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Home , Attrition (dental), Focal infection theory, Human tooth

INVITED ARTICLE AGING AND INFECTIOUS DISEASES Thomas T. Yoshikawa, Section Editor

Infectious Complications of Dental and Periodontal Diseases in the Elderly Population

Kenneth Shay

Geriatrics and Extended Care Service Line, Veterans Integrated Services Network 11, Geriatric Research Education and Clinical Center and Dental Service, Ann Arbor Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 Veterans Affairs Healthcare System, and University of Michigan School of , Ann Arbor

Retention of teeth into advanced age makes caries and periodontitis lifelong concerns. Dental caries occurs when acidic metabolites of oral streptococci dissolve enamel and . Dissolution progresses to cavitation and, if untreated, to bacterial invasion of dental , whereby oral access the bloodstream. Oral organisms have been linked to of the endocardium, meninges, mediastinum, vertebrae, hepatobiliary system, and prosthetic joints. Periodontitis is a pathogen- specific, lytic inflammatory reaction to that degrades the attachment. is more severe and less readily controlled in people with diabetes; impaired glycemic control may exacerbate host response. Aspiration of oropharyngeal (including periodontal) pathogens is the dominant cause of nursing home–acquired pneumonia; factors reflecting poor oral health strongly correlate with increased risk of developing aspiration pneumonia. Bloodborne peri- odontopathic organisms may play a role in atherosclerosis. Daily practice and receipt of regular dental care are cost-effective means for minimizing morbidity of oral infections and their nonoral sequelae.

More than 300 individual cultivable of microbes have growing importance in the elderly population. In 1957, nearly been identified in the mouth [1], with an estimated 1014 70% of the US population aged 175 years had no natural teeth. individual microscopic organisms occupying the mouth and or- Due to water and dentifrice fluoridation, preventive dental be- opharynx at a time [2]. The most prevalent oral infectious dis- haviors, and an expanded dental profession, !35% of Americans eases, caries and periodontal disease, are historically the province aged 175 years now are missing all teeth [9]. This extends the of dentists for diagnosis and treatment. However, the effect of likelihood of risk for dental and periodontal disease into a time these oral diseases often extends systemically, particularly in older in life often marked by impaired self-care. This article will discuss adults. Hematogenous seeding from an oral source is a dominant the and, particularly, the systemic consequences cause of bacterial [3] and is implicated in late pros- of these 2 oral infections in elderly people. thetic joint (LPJI) [4]. Periodontal disease impairs gly- cemic control in people with diabetes [5], and poorly controlled MICROECOLOGIC NICHES OF THE MOUTH diabetes may exacerbate periodontal disease [6]. Aspiration of oropharyngeal secretions is the predominant cause of nosocomial The mouth offers multiple microbiologic environments, several pneumonia in elderly persons [7]. Periodontopathic bacteria in of which involve the teeth. Tooth surfaces most apparent in the bloodstream have been linked to atherosclerosis, coronary the mouth are covered by enamel, an acellular material that is artery disease, and stroke [8]. ∼95% hydroxyphosphate () microcrys- This review focuses on caries and periodontal disease and their tals and 5% organic material [10]. Biting surfaces of teeth are marked by grooves and fissures that shelter bacterial colonies, Received 5 October 2001; revised 18 December 2001; electronically published 2 April although these irregularities in aged teeth have commonly been 2002. obliterated through years of or . The Reprints or correspondence: Dr. Kenneth Shay, Geriatrics and Extended Care Service Line, Veterans Integrated Services Network 11, PO Box 134002, Ann Arbor, MI 48113-4002 sides of teeth that contact one another represent a second mi- ([email protected]). croenvironment. This contact area, which is surrounded by Clinical Infectious Diseases 2002;34:1215–23 2002 by the Infectious Diseases Society of America. All rights reserved. tooth structure and gingiva, is sheltered from debris and 1058-4838/2002/3409-0009$03.00 oral hygiene and shelters adherent bacteria.

AGING AND INFECTIOUS DISEASES • CID 2002:34 (1 May) • 1215 Near the gingiva, the tooth surface abruptly changes from DENTAL CARIES: PATHOGENESIS acellular enamel into , which is cellular tissue that AND LOCAL SEQUELAE is nearly 30% organic [11]. Initially, after a tooth’s eruption, the cemento-enamel junction is covered by gingiva; accumu- Dental caries is initiated by the nonhemolytic viridans strep- lated disease, trauma, and maturation expose it. In time, tooth- tococci [2], termed “mutans streptococci,” most commonly brushing and professional cleanings remove cementum and mutans and Streptococcus sobrinus. These organ- expose underlying dentin. Dentin is also ∼30% organic and isms are not present in newborns but appear as primary den- cellular. The tooth surface adjacent to the gingiva is a distinct tition erupts. DNA analysis confirms that transmission occurs microenvironment constantly bathed in plasma ultrafiltrate usually from mother to child, probably through shared food (“sulcular fluid”) seeping out of the sulcus between the gingiva implements [19]. The organisms thrive on , which they and the tooth. In the absence of gingival or periodontal disease, convert into organic and sticky polysugar (dextrans), the tooth-gingiva attachment is 1–3 mm from where the tooth which adheres the organisms to tooth surfaces [20]. Oral sites emerges from soft tissue (figure 1). The sulcular or subgingival that are not regularly disturbed, such as fissures and contact Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 microenvironment offers a continuum of conditions: the sulcus areas, thereby become susceptible to dental decay. entrance supports aerobic organisms; regions at increasing Tooth structure is in chemical equilibrium with under depth are associated first with facultative species, then with neutral pH. Increasing acidity to pH 5.4 by exposing plaque to anaerobic species, that build adherent multispecies colonies causes a net efflux of calcium and from the (plaque) on the tooth [12]. enamel into saliva [21]. Initially, crystals of surface hydroxyapatite Another ecologic niche, saliva, is partially removed (and re- dissolve, leaving behind an organic matrix of the sparse inter- newed) continuously. Saliva is a variable and complex solution crystalline material. When neutrality is reestablished through sal- of water, glycoprotein, and organic and inorganic ions. Under ivary dilution and buffering, hydroxyapatite reforms on the ma- normal circumstances, saliva protects the oral cavity and its trix. However, an undisturbed plaque colony limits the effects contents [13]. Through chemical buffer systems (predomi- of saliva, even as colonies maintain a low pH at the underlying nantly bicarbonate), saliva maintains oral pH at nearly neutral tooth surface. When dissolution has proceeded to the point that values. Long-chain glycoproteins, enzymes, statins, and im- the matrix collapses, a cavity forms. When cavitation extends munoglobulins temper microbial growth. Calcium and phos- through the enamel to the dentin, the caries process shifts as phate in solution maintain equilibrium between the soluble proteolytic organisms, particularly Lactobacillus species, exploit tooth structure and saliva [14]. Diminished salivary flow and the more organic substrate [20]. modified saliva composition allow oral pH to decrease, dis- Older people frequently have dentin exposed near the gin- turbing the equilibrium between tooth structure and oral fluids, giva, and root caries initiates there. Root caries is started by and permitting uninhibited microbial growth [15]. Flow from mutans streptococci, and there is early involvement of prote- parotid [16], submandibular [17], and minor salivary glands olytic Actinomyces species, including Actinomyces viscosus, Ac- remains largely unaffected in healthy persons, regardless of age. tinomyces odontolyticus, and Actinomyces naeslundii. Root caries It has been reported that a reduced flow rate can potentially is relatively uncommon before the age of 30 years, but it rapidly accompany use of the majority of medications commonly pre- increases in incidence in the succeeding decades of life. In scribed for older people [15]; saliva composition and flow are contrast, the attack rate of enamel caries remains stable commonly deleteriously altered in elderly individuals [18]. throughout a person’s life [22].

Figure 1. Schematic representation (not to scale) of selected dental and periodontal structures in healthy persons

1216 • CID 2002:34 (1 May) • AGING AND INFECTIOUS DISEASES Without dental treatment, natural progression of caries fol- Bacterial endocarditis is the most common of these condi- lows 1 of 2 paths. In younger people, tooth pulp begins to be tions. Approximately 27% of cultured cases of bacterial en- affected when caries invades dentin [23]. Dental pulp consists docarditis are caused by mutans streptococci [30]. A link be- of capillaries, nerves, and surrounded by os- tween these strictly oral organisms and endocardial disease, and teoblast-like cells () that secrete the precalcified the somewhat less clear association with dental treatment, has matrix that will become additional dentin. Odontoblasts have resulted in published regimens for prophylaxis for thin cellular processes extending the thickness of dentin. When certain at-risk patients before they undergo many dental pro- tooth structure is lost as a result of caries, odontoblastic pro- cedures (table 1) [31]. The highest-risk groups of patients are cesses, now less insulated from the mouth, expand and contract those with prosthetic heart valves and acquired valvular dys- more readily in response to oral environmental shifts (e.g., hot, function, both of which occur predominantly in aged people. cold, sweets, air), and sensory nerves in the pulp’s odontoblastic Without results from a prospective, blinded (which layer transmit the sensation of [24]. As caries progresses, has not been performed for ethical reasons), it is unknown bacteria irritate the cellular processes and trigger an inflam- whether the prescribed regimen is appropriate or effective, but Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 matory reaction in pulp. In the closed space of the pulp cham- it is a standard of practice that is unwise to ignore. Nevertheless, ber, an increase in tissue causes severe pain () Wahl [30] has focused on potential long-term effects of indis- and, ultimately, . Commonly, oral debris occluding criminate antibiotic use to argue for conducting such a trial. the cavity forces the inflammatory process to extend out to the Staphylococcus aureus and Staphylococcus epidermidis are root apex. From there, infection spreads through and into found both in patients with dental infection (particularly ab- soft tissue. scess) and in those with infected joint prostheses. These or- It is more common for untreated caries in older people to ganisms, which usually have a nonoral source, together account have a self-limiting course. Odontoblasts, as described above, for nearly two-thirds of cases of LPJI of the [32]. Nearly add dentin onto the walls of the pulp chamber to the extent 250,000 hip prostheses are placed in the United States annually, that diminished chamber size in advanced age is perceptible mostly in people aged 165 years [33]. Temporal associations on dental radiographs [25]. Analogous processes reduce the between dental infection and LPJI historically resulted in wide- number and diameter of dentinal tubules [26]. As a result, acute spread acceptance among orthopedists of the need for admin- dental pain is an uncommon complaint in older people [27]. istration of to arthroplasty patients before they un- Greater tooth destruction occurs before the dental pulp is af- dergo dental treatment [34]. More-recent deliberations, done fected, because the dentin is thicker. Loss of tooth structure in light of better data, more-sophisticated analysis of risks and reduces shelter for bacterial colonies, and natural salivary de- benefits [35], and growing concerns about the long-term con- fenses are able to arrest the process. sequences of widespread antibiotic use have resulted in pub- The associated with and cel- lished recommendations by a panel of dentists, orthopedists, lulitis are generally not the microorganisms associated with and infectious disease doctors to limit such coverage to recip- caries but are anaerobic species from deep within the gingival ients of total hip replacements who are at high risk, and then sulcus that thrive in debris-filled pulp chambers. Infections are only for specific dental procedures (table 2) [36]. most commonly combinations of у3 obligate anaerobes (such as Peptostreptococcus species, Porphyromonas gingivalis, Prevo- tella intermedia, and Prevotella melaninogenica) and Fusobac- PERIODONTAL DISEASE PATHOGENESIS terium nucleatum. Less commonly identified are the facultative anaerobes Streptococcus milleri, Streptococcus sanguis, and Ac- Two distinct types of disease of the are of interest tinomyces species [28]. in older . Nonspecific is a reversible inflam- mation of the adjacent to the teeth that is caused by presence of bacterial plaque (figure 2) [12]. Improved oral hy- DENTAL CARIES: METASTATIC SEQUELAE giene resolves the condition, although, in older people, inflam- mation forms faster in response to plaque and resolves more Hematogenous spread of oral pathogens becomes a potential slowly when plaque is removed [37]. Adult periodontitis occurs result of untreated dental decay once bacteria enters the pulp when an inflammatory reaction to gingival pathogens extends chamber. Navazesh and Mulligan [29] reviewed 15 years’ worth into the epithelial attachment between the tooth and the bone of medical literature to identify reports linking oral pathogens and into the bone itself (figure 3). with systemic disease in adults aged 150 years and reported As the plaque colonies that cause gingivitis mature, they that oral streptococci had been linked to mediastinal abscesses, become depleted in gram-positive organisms and cocci, and meningitis, vertebral osteomyelitis, hepatobiliary disease, and they begin to favor obligate anaerobes over facultative species bacterial endocarditis. [30]. Clinically, tissues become red and edematous and gums

AGING AND INFECTIOUS DISEASES • CID 2002:34 (1 May) • 1217 Table 1. Recommendations for antibiotic prophylaxis for bac- Table 1. (Continued.) terial endocarditis in patients scheduled to undergo dental procedures.

Cardiac conditions for which prophylaxis is recommended Other notes High risk Poor dental hygiene and periodontal or periapical infections produce bac- Prosthetic heart valves teremia even in the absence of dental procedures, so people at risk should establish and maintain the best possible oral health Previous diagnosis of endocarditis Antiseptic mouth rinse applied immediately before dental procedures may Complex cyanotic congential heart disease reduce magnitude and incidence of bacteremia; agents include 0.12% Surgically constructed pulmonary shunts or conduits gluconate and 10% povidone-iodine Moderate risk For patients already taking antibiotics, an agent different from the one currently being used should be selected from among those listed Patent ductus arteriosus above Ventricular septal defect Status after cardiovascular procedures Primum atrial septal defect There is no evidence that coronary artery bypass graft introduces a risk

Aortic coarctation for endocarditis Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 Bicuspid aortic valve “Noncoronary vascular grafts may merit antibiotic prophylaxis for the Acquired valvular dysfunction (e.g., rheumatic heart disease or first 6 months after implantation” [31] vascular disease, such as lupus erythematosus) NOTE. Data are from [31]. Hypertropic cardiomyopathy Mitral valve prolapse with regurgitation evidenced by audible clicks and murmurs or Doppler-demonstrated mitral insufficiency (this includes myxomatous mitral valve degeneration and exercise-induced mitral unless changes in local conditions or generalized host suscep- insufficiency in men aged 145 years) tibility occur [39]. When the host/pathogen balance tips, the Dental procedures before which prophylaxis is recommended lymphocytic nature of the gingivitis inflammatory infiltrate Interligamentary injections Placement of orthodontic bands, but not brackets changes to a plasma lesion as pathogens evade neutrophils Subgingival periodontal procedures (e.g., scaling or root planing) and elaborate proteolytic collagenase and hyaluronidase [38] Periodontal probing that degrade junctional . The specific pathogens that Tooth extraction are most commonly implicated are P. gingivalis and Bacteroides Periodontal surgery forsythus [1], which are transmitted both vertically and hori- Periapical surgery zontally—that is, between parents and children [1] and between Placement of medicated fibers into a periodontal pocket Dental prophylaxis (unless no bleeding is anticipated) spouses [40], respectively. placement and reimplantation of avulsed teeth In response to the invasion of the junctional epithelium, an Dental procedures before which prophylaxis is not recommended reaction is initiated and may successfully limit disease. Suture removal But, if the antibody response is inadequate, deeper bacterial Restorative dental procedures with or without use of a retraction cord penetration results in monocytic activation with elaboration of Intraoral injection of local anesthetic, if not intraligamentary Endodontic procedures, if not extended beyond the root apex cytokines and other inflammatory mediators. and Impressions in turn secrete matrix metalloproteinases that de- Dental radiography stroy collagen, glycosaminoglycans, and bone [39]. The process Placement of a rubber dam is painless, although the host may note a disagreeable taste or treatment odor. Bony support of the tooth is lost as the sulcus base Adjustment of an orthodontic appliance migrates toward the end of the tooth root. Initially, the height Recommended regimens Standard recommendation: amoxicillin, 2.0 g given 1 h before the of gingiva on the tooth is unchanged, resulting in deepening procedure of the sulcus (now termed the “periodontal pocket”). The Regimen for patients unable to take medications orally: ampicillin sodium, 2.0 g given im or iv before the procedure pocket’s bacterial population becomes dominantly anaerobic Possible regimens for patients allergic to penicillins [28]. Clindamycin, 600 mg given 1 h before the procedure Clinical and epidemiologic evidence indicates that the pre- Cephalexin or cefadroxil, 1.0 g given 1 h before the procedure ceding description applies, in most cases, to relatively brief Azithromycin or clarithromycin, 2.0 g 1 h before the procedure (duration, days to weeks) disease episodes, followed by much (continued) longer periods during which host defenses dominate [41]. Over years and decades, measurable loss of osseous support around bleed upon brushing; the flow of sulcular fluid increases and teeth occurs; in the most extreme case, affected teeth are ex- becomes enriched in and [38]. His- foliated. More than 95% of dentate adults older than 50 years tologic findings include vasculitis and lymphocytic infiltration of age show clear evidence of this process (hence the use of of the gingiva and the junctional epithelium (i.e., the sulcus “growing long in the tooth” as a metaphor for aging), although base tissue) [12]. Gingivitis can remain in the state described only ∼20% such adults at any given point in time will show for months and years and will not progress to periodontitis, signs consistent with active periodontal destruction [42].

1218 • CID 2002:34 (1 May) • AGING AND INFECTIOUS DISEASES Table 2. Recommendations for antibiotic prophylaxis for pros- [49, 50]. Studies have also focused on whether periodontitis, as thetic joint infection in patients scheduled to undergo dental an infectious disease, impairs glycemic control in people with procedures. diabetes. At least 1 investigation contradicted this theory of cau-

Patients at elevated risk for prosthetic joint infection sation [51], although others have supported it [52, 53]. Im- Patients whose joint prostheses have been implanted within the previous proving periodontal health to improve glycemic control has also 2 years been studied, but, to date, studies have failed to demonstrate Patients with Patients who are immunosuppressed due to pharmacotherapy causation [54]. or immunocompromised due to disease Explanations for the interaction between periodontitis and People with type 1 diabetes diabetes are still hypothetical. Salvi et al. [55] documented that Patients receiving corticosteroid therapy the type 2 diabetic inflammatory response includes exaggerated Patients who have previously experienced a prosthetic joint infection Dental procedures for which prophylaxis is recommended secretion of several inflammatory mediators, notably IL-1b,

Interligamentary injections prostaglandin E2 (PGE2), and TNF-a, in response to the pres- Placement of orthodontic bands, but not brackets ence of gram-negative cell-wall lipopolysaccharides, with con- Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 Subgingival periodontal procedures (e.g., scaling or root planing) sequent extensive tissue lysis. A second hypothesis is that ad- Periodontal probing vanced glycation end products formed in response to Tooth extraction hyperglycemia, elevated serum low-density lipoprotein levels, Periodontal surgery Periapical surgery and elevated triglyceride levels alter the phenotype Placement of medicated fibers into a periodontal pocket involved in periodontal lesions. Increased inflammatory tissue Dental prophylaxis (unless no bleeding is anticipated) destruction and alveolar bone loss result from that phenotype’s Dental implant placement and reimplantation of avulsed teeth excessive cytokine production [56]. Dental procedures for which prophylaxis is not recommended Suture removal Restorative dental procedures with or without use of retraction cord Intraoral injection of local anesthetic, if not intraligamentary ORAL CONDITIONS OF PERIODONTAL Endodontic procedures if not extended beyond the root apex DISEASE AND ASPIRATION PNEUMONIA Impressions Dental radiography The leading cause of death among nursing home patients and Placement of a rubber dam the second most–common cause for hospitalization in this pop- Fluoride treatment ulation is nursing home–acquired pneumonia [57]. Unlike Adjustment of orthodontic appliance community-acquired pneumonia, which is largely caused by Recommended regimens Standard recommendation: amoxicillin, 2.0 g given 1 h before the proce- viral and pneumococcal pathogens [58], nosocomial pneu- dure; cephalexin or cefadroxil, 1.0 g given 1 h before the procedure; or monia, in general, and nursing home–acquired pneumonia, clindamycin, 600 mg given 1 h before the procedure Other notes specifically, is almost entirely caused by anaerobic gram-neg- Late prosthetic joint infection has not been reported as a consequence of ative bacilli [59]. Reports have established the propensity of dental management in the absence of dental infection; therefore, dental severely ill people to experience oropharyngeal colonization and periodontal infection in a patient with a prosthetic joint should be treated immediately and definitively with gram-negative rods [60], which, in turn, have been dem- Antiseptic mouth rinse applied immediately before dental procedures may onstrated to populate the dental plaque of patients in intensive reduce magnitude and incidence of bacteremia; agents include 0.12% chlorhexidine gluconate and 10% povidone-iodine care units [61] and nursing homes [62]. Finegold [63] specified Presence of other osseous implants, such as plates, screws, and pins, do several prominent periodontal pathogens (including Bacteroides not dictate the need for antibiotic prophylaxis before dental procedures and Fusobacterium species) among “anaerobic bacteria that are NOTE. Data are from [36]. most important as causes” of aspiration pneumonia. A long- term prospective study of 1350 elderly veterans residing in a PERIODONTAL DISEASE AND DIABETES Department of Veterans Affairs (VA) nursing home found sig- nificant correlations between nursing home–acquired pneu- Dental clinicians have long observed that periodontal disease is monia and swallowing dysfunction, dependence in feeding, xe- worse in people with diabetes [43], to the extent that periodontitis rostomia, and presence of S. aureus, the periodontal pathogen has been considered a sixth addition to the 5 complications of P. gingivalis, and the decay organism S. sobrinus [64–66]. A diabetes (i.e., peripheral neuropathy, retinal degeneration, renal consistent picture emerges that conditions of poor oral hygiene, insufficiency, atherosclerosis, and microangiopathy) [44]. Dia- plaque accretion, and compromised host defense that accom- betes is a strong risk factor for bone loss caused by periodontitis pany periodontal breakdown also provide conditions favorable [45]. Poor control of diabetes is correlated with markers of peri- for proliferation and subsequent aspiration of orally incubated odontal disease activity [46–48]. The dominant periodontal path- pulmonary pathogens [67, 68]. ogens are the same for persons with and persons without diabetes Clinically, the critical question is whether control of peri-

AGING AND INFECTIOUS DISEASES • CID 2002:34 (1 May) • 1219 Figure 2. Schematic representation (not to scale) of selected dental and periodontal structures involved in gingivitis. Refer to figure 1 for a description of unmarked anatomic structures. Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 odontal disease would reduce the incidence of pneumonia. nificant for men, even after adjusting for age, blood lipid level, Yoneyama et al. [69] reported that Japanese nursing home res- body-mass index, smoking, and socioeconomic factors. De- idents subjected to daily and weekly oral hygiene interventions Stefano et al. [74] demonstrated that, among National Health experienced fewer bouts of pneumonia, fewer fevers, and fewer and Nutrition Examination Survey (NHANES) II participants, hospitalizations than did control subjects. The findings are in- there was a doubling of risk for coronary heart disease for those triguing and merit independent confirmation and possibly con- with periodontal disease and , even after controlling sideration for broader implementation. for the patient’s sex, smoking, and socioeconomic factors. Josh- ipura et al. [75] noted significant multifactorial correlations between periodontal disease and subsequent cardiovascular dis- CONCERNS ABOUT POSSIBLE ease in 151,000 health care professionals observed prospectively. HEMATOGENOUS EFFECTS OF PERIODONTAL Loesche et al. [76] reported significant correlations between PATHOGENS periodontal disease, lack of periodontal care, and cerebrovas- The edematous state of the diseased periodontal pocket and cular disease in 1350 elderly veterans. Beck et al. [77] found the robust pathogenic bacterial population thriving within significant correlations between bone loss and coronary artery readily lead to periodontopathic bacteria entering the blood- disease, fatal coronary artery disease, and cerebrovascular ac- stream. Cobe [70] reported that gentle toothbrushing and even cident in the 1147 veterans of the VA Normative Aging Study/ chewing caused cultivable anaerobic and aerobic bacteremia in Dental Longitudinal Study, even after adjusting for age, smok- patients with and patients without periodontal disease. In- ing, diet, and other obvious potential confounding variables. creased gingival inflammation correlates with increasing inci- Herzberg and Meyer [78] and Loesche and Lopatin [67] have dence and severity of bacteremia after toothbrushing [71]. Peri- suggested that cell-wall lipopolysaccharides of bloodborne peri- odontal pathogens are among the organisms implicated in both odontopathic bacteria activate conversion of fibrinogen to fibrin, bacterial endocarditis and LPJI [31, 35]. triggering thrombus formation. Haraszthy et al. [79] examined Mattila et al. [72] and Syrja¨nen et al. [73] independently atherosclerotic plaques recovered from endarterectomies and noted correlations between , cerebrovas- identified cellular remnants (in 42% of specimens) and DNA cular disease, and indices of oral health reflecting both caries fragments (in 72% of specimens) from P. gingivalis, Prevotella and periodontal disease activity. Relationships remained sig- intermedia, B. forsythus, and Actinobacillus actinomycetemcomi-

Figure 3. Schematic representation (not to scale) of selected dental and periodontal structures involved in adult periodontitis. Refer to figure 1 for a description of unmarked anatomic structures.

1220 • CID 2002:34 (1 May) • AGING AND INFECTIOUS DISEASES tans. Beck et al. [77] and Offenbacher et al. [80] proposed an ably apply concentrated sodium fluoride gel daily and schedule alternative model for the periodontitis/vascular disease connec- more frequent dental visits. People who have had missing teeth tion that was related to the aforementioned mechanism described replaced by dental appliances may need to become adept with by Salvi et al. [55], which involved injury to the endothelium 1 or more of a variety of specialized dental brushes to clean caused by inflammatory mediators, such as C-reactive , nonanatomic surfaces. Someone who has experienced advanced

IL-1b, PGE2, and TNF-a, elaborated by bloodborne periodon- bone loss due to periodontal disease will need to devote extra topathic bacteria. effort to clean exposed root surfaces. In older persons, the To date, no intervention studies have been published that preceding 3 factors, plus others—finances, motivation, social indicate that there are positive cardiovascular effects resulting setting—may impede the efficacy of preventive dentistry. from periodontal therapy. Hujoel et al. [81] expressed concern Daily provision of oral hygiene is more than a matter of that reports linking periodontal and vascular diseases might grooming. Effective use requires a level of manual inspire a return to the practice of premature full-mouth ex- dexterity, tactile acuity, and visual ability that has likely dimin- tractions that occurred early in the 20th century, when the ished in an older person who requires assistance with other Downloaded from https://academic.oup.com/cid/article/34/9/1215/463157 by guest on 02 October 2021 “focal infection” theory of oral disease metastatic to other sites care. Frail elderly persons are understandably encouraged to was accepted as a cause for inflammatory conditions [82]. Hu- participate in their own daily hygiene routines as much as joel et al. [81] reviewed studies correlating periodontal and possible. But a caregiver must recognize when minimal stan- vascular diseases and concluded it was, at present, imprudent dards of oral cleanliness are not being maintained. Sadly, nurse to recommend extraction of periodontally involved teeth for aides are themselves seldom aware of the importance of and patients solely to improve cardiovascular or cerebrovascular techniques for maintaining oral health, either for themselves status. or for those under their care, and they are rarely sanctioned for failing to provide oral care; therefore, they consider the chore to be among the lowest priorities in their overcrowded CLINICAL RECOMMENDATIONS daily routines [83]. In response to the endemically unclean mouths among de- Oral bacteria are unquestionably related to disease outside the pendent elderly individuals, some chemotherapeutic ap- oral cavity, particularly in older people. Hematogenous metas- proaches for sanitizing the oral cavity have been used. Unfor- tasis of caries-derived and periodontally derived infectious or- tunately, the agents introduced to date have limited efficacy ganisms causes serious cardiac and orthopedic disease. Aspi- against caries and periodontal disease unless combined with ration of pathogens that colonize the oropharynx significantly traditional daily oral hygiene. The topical antiseptic agent chlor- contributes to geriatric mortality, morbidity, and health care hexidine gluconate is available as 0.12% mint-flavored oral expense. The total area of the inflamed epithelial lining of peri- rinse. Twice-daily 60-s rinses reduce the counts of gingivitis odontal pockets in a person with a full may exceed pathogens and, to a lesser extent, cariogenic organisms; gingival 2 25 cm [41]. A bleeding cutaneous wound of this dimension inflammation is reduced as well [84]. Yoneyama et al. [69] used should receive immediate medical and nursing attention. But a a 10% povidone-iodine solution swabbed onto the and combination of factors has allowed much of the mainstream oropharynx in conjunction with toothbrushing to reduce the medical system, the caregiving population, and elderly persons pathogenicity of oropharyngeal aspirates. themselves to passively accept or simply ignore oral disease in If poor oral health did not lead to serious disease, unclean advanced age. These factors include the historic schism between mouths would merely be an aesthetic concern. But uncontrolled dentistry and medicine, the expense of dental care in the of dental and periodontal diseases lead to serious morbidity, mor- the relative scarcity of third-party dental coverage among older tality, and considerable avoidable health care costs. Sadly, the Americans, people’s resignation to the dental deterioration as- avoidable but undeniable status quo of poor oral hygiene sociated with advancing age, the aversion of most adults to having among frail elderly persons will remain unchanged until the their teeth brushed by someone else, the aversion of most people public demands a higher standard of oral care for their de- to cleaning another person’s mouth, and many adults’ aversion pendent forebears, or until those who control distribution of to dental treatment because of unpleasant memories. health care resources realize that the added expense of daily Caries and periodontal diseases are preventable through oral care is lower than the cost of ignoring it. widely known measures: use of a toothbrush and fluoridated dentifrice at least twice daily, some means for cleaning between teeth and at the gumline, receipt of regular dental examinations References with professional cleaning, and limited intake of refined sugar. 1. 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