Oral hygiene and oral health in older people with dementia: a comprehensive review with focus on oral soft tissues

Background The number of older people with dementia and a natural dentition is growing. Recently, a systematic review concerning the oral health of older people with dementia with the focus on diseases of oral hard tissues was published. Objective To provide a comprehensive literature overview following a systematic approach of the level of oral hygiene and oral health status in older people with dementia with focus on oral soft tissues. Methods A literature search was conducted in the databases PubMed, CINAHL, and the Cochrane Library. The following search terms were used: dementia and oral health or stomatognathic disease. A critical appraisal of the included studies was performed with the Newcastle-Ottawa scale (NOS) and Delphi list. Results The searches yielded 549 unique articles, of which 36 were included for critical appraisal and data extraction. The included studies suggest that older people with dementia had high scores for gingival bleeding, periodontitis, plaque, and assistance for oral care. In addition, candidiasis, stomatitis, and reduced salivary flow were frequently present in older people with dementia. Conclusions The studies included in the current systematic review suggest that older people with dementia have high levels of plaque and many oral health problems related to oral soft tissues, such as gingival bleeding, periodontal pockets, stomatitis, mucosal lesions, and reduced salivary flow. Scientific rationale for study With the aging of the population, a higher prevalence of dementia and an increase in oral health problems can be expected. It is of interest to have an overview of the prevalence of oral problems in people with dementia. Principal findings Older people with dementia have multiple oral health problems related to oral soft tissues, such as gingival bleeding, periodontal pockets, mucosal lesions, and reduced salivary flow. Practical implications The oral health and hygiene of older people with dementia is not sufficient and could be improved with oral care education of formal and informal caregivers and regular professional dental care to people with dementia. Electronic supplementary material The online version of this article (10.1007/s00784-017-2264-2) contains supplementary material, which is available to authorized users.


Introduction
Aging of the world population has occurred at an unprecedented rate in the twentieth century and is forecasted to increase further [1]. Given the increase of general health problems with aging [2], Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00784-017-2264-2) contains supplementary material, which is available to authorized users. and the presence of many interactions between general health and oral health [3,4], an increase of oral health problems is to be expected.
Common oral health problems in older people are caries, periodontitis, reduced salivary flow, candida, and mucosal lesions [5,6]. In developed countries, caries has a high prevalence in older adults with a mean number of decayed and filled coronal surfaces ranging from 22 to 35 and a mean number of decayed and filled root surfaces ranging from 2.2 to 5.3 [6][7][8]. In developing countries, these data are scarce [6]. Furthermore, periodontal disease is frequently present in older adults [9]. Specifically, mild periodontitis, with periodontal pockets of 4-5 mm, is present in 62-97% of the older persons [9]. More severe periodontitis, with pockets of 6 mm or more, is present in 20-48% of the older persons [9]. In addition, the prevalence of oral dryness increases with age, affecting approximately 30% of the older adults [10,11]. Salivary flowrate decrease can result in difficulties with swallowing, eating, and communication [11]. Moreover, reduced salivary flow can cause halitosis, a higher prevalence of inflammation of the mucosa and parotid, candidiasis, dental caries in dentate persons, and frictional lesions in denture wearers [11]. The majority of oral diseases, including oral cancer, occur in older adults [12]. Among oral mucosal lesions, denture-related lesions, such as stomatitis, angular cheilitis, ulcers, and hyperplasia, are most common [13]. The above-mentioned oral health problems do not only affect oral health and functioning but may also cause orofacial pain or discomfort, and can have a negative impact on the quality of life [14,15].
Compared to older people who are cognitively intact, older people who develop dementia are at increased risk of establishing oral health problems, as a result of decline in self-care and motor skills [16,17]. Conversely, tooth loss and periodontitis may be risk factors for cognitive decline, although the exact presence and causality of the association between oral health problems and the development of dementia remains unclear [18,19].
Several studies described oral disease as a risk factor for the development of dementia, but did not provide separate oral health data for the group of participants with dementia [20][21][22][23][24][25][26][27]. It is important to have an up-to-date overview of the oral health of older people with already present dementia, because the number of older people with natural dentition and possible risk factors for dementia is still increasing. Therefore, the aim of this study was to provide an up-to-date overview of studies about oral health in people with dementia. A previous review focused on dental hard tissues [28] and this review will aim at the oral soft tissues and oral hygiene of older people with dementia.

Material and methods
For this review, the PRISMA statement [29] was followed and a protocol for the review process was developed in advance.
The main question for the review was what is the prevalence of oral health problems in older people with dementia? The subquestion was how is the oral health of older people with dementia, compared with older people without dementia? The search terms were oral health, stomatognathic disease, and dementia. No separate oral health terms were used for the main search. The multidisciplinary team consisted of a professor in dentistry (FL), a professor in neuropsychology (ES), a professor in geriatric medicine and ethics (CH), a professor in palliative care and specialist in methodology (RP), a dentist with experience in gerodontology (SD), and a neuropsychologist with experience with older people with dementia (TB).

Criteria
Studies that were included were (randomized) controlled trials and observational studies with and without control groups (cohort, case-control, cross-sectional). Studies that were not included were reviews and case reports. The inclusion criteria for this study were diagnosis of dementia, age 60 years or older, useable quantitative data concerning oral health in a group of participants with dementia, and stomatognathic disease.

Search
The search strategy was developed in collaboration with the university library of the VU Medical Centre in Amsterdam. The search was performed in PubMed, CINAHL, and the Cochrane Library. The last updated search was performed on 12 January 2017. In PubMed, the following search query was used: (

Study selection
The titles, abstracts, and full texts in Dutch, English, and German were screened independently by two reviewers (SD and TB) according to the pre-established protocol and the inclusion and exclusion criteria mentioned above. Disagreements between reviewers were resolved by consensus. Articles in languages other than Dutch, English, or German were assessed by a native speaker with a background in dentistry, after instruction by the authors. If the diagnosis dementia or data related to oral health were unclear, the corresponding authors were contacted, up to a maximum of three times over a period of 4 months. If this did not lead to usable data, the article was excluded.

Critical appraisal
The risk of bias within studies was critically appraised by two reviewers (SD and TB). For cross-sectional, case-control, and cohort studies, the Newcastle-Ottawa scale (NOS) was used [30] and for (randomized) controlled trials the Delphi list [31]. The diagnosis of dementia was considered adequate if the following criteria for dementia diagnosis were used: the Diagnostic and Statistical Manual of Mental Disorders (DSM-III and IV) [32], International Classification of Disease (ICD-9 and 10) [33], and the Alzheimer's criteria by the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer's disease and Related Disorders Association (NINCDS-ADRDA) [34,35].
For studies with cases (with dementia) and controls (without dementia), the groups were considered comparable if the group means for age and gender were not statistically different at the .05 level.
The oral health examination was considered adequate if a structured dental examination by a dentist took place. The person who performed the oral health examination was considered 'blinded' if (s)he did not know the cognitive status of the participants in advance. The follow-up of cohort studies was considered long enough if it was longer than 3 months and considered adequate if not more than 20% of the participants was lost to follow-up.

Data extraction
The data extraction was performed by one reviewer (SD) and was checked by two other reviewers (TB and FL). The following data was extracted: (1) participant characteristics, including age and dementia diagnosis, (2) study design, e.g., cross-sectional, case-control, cohort study, or (randomized) controlled trial, and (3) baseline outcome measures, including periodontal health and treatment need, oral hygiene, assistance need with oral care, oral mucosal status, and salivary flow. The principal outcome measures were means and percentages. The methodological and clinical heterogeneity of the data was checked.

Search results
The search yielded a total of 561 articles and after adjusting for duplicates, 548 studies remained. Of these, 445 studies were excluded based on title and abstract. The full texts of 103 studies were assessed in more detail, and 67 were subsequently excluded. Supplementary list 1 provides an overview of articles that were excluded after full text screening, including the reasons of exclusion. After screening the reference lists of the remaining 35 articles, 1 study was added. The flowchart of the search is presented in Fig. 1. A total of 36 studies met the inclusion criteria and were processed for critical appraisal and data extraction. During the review process, 14 authors were contacted for further i n f o r m a t i o n , a n d 11 o f t h e m r e s p o n d e d ( s e e Acknowledgements).

Study characteristics
An overview of the 36 included studies is presented in Table 1; 14 were cross-sectional studies, 10 were case-control studies, 10 were cohort studies, and 2 were (randomized) controlled trials. Most of the studies were in English; the article of Sumi et al. was in Japanese [65]. All papers, except for the Japanese study, were assessed by the authors SD and TB. The Japanese study was assessed by a native Japanese speaker with dental knowledge (EY, see Acknowledgements).

Critical appraisal
The results of the critical appraisal with the Newcastle-Ottawa scale are presented in Supplementary Table 1a-c. The total scores of the 34 articles appraised with the NOS ranged from 1 to 9, the mean score was 4.8 (SD 1.9), and the median was 5.0. Thirteen studies scored below and 12 studies scored above the median score. Hereafter, the separate NOS categories will be discussed. The DSM or ICD was used for the classification of the dementia diagnosis in half of the studies. The cases, i.e., older people with dementia, demonstrated good representativeness of the group of older persons with dementia in 24 (= 70.6%) of the 34 studies. The controls, i.e., older people without dementia, came from other sources than the cases in 12 (= 35.3%) of the 34 studies. For respectively 16 (= 47.1%) and 14 (= 41.2%) of the studies, age and gender were comparable between the groups with and without dementia. A standardized structured dental examination by a dentist was done in 29 (= 85.3%) of the studies. The non-response rate was described in only 2 (= 8.3%) of the 24 non-cohort studies. The follow-up period was longer than 3 months in 9 out of 10 (= 90.0%) cohort studies. The number of subjects lost to followup was described in 4 of 10 (= 40.0%) of the cohort studies.
The results of the critical appraisal of the two (randomized) controlled trials with the Delphi list are presented in Supplementary Table 2.

Individual outcome variables
Gingival and periodontal disease Table 2 and 3 show gingival and periodontal disease in older people with dementia in percentages and means. Gingival bleeding was absent in 0.0 to 9.4% of the participants with dementia [41,64]. Consequently, most of the participants had gingival bleeding or inflammation [40,42,60]. More specifically, gingivitis was present in 13.6 to 38.9% [45,46,55], moderate periodontitis in 6.9 to 36.0%, and severe periodontitis in 11.9 to 24.5% of the participants with dementia [41,46,55,75]. The mean percentage of the Gingival Bleeding Index was 46.0% in a study by De Souza Rolim [46] and 43.8-53.8% in the publications by Zenthöfer [68,70,76].
When examining studies that compared gingival and periodontal disease of participants with and without dementia, seven studies showed no significant differences [44,53,59,60,66,70,75] and six studies showed significantly more (severe) periodontal disease in older people with dementia [42,46,50,67,68,70]. De Souza Rolim et al. reported significantly more periodontal infection in participants with dementia (58.6%) than in participants without dementia (26.7%) [46]. Zenthöfer et al. found significantly more periodontitis in participants with dementia (100.0%) than in participants without dementia (73.9%) [68]. Furthermore, the community periodontal index of treatment needs was significantly higher in participants with dementia (3.1-3.4) than without dementia (2.7-2.8) [68,70]. When specifically looking at nursing home residents, a significantly higher percentage of participants with dementia had a high amount of calculus, plaque, or gingival bleeding (40.4%), when compared to people without dementia (26.2%). A study by Warren et al. found that the Gingival Index was significantly higher in people with Alzheimer's disease (1.1) than in people without dementia (0.7), while people with dementia other than Alzheimer's disease scored not significantly different (0.9) from people with Alzheimer's disease and people without dementia [67].
Oral hygiene and assistance need    [48]. Furthermore, a significantly higher O'Leary Plaque Index was found in participants with dementia (90.1%), compared to participants without dementia (73.3%) [68]. In addition, a significantly higher Oral Hygiene Index by Greene and Vermillion was found in participants with dementia (4.5) than in participants without dementia (2.2) [61]. A recent study found significantly more plaque with the Plaque Index of Silness and Loe in cases (2.5) than controls (1.6) [50].
Warren examined the Debris Index for dementia subtypes and severities and found no significant differences between dementia subtypes and controls, but found a significantly higher Debris Index in people with moderate to severe dementia, compared to people without dementia [67].
Studies about assistance need for oral care (Supplementary Table 3) reported a need of 21% and higher for both cleaning teeth and dentures in participants with dementia [38,41,42,60,64,72,75]. Chalmers et al. reported a significantly higher need for assistance with oral hygiene care with an increasing severity of cognitive impairment [72]. In this study, the assistance need was 57.2% for cleaning teeth and 97.3% for cleaning dentures in people with moderate dementia, and 100.0% for cleaning teeth as well as dentures in people with severe dementia [72]. In all except 1 of 7 the comparing studies the assistance need for oral care or cleaning teeth and dentures was significantly higher in people with dementia than in those without [41,42,60,72,75]. Table 4) was present in 3.6 to 30.0% of the cases, i.e., older people with dementia, and 0.0 to 5.0% of the controls, i.e., older people without dementia [44,46,47,58]. The study by De Souza Rolim et al. (2014) found significantly more candidiasis in cases than in controls. Stomatitis was present in 18.1 to 59.1% of the cases and 0.0 to 7.4% of the controls [38,52,56]. The only study that compared stomatitis in cases and controls found significantly more stomatitis in cases than in controls [52]. found significantly more xerostomia in people with dementia subtypes other than Alzheimer's disease (22.0%) than in people without dementia (8.4%) in their clinician assessment of xerostomia. In addition, xerostomia was found in 9.1% of the people with Alzheimer's disease in this study [67]. A recent study found significantly more drug-induced xerostomia in cases (68.5-72.2%) than in controls (36.5%) [51].

Candidiasis (Supplementary
In addition, various studies indicated that people without dementia have significantly more unstimulated salivary flow (Supplementary Table 5) than people with dementia [39,44,58]. One study indicated that people without dementia have more stimulated submandibular flow than Alzheimer's disease [39]. The study of Leal et al. (2010) showed the buffering capacity is higher in people without dementia and without medication than in people with dementia and medication [58].

Discussion
The main aim of this study was to provide a comprehensive overview with critical appraisal of studies concerning the health of oral soft tissues and oral hygiene in older people with dementia. The additional aim was to compare oral health of older people with and without dementia. The studies included in this review suggest that older people with dementia have much plaque and many oral health problems related to oral soft tissues, such as gingival bleeding, periodontal pockets, stomatitis, mucosal lesions, and reduced salivary flow.
While oral health in people with dementia is poor [42,66,68], the subtype of dementia, e.g., Alzheimer's disease, vascular dementia, does not seem to be an essential determinant of oral health [38,66,67]. However, the severity of cognitive decline does seem to play a role in the oral health of older people with dementia, with more plaque and oral disease in people with more cognitive decline [36,38,66,67,72]. An exception to this finding is the study of Srisilapanan et al. [64], which was explained by the fact that people visiting the memory clinic in this study also got dental treatment with every visit. The people included in this study had better access to oral care compared to the general population. In addition, living environment, e.g., nursing home, community, might play a role in the oral health of older people with dementia [61,72]. Some studies found no significant differences between living environments, but a poor oral health in people with dementia, regardless of residency [38,41]. Some studies found more problems in nursing home residents compared to community Clinical attachment level (in mm) 2.9 mm (1. living elderly [61,72]. This can be explained by a higher degree of cognitive and functional impairment in the nursing home population [41]. The deterioration of cognitive functions, such as executive functioning, working memory, attention, and apraxia, complicates the ability to perform oral care in people with dementia [42], which results in more plaque [60,68]. Furthermore, functional changes in dementia, like declined hand grip strength and motor skills, can complicate oral care [52,61]. Dental plaque is the primary cause of gingivitis and subsequently periodontitis [77]. Therefore, with a high amount of plaque in older people with dementia in the evaluated articles, a high amount of gingivitis and periodontitis could be expected. Periodontitis has been associated with multiple systemic health conditions (mainly diabetes mellitus type 2 and cardiovascular disease) [4]. Therefore, treatment of periodontitis is important to reduce systemic health risks.
Recently, the association between oral health and cognitive decline was systematically reviewed. The authors concluded that the association was still unclear [18,19].
Within the included papers, salivary function appeared to be intact in the healthy aging sample. However, objective (hyposalivation) or subjective (xerostomia) dry mouth is more likely to be present in older people with medication use, history of radiotherapy in the head and neck region, and autoimmune disease, such as Sjögren syndrome [5,11,78]. In addition, people with Alzheimer's disease have significantly lower stimulated submandibular and unstimulated salivary flow rate [39,44,58]. This might be explained by neuropathological changes characteristic for Alzheimer's disease, leading to changes in the autonomic nervous system [39,44].

Critical appraisal
The NOS comprises five categories concerning a control group, which means studies without control group consequently receive a lower score. Six of the 14 included studies with cross-sectional design did not have a control group and therefore had a NOS score below the median score of 5. Consequently, for the studies without a control group, it was not possible to compare older people with and without dementia. Furthermore, most of the included studies did not describe the non-response rate and consequently lacked a point on the NOS for this category. An issue worth mentioning, is that for the data-extraction of this review only baseline data was used, while the NOS also includes two items concerning follow-up studies for cohort studies. These two follow-up items in the 10 included cohort studies are not relevant for this review, but might be of interest for further appraisal of the studies.

Strengths and limitations
The main strengths of this review are the critical appraisal of the articles, the summary tables of the dementia and oral health variables, and the involvement of a multidisciplinary team. Concerning the critical appraisal, most studies demonstrated good representativeness of older people with dementia, and almost all included studies followed a standardized structured dental examination by a dentist. The involvement of the multidisciplinary team critically evaluated the dental, neuropsychological, medical, ethical, and methodological aspects of this study.
Limitations of this review are the following: the included studies used a broad range of outcome measures, most studies had a cross-sectional design, and the number of studies with a NOS score below 5 was considerable. However, if these studies would have been excluded, the tendency of the results for the group of older people with dementia would have remained the same. It was therefore decided to keep the studies with a NOS score below 5 in the overview of the results. In addition, the methodological and clinical heterogeneity between the studies was considered too large to perform a meta-analysis. Furthermore, many of the included studies did not use a formal dementia diagnosis or diagnostic instruments, but screening instruments for cognition. In these studies, it might be more appropriate to address to the participants as people with cognitive impairment instead of people with dementia. In addition, the non-response rate was rarely described, which complicates the assessment of potential selection-bias.

Implications and clinical suggestions
In order to improve the oral health of older people with dementia, oral health assessment tools, oral hygiene care  strategies, and guidelines should be used [79][80][81][82][83]. To maintain good oral health, daily removal of dental plaque by brushing the teeth is essential [84]. Therefore, oral hygiene care for dependent people should be in the daily activities of care [81,85] and oral health care education might improve the knowledge and attitude of caretakers [86]. Although providing oral care and dental treatment can be complicated by challenging behavior, strategies that approach it as threat perception might help the well-being of people with dementia [87]. Regular assessment of the oral health should take place by caretakers, as well as dentists [81]. An oral health assessment tool can be used to identify risk factors and should consist of intra-oral examination, observation of behavior, and (if possible) an evaluation of the client perception of treatment need [82,88]. For oral care, treatment planning, and behavioral management for people with dementia, the level of cognitive impairment and cooperation of the patient, as well as the input from the multi-disciplinary team of health care professionals, and formal and informal caretakers should be taken into account [17,89].

Future research
For future research, it is suggested to use a formal diagnosis for dementia [90]. If neuropsychological testing is no longer possible, a short cognitive screening instrument, such as the Mini-Mental State Examination (MMSE), can be used to get an impression of the level of cognitive functioning [91]. However, a low score on the MMSE is only an indication of cognitive impairment and does not replace the diagnostic examination required for a dementia diagnosis [92]. For the oral health assessment in older people with dementia, an international, standardized method can be useful. Although the manual WHO Oral Health Survey Basic Methods provides no information on assessing the oral health status of older people with dementia [93], guidelines for oral health care for institutionalized older people do exist [81,82,94].

Conclusion
The studies included in the current systematic review suggest that older people with dementia have high levels of plaque and many oral health problems related to oral soft tissues, such as gingival bleeding, periodontal pockets, stomatitis, mucosal lesions, and reduced salivary flow.
The oral hygiene and oral health of older people with dementia should be improved. This could be achieved by oral care education of formal and informal caregivers, the use of oral health screening tools, and regular professional dental care for people with dementia.