontal diseases were associated with an increased risk of death (37). According to church registries 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 for many populations have drastically reduced the mortality rate resulting from dental infections, there are still approximately 21,000 hospital admissions and at least 150 deaths caused by odontogenic infections in the USA every year (53) and approximately 770,000 cases of life-threatening noma worldwide (17, 98). Oral biolms represent an abundant reservoir of microorganisms that may spread via transient bacteremia, as demonstrated by the types of oral biolms isolated from infections remote from the oral cavity (81). Shedding and subsequent hematogenous dissemination of oral biolm bacteria have been associated with some forms of infective endocarditis,

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Table 2. Reasons presented for tooth extraction related to oral biolm-associated diseases in various geographic regions
Author Cahen et al. (27) Kay and Blinkhorn (70) Agerholm and Sidi (1) Chauncey et al. (29) Klock et al. (73) Stephens et al. (130) Reich and Hiller (117) Phipps and Stevens (114) Ong et al. (107) Angelillo et al. (9) Murray et al. (100) McCaul et al. (91) Trovik et al. (140) Richards et al. (118) Aida et al. (2) Al-Shammari et al. (4) Weighted mean Year 1985 1986 1988 1989 1991 1991 1993 1995 1996 1996 1997 2001 2001 2005 2006 2006 Country France Scotland Enland Wales US Norway Canada Germany US Singapore Italy Canada Scotland Norway South Wales Japan Kuwait Extracted teeth Dental caries (%) (n) 14621 2190 5274 1142 985 2510 1215 1877 272 1056 1710 2558 1495 558 9115 2783 49 50 48 33 35 63 21 51 35 34 29 55 40 59 33 44 Periodontal disease (%) 32 21 27 19 19 34 27 35 36 33 26 17 24 29 42 37 Total (%) 81 71 75 52 54 97 48 86 71 68 55 72 64 88 75 81 76

acute bacterial myocarditis, brain abscess, liver abscess, 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 biolm 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 1.76.2 cases per 100,000 patient years. Men are twice as often affected 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 proportional 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 infective endocarditis. The notion that oral biolms may impact systemic health by inammatory mechanisms is supported by cross-sectional studies reporting elevated systemic inammatory markers in patients with periodontitis (28, 33, 36, 83, 128). Strong evidence supports the oral

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1 systemic link between periodontitis and cardiovascu2 lar diseases, cerebrovascular diseases and diabetes 3 mellitus, all of which have an inammatory etiology. A 4 number of cross-sectional and cohort studies have 5 demonstrated consistent associations between peri6 odontitis and cardiovascular disease, irrespective of 7 common underlying risk factors or confounders such 8 as smoking, age, education, body mass index and 9 lifestyle factors (112). Hazard ratios and relative risk 10 ratios for fatal and nonfatal coronary events have been 11 reported to range from 1.5 to 2.0 in individuals with 12 periodontitis (20, 38); the adjusted risk ratio for cere13 bral ischemia is 7.4 (31, 40). In diabetic patients, peri14 odontitis has been identied as a risk factor for poor 15 glycemic control (31, 82, 104, 132). The association of 16 periodontitis with adverse pregnancy outcomes, 17 osteoporosis, cancer and chronic obstructive pulmo18 nary diseases remains controversial (14, 47, 72, 150). 19 There is some evidence to support that treatment 20 of periodontitis may improve glycemic control in 21 diabetic patients (50). Periodontal therapy also has 22 been shown to reduce inammatory biomarkers, 23 improve surrogate measures of vascular endothelial 24 function (136) and thereby possibly exert an effect on 25 inammatory vascular diseases. However, direct 26 evidence that periodontal therapy may reduce the 27 risk for cardiovascular or cerebrovascular diseases is 28 lacking. With regard to adverse pregnancy outcomes, 29 an intervention trial with more than 800 enrolled 30 patients demonstrated that treatment of periodontal 31 disease improved periodontal conditions, but did not 32 signicantly reduce the risk of adverse pregnancy 33 outcomes (97). 34 35 36 Financial expenditures for dental 37 services related to oral biolm38 39 associated diseases 40 In order to estimate the costs of managing oral bio41 lm-associated diseases, the national expenditures 42 for professional dental services related to these dis43 eases were calculated. For this purpose, the 500 + 44 45 10 dental procedures listed in the Current Dental Terminology 2009 2010 of the American Dental Asso46 ciation (11) were categorized based on whether they 47 are used primarily for the prevention (A), diagnosis, 48 or treatment of oral biolm-associated diseases and 49 their sequelae, primarily for conditions unrelated to 50 oral biolm-associated diseases (B) or for oral bio51 lm-associated diseases as well as other oral condi52 tions (C). Although there may be instances in which 53

procedures that were assigned to category A or category 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 biolm-associated diseases or other oral conditions were determined. 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 conditions other than oral biolm-associated diseases. The same proportions (i.e. 8614%) were applied to restorations, such as xed prostheses or implant-supported restorations, aimed at replacing lost teeth. For other procedures where no reliable data were available, the proportion of each procedure used for the management of biolm-associated diseases was estimated using expert opinion (Table 3). Using the ADA 200506 Survey of Dental Services Rendered 11 (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 biolm-associated diseases in dental ofces; the cost of these dental procedures corresponded to 90% of the national expenditures for dental services, amounting to $81 billion in 2006 (124). These gures do not include the approximately $9 billion in expenditures for oral hygiene products sold in the USA in 2006 (90).

Oral biolm-associated diseases are among the most costly medical conditions
The estimated national expenditures for oral biolmassociated diseases in the USA have almost doubled from 1997 to 2006. In 2006, the estimated national expenditures for oral biolm-associated diseases totaled $81 billion and were greater than for any one of the ve 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 disorders ($57.2 billion); and pulmonary conditions ($51.3 billion) (Fig. 6) (106, 124, 129).

Concluding remarks
Oral biolm-associated diseases, and their subsequent diseases and conditions, have broad impli-

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Table 3. Procedures assumed to be performed that are unrelated to oral biolm-associated diseases
Estimated percentage unrelated to oral biolm-associated diseases (%)

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CDT code Diagnostic D0120 D0140 D0150 D0160 D0170 D0180 D0210D0230 D0270D0274 D0330 D0340

Description

Periodic oral evaluation* Limited oral evaluation* Comprehensive oral evaluation* Detailed and extensive oral evaluation* Re-evaluation* Comprehensive periodontal evaluation* Intra-oral radiographs, peri-apical radiographs* Bitewing radiographs* Panoramic lm* Cephalometric lm

10 10 10 10 10 10 10 10 23 100

D0350 D0431

Oral facial photographic images Adjunctive test for mucosal abnormalities

100 100

D0460 D0470 Preventive D1510 1515 D1520 1525

Pulp vitality tests* Diagnostic casts*

10 10

Space maintainer xed Space maintainer removable

100 100

Restorative D2330 D2391 Resin-based composite one surface, posterior D27102794 D2950 Core buildup D29522954, 2957 D29602962 Labial veneer Endodontics D33513353 Apexication recalcication 100 Post and core 10 100 Crown single restoration 10 10 Resin-based composite one surface, anterior 20 20

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Table 3. (Continued)
Estimated percentage unrelated to oral biolm-associated diseases (%)

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CDT code Periodontics D4270,4271

Description

100 Free soft tissue graft, subepithelial connective tissue graft

Maxillofacial prosthetics D5982 5988 Implant services D6010 D6053 6054 Implant abutment-supported removable denture D6056 D6057 Custom abutment D60586067, 6094 Abutment- or implantsupported supported crown D60686077, 6194 Prosthodontics (xed) D62056252 D67106792, 6794 Oral and maxillofacial surgery D7111, 7140 D7210, 7210 D7220 D72307241 D7261 D7280 D7283 D7340 7350 D7410-7411 D7412 Extraction Surgical extraction

Surgical stent, surgical splint

100

Surgical placement of implant body

14 14

Prefabricated abutment

14 14 14

Abutment- or implantsupported retainer

14

Pontic Crown

24 24

14 14 100 100 100 100 100 100 100 100

Removal of impacted tooth soft tissue Removal of impacted tooth bony Primary closure of a sinus perforation Surgical access of an unerupted tooth Placement of device to facilitate eruption Vestibuloplasty ridge extension Excision of benign lesion Excision of benign lesion, complicated

10

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Table 3. (Continued)
Estimated percentage unrelated to oral biolm-associated diseases (%) 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100

18

CDT code D74137415 D7450 7460 D7451 7461 D7471 7485 D7472 7473 D7610 7620 D7630 7640 D7670 7671 D7680 D7710 7720 D7730 7740 D7780 D7820 D7865 D7870 D78727877 D7880 D7941 7943 D7945 D7950 D7955 D7960 7963 Orthodontics D8010 D8020 D8030 D8040 D8050

Description Excision of malignant lesion Removal of benign odontogenic cyst or tumor Removal of benign odontogenic cyst or tumor Removal of lateral exostosis Removal of torus palatinus or torus mandibularis Simple fracture maxilla Simple fracture mandible Alveolus simple Facial bones simple complicated reduction Compound facture maxilla Compound fracture mandible Facial bones compound complicated reduction Closed reduction of dislocation Arthroplasty Arthrocentesis Arthroscopy surgical Occlusal orthotic device Osteotomy mandibular rami Osteotomy body of mandible Osseous, osteoperiosteal, or cartilage graft Repair of maxillofacial soft and or hard tissue defect Frenulectomy or frenotomy

Limited orthodontic treatment primary dentition Limited orthodontic treatment transitional dentition Limited orthodontic treatment adolescent dentition Limited orthodontic treatment adult dentition Interceptive orthodontic treatment of the primary dentition

100 100 100 100 100

11

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

Table 3. (Continued)
Estimated percentage unrelated to oral biolm-associated diseases (%) 100

18

CDT code D8060

Description Interceptive orthodontic treatment of the transitional dentition Comprehensive orthodontic treatment of the transitional dentition Comprehensive orthodontic treatment of the adolescent dentition Comprehensive orthodontic treatment of the adult dentition Removable appliance therapy Fixed appliance therapy Pre-orthodontic treatment visit Periodic orthodontic treatment visit Orthodontic retention Orthodontic treatment (alternative billing) Repair of orthodontic appliance Replacement of lost or broken retainer Unspecied orthodontic procedure

D8070

100

D8080

100

D8090

100

D8210 D8220 D8660 D8670 D8680 D8690 D8691 D8692 D8999 Adjunctive general services D9220 D9221

100 100 100 100 100 100 100 100 100

Deep sedation general anesthesia rst 30 minutes Deep sedation general anesthesia each additional 15 minutes Analgesia, anxiolysis, inhalation of nitrous oxide Intravenous conscious sedation analgesia Nonintravenous conscious sedation Therapeutic parenteral drug Desensitizing medicament resin Behavior management

100 100

D9230 D9241 9242 D9248 D9610 D9910 9911 D9920

100 100 100 100 100 100

12

Oral biolm-associated diseases

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

Table 3. (Continued)
Estimated percentage unrelated to oral biolm-associated diseases (%) 100 100 100 100 100 100

18

CDT code D9940 9941 D9942 D9951 9952 D9970 D9972 9973 D9974

Description Occlusal guard athletic mouthguard Repair and or reline of occlusal guard Occlusal adjustment Enamel microabrasion External bleaching Internal bleaching

COLOR

90 80 70 60

50 40 30 20 10 0 1997 2002 Year Oral biofilm-associated diseases Heart conditions Trauma-related disorders Cancer Mental disorders Pulmonary conditions 2006

Fig. 6. National expenditures for the most costly medical conditions and oral biolm-associated diseases in the USA in 1997, 2002 and 2006. Expenditures are dened 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 Classication of Diseases, Ninth Revision (ICD-9) condition codes are aggregated into clinically meaningful categories that group similar conditions using Clinical Classication System (CCS) software. Cancer includes CCS codes 1145; heart conditions, CCS codes 96, 97 and 100108; pulmonary 16 conditions (COPD, asthma), CCS codes 127134; trauma, CCS codes 225236, 239, 240 and 244; and mental disorders, CCS codes 650663. Expenditures for oral biolm-associated diseases are estimates corresponding to 90% of the national expenditures for dental services (106, 124, 129).

cations on systemic health and oral health-related quality of life, and pose a signicant cost burden on societies. Considerable strides have been made in the prevention and management of oral biolm-associated diseases and their sequelae. Caries is a formidable 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 worlds population remain affected by oral biolm-associated diseases. If the disease burden is to be further reduced, new and more cost-effective prevention and treatment strategies are needed that result in sustained oral health with minimal 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 employed for both oral biolm-associated and other conditions. as 10% of all therapeutic procedures were found to be unrelated to oral biolm-associated diseases, the same proportion of all diagnostic procedures was assumed to be unrelated to oral biolm-associated diseases. Panoramic lms 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 proportion of procedures aimed at replacing lost teeth

$ billions

13

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

was assumed to be unrelated to oral biolm-associated 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.

17.

18.

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