METHODS ^ J lz h e im e r ’s disease, an age- ABSTRACT
related, progressive and chronic Forty-one comm unity-dwelling
neurodegenerative disorder, is G e n e r a l ly h e a lth y , w hites (22 m en and 19 women) the m ost common form of u n m e d ic a te d p a tie n ts with a clinical diagnosis of dem entia am ong th e elderly.1,2 w i t h A lz h e im e r ’s d is e a s e Alzheim er’s disease were The disease is characterized by evaluated as p a rt of an ongoing h a v e f e w b u t s ig n if i c a n t neurological, cognitive and longitudinal study a t the c h a n g e s in th e ir o ra l N ational In stitu te on Aging behavioral sym ptom s with severe consequences to m any h e a l t h . S tu d y r e s u l t s (NIA) a t the Clinical C enter of organ system s. re in fo rc e p re v e n tiv e o ra l the N ational In stitu tes of Incidence of Alzheim er’s h y g ie n e f o r t h e s e H ealth. The average age was increases dram atically w ith p a tie n ts . 68.2 ± 9.3 years (m ean ± SD) age, from about 0.1 percent a t w ith a range of 48 to 83 years. age 60 to 65 to as high as 47 elderly dem ented have poorer A diagnosis of definite, percent a t age 85.3 Intellectual personal oral hygiene habits.4 probable and possible faculty deterioration m ay be ■■ S ubm andibular salivary Alzheim er’s was m ade caused by reduced synaptic gland dysfunction in according to NINCDS-ADRDA connectivity, partially unm edicated Alzheim er’s criteria,19 after patien ts were attrib u ted to neuronal loss.2 p atients was reported recently, screened vigorously to exclude Definitive diagnosis requires suggesting th a t neuronal other medical, neurological or neuropathological confirmation degeneration also influences psychiatric conditions. The and, unfortunately, th ere is no oral physiology.5 study population included two effective tre a tm e n t for the Published reports definite, 34 probable and five intellectual and functional recom mend preventing oral possible patients. im pairm ent resulting from the disease and m aintaining oral All patien ts were extensively disease. health and function for patients evaluated w ith diagnostic radio Recent research advances as long as possible.618 There is graphs, computed tom ographic allow a better u n d erstanding of no available inform ation on the brain scans, m agnetic Alzheim er’s b u t little h as been general oral h ealth of patients resonance imaging, positron reported about its oral signs. w ith A lzheim er’s, nor have any emission tom ography and Only two studies have specific oral h ealth needs been neuropsychological and medical exam ined a component of oral identified for th is population, tests.20-23 None was tak in g any health in patients w ith the based on th eir oral condition. m edication for system ic disease, disease: This investigation exam ines nor being treated for other "> D entures among th e elderly gingival, periodontal, dental, disorders. Tw enty-three w ith early stages of senile oral m ucosal and salivary subjects were included in a dem entia were older and less p aram eters in unm edicated, previous study of salivary gland clean compared w ith a control essentially healthy p atients function in patients w ith population, im plying th a t the w ith Alzheim er’s. Alzheim er’s disease.5 The Mini-
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M ental S tate Exam ination subgingival calculus. The exact tests were performed for (MMSE) was adm inistered to distance from the free gingival prevalence data. estim ate the severity of m argin to th e cementoenamel C orrelation analyses were cognitive im pairm ent24; the junction and the distance from performed on patients with average value was 18.2 ± 1.0 the FGM to the bottom of the Alzheim er’s to determ ine if a (Mean ± SEM) of a m aximum sulcus or pocket was m easured relation existed betw een level of 30 points. w ith an NIDR color-coded dem entia (as determ ined from Forty-nine healthy white periodontal probe. Later, the the MMSE score) and an people (25 m en and 24 women) percentage of tooth surfaces for individual oral health were selected as controls. The each subject w ith dental plaque, param eter. One-way ANOVA average age was 64.1 ± 8.2 gingival bleeding and calculus tests were performed on the years (m ean ± SD) w ith a range was calculated and the am ounts Alzheim er’s population to of 50 to 82. All were volunteer of gingival recession, pocketing m easure any possible participants in a norm ative and attach m en t loss were association between diagnosis aging program conducted by the recorded. (definite, probable and possible NIA. All were community- All intraoral structures were Alzheim er’s) and any of th e oral dwelling individuals who assessed w ith a modified health clinical m easurem ents. underw ent rigorous medical, mucosal ratin g scale.31 Normal D ata were analyzed using the neurological and laboratory RS3 software package (BBN screening.20,25 Control Patients with Alzheimer’s Software Products Corp.) A individuals were n either being had significantly more criterion of P<0.05 was accepted tre a te d for any systemic disease for significance in all statistical nor tak in g prescription sites with gingival tests. m edications. The average plaque, bleeding and R ESU LTS MMSE value for control calculus, compared with subjects was 29.4 ± 0.7 (m ean ± As no gender differences were SD). controls observed for any of the clinical The diagnosis of each patient param eters, analyses were was unknow n a t the tim e of the mucosal or mild changes (dry, performed w ith m en and clinical exam ination. I pale or glossy m ucosa and women combined. P atients with interview ed all participants and alterations in mucosal Alzheim er’s had significantly perform ed a clinical topography) were rated zero, more sites w ith gingival plaque, exam ination, as follows 26,27: and m oderate or severe changes bleeding and calculus, ■“ D ental, periodontal and (erythem ic or leukoplakic com pared w ith controls (Figure m ucosal m easurem ents. The lesions, ulcerations and l).To determ ine the severity of num ber of tee th (excluding erosions) were rated one.32 Oral gingival disease, the num ber of th ird m olars), decayed-missing- candidal lesions (atrophic, study subjects w ith dental filled-teeth score, and the pseudom em branous and plaque, gingival bleeding and num ber of tee th w ith coronal denture stom atitis) were calculus on 75 percent or more and cervical caries and clinically diagnosed and of all dental sites surveyed was restorations were recorded.28 grouped together.33 analyzed. The mesiobuccal, midbuccal, ■■ S tatistical analysis. The Forty-four percent of the distobuccal, m esiolingual, mid- d ata were analyzed for patients (17 of 39; two patients lingual and distolingual differences betw een Alzheim er’s were edentulous) had dental surfaces of the six teeth p atients and control subjects, plaque on a t least 75 percent of proposed by Ram fjord29were and betw een m en and women all surveyed tooth sites, which exam ined for periodontal w ithin each group. A S tudent’s was statistically greater th an p aram eters,30 according to ¿-test was used when m ean the 11 percent (five of 49) found NIDR criteria.28 values had a norm al in th e controls. Sim ilar analyses Briefly, the 36 tooth surfaces distribution, and a Mann- for gingival bleeding and were assessed for presence or W hitney U procedure was used calculus showed no statistical absence of dental plaque, for non-param etric values. Chi- differences between study gingival bleeding and supra- or square and two-way F isher’s groups.
54 JADA, Vol. 123, January 1992
No statistically significant coronal and cervical surfaces one removable prosthesis differences for any of th e three and coronal restorations were (complete or partial). Analyzing periodontal param eters were not statistically different the prevalence of denture observed (Figure 2). W hen an between groups (Table 1). stom atitis, erythem a or analysis was perform ed to A lternatively, DMFT and the ulceration showed no determ ine if any correlations num ber of teeth w ith cervical differences betw een these two existed betw een MMSE scores restorations were greater prosthesis groups, although and gingival and periodontal am ong patients with about 50 percent of both param eters in patients, a Alzheim er’s compared w ith populations had some form of significant correlation was controls. Significant negative denture stom atitis (six of 12 found for periodontal pocketing. correlations were found Alzheim er’s, five of 12 controls). Increased periodontal pocketing betw een th e MMSE score and No correlations were identified was associated w ith a num ber of teeth w ith coronal between MMSE scores and any decreasing MMSE score. B ut no caries and cervical caries. No of the oral mucosal param eters other correlation was other statistically significant investigated in th e Alzheim er’s statistically significant. correlations were identified for patients. There were no statistical the dental param eters. D IS C U S S IO N differences am ong the three Intraoral mucosal p atien t types (definite, exam ination showed no Studying th e oral health of probable, possible) for any of significant differences betw een unm edicated patien ts w ith the gingival and periodontal groups. There was a Alzheim er’s disease revealed m easures, except gingival statistically significant greater few yet significant differences bleeding. Definite (n=2) and prevalence of dry and cracked in comparison w ith healthy, probable (n=32) Alzheim er’s lips among patients with unm edicated control subjects. subjects had a greater Alzheim er’s (13 of 41) compared Since th is is th e first available percentage of sites w ith gingival w ith controls (five of 49). There general oral h ealth exam ination bleeding th an the possible were no differences in the of p atients w ith Alzheim er's group (n=5). Two probable presence of oral candidiasis disease, no comparisons can be subjects were edentulous. among the two groups. made w ith other populations of The total rem aining teeth, Twelve patients and 12 patients w ith Alzheim er’s. num bers of teeth w ith decayed controls were w earing a t least P atien ts in this study were carefully screened for TA BLE 1 Alzheim er’s disease.19To isolate the effects of Alzheim er’s DENIAL PARAMETERS IN PATIENTS WITH ALZHEIMER'S DISEASE AND CONTROLS* disease on oral health and to DENTAL ALZHEIMER'S CONTROLS DIFFERENCE elim inate the influence of other PARAMETER (n=41) (n=49) disorders or medical tre a tm e n t No. teeth 21.1 ± 1.2 22.2 ± 1.1 NS f as potential confounding DMFT 21.1 ± 0.6 18.5 ± 0.8 P = 0.02$ variables, only community- No. teeth with dwelling patients who were not coronal caries 0.8 ± 0.3 0.4 ± 0.1 NS being tre a te d for any other No. teeth with systemic disease and did not cervical caries 0.6 ± 0.2 0.6 + 0.2 NS take m edications were included. No. teeth with Alzheim er’s p atients had coronal dim inished gingival health. restorations 13.8 ± 1.0 12.3 ± 0.9 NS There were greater gingival No. teeth with plaque, bleeding and calculus in cervical patients compared with restorations 2.2 ±0.4 1.8 ± 0.4 P = 0.03§ controls. For alm ost h alf (44 percent) of the patients, 75 * Results expressed a t M ± SEM. t NS = not significant. percent or more of their t S tu d en t’s i-test. surveyed tooth surfaces were § M ann-W hitney test. covered w ith dental plaque. The
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FIGURE 1 evidence th a t dental decay had 80 increased recently in patients w ith Alzheim er’s. P atients had Ul 70 22 percent more teeth w ith I/) cervical restorations th an did « z 60 controls. Although the tim e of < caries development in the study III population was unknown, it is I 30 known th a t cervical decay V) Ul increases w ith age.28As the I- patients were 48 years or older, 35 cervical restorations were likely IL 0 30 placed later in life. h These findings suggest a Z different disease p a tte rn in 111 2 0 0 Alzheim er’s patients compared cc w ith controls. P atients w ith the Ul tL i o disease m ay be susceptible to cervical decay. Salivary gland hypofunction is associated with PLAQUE GINGIVAL BLEEDING CALCULUS cervical decay,39 and decreased salivary output was previously CONTROL SUBJECTS identified in unm edicated Alzheim er’s patients.5 PATIENTS WITH ALZHEIMER'S DISEASE The num ber of teeth with coronal and cervical caries increased w ith increasing Gingival parameters in 41 unmedicated patients with Alzheimer’s disease and 49 healthy controls. Results are expressed as percent of dem entia severity (determ ined sites with plaque, gingival bleeding, or calculus (M ± SEM). Columns by decreasing MMSE scores24). that share a common subscript are significantly different at #»<0.0001 Except for periodontal (a), PcO.OI (b), P<0.04 (c). pocketing, there were no other correlations of oral health greater prevalence of plaque m easured adequately). param eters and level of accum ulations found in patients The periodontal health of cognitive function. There were partially accounts for the patients was statistically indis no additional associations increased gingival bleeding and tinguishable from th a t of betw een Alzheim er’s diagnosis calculus compared with controls. This finding is (definite, probable and possible) controls. surprising, since tradition and any oral health Since cognitive im pairm ent, dictates th a t periodontitis is m easurem ents except gingival m otor restlessness and apraxia preceded by gingivitis.34 bleeding. are common in Alzheim er’s, it is Relatively recent findings, However, none of these not surprising th a t patients in however, report th a t gingivitis significant correlations or this study had more gingivitis may not be a harbinger of associations was statistically th a n controls. Satisfactory oral im pending periodontal strong in patients w ith hygiene requires cognitive and destruction.35'38 Possibly for Alzheim er’s. It is not known if voluntary m otor skills. Alzheim er’s patients in this dental caries, gingival bleeding Im pairm ent of these skills m ay study, gingivitis has not been and periodontal pocketing will resu lt in poor dental plaque present long enough to resu lt in advance in a patient with removal. Decline in memory, periodontal disease. progressive degenerative prom inent among Alzheim er’s In the two groups, no differ dem entia. But given the patients, m ay cause infrequent ences were detected in the presence of salivary gland or irreg u lar oral hygiene (unfor num bers of teeth with coronal dysfunction and gingivitis, the tunately, this cannot be or cervical decay. B ut th ere was incidence of dental caries,
56 JADA, Vol. 123, January 1992
gingival and periodontal disease controls, according to Saliva’s flushing action clears probably will increase w ith the established techniques.4142 plaque and bacteria from dental dem entia’s progression. The findings were sim ilar to and oral mucosal surfaces. If The oral m ucosal condition of those reported earlier using 23 salivary output is diminished, Alzheim er’s patien ts was of 41 subjects. Briefly, parotid patients m ay be more likely to sim ilar to th a t of controls, but output was u n altered by develop gingivitis and cervical more p atients had dry, chapped Alzheim er’s disease in these caries. The lack of saliva m ay lips. D im inished saliva patients, b u t subm andibular also partially account for the secretion has been associated flow rate s were decidedly increased prevalence of dry w ith changes in th e appearance diminished. Several hypotheses labial mucosa am ong these of labial m ucosa.40 Although we for these findings were patients. found a high prevalence (about suggested,5 including The findings from this study 50 percent) of denture neurological deficiencies and have fu rth e r im plications for stom atitis, erythem a or dehydration. the clinical care of Alzheim er’s ulceration in the Alzheim er’s Salivary gland dysfunction patients since all study subjects patients, the control group had m ay be im plicated in altered were unm edicated. The sim ilar problems. gingival h ealth and increased psychotropic drugs used to tre a t Because of th e im portance of cervical restorations in Alzheim er’s patien ts for mood salivary gland function in these Alzheim er’s patients. Saliva is disorders1and for reversing patients, u n stim ulated and 2 essential to m ain tain oral cognitive losses44 are frequently percent citrate-stim ulated health.43 It protects the m outh, associated w ith salivary gland parotid and subm andibular upper airw ay and digestive hypofunction.16 W hen these salivary gland flow rate s were tra c t and facilitates m any medications are given to people collected from p atients and sensorim otor phenomena. w ith Alzheim er’s, they m ay develop fu rth e r alterations in FIGURE 2 salivary fluid output, 3 subsequently leading to dim inished oral health. 2.5 CONCLUSIONS
From th is study’s findings,
2 Ul several oral h ealth care ID 2 m easures for Alzheim er’s 4 1 patients are recommended. z < M anual or m echanical H I 1.5 toothbrushing and flossing, ideally after each m eal, will help prevent gingival and dental disease. Chlorhexidine sprays have proved efficacious as an adjunct to oral hygiene in 0.5 physically handicapped adults.45 P atien ts need help w ith th eir oral hygiene. W hen friends and relatives participated in POCKETS ATTACHMENT LOSS RECESSION p atients’ plaque control program s, plaque and gingivitis CONTROL SU BJECTS levels were reduced.46 F requent PATIENTS WITH ALZHEIM ER'S DISEASE toothbrushing and regular dental check-ups lowered root caries rate s.47 Fluoridated Periodontal parameters in 41 unmedicated patients with Alzheimer’s disease and 49 healthy controls. Results are expressed in millimeters dentifrices,48 fluoridated w ater (M ± SEM). supplies49 and topical fluoride
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pharmacological m anagem ent of th e Alzheimer’s 36. Haffajee AD, Socransky SS, Goodson JM. gels50 prevent root surface patient. Gerodontology 1987;6:59-66. Clinical p aram eters as predictors of destructive caries. 17. Walshe T. Approach to patien ts w ith degenerative disorders of th e nervous system . periodontal disease activity. J Clin Periodontol 1983;10:257-65. Prescribe fluorides for Gerodontics 1988;4:156-7. 37. Socransky SS, Haffajee AD, Goodson JM, 18. Yow WS, H aley KR, Griffin MA, F eller RP. Lindhe J. New concepts of destructive periodontal patients w ith salivary gland D ental m anagem ent of a p atien t w ith cognitive disease. J Clin Periodontol 1984;11:21-32. im pairm ent: A case report. G erodontics 1988;4:174-5. 38. Goodson JM , T anner ACR, Haffajee AD, dysfunction. The complaint of a 19. McKhann G, D rachm an D, Folstein J , Katzm an Sornberger GC, Socransky SS. P attern s of dry m outh (xerostomia) and R, Price D, S tadlan EM. Clinical diagnosis of progression an d regression of advanced periodontal A lzheimer’s disease: R eport of th e NINCDS-ADRDA disease. J Clin Periodontol 1982;9:472-81. salivary gland dysfunction can Work Group u n d er th e auspices of D epartm ent of 39. K itam ura M, Kiyak HA, M ulligan K. Predictors H ealth and H um an Services T ask Force on of root caries in th e elderly. Comm unity D ent Oral be m anaged w ith fluoride A lzheimer’s Disease. Neurology 1984;3:939-44. Epidemiol 1986;14:34-8. supplem ents plus sugarless 20. D uara R, G rady CL, Haxby JV, e t al. H um an brain glucose utilization an d cognitive function in 40. Sreebny LM, Valdini A. Xerostomia. P a rt I: Relationship to other oral symptoms an d salivary candies, chewing gums and relation to age. Ann Neurol 1984;16:702-17. gland hypofunction. O ral Surg Oral M ed Oral Pathol 21. D uara R, G rady CL, Haxby JV, e t al. Positron 1988;66:451-58. artificial salivas.51 Finally, emission tom ography in Alzheimer’s disease. 41. Baum BJ. Evaluation of stim ulated parotid Neurology 1986;36:879-87. saliva flow rate in different age groups. J D ent Res regular dental care not only 22. Koss E, Weiffenbach JM , Haxby JV, Friedland 1981;60:1292-6. assists in preventing oral RP. Olfactory detection and identification 42. Tylenda CA, Ship JA , Fox PC, Baum BJ. performance are dissociated in early Alzheimer’s E valuation of subm andibular salivary flow rate in disease, it also can find and disease. Neurology 1988;38:1228-32. different age groups. J D ent Res 1988;67:1225-8. 23. Schapiro MB, Haxby JV, G rady CL, Rapoport 43. M andel ID. The role of saliva in m aintaining tre a t problems before oral SI. Topographical comparison of lesions in Trisomy oral homeostasis. JADA 1989;119:298-304. function is 21 and Alzheimer’s disease: A study w ith PET, anatom ical and neuropathological investigations. In: 44. Goodnick P, Gershon S. Chem otherapy of cognitive disorders in geriatric subjects. J Clin Psych im paired. ■ Rapoport SR, P e tit H, Leys H, C hristen Y, eds. 1984;45:196-209. Imaging, cerebral topography and A lzheimer’s 45. Kalaga A, Addy M, H u n ter B. The use of 0.2% The author disease. Berlin: Springer Verlag; 1990;97-107. chlorhexidine spray as an adjunct to oral hygiene and acknowledges th e 24. Folstein MF, Folstein SE, McHugh PR. “M ini gingival h ealth in physically and m entally contributions of Dr. m ental state”: A practical m ethod for grading the handicapped adults. J Periodontol 1989;60:381-5. Bruce Baum , Clinical cognitive state of p atien ts for th e clinician. J 46. Lim CS, W aite IM, C raft M, Dickinson J, D irector and Chief, P sychiatrR es 1975;12:189-98. Croucher R. An investigation into th e response of CIPCB, NIDR, for 25. D uara R, M argolin RA, Robertson-Tchabo EA, subjects to a plaque control program m e as influenced research guidance; Drs. e t al. C erebral glucose utilization, as m easured with by friends and relatives. J Clin Periodontol 1984; Ja n e A tkinson a n d Ingrid positron emission tom ography in 21 resting healthy 11:432-42. Dr. Ship is Senior Valdez (S taff Fellows, men between th e ages of 21 an d 83 years. B rain 47. V ehkalahti MM, Paunio IK. Occurrence of root Investigator, NIDR, CIPCB, NIDR) for critical 1983;106:761-75. caries in relation to dental health behavior. J D ent NIH, 9000 Rockville review of th e m anuscript; 26. Fox PC, Van der Ven PF, Sonies BC, Res 1988;67:911-4. Pike, Building 10, Dr. M ark Schapiro Weiffenbach JM , B aum BJ. Xerostomia: evaluation of 48. Jen sen ME, Kohout F. The effect of a (Chief, BADS, LNS, NIA); a symptom w ith increasing significance. JADA fluoridated dentifrice on root and coronal caries in an Room 1N-113, th e LNS physicians and 1985;110:519-25. older ad u lt population. JADA 1988;117:829-32. Bethesda, Md th e NIH Clinical C enter 27. Ship JA , Fox PC, B aum BJ. How much saliva is 49. Stam m JW , B anting DW, Im rey PB. A dult root 20892. Address 6D nurses for patien t enough? Normal function defined. JADA caries survey of two sim ilar com m unities with requests for reprints care; and control subjects 1991;122(3):63-9. contrasting n atu ral w ater fluoride levels. JADA to Dr. Ship. and Alzheimer’s patients 28. U.S. D epartm ent of H ealth an d H um an 1990;120:143-9. for th e ir cooperation. Services. O ral h ealth of U nited S tates adults. NIH 50. Billings R J, Brown LR, K aster AG. publication no. 87-2868. N ational In stitu tes of C ontem porary tre atm en t strategies for root surface 1. H ealth, K atzmPublic an R.H ealth Service, 1987. dental caries. Gerodontics 1985;1:20-27. Alzheimer’s disease. N Engl J Med 1986;315:964-73. 29. Ramfjord SP. Indices for prevalence and 51. W right WE. M anagem ent of oral sequelae. J 2. K atzm an R, Saitoh T. Advances in Alzheim er’s incidence of periodontal disease. J Periodontol D ent Res 1987;66:699-702. disease. FASEB J 1991;5:278-86. 1959;30:51-9. 3. Evans DA, F unkenstein H, Albert MS, et al. 30. Ship JA, Wolff A. Gingival and periodontal Prevalence of A lzheim er’s disease in a com munity param eters in a population of healthy adults, 22-90 population of older persons. JAMA 1989;262:2551-6. years of age. Gerodontology 1988;7:55-60. 4. W hittle JG , G ran t AA, W orthington HV. The 31. Wolff A, Fox PC, Ship JA , A tkinson JA, dental health of th e elderly m entally ill: A M acynski AA, Baum BJ. O ral mucosal s ta tu s and prelim inary report. B r D ent J 1987;162:381-3. m ajor salivary gland function. O ral S urg O ral Med 5. Ship JA, D eCarli C, Friedland RP, B aum BJ. O ral Pathol 1990;70:49-54. D iminished subm andibular salivary flow in dem entia 32. Wolff A, Ship JA , Tylenda CA, Fox PC, Baum of th e Alzheimer type. J Gerontol 1990;45:M61-66. BJ. O ral mucosal appearance is unchanged in 6. Fabiszewski KJ. 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Spec Care D entist 1986;6:6-12. 12. Niessen LC, Jones JA. Oral health and the p atient w ith dem entia. Spec Care D entist 1987;7:36- 8. 13. N iessen LC, Jones JA. Professional dental care for patients w ith dem entia. Gerodontology 1987;6:67- 71. 14. Niessen LC, Jones JA , Zocchi M, G urian B. D ental care for th e patien t w ith Alzheimer’s disease. JADA 1985;110:207-9. 15. Shapiro S, Hamby CL, Shapiro DA. A lzheimer’s disease: An em erging affliction of th e aging population. JADA 1985;111:287-92. 16. Somerm an MJ. D ental im plications of