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poor oral health and kidney diseases

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Changes in the oral cavity, such as periodontitis and other manifestations of poor oral health, are common in patients with chronic kidney disease (CKD) and may contribute to increased morbidity and mortality because of systemic consequences such as inflammation, infections, protein-energy wasting, and atherosclerotic complications. Poor oral health in CKD patients may thus represent an important, but often overlooked, problem. Several studies show that uremic patients have higher rates of decayed, missing, and filled teeth, loss of attachment, and periapical and mucosal lesions than the general population. The consequences of poor oral health may be more severe in CKD patients because of advanced age, common comorbidities such as diabetes, concurrent medications, and a state of immune dysfunction that may increase the risk for systemic consequences of periodontitis and other oral and dental pathologic conditions. Poor dentition and other signs of poor oral health should be an alarm clock also at early stages of CKD. However, it remains to be determined whether more successful management of poor oral health and periodontitis will reduce the risk of inflammation, infection, protein-energy wasting, and atherosclerotic complications in CKD patients. This review explores etiological factors and potential systemic consequences of poor oral health in CKD patients as well as possible preventive and therapeutic strategies
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  Systemic Consequences of Poor Oral Health inChronic Kidney Disease Patients Harun Akar,*  †  Gulcan Coskun Akar,*  ‡§   Juan Jesu´s Carrero,*   Peter Stenvinkel,* and Bengt Lindholm*  SummaryChanges in the oral cavity, such as periodontitis and other manifestations of poor oral health, are common inpatients with chronic kidney disease (CKD) and may contribute to increased morbidity and mortality becauseof systemic consequences such as inflammation, infections, protein-energy wasting, and atherosclerotic com-plications. Poor oral health in CKD patients may thus represent an important, but often overlooked, problem.Several studies show that uremic patients have higher rates of decayed, missing, and filled teeth, loss of at-tachment, and periapical and mucosal lesions than the general population. The consequences of poor oralhealth may be more severe in CKD patients because of advanced age, common comorbidities such as diabe-tes, concurrent medications, and a state of immune dysfunction that may increase the risk for systemic conse-quences of periodontitis and other oral and dental pathologic conditions. Poor dentition and other signs of poor oral health should be an alarm clock also at early stages of CKD. However, it remains to be determinedwhether more successful management of poor oral health and periodontitis will reduce the risk of inflamma-tion, infection, protein-energy wasting, and atherosclerotic complications in CKD patients. This review ex-plores etiological factors and potential systemic consequences of poor oral health in CKD patients as well aspossible preventive and therapeutic strategies. Clin J Am Soc Nephrol  6: 218–226, 2011. doi: 10.2215/CJN.05470610 Introduction Cardiovascular disease (CVD), which is often due toor combined with atherosclerosis and infectious com-plications, is the main cause of death in patients withchronic kidney disease (CKD) (1,2). A number of tra-ditional, novel, and uremia-specific risk factors coex-ist in CKD and contribute to the increased cardiovas-cular risk in CKD population (1). Poor oral health,which is related to advanced age and diabetes melli-tus, may constitute an under-recognized novel riskfactor, because recent studies have shown how peri-odontitis associates with coronary heart disease andcerebrovascular disease in the general population (3)as well as in hemodialysis (HD) patients (4). A plau-sible explanation would involve bacterial pathogenscausing peridontitis, leading to systemic inflamma-tion as induced by lipopolysaccaride coats and thustriggering atherogenesis, thrombus formation, andplatelet aggregation (5). However, periodontal dis-eases are treatable and modifiable risk factors (6,7).Furthermore, novel links between manifestations of poor oral health and systemic complications in CKDsuchasprotein-energywasting(PEW),infections,andatherosclerotic complications are being established(Figures 1 and 2). In this review, we explore theselinks and possible measures to tackle these problems. Common Orofacial Problems in CKD Patients As a consequence of a number of uremic metabolic,endocrinological, and immunological imbalances,CKD patients suffer from numerous systemic compli-cations that may contribute to poor oral health (8).Although there are no specific signs in the oral cavityindicating the presence of CKD (9), a whole range of changes occur in the oral cavity that are associatedwith CKD itself or with the CKD therapy (10,11)(Figure 3). Indeed, CKD has been reported to affectthe teeth (9,12–15), oral mucosa (10,16–20), bone(11,12,21–26), periodontium (27–30), salivary glands(17,31,32), tongue (10,33), mouth cavity (34–36), andtemporomandibular joint (37).Several studies have demonstrated higher rates of oral pathology in dialysis patients (16,17,27) with oneor more oral symptoms (17,35,38) such as xerostomia,taste disturbances, uremic odor, tongue coating, mu-cosal inflammation, mucosal petechia/ecchymosis,oral ulceration, or enamel hypoplasia (16,36,39). Xe-rostomia (or dryness of the mouth) may predispose tocaries and gingival inflammation as well as contributeto difficulties with speech, denture retention, masti-cation, dysphagia, sore mouth, loss of taste, and in-fections (40). CKD patients are also often prone toretrograde parotitis, which is believed to result from acombination of direct gland involvement, chemicalinflammation, side effects of drug therapy, dehydra-tion, and mouth breathing (34). Patients with renalfailure often complain of an ammonia-like bad odor,perhaps because of the high urea content in saliva andits subsequent breakdown to ammonia. Increaseddental calculus has been observed, perhaps as a con-sequence of a high salivary urea and phosphate lev-els. Interestingly, however, the antibacterial effect of  *Divisions of RenalMedicine and BaxterNovum, Department of Clinical Science,Intervention andTechnology, KarolinskaInstitutet, Stockholm,Sweden,  † AdnanMenderes UniversitySchool of Medicine,Division of Nephrology,Aydin, Turkey, ‡ Department of Prosthodontics, EgeUniversity, School of Dentistry, Izmir,Turkey,  § Ege University,Atatu¨rk MedicalTechnology VocationalTraining School, Izmir,Turkey, and   Centre forGender Medicine,Karolinska Institutet,Stockholm, Sweden Correspondence: Dr. Bengt Lindholm,Divisions of RenalMedicine and BaxterNovum, K56 KarolinskaUniversity HospitalHuddinge, 141 86Stockholm, Sweden.Phone: 46-8-58582601;Fax: 46-8-58583925;E-mail: bengt.lindholm@ki.se 218  Copyright © 2011 by the American Society of Nephrology www.cjasn.org Vol 6 January, 2011 In-Depth Review  urea may also be responsible for a lower caries rate asreported in HD patients (28,35). A spectrum of oralmucosal lesions, including white and erythematouspatches and/or ulceration, lichen planus-like disease,oral hairy leukoplakia, histopathologically similar le-sions to Epstein-Barr virus, macules, nodules, andnon-Hodgkin’s lymphoma and/or Kaposi’s sarcoma,has been described in dialysis patients and in kidneytransplant recipients secondary to both drug-relatedimmunosuppression or an associated drug (17). Theprevalence of cyclosporin-induced gingival hyperpla-sia in renal transplant patients varies from 22 to 58%in different reports and is more common in patientswith increased cyclosporin dosage, in those with in-creased dental plaque and gingival inflammation, andin younger patients (41). The incidence of tacrolimus-induced gingival hyperplasia in renal transplant pa-tients is lower, generally between 0 and 15% (41).Although rare, uremic stomatitis is another clinicalfinding in advanced uremia; it consists of erythemop-ultaceous, ulcerative, hemorrhagic, and hyperkera-totic forms (42). The first two forms may occur aspainful anterior mucosal lesions on the ventral tonguethat usually heal spontaneously, after treatment of uremia (43). The hemorrhagic and hyperkeratoticforms may occur because of bleeding diathesis andlong standing uremia, respectively (42). An intraoralform of “uremic frost” that can be observed in un-treated uremia results from remaining urea crystalsleft on epithelial surfaces after saliva evaporation.Erosions of the dentition may occur because of regur-gitation resulting from nausea (25). The manifesta-tions of renal osteodystrophy in mandible, maxilla,and the oral cavity include demineralization, de-creased trabeculation, loss of lamina dura, radiolucentgiant cell lesions, macrognathia, metastatic soft-tissuecalcifications, tooth mobility, malocclusion, enamelhypoplasia, and pulp stones (21,44,45). Poor Oral Health as a Source of Inflammation Gingivitis (defined as inflammation of the gingiva)and periodontitis (inflammation of the gingiva plussupporting tissues of the teeth) are common manifes-tations of poor oral health. Periodontitis represents apotential source of inflammation, and during the for-mation of peridontal pockets colonized with gram-negative anaerobic bacteria, an inflammatory cell in-filtrate is recruited into the lesion that secretesproinflammatory mediators (41,46). Both gingivitisand periodontitis are seen more frequently in ESRDpatients (47–49). Gingival hyperplasia is a relativelycommon periodontal complication in renal transplan-tation patients that has been attributed to cyclosporindosage and the presence of dental plaques, likelycontributing to gingival inflammation (50). Estimatesof the prevalence of periodontitis vary across studies(Table 1): a 14% prevalence of moderate to severeperiodontitis was reported among individuals   20years of age in the United States population (51) and13% of subjects had severe periodontitis in a normalSwedish population (52). This divergency in preva-lence depends on methodological, etiological, age-related, racial, ethnic, socioeconomic, cultural, and behavioral factors that may be specific for each coun-try. To exemplify this, although a Spanish report (27)showed significant higher plaque and calculus indicesand lower salivary secretions in HD patients as com-pared with healthy controls, a report from The Neth-erlands (37) described comparable levels for mostdental aspects. Undoubtedly, cross-cultural studiesare needed on this neglected issue of dental problemsin patients with ESRD. For comparative analyses itwould be desirable to follow World Health Organi-zation recommendations for a systematic classifica-tion on the basis of the severity of different aspects of periodontal disease including gingival index, papil-lary bleeding index plaque index, and clinical attach-ment level (53).The causes of increased periodontitis are not fully Local infections around or beneath the teethPeriodontal Problems Atherosclerotic Plaque Formation Periodontal Pocket Blood Vascular Wall  Albumin  E-SelectinGram (-) Facultative AnaerobicBacteria Loss of AppetiteProtein Energy WastingInflammation Figure 1.  | Hypothetic model for how peridontitis may act as apotential cause of local and systemic inflammation in chronickidney disease patients. SAA, serum amyloid A; CRP, C-reac-tive protein; MMP, matrix metalloproteinase. Bad Odor  Protein EnergyWasting Decreased Nutrient Intake Metalic Taste Drugs (antihypertensive,immunosuppresive) Taste DisturbancesXerostomiaOral Ulcers/StomatitisXerostomiaHighSalivaryUreaHighSalivaryPO 4 Renal OsteodystrophiaTMJProblems Poor Oral HygienePsychological Problems ChewingProblemsUnfitting DentalProsthesisIncreasedCariesChewingProblemsUnfitting DentalProthesisDental ProsthesisEdentulousness MasticatoryDefficiency Uremia Figure 2.  | Possible contribution of poor oral health in uremiato reduced nutrient intake and protein-energy wasting inchronic kidney disease patients. Clin J Am Soc Nephrol 6: 218–226, January, 2011 Consequences of Poor Oral Health in CKD, Akar et al. 219  elucidated, but it has been proposed that repeatedsystemic anticoagulation may predispose HD patientsto gingival bleeding and facilitate bacterial coloniza-tion (53). At the same time, oral barriers might havedeteriorated because of disturbed humoral defense(46). Commencement of dialysis therapy appears to be accompanied by major changes in the oral condi-tion (46), and therefore periodontal disease has beenreported to progress in severity across predialysis,peritoneal dialysis (PD) and HD patients, respectively(53). Unfortunately, very few studies compared theprevalence of these symptoms between HD and PDpatients. One study, however, reports periodontitis to be less severe in PD patients—and moderate in pre-dialysis CKD patients—as compared with HD pa-tients (53). Transplant patients were reported to haveless halitosis when compared with HD, PD, and pre-dialysis patients, leading to the hypothesis that spe- Figure 3.  | Common orofacial problems associated with chronic kidney disease itself or caused by therapy. Table 1. Estimates of the prevalence of periodontitis and gingivitis in CKD patients Study Country Treatmentand VintageSampleSizeMean Age(Years)DM(%)Periodontitis(%)Gingivitis(%) Naugle  et al.  (16) USA HD 1 to 3years45 28 36Klassen and Krasko(11)Canada HD 25  30months94 51.1  18.8 33 99Al-Wahadni andAl-Omari (49) Jordan HD 1 to 3years47 42.9  12.5 NA 29.8  b 100Chen  et al.  (48) Taiwan HD 49  3months253 58.8  0.8 39.5 58.9 c Kshirsagar  et al. (46)USA HD 4 years 154 54.6  13.3 22 23Buhlin  et al.  (47) Sweden Predialysis a 51 55.9 27.5 36 d 46Cengiz  et al.  (82) Turkey PD 110 44.3  0.6 NA 67.3 c DM, diabetes mellitus; NA, not applicable. a Close to starting dialysis.  b Moderate periodontal disease. c Moderate to severe periodontitis. d Severe periodontitis. 220 Clinical Journal of the American Society of Nephrology  cific uremic toxins may determine halitosis in theCKD population (8). Additionally, renal transplanta-tion also enhances salivary flow and decreases symp-toms of xerostomia and thirst (54).Several possible reasons have been proposed toaccount for the poor oral health in uremia that has been associated with immune dysfunction includingdefects in lymphocyte and monocyte function (41).Altered cellular immunity along with malnutritioncontributes to a immunodeficient state in uremia.Uremic patients are more prone to bacterial infections because of malnutrition, which leads to a diminishedability to produce antibodies (35). In support of this,increased gingival inflammation has been reported inassociation with longer dialysis vintage (48), althoughthis finding could not be observed in a more recentstudy (4). Because a strong association exists in thegeneral population between diabetes and periodonti-tis (55), it has been proposed that the increasedprevalence of diabetes in ESRD could also contrib-ute to the over-representation of periodontitis (41).Psychological factors and depressive symptomsmay decrease the priority of maintaining good oralhealth in ESRD population (11,16,41). Finally, sec-ondary hyperparathyroidism has been suggested asa possible cause of peridontal disease in ESRD pa-tients, but this has not been confirmed in recentexploratory analyses (56).A proposed model for how peridontitis could act asa potential cause of local and systemic inflammationin CKD patients is shown in Figure 1. At least tworeports support the hypothesis that periodontitis maycontribute to the systemic inflammatory burden in theESRD population (48,57). Poor oral health status wasfound in 80% of 253 HD patients with periodontaldisease and was associated with both high C-reactiveprotein and low serum albumin levels in univariateanalysis but not in multivariate (48). On the basis of these findings, it is important to monitor and main-tain the oral health status of patients undergoing di-alysis, as well as in patients who are considered aspotential renal transplant candidates. When a patientis considered for renal transplantation, ensuringhealthy dentition becomes important because of theuse of immunosuppressive drugs, which may furtherpredispose to oral and possibly disseminated infec-tion (11). AlthoughanumberofstudiessuggestthattheoralhygienestatusofESRDpatientsmaybeworsethanin the general population, only very few assessed thefrequency of tooth brushing, flossing, and dental visitsin these patients: tooth brushing was reported to bedoneonceormoredailyin79%ofthepatients,lessthanonce daily in 14% and never in 7% of the patients (11).The last dental visit(s) was reported as  1 year ago, 1 to2 years ago, 2 to 5 years ago, and  5 years ago in 37, 20,7, and 35%, respectively, among dentated dialysis pa-tients. Another study reported tooth brushing frequen-cies as twice a day, once a day, irregular, and never in14, 29, 40, and 17% of the patients, respectively (58).In a study comprising 86 dentated HD patients inwhom sera were assayed for IgG-antibody levels tosix periodontal species, the IgG antibody levels to Porphyromonas gingivalis  were elevated in patientswith systemic inflammation (57), leading the authorsto propose such antibodies as a serum marker of destructive periodontal disease. Elevation of salivarymacrophage inflammatory protein-1  , a chemokinethat recruits osteoclast progenitors, was suggested asa biomarker of early events in inflammatory-inducedperiodontal bone loss that precedes radiographic ev-idence in carriers of   Aggregatibacter actinomycetem-comitans , an oral commensal that can cause severeinfections in the periodontium (59). Poor Oral Health as a Contributor to InfectiousDiseases Periodontitis represents a potential source of epi-sodes of bacteremia, especially in the immunocom-promised patient. This may not be surprising consid-ering that the overall size of periodontal lesions mayrange from 1500 to 2000 mm 2 (60) and that the num- ber of bacteria can exceed 1    10 8 in a single peri-odontal pocket (61). Although bacteremia can occurafter almost any type of dental manipulations includ-ing tooth brushing and flossing, these episodes are,however, usually transient and inconsequential forhealthy individuals. In contrast, bacteremia in pa-tients with dental caries and periodontal diseasetends to be more sustained, raising the risk of hema-togenous dissemination of the dental infection (62).Bacteria can adhere to damaged heart valves andcause endocarditis, and for this reason prophylacticantibiotics are recommended in patients with valvu-lar heart disease (62). It is possible that the immunedysfunction in uremia (2) may substantially increasethe risk for such systemic consequences of periodon-titis and other oral pathologic conditions because wecannot fully explain why these patients suffer fromsuch high rates of inflammation, infection, and CVD.Although links between oral health and infectionshave not been systematically studied, there are sev-eral reports in the literature. Bacteria from oral bio-films may be aspirated into the respiratory tract andmay cause the initiation and progression of systemicinfectious conditions such as pneumonia in high-risksubjects (63). A recent Swedish study showed that32%ofESRDpatientsand11%ofhealthycontrolshadfungal hyphae through microscopy on buccal smears(64). Clinical signs, including oral lesions associatedwith fungal infection, membranous candidiasis, ery-thematous oral stomatitis, and angular chelitis werefound in 15% of the ESRD patients but not in thecontrol group. Patients and controls with self-experi-enced mouth dryness were both likely to have fungalhyphae. Fungal colonization in the oral mucosalmembranes may therefore have potential conse-quences like sepsis. Poor Oral Health as a Contributor to AtheroscleroticComplications In response to an infectious and inflammatory trig-ger, nonspecific innate and more specific adaptive Clin J Am Soc Nephrol 6: 218–226, January, 2011 Consequences of Poor Oral Health in CKD, Akar et al. 221
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