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    Review

    Effect of oral health education programs for caregivers on oralhygiene of the elderly: A systemic review and meta-analysis

    Tze-Fang Wang a ,*, Chiu-Mieh Huang a , Chyuan Chou b , Shu Yu aa School of Nursing, National Yang Ming University, Taipei, Taiwanb Bloomberg School of Public Health, Johns Hopkins University, D.D.S., Dr.PH., USA

    What is already known about the topic?

    Poor oral health in the elderly is associated withmalnutrition, cognitive decline, and a higher risk forcardiovascular disease and infectious respiratory dis-eases.

    Various oral health education programs have beenpresented to nursing personnel with anticipation thatthe elderly may benet from caregivers’ improvedexpertise in personal hygiene procedures.

    Regarding the improvement of oral health of the elderly,many studies reported conicting conclusions of theseoral health education programs on caregivers.

    What this paper adds

    This meta-analysis analysis, involving 602 elders, foundthat the percentage of elderly with normal oral mucosa,with no visible plaque, and with no detectable denture

    International Journal of Nursing Studies 52 (2015) 1090–1096

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    Article history:Received 22 July 2014Received in revised form 26 January 2015Accepted 28 January 2015

    Keywords:Meta-analysisOral hygieneDental health educationCaregiversElderlyDental hygiene

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    Objectives: To evaluate the effects of oral health education for caregivers on the oral healthstatus of the elderly.Design: A systematic review and meta-analysis.Data sources: The Medline, EMBASE, Cochrane Library (CENTRAL), PsycINFO, CINAHLweresearched up to September, 2014.Review methods: Randomized controlled trials or comparative before-and-after studiesinvolving an oral health education program for caregivers of the elderly ( 65 years old)were identied by two independent reviewers. Primary outcome was the percentage of patients with normal mucosa in the oral cavity. The secondary outcomes were thepercentage of patients with no visible plaque and the percentage of patients withoutdenture stomatitis.Results: A total of vestudies, involving602 elders, metthe eligible criteria forinclusion in

    the meta-analysis. It was found that the percentage of residents with normal oral mucosa(odds ratio (OR) = 1.81, P = 0.027), no visible plaque (OR = 1.54, P = 0 .001), and nodetectable denture stomatitis (OR = 2.89, P < 0.001) signicantly increased after the groupwas treated by caregivers who had received a recent oral health education program.Conclusions: The systemic review and meta-analysis found limited evidence that oralhealth education for caregivers may be effective for improving the oral health of theelderly.

    2015 Elsevier Ltd. All rights reserved.

    Abbreviations: CI, condence interval; OR, odds ratio; RCT, random-ized clinical trial.

    * Corresponding author. School of Nursing, National Yang MingUniversity, No. 155, Section 2, Li-Nong Street, Shi-Pai, Taipei 112, Taiwan.Tel.: +886 2 28267000x7907; fax: +886 2 28202487.

    E-mail address: [email protected] (T.-F. Wang).

    Contents lists available at ScienceDirect

    International Journal of Nursing Studies

    journal homepage: www.elsevier.com/ijns

    http://dx.doi.org/10.1016/j.ijnurstu.2015.01.0150020-7489/ 2015 Elsevier Ltd. All rights reserved.

    http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015mailto:[email protected]:[email protected]://www.sciencedirect.com/science/journal/00207489http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://www.sciencedirect.com/science/journal/00207489mailto:[email protected]://dx.doi.org/10.1016/j.ijnurstu.2015.01.015http://crossmark.crossref.org/dialog/?doi=10.1016/j.ijnurstu.2015.01.015&domain=pdfhttp://crossmark.crossref.org/dialog/?doi=10.1016/j.ijnurstu.2015.01.015&domain=pdf

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    stomatitis all signicantly increased after the group wastreated by caregivers who had received a recent oralhealth education program.

    An oral health education for caregivers may signicantlyimprove the oral health of the elderly.

    1. Introduction

    The prevalence of elderly who lacked dental careranged from approximately 17% in France (Herr et al.,2013 ) to > 63% in institutionalized elderly in Spain(Cornejo et al., 2013 ), 82% in nursing home residents inCanada (Chen et al., 2013 ), and > 90% in homeboundelderly in the USA (Gluzman et al., 2013 ). Poor oral healthin the elderly is associated with malnutrition, cognitivedecline, and a higher risk for cardiovascular disease andinfectious respiratory diseases, including pneumonia(Adachi et al., 2007; Awano et al., 2008; Juthani-Mehtaet al., 2013 ).In fact, oral bacteria were the major pathogensin 15% of cases of community acquired pneumonia(Yamasaki et al., 2013 ). The ability of elders to maintainadequate oral health may be reduced by cognitive decline,reduced hand function (Padilha et al., 2007 ), sarcopenia(Walls, 2014 ), and loss of autonomy. Since poor oral healthmay exert a negative impact on the general health of theelderly and increase the cost of their care, effectivemethods that improve the oral health of elders iswarranted.

    A promising approach is the education of the caregiversfor the elderly. Various oral health education programshave been presented to nursing personnel with anticipa-tion that patients may benet from caregivers’ improvedexpertise in personal hygiene procedures. Many studiesevaluated the effectiveness of the educational program onthe improvement of knowledge, attitude, and perception of caregivers (Khanagar et al., 2014; Paulsson et al., 1998;Reed et al., 2006 ). These programs produced conictingconclusions regarding oral health, level of knowledge,benets over time (Brand et al., 2013; Sjogren et al., 2010 ),and attitudes toward dental issues of elderly (Isakssonet al., 2000; Kullberg et al., 2009; Reed et al., 2006; Simonset al., 2000 ). Therefore, we conducted a meta-analysis toevaluate the effects of oral health education of thecaregivers on the oral health status of the residents.

    2. Materials and methods

    2.1. Search strategy

    The systematic review and meta-analysis was con-ducted in accordance with Preferred Reporting Items forSystematic Reviews and Meta-Analyses (PRISMA) guide-lines (Liberati et al., 2009 ). The Medline, EMBASE, CochraneLibrary (CENTRAL), PsycINFO, CINAHL were searched forthe keywords, ‘‘(frail OR aging OR aged OR dementia OR elderly OR older OR elder OR institutionalization) AND(dental OR oral) AND health AND (education OR Promo-tion) AND (nurses OR caregivers OR nurse OR caregiver)’’for articles published up to September, 2014. The selectioncriteria were for research articles on one or more oral

    health

    education

    program(s)

    for

    caregivers

    of

    the

    elderly( 65 years old). The elderly were living in the community,

    assisted living facilities, nursing homes, or other institu-tions. Additional inclusion criteria for the full meta-analysis were (a) a primary research article, (b) effectsof oral educational program for caregivers on the oralhealth of the elderly, and (c) randomized controlled trialsor comparative before-and-after studies that evaluated theelders’ oral health after the caregivers’ completion of

    educational

    program.

    Exclusion

    criteria

    were

    (a)

    caregiversof younger groups (< 65 yrs) or (b) educational interven-tions for only the patients. Non-English articles wereexcluded.

    2.2. Data extraction

    Two independent reviewers identied studies by thesearch strategy. If the eligibility of a study was notunanimous, a third reviewer was consulted. The reviewersnoted the reference (rst author, year published, journalcitation) and compiled the following data from the includedstudies: study design, participants’ demographics (age and

    gender),

    number

    of

    participants

    before-and-after

    healtheducation program, protocol of education program, durationof follow up period, and primary and secondary outcomes.

    2.3. Assessment of quality of study

    The two reviewers assessed the quality of the publica-tion by using Newcastle-Ottawa Scale (Wells et al., 2006 )to score across three categories: selection of study groups(four questions), comparability of study groups (twoquestions), and ascertainment of the outcome of interest(three questions). While most questions had a score of 1,separate points were awarded for controlling for age and

    sex

    (maximum,

    2

    points).

    2.4. Outcome measures

    The different studies had used different scales tomeasure abnormalities in mucosa, plaque, and denturestomatitis. Because each scale included one common grade– the identication of normal mucosa (Table 1), theprimary outcome was the percentage of patients withnormal mucosa in the oral cavity. Normal mucosa wasdened as no inammation, no erythema, no swelling, no

    Table 1

    Comparison

    of

    the

    scales

    for

    evaluating

    normal

    mucosa..

    Study Scale for evaluating oralmucosa

    Referencefor scale

    Portellaet al. (2013)

    1: normal appearance2: mild inammation3: moderate inammation4: severe inammation

    Henriksenet al. (1999)

    Boczkoet al. (2009)

    1: normal2–4: abnormalities inincreasing severity

    Nicolet al. (2005)

    Absent or present of mucosal disease

    Isakssonet al. (2000)

    1: normal appearance2: mild inammation3: moderate inammation4: severe inammation

    Henriksenet al. (1999)

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    atrophy, no ulceration or lesions on oral mucosa andgingival (Henriksen et al., 1999 ). The secondary outcomeswere the percentage of patients with no visible plaque andthe percentage of patients without denture stomatitissince the scales in all articles had used these categories.

    2.5. Statistical analysis

    The effect of the health education on the caregivers wasevaluated by assessing the improvement in the elders’dental hygiene: the percentages of patients with normalmucosa, no visible dental plaque rate, and lack of denturestomatitis before-and-after health education program. Ax

    2 -based test of homogeneity was performed and theinconsistency index (I 2 ) and Q statistics were determined.If an I 2 of < 25% indicated that the studies werehomogeneous, the xed-effects models (Mantel-Haenszelmethod) were utilized. If an I 2 of > 50% or > 75% indicatedthat the trials were heterogeneous or highly heteroge-neous, respectively, a random-effects model (DerSimo-

    nian–Laird

    method)

    was

    utilized.

    Otherwise,

    pooledsummary statistics (odds ratio (OR) and corresponding95% condence interval (C.I.)) were shown for theindividual studies. Pooled OR (95% CI.) were calculatedand a 2-sided P value < 0.05 was considered to indicatestatistical signicance.

    The primary outcome was considered for the sensitivityanalysis which utilized the leave-one-out approach.However, the publication bias was not performed due tothe small number of selected studies (Sutton et al., 2000 ).All statistical analyses were performed using the statisticalsoftware Comprehensive Meta-Analysis, version 2.0 (Bio-stat, Englewood, NJ, USA).

    3. Results

    3.1. Literature search

    A total of 570 articles remained after removingduplicates. Screening of titles and abstracts resulted inremoval of 553 articles that were irrelevant to this meta-analysis.

    Full text review of the 17 articles indicated that vestudies met the inclusion criteria (Fig. 1) (Boczko et al.,2009; Frenkel et al., 2001; Isaksson et al., 2000; Nicol et al.,2005; Portella et al., 2013 ). Four of the twelve excluded

    studies

    did

    not

    provide

    quantitative

    data

    of

    the

    outcome

    of interest (Kullberg et al., 2010; MacEntee et al., 2007;Simons et al., 2000; Sjogren et al., 2010 ). Four studies(Frenkel et al., 2002; Gammack and Pulisetty, 2009;Khanagar et al., 2014; Reed et al., 2006 ) did not evaluatethe oral health of the elderly. Two articles described the

    Fig. 1. Flow chart for study selection.

    T.-F. Wang et al. / International Journal of Nursing Studies 52 (2015) 1090–1096 1092

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    effects of an educational program on oral health providedto the elderly, not to the caregivers (Little et al., 1997;Persson et al., 1998 ) and two articles were review articles(Watt and Marinho 2005 ; Stein and Henry, 2009 ). The veincluded studies reported the effect of the caregivers’ oralhealth education on the oral health status of 602 combinedelderly residents (Boczko et al., 2009; Frenkel et al., 2001;

    Isaksson

    et

    al.,

    2000;

    Nicol

    et

    al.,

    2005;

    Portella

    et

    al.,

    2013 ).

    3.2. Study characteristics and quality assessment

    The characteristics and quality assessment of the veincluded studies are summarized in Table 2. The educa-tional programs given to caregivers covered oral health,oral hygiene, dental diseases, common risk factors, and oralhygiene instruction. Four of the ve educational programsincluded demonstrations of proper oral care and aninteractive instructional period (Boczko et al., 2009;Frenkel et al., 2001; Nicol et al., 2005; Portella et al.,2013 ) using models and manikins. The program in the

    Broczko

    et

    al.

    study

    also

    included

    discussions

    on

    over-looked patients and residents with behavior problems(Boczko et al., 2009 ). The program in the Nicol study (Nicolet al., 2005 ) also included discussion time between thecaregivers and residents to discuss common oral condi-tions and oral health challenges of the residents. Theteachers of the programs ranged from a professor anddental students (Portella et al., 2013 ), two speech languagepathologists (Boczko et al., 2009 ), dentist and/or dentalhygienists (Isaksson et al., 2000; Nicol et al., 2005 ), or ahealth promoter trained in dental and oral care (Frenkel

    et al., 2001 ). The length of the educational program rangedfrom 1 h (Boczko et al., 2009 ) to 4 h (Isaksson et al., 2000 ).According to Newcastle-Ottawa Scale, four studies (Boczkoet al., 2009; Isaksson et al., 2000; Nicol et al., 2005; Portellaet al., 2013 ) provided pre and post oral health evaluationsof the patients by the educated caregivers and wereconsidered moderate quality. The Frenkel et al. study

    (Frenkel

    et

    al.,

    2001 )

    used

    a

    randomized

    clinical

    trial

    (RCT)design and had a higher quality assessment.

    3.3. Study outcomes

    Fig. 2A shows the forest plot of the primary outcome –percentage of normal mucosa of the residents evaluatedbefore-and-after the caregivers had received healtheducation program – by using pooled summary odds ratio(OR) statistics with 95% CI. The Frenkel et al. (2001) studydid not provide numerical information on oral mucosa.Finally, four studies (Boczko et al., 2009; Isaksson et al.,2000; Nicol et al., 2005; Portella et al., 2013 ) involving 401

    residents

    were

    included

    in

    the

    meta-analysis.

    The

    hetero-geneity test (Q = 20.92, I 2 = 85.7%, P < 0.001) indicated theuse of the random effect model. The pooled summarystatistics were observed as OR = 1.81 (95% CI. = [1.07,3.05]). Thus, the percentage of residents’ normal mucosasignicantly increased by 81% after the caregivers im-proved delivery of oral care due to the health educationprogram (P = 0.027).

    Sensitivity analysis implied that the direction andmagnitude of pooled estimates might be affected by that(Boczko et al. 2009 ) study (Fig. 2B). Thus, we excluded it

    Table 2Patients’ demographics, characteristics and quality assessment of the ve studies.

    Study name (year) Type of study

    Number of patients Age (yrs) Female (%) Education program Follow-up (months) Qualityassessment *

    Baseline Follow up

    Portella et al.(2013)

    Pre-post 80 55 80, 59.2% 71.7 Dental professor and studentsgave 2 h lecture on oral and bodyhygiene, video w/instructionsand Q & A.

    12 5

    Boczko et al.(2009)

    Pre-post 112 104 NA NA Two speech languagepathologists gave a 1 hr PPpresentation on oral hygiene,good oral care, risk factors,difcult patients, and demo onoral care.

    NA 5

    Nicol et al.(2005)

    Pre-post 39 31 84 (35–99) a 82.1 Dentist and dental hygienistgave 90 min training programDVD, and demos on oral health,oral hygiene and care withdemos.

    18 5

    Frenkel et al.(2001)

    RCT 201 155 84.9 (8.2) b 81.1 Health promoter gave 1 hrsession on oral health, hygiene,and staff had practice session onmanikins

    6 NA

    Isaksson et al.(2000)

    Pre-post 170 158 84.6 (51–99) c 70 Specially trained dentalhygienists gave single, four-hoursession on healthy oral cavity

    3–4 5

    NA, not available; RCT: randomized controlled trial.a Data are displayed as median (range).b Data are displayed as mean (standard deviation).c

    Data are displayed as mean (range)* Assessed independently by 2 of the authors using the Newcastle-Ottawa Scale.

    T.-F. Wang et al. / International Journal of Nursing Studies 52 (2015) 1090–1096 1093

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    (Boczko et al., 2009 ) from the meta-analysis. The result

    indicated

    that

    the

    percentage

    of

    the

    residents’

    normalmucosa after caregivers’ health education program signi-cantly increased by 2.29 times compared to the baselinenormal mucosa measurements obtained prior to care-givers’ educational program (P < 0.001).

    Fig. 3 shows the forest plot of secondary outcomes –percentage of elderly with no visible plaque and withoutdenture stomatitis – by using pooled summary statistics of OR with 95% CI. before-and-after the caregivers’ health

    education. Only two studies, Isaksson et al. (2000) and

    Portella

    et

    al.

    (2013) , had

    complete

    information

    on

    dentalplaque of a combined 250 residents before-and-after thecaregivers’ health education. A xed effect model was usedaccording to the heterogeneity test (Q = 0.86, I 2 = 0%,P = 0.352). The OR = 1.54 (95% CI. = [1.19, 2.00]) indicatedthat the percentage of no visible plaque in the residentswas signicantly higher after the caregiver received oralhealth education than that before the caregivers’ education(P = 0.001) (Fig. 3A).

    Fig. 2. The results of primary outcome, the rate of normal mucosa before-and-after health education program. (A) Forest plot, (B) Sensitivity analysis for theinuence of each individual study on pooled estimate by the means of leave-one-out, (C) The result of forest plot in which Boczko et al. (2009) was excluded.

    Fig.

    3.

    Forest

    plot

    of

    secondary

    outcomes.

    (A)

    Percentage

    of

    patients

    with

    no

    visible

    plaque,

    the

    percentage

    of

    elderly

    residents

    with

    no

    visible

    plaque

    and

    (B)the percentage of patients without denture stomatitis, the rate of patients without denture stomatitis.

    T.-F. Wang et al. / International Journal of Nursing Studies 52 (2015) 1090–1096 1094

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    Two studies (Frenkel et al., 2001; Nicol et al., 2005 )presented the denture stomatitis before-and-after thecaregivers’ health education program of a combined 240residents. A random effect model was used according tothe heterogeneity test (Q = 3.73, I 2 = 73.2%, P = 0.053). Fig. 3B indicated a signicant increase in the percentage of elderly without denture stomatitis after the caregivers had

    received

    the

    health

    education

    program

    (OR

    =

    2.89,

    95%

    CI.[1.64, 5.10], P < 0.001).

    4. Discussion

    We had hypothesized that providing oral healtheducation to the nursing personnel would increase theirknowledge and improve their attitudes toward oral healthcare of the elders in their units and improve not onlydelivery of oral health care but ultimately improve the oralhealth of the 602 residents. Taken together, these studies(Boczko et al., 2009; Frenkel et al., 2001; Isaksson et al.,2000; Nicol et al., 2005; Portella et al., 2013 ) showed that

    the

    percentage

    of

    residents

    with

    normal

    oral

    mucosa,

    novisible plaque, and no detectable denture stomatitissignicantly increased after the group was treated bycaregivers who had received a recent oral health educationprogram.

    Instruction on oral health care, its associations withinfectious disease, and other degenerative diseases canimprove the attitude of the caregivers toward theimportance of oral health of the elderly residents (Kullberget al., 2009 ). Repeated oral health education programs forthe caregivers improved the oral health of the elderlyresidents at least in some facilities (Kullberg et al., 2010 ), inagreement with the results of this meta-analysis. Further-

    more,

    improved

    oral

    health

    of

    elderly

    residents

    helpedreduce the incidence of pneumonia (Kullberg et al., 2010 ).However, several studies that investigated the effect of anoral health education program for the caretakers did notobserve a signicant improvement in the oral health statusof the elderly residents (Gammack and Pulisetty, 2009;MacEntee et al., 2007; Simons et al., 2000 ) whereas otherstudies did observe an improvement (Boczko et al., 2009;Frenkel et al., 2001; Isaksson et al., 2000; Kullberg et al.,2009; Nicol et al., 2005; Portella et al., 2013 ). Sjogren et al.(2010) indicated that a single oral health education of thecaregivers yearly was insufcient to improve the oralhealth status of the residents after 1.5 yrs. Possible reasons

    for

    the

    lack

    of

    a

    signicant

    impact

    of

    the

    caregivers’training on the oral health status of the elderly residentsmay include relatively good oral health status of residentsat baseline (MacEntee et al., 2007 ), less sensitive measure-ment scales for the oral health assessments (Gammack andPulisetty, 2009 ), too small a sample size to detect a 20%difference (MacEntee et al., 2007 ), short presentationwithout adequate training or theory of improved oralhealth care (Gammack and Pulisetty, 2009 ), insufcienttime due to competing personal care duties (Gammack andPulisetty, 2009; Reed et al., 2006; Simons et al., 2000 ),inadequate stafng intensity at facility (Gammack andPulisetty, 2009; Reed et al., 2006; Simons et al., 2000 ),

    insufcient

    supplies

    for

    oral

    health

    care

    (Coleman,

    2005 ),the Hawthorne effect on the facilities and staff (MacEntee

    et al., 2007 ), and a relatively high turnover of staff at thefacility between the pre and post training assessments(Simons et al., 2000 ). Multiple oral health educationsessions augmented the oral health knowledge andpractical oral hygiene procedures of the caregivers (Reedet al., 2006 ), but some facilities hesitated to provide theextra time for staff training due to workload (Simons et al.,

    2000 ).The limitations of this meta-analysis included that moststudies were not randomized clinical trials but insteadprovided pre and post assessments of the oral health of theelderly residents who had received care from caregiverstrained in an oral health program. Although these studieswere deemed to be of only moderate quality, theadvantage of the pre and post measurements is thepotential to reduce the inter-patient variability. A secondlimitation was that the different studies used differentscales to measure abnormalities in the muscosa whichmade comparison of studies difcult, similar to Watt andMarinho (2005) . However, all studies listed the percentage

    of

    patients

    with

    normal

    mucosa

    which

    facilitated

    compar-ison between studies. Similarly, all studies used thepercentage of patients with no plaque and the percentageof patients without denture stomatitis. A third limitationwas that publication bias could not be adequately assesseddue to the small number of studies. While ve studiesinvolving 602 elderly residents may be considered arelatively small sample size for meta-analysis, the resultssuggest that an oral health education program forcaregivers can improve the oral hygiene of the elderly.

    In conclusion, this systematic review and meta-analysisfound limited evidence that oral health education forcaregivers may be effective for improving the oral health of

    the

    elderly.

    Conict of interest

    None declared.

    Funding

    No external funding.

    Acknowledgments

    We thank MedcomAsia and K. Molnar-Kimber, Ph.D. foreditorial assistance, which was funded by the authors.

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