Oral Health Status and Need for Oral Care in an Aging Population: A Systematic Review

Background. The world population is aging. This phenomenon is accompanied by an increase in the number of elderly with dementia, whose oral hygiene care is a challenge. Objective. This paper presents a literature review of oral health status and the need for oral care in people with dementia, as compared to people without dementia and also of the relationship between periodontal disease and cognitive impairment. Methods. A systematic review was conducted in PubMed, CINAHL, and the Cochrane Library. Fifty-six articles met the inclusion criteria and were consequently included for quality assessment and data extraction. Results. No significant differences were found between both groups with regard to the number of present teeth, DMFT Index, edentulousness/use of denture, and orofacial pain. Coronal/root caries and retained roots were more common in people with dementia than in those without dementia. Most of the participants with dementia presented gingival bleeding or inflammation and they suffered from the periodontal disease more than people without dementia. Conclusions. Poor oral health is a common condition among the elderly with dementia. The education process of caregivers might improve the oral health status of people with dementia. Finally, periodontal disease might contribute to the onset or progression of dementia.


Introduction
The transition from high to low mortality and fertility that accompanied the socioeconomic development of this century has meant a shift in the leading causes of disease and death and an increase of general health problems [1].
As a consequence, a decline of the oral health conditions of the elderly, such as dental caries and periodontal disease, is to be expected [2]. Poor oral health is more common in the elderly suffering from dementia, a disorder that will become prevalent with advancing age of the world population. Several studies analyzed the relationship between poor oral health and cognitive impairment, which suggests that cognitive decline might negatively impact oral health and also that poor oral health might lead to cognitive decline via specific biological mechanisms [3]. Conversely, in a recent systematic

Rationale of the Systematic Review
The most important risk factor that is associated with the onset of dementia is age and in an aging society, the impact of the phenomenon will be of alarming dimensions. Dementia reduces the quality of life of patients also with regard to oral health. It has been demonstrated that oral health of the elderly with dementia is poorer than oral health in people with normal cognitive function [13,14]. However, it is currently unclear how or whether oral health and cognitive status are related [15,16]. This study is aimed at reviewing literature, in order to evaluate oral health status in elderly with dementia, while comparing the data with those of elderly without dementia and to establish and assess the need of specific oral care strategies, which could improve their quality of life. This research was also conducted to review the available data regarding the influence of periodontal disease on the progression of cognitive impairment.

Objectives
The purpose of this systematic review was to examine studies about oral health in elderly with and without dementia, focusing the research on coronal and roots caries, number of remained teeth and retained roots, Decayed Missing Filled Index, periodontal disease, utilization of dentures, salivary flow, oral hygiene, oral mucosal lesions, orofacial pain, and on the analysis of periodontal disease as a potential risk factor for dementia.
This study reviewed cohort, case-control, cross-sectional studies, and randomized controlled clinical trials in order to examine oral health comparing the elderly with and without dementia. Inclusion criteria of participants were a diagnosis of dementia and the availability of data related to their oral health.

Clinical Question (PICO):
• P: A population of participants with diagnosis of dementia aged 60 years or older • I: Analysis of the oral health status and of the association between periodontal disease and dementia • C: Comparison between oral health of elderly with and without dementia • O: Prevalence of oral disease (affecting hard and soft tissues) in elderly with dementia compared to those without dementia, to define their need of oral care. Role of tooth loss due to periodontal disease in the onset/progression of dementia.

Protocol and Registration
Methods and inclusion criteria were selected following the PRISMA statement [17], which offers a protocol with respect to the reference items that were included in this systematic review.

Inclusion and Exclusion Criteria
In this systematic review, all of the articles concerning oral health in the elderly with dementia meeting the following requirements were included: • Participants must have been diagnosed with dementia • Quantitative data about oral health problems • Participants had to be available • Participants had to be 60 years or older • Cohort, case-control, cross-sectional studies, and clinical trial were considered The exclusion criteria were as follows: • Case report and reviews • No quantitative data available • Age of participants below 60 years

Search
An electronic research was conducted to identify relevant studies that have been published within 2019, but no restrictions were imposed with regard to language of the primary studies or methodology. The following electronic databases were used: PubMed, CINAHL, and Cochrane Library. The keywords used were the same for all three databases and they were combined with the Boolean term "AND": "oral health", "aging population", "oral disease", "association with periodontal disease" and "OR": "oral care need", and "oral care strategies". The research was completed on May 2019.

Study Selection
Two researchers (G.M., D.L.) independently analyzed the title, abstract, and full text of each English article to identify those that were eligible for the systematic review, according to the inclusion and exclusion criteria established above. Disagreements between reviewers were resolved by consensus. Articles that were published in other languages were assessed by a native speaker specialized in medical language. Articles in which the diagnosis of dementia was not defined or quantitative data were not available were excluded.

Data Collection Process
Two reviewers (G.M., D.L.) extracted the data, who also checked their methodological and clinical heterogeneity (D.L.). The information extracted from each article were as follows: study design (cohort, case-control, cross-sectional studies, or randomized clinical trial), participants characteristics, such as age and diagnosis of dementia, and quantitative data on participants (outcome measures), including the number of teeth present, number of retained roots, DMFT Index (Decayed Missing Filled Teeth Index), edentulousness and dentures, coronal and root caries, periodontal health, and its association with the onset or progression of dementia, oral mucosal disease, salivary flow, orofacial pain, oral hygiene, and need for dental treatment. Means and percentages were used for the principal outcome measures.

Quality assessment
Newcastle-Ottawa scale (NOS) [18] was used to assess the quality of the studies (Tables 1-4). The highest score was 9 and the lowest one was 1 (average score was 5.5 or cohort studies, 6.1 for case-control studies, 4.6 for cross-sectional studies, and 5.5 for RCT). Most articles used the standardized method to examine oral health and the examination was considered to be adequate if a dentist performed it. With regard to "Comparability", 30 of all the studies controlled for age or gender or both and in the case-control, cross-sectional studies, and RCT only 5 (1.98% of the non-cohort studies) described the non-response rate [14,19,20]. In almost all studies, the duration of follow-up period was longer than three months. The evaluated quality parameters are shown in Additional file 1-4.

Study Selection and Characteristics
A total of 922 studies that were published between 1990 and 2019 were identified from database searches. Among these articles, after examining titles and abstracts and the full texts of the remaining, only 56 met the inclusion criteria and were consequently included for quality assessment and data extraction. One study was added after scanning the reference list of the included articles [39]. All of the studies were analyzed with regard to quality while using the Newcastle-Ottawa Scale (NOS). Figure 1 shows the flow chart of publication assessment. the studies were analyzed with regard to quality while using the Newcastle-Ottawa Scale (NOS). Figure 1 shows the flow chart of publication assessment. The detailed characteristics about the 56 included studies are presented in Table 5, and Table 6, with reference to author and year of publication, study design, case and controls, mean age of participants, dementia measure, and measure of oral health. This review included 19 cohort studies, 9 case-control-studies, 26 cross-sectional studies, and two randomized clinical trials. Almost all of the articles were in English, except for Sumi et al. article, which was written in Japanese [33]. A native Japanese speaker, who extracted the data included in the review, examined this article.
The studies that were selected for the review included in total 8466 participants with dementia and 6797 participants without dementia. In particular, selected studies regarding the association between periodontal disease and dementia included 4698 participants with periodontal disease or history of teeth extraction, 3132 elderly without periodontal disease, 60 subjects with dementia, and 2885 without dementia. In the included studies, the diagnosis of dementia was performed while using DSM-III and IV [70], ICD-9 and 10 (International Classification of Disease [71]), NINCDS-ADRDA (National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer's disease and Related Disorders Association [72]), Minimental State examination [73] (MMSE), and other additional measures (e.g., computed tomography, magnetic resonance imaging, CDR [74]). The detailed characteristics about the 56 included studies are presented in Table 5, and Table 6, with reference to author and year of publication, study design, case and controls, mean age of participants, dementia measure, and measure of oral health. This review included 19 cohort studies, 9 case-control-studies, 26 cross-sectional studies, and two randomized clinical trials. Almost all of the articles were in English, except for Sumi et al. article, which was written in Japanese [33]. A native Japanese speaker, who extracted the data included in the review, examined this article.
The studies that were selected for the review included in total 8466 participants with dementia and 6797 participants without dementia. In particular, selected studies regarding the association between periodontal disease and dementia included 4698 participants with periodontal disease or history of teeth extraction, 3132 elderly without periodontal disease, 60 subjects with dementia, and 2885 without dementia. In the included studies, the diagnosis of dementia was performed while using DSM-III and IV [70], ICD-9 and 10 (International Classification of Disease [71]), NINCDS-ADRDA (National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer's disease and Related Disorders Association [72]), Minimental State examination [73] (MMSE), and other additional measures (e.g., computed tomography, magnetic resonance imaging, CDR [74]). Table 5. List of studies about coronal/root caries, number of remained teeth/retained roots, DMFT, periodontal disease, utilization of dentures, salivary flow, oral hygiene, and oral mucosal lesions in elderly with and without dementia.

Results of Individual Studies
The number of present teeth was one of the most used measures for assessing oral health. In particular, from the included studies it came to light that the range within the two groups varied between 2.0 to 20. 2 for people without dementia and between 1.7 to 20.5 for people with dementia. According to Delwel et al. [53], the number of present teeth was lower in the participants with dementia (median = 2.0, IQR = 0.0-18.0) than in people with MCI (median = 18.0, IQR = 5.5-24.0). However, this study underlined that, if only dentate participants were considered, no significant differences were recorded between the two groups (median = 18.0, IQR = 9.0-24-0) ( Table 7). The review showed that coronal and root caries were more common in people with dementia that in people without dementia: coronal caries varied between 0.1-2.9 [43,54,55] and 0.0-1-0, respectively [21,54], and root caries varied between 0.6-4.9 [43,54,55] in participants with dementia and 0.3-1.7 [13,54,55] in normal cognitive participants. For retained roots, the range was between 0.0-1.2 [54] in people without dementia and between 0.2-10 [21,54] in people with dementia. Moreover, Delwel et al. [53] demonstrated that dentate participants with dementia had more coronal caries (median = 1.0, IQR = 0.0-2.0), root caries, and retained roots (median = 0.0, IQR = 0.0-1.0) than dentate people with MCI (Table 8. With regards to the DMFT Index (Table 9), the lowest one was 14.9 in the study by Srilapanan et al. In general, the DMFT index did not show a significant difference within the two groups (19.7-26.1 in healthy people and 14.9-28.0 in people with dementia), except for one study, which demonstrated that the DMFT Index was 25.5 in people without dementia and 28.0 in people with dementia.
Most of the participants with dementia presented gingival bleeding or inflammation [23,48] (Table 10). According to De Souza [24], the Gingival Bleeding Index was 46.0% in the elderly with dementia and periodontal infections were most common in the latter (58.6%) than in normal cognitive participants (26.7%). 73.8% of the Delwel et al. [53] study included patients had periodontal pockets of ≥4 mm, 18.8% of them had one or more teeth with mobility grade 2, and 5.8% had one or more teeth with mobility grade 3.       Zenthöfer [36,37,44] demonstrated that the Gingival Bleeding Index of people with dementia was 43.8 to 53.8% and confirmed De Souza's results, proving that people with dementia suffer from periodontitis more than people without dementia (community periodontal index of treatment needs was 3.1-3.4 in dementia people and 2.7-2.8 in non dementia people [36,37]).
Nine of the included studies found no significant differences between both groups with regards to oral hygiene [21,22,27,45,61,62,[64][65][66][67] and five studies demonstrated a higher level of plaque in dementia people [14,36,43,56,65]. The Plaque Index by Silness and Loe was 0.7 in the study by Chalmers et al. [13], 2.5 in the study by Gil-Montoya [14] in the elderly with dementia, and 2.0 in the study by Delwel et al. [53]. Sumi et al. [33] showed a Plaque Index by Quigley and Hein of 1.6. O'Leary Plaque Index was significantly higher in dementia people (90.1%) than in non dementia people [36] (73.3%). Finally, Ribeiro [65] et al. established that the Oral Hygiene Index by Green and Vermillion is higher in participants with dementia (4.5) than in participants without dementia (2.2). A significantly higher Debris Index in people with moderate to severe dementia was found [43].
Furthermore, edentuloussnes was a condition that affected a large percentage of the elderly, in particular 11.6 to 72.7% of the elderly with dementia [66,67] and 14.0 to 70% of the elderly without dementia [38,45]. Within partially or totally edentulous participants, denture utilization varied between these percentages: 17.0-81.8% in normal cognitive people and 5.0 to 100% in people with cognitive impairment [27,31] (Table 11). Data about orofacial pain were extracted from seven of the included studies [13,24,39,40,45,52]. The percentage of the elderly with dementia suffering from orofacial pain was higher than that of participants without dementia: 7.4 to 21.7%, 6.7 to 18.5%, respectively. The cross-sectional study by Delwel et al. [53] carefully examined the presence of orofacial pain in the elderly with dementia or MCI, while using the OPS-NVI [12] and self reported pain. The OPS-NVI was 4% in rest, 10% during drinking, 19% during chewing, and 22% during oral hygiene care. Pain reported by participants with dementia or MCI was 25.7% overall (Table 12). The feeling of a dry mouth or xerostomia reached the percentages of 22.0% in people with dementia and 8.4% in people without dementia [33] and it was present in 9.1-45% of the cases and 8.4-20.0% of the controls [40][41][42][43]. Gil-Montoya [58] showed a more drug-induced xerostomia in cases (68.5-72.2%) than in the controls (36.5%).
In conclusion, with regards to the oral care need, the included studies [13,47,49,50,61,64,67] reported a need of 21% for cleaning teeth and dentures in the elderly with dementia. Chalmers et al. [47] demonstrated that, with an increasing severity of cognitive impairment, there is also an increase of oral care need: the assistance need for cleaning teeth and dentures in severe dementia was 100.0%, as compared to the assistance need in moderate dementia, which was 57.2% (teeth) and 97.3% (dentures). Regarding periodontal disease (Table 13), Dintica et al. [25] and Ide et al. [31] found that the mean change (decrease) in MMSE score due to tooth loss was, respectively, −0.94 to 0.37 (nine months follow-up, adjusted for age, sex, and education) and −3.6 to −0.03 (six months follow-up), establishing a significant association between tooth loss and the progression of cognitive impairment. The crude hazard ratio of dementia according to the number of remaining/lost teeth was 1.6 [10,34]. Tiisanoja et al. [68] demonstrated that subjects with pocket depth ≥4 mm had an increased, but not statistically significant, risk of developing Alzheimer's Disease (Relative risk: 1.54). Furthermore, Yoo et al. [35] demonstrated that periodontal treatment lead to a significant decrease in the incidence of dementia. The prospective community-based study by Kato et al. [30] showed that the number of natural teeth was significantly associated with an individual's MMSE score: the percentage of cognitively normal subjects (MMSE scores: 27-30) significantly decreased with a decrease in the number of natural teeth (number of teeth = 5-9, percentage of participants without cognitive impairment = 26.7%; number of teeth = 15-19; and, percentage of normal cognitive participants = 44.8%). Kato et al. also demonstrated that the use of artificial teeth was associated with cognitive function preservation.

Discussion
The purpose of this systematic review was to examine studies regarding oral health in the elderly with and without dementia and to investigate the relationship between periodontal status and dementia. As reported in a recent review by Delwel et al. [75], the analysis of this study showed no significant differences between the case and controls with regards to the number of present teeth [13,21,29,43,53,56,61,67,69] and to the DMFT Index [27,38,61,65]. However, the DMFT categories separately, "decay", "missing", and "filled", give a better indication of disease and treatment need compared to the index, which reports dental caries history as a whole. Coronal and root caries and retained roots are most common in people with dementia [21,56,65], and this condition might be explained by cognitive and behavioral deterioration, which reduced the ability to perform routine oral care [76]. In the elderly with dementia saliva flow rates decreases [32], eating habits change (more cariogenic food) [51,56,61,77], and motor skills and coordination worsen [65], which leads to a lower chewing and swallowing efficiency [56,77].
Another important point to be considered is the oppositional and aggressive behavior towards oral care and decreased communication skills, which represent barriers to oral hygiene and assistance. These obstacles could be overcome by performing oral care education to caregivers and by increasing dental checks of the elderly with dementia [62,78,79].
Moreover, the recent observational study by Delwel et al. [53] recorded a significant correlation between the cognitive impairment level and the number of present/missing/restored teeth and retained roots, which suggests that dementia could have a negative impact on oral health.
Concerning oral soft tissues, this study confirmed Delwel's et al. review results [80]: gingival bleeding, periodontal disease, mucosal lesions, and xerostomia were found at higher rates in participants with cognitive impairment. Dry mouth was more common in the elderly, who used medication or had radiotherapy history (head and neck) or autoimmune disease [32].
Approximately the same percentage of the elderly either with or without dementia wore dentures [13,42]. However, people with an advanced dementia degree showed a lower use of dentures, as compared to people with moderate dementia, because of the musculature, salivary flow decrease, and lower tolerance of dentures.
The deterioration of verbal communication skills and the higher prevalence of oral disease might cause a higher suffering to people with dementia, due to orofacial pain [45,50,52,53]. In this systematic review, the new information included concern the potential role of periodontal disease as a risk factor for developing cognitive impairment. In fact, all of the studies included in Table 10 demonstrated an association between teeth loss due to periodontal disease and the onset of dementia [10,25,30,31,34,35,60]. This association is based on biological mechanisms: subjects with periodontal disease or antibodies to periodontal bacterial flora show an increased systemic proinflammatory state, which lead to an increase of the cognitive decline rate [31]. According to Yoo et al., the more teeth are lost, the higher incidence of dementia is. The author also stated that monitoring cognitive status in patients with extensive teeth loss could lead to an early diagnosis of dementia. The significant association between the number of natural teeth and the MMSE score was also confirmed in the study by Kato et al., which suggest that the use of artificial teeth could help to preserve the cognitive function.

Strengths and Limitations
The most important limitation of this study is the result of the quality assessment of the articles, since more than half of the included studies have a score equal or below 5. The number of high quality studies was low and no homogeneity can be found. For this reason, it was impossible to perform a meta-analysis. In the included studies, several different measures were used to evaluate oral health status and some studies did not distinguish between the elderly with and without dementia.
The main strength of this review is the systematic approach and involvement of a multidisciplinary team (dentists, neuropsychologist, pain specialist). In addition, in almost all of the studies reviewed, oral examinations are structured and standardized, and were carried out by dentists.

Conclusions
The elderly with dementia show a higher level of plaque, coronal and root caries, retained roots, gingival, and periodontal disease. Further attention is needed regarding orofacial pain, which is very common in dementia people. Poor oral health within this group could be increased by the reduction of submandibular salivary flow, deterioration of cognitive functions, motor and communication skills, and aggressive behavior. Caregivers should be educated and dentist's checks in nursing homes should be enhanced in order to improve the oral health status of the elderly with dementia. Our contribution highlights the relationship between periodontal disease and dementia. Teeth loss due to periodontal disease increases the risk of cognitive function deterioration. However, the specific mechanisms of this association need further investigation.