Relationship between oral health and its impact on the quality life of Alzheimer’s disease patients: a supportive care trial

Abstract

Dental infections have recently been related with a possible risk factor for Neurodegenerative pathologies like Alzheimer’s disease (AD). Even if there are no specific studies investigating orofacial pain in this patient group, dental health is known to be a potential cause of pain and to influence quality of life and disease progression. The aim of this study was to investigate how the AD patients’ oral health status may influence their quality of life. 158 patients affected by AD were evaluated using Decayed Missed Filled Teeth (DMFT), Oral Health Impact Profile-14 (OHIP-14) and Clinical Investigation consisting in the detection of cavities and measurement of the probing depth in each patient; other parameters like gingival bleeding, biofilm index and tooth mobility degree test have been recorded. The ratio between diagnosis of periodontal disease and impact on quality of life was significant in individuals with periodontitis (p < 0.001) and missed filled teeth. Gingival bleeding, and probing depth > 4 mm were associated with intensely negative impact on quality of life (p = 0.013, p < 0.001, and p = 0.012 respectively). Moreover, the absence of more than 2 molar teeth increases the chewing inability decreasing the patient quality of life. Conclusion: It was observed a correlation between the age and the high index of pathologies analyzed, due to the progressive nature of the disease. Concepts of health and disease determined by clinical diagnostic criteria may influence the assessment of the impact of periodontal disease on Alzheimer’s quality of life.

Introduction

The general health condition improvement observed in the second half of the last century, increased the average age of death in the developed countries [1] and, according to previsions, the elderly people rate in the next years will reach significant levels [2]. On the other hand, the incidence of tumors or degenerative diseases raised to worrying alarm levels. AD is an age-related neurodegenerative disorder caused by the loss of synapses, extracellular Beta-amyloid peptide and hyperphosphorylated tau protein [3]. As with many other diseases, a diagnosis of AD is made through a combination of clinical signs, physical, and neurologic evaluation, and laboratory exams. Clinical evaluation of persons for AD, performed with the aid of formal neuropsychological performance testing, has firstly to determine as accurately as possible if the person has dementia. Then clinicians should evaluate whether its presentation and course are consistent with a diagnosis of AD to assess evidence for any alternate diagnoses, especially if the presentation and course are atypical for AD. Finally it is fundamental to check the evidence of other, coexisting, diseases that may contribute to the dementia [1-3].

Dentist should focus on this topic for several reasons: domiciliary oral hygiene, in fact, is strongly compromised in patients affected by AD, because learning and attention processes are seriously injured [3]. Patients could also forget to brush their teeth because of the loss of memory, a classic sign of AD. Another sign that could prevent normal daily activities is gradual disorientation in space and time [3]. Many risk factors like familiar history, advanced age, Down’s syndrome, apolipoprotein E and female gender are involved in the etiology of AD [4,5]. However, the prevalence of AD is strictly connected with the age increasing: it reach almost 20% for subjects between 75 and 84 and almost 50% for patients older than 85 [6]. The disease is characterized by a progressive worsening of the signs and, in the severe stage, also by a decreased cognitive performances, mood instability and loss of independence of the patient. Even if there are a variety of medications that seem to slow the disease progression maintaining mental functions, there is no official cure for AD, and the absence of a way to prevent the nerve damage within the brain will increase the number of persons with AD in the next future [7]. Eventually the quality of life and the general health, especially for the elderly is reduced; they may have also difficulties in motor skills increasing risk for developing dental complications due to the incapacity to perform oral care. The relatives of the needing, even if represent the primary providers to these patients when the disease progresses from early to more advanced stages [8], could also have an inadequate ability to perform daily oral care in other persons [9], especially in demented, being not able to remove food debris, plaque biofilm or to recognize carious lesions or the first signs of periodontal disease like bleeding, deep probing or light mobility. Furthermore caring for someone with Alzheimer’s can be physically and mentally taxing, leading to a syndrome called “Caregivers Burnout”, characterized by signs like sadness, anger, back pain, headaches or difficulty sleeping, reducing the patient’s and the caregivers’ oral health condition too [10]. The average oral status observed in AD patients has lower standard if compared to people without the disease [11,12]. Poor dental hygiene and periodontal health, moreover, may be considered a consistent risk factor for progression of related diseases like diabetes mellitus, pulmonary disease, atherosclerosis, cardiovascular disease and stroke [13]. The low oral hygiene condition and the high plaque index may cause also the appearance of unpleasant smell [14], hindering eventually third person’s assistance and worsening the self-esteem status and the quality of life. Evaluation of the impact of oral health on quality of life could be an important aspect to investigate in disabled elderly patients [15,16] because clinical signs alone cannot describe their satisfaction or ability to perform daily activities. The oral health-related quality of life indicator (OHR-QoL) could represent an excellent aid. Oral Health Related Quality of Life underlines the interaction between the conditions of oral cavity health, general state of health and quality of life related to the subjects involved in the study [17]. The OHRQoL is a test including the analysis of physical health state and the subjective perceptions of the general health, satisfaction and self-esteem [18]. Among many instruments for measuring the perception of oral health state and the related quality of life, only a few have been recommended for possible use in the elderly.

One of the most used scale is the Oral Health Impact Profile in short form (OHIP-14) that developed by Slade based on Locker’s hierarchical paradigm of oral health (Table 1). It lies in a self-filled questionnaire composed by seven points that focuses on functional limitation, physical pain, psychological discomfort, handicap, physical, psychological and social disability with participants being asked to respond according to frequency of impact on a 5-point Likert scale coded never (score 0), hardly ever (score 1), occasionally (score 2), fairly often (score 3) and very often (score 4). Evaluating the incidence, the psycho-social costs of AD and the numerous cross points with the oral pathologies the general dentists should record an overview of the patient’s AD clinical features to increase the patients’ AD oral and general health. Our objective was to describe the relationship between caries, periodontal disease frequency and quality of life in AD patients evaluated at the IRCSS Neurolesi Bonino-Pulejo in Messina, Italy.

Table 1.

Sample of OHIP14 used in the study

QUESTIONNAIRE OHIP14
1. Have you had any trouble pronouncing any words?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
2. Have you felt that your sens of taste has worsened?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
3. Have you had painfulaching in your mouth?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
4. Have you found it uncomfortable to eat any foods?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
5. Have you been self-confused?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
6. Have you felt tense?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
7. Has your diet been unsatisfactory?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
8. Have you had to interrupt meals?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
9. Have you found it difficult to relax?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
10. Have you been a bit embarrassed?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
11. Have you been a bit irritable with other people?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
12. Have you had difficulty doing your usual jobs?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
13. Have you felt that life in general was less satisfying?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □
14. Have you been totally unable to function?
NEVER □	HARDLY EVER □	OCCASIONALLY □	FARILY OFTEN □	VERY OFTEN □

Material and methods

In the between September and December 2012 the oral condition about caries prevalence and periodontal health were recorded in 158 patients affected by AD with an age ranged between 65 to 87 years old, excluding the complete edentulous patients. AD Patients were consecutively recruited from IRCSS Neurolesi Bonino-Pulejo and sequentially lead to the Odontostomatology Department of Messina Policlinic, where they came for routine dental visit (Figure 1). All subjects and their proxies provided written informed consent and the Institutional Ethical Committee Board of IRCCS Centro Neurolesi “Bonino-Pulejo” Messina approved protocol. After collecting all the general demographic data, dental specialist visits and Orthopantomography X ray exam were performed in each patients. All the decayed, missing or filled teeth were recorded. A periodontal examination completed the clinical visit, checking parameters like probing depth, bleeding and mobility.

Figure 1.

Clinical investigation performed by periodontal probe on Alzheimer disease’s patient.

The OHIP-14 has been chosen for its wide range of coverage, good psychometric properties and ease of use in a clinical context and was conducted according to the principles of the Declaration of Helsinki. In addition, the OHIP-14 is intended to assess the impact of chronic oral problems on everyday life through items that analyse oral function limitations, pain and discomfort caused by oral problems and psychological and social factors related to oral health status. In this research authors considered ‘No answer’ and ‘Don’t know’ responses as missing values and later recorded with the mean value of all the valid responses to the equivalent subscale for each patient. The exclusion criteria are a total edentulism, to focus mainly on caries and periodontal disease, and the presence of a cognitive impairment that doesn’t allow proper completion of the questionnaire by patients.

Furthermore, an Italian version of Oral Health Impact Profile (OHIP-14) questionnaire was self-reported. The questions were related to the analysis of the perception of their own oral health within 3 months prior to the test. The total score was calculated through the “additive method”, summing the results of each item (range 0-56). The distribution of responses for the seven categories was evaluated with mean, standard deviation, variance, median and mode of all domains. Statistical reliability was evaluated with Cronbach’s alpha coefficient (significance α > 0.70), in order to analyse the homogeneity of polytomous independent values, i.e. items with more than 2 possible answers.

Results and discussion

The patient group was formed by 57 males (36%) and 101 females (64%), aged from 65 to 87 years old (mean and standard deviation of age: 74.37 ± 5.38). Considering a total dentition composed by 28 teeth, the DMFT index was 23.56 ± 2.78, with 6.89 ± 3.02 being Decayed, 14.04 ± 4.39 Missing and 2.62 ± 1.79 Filling teeth. The Plaque Index (PI) registered was of 70.86 ± 13.76%. The percentage of remaining teeth was of 50% while the periodontal disease, confirmed by a probing depth deep 4 mm or more, affected around 87.2% of them (on average 12.21 ± 3.77 teeth). Gingival bleeding was observed in 9.15 periodontal compromised teeth with a percentage value of 75% and a severe stage of mobility (grade 3) in 37.34% periodontal teeth. Comparing the ages we observed also that the patients with more missing teeth were older than the ones with a more complete, but unhealthy, dentition, correlating the incidence of oral diseases with the progressing of AD. The internal consistency of the overall OHIP-14 was expressed by Cronbach’s coefficient α = 0.853, which put in evidence a high statistical significance. Internal consistency scores for the total OHIP and the seven domains are registered in Table 2. All standard deviations calculated within the 7 domains are included between 0.98 and 1.15 (Table 3). These values are indicators of an acceptable agreement with the expectations of the probabilistic model. There is no item with ‘underfit’ or ‘overfit’. Items related to psychological discomfort and disability achieved the highest score with average values of 2.94 and 2.56 respectively (Table 3); the item number 11 about tense and irritable status against others registered the lower value (mean 1.84 ± 0.95).

Table 2.

Internal consistency scores of OHIP-14 domains

	Cronbach’s α score
OHIP-14	0.853 (n = 158)
OHIP-14 domains:
Functional limitation	0.473 (n = 158)
Physical pain	0.686 (n = 158)
Psychological discomfort	0.443 (n = 158)
Physical disability	0.662 (n = 158)
Psychological disability	0.574 (n = 158)
Social disability	0.660 (n = 158)
Handicap	0.604 (n = 158)

Table 3.

Descriptive statistics: OHIP-14 and its seven domains

Domains	Mean	St. Dev.	Variance	Median	Mode
Total OHIP scores	2.5	1.07	3.64	3	3
Functional limitation	2.41	1.15	1.31	2	2
Physical pain	2.38	0.98	0.96	2	2
Psychological discomfort	2.94*	1.04	1.09	3	4
Physical disability	2.49	0.98	0.95	3	2
Psychological disability	2.56	1.07	1.14	3	2
Social disability	2.29	1.1	1.2	2	2
Handicap	2.4	1.02	1.04	2	2

^*Higher mean value registered.

In the total OHIP-14 the lowest scores that have been recorded are closely related to a younger age and a better periodontal health condition of AD patients. The majority of AD patients (65.2%) had accumulated an elevated total score in the range of 29-42 points; also the highest scores in the range of 43-56 points were achieved by the 16.45% of patients (Table 4). Furthermore, the authors highlight that the response that has been given more frequently is the score 4 (41%) which corresponds to “very often”. It is followed by the score 3 “fairly often” (32%) and the score 2 “occasionally” (19%). Scores 0 “never” and 1 “Hardly ever” are reported only in the 1% and 7% of the cases respectively (Figure 2).

Table 4.

Frequency (%) of range scores (included extremes) among AD patients

Range	Total scores	Number of patients	Percentage (%)
1	0-14 pt	3	1.9%
2	15-28 pt	26	16.45%
3	29-42 pt	103	65.2%
4	43-56 pt	26	16.45%

Figure 2.

Percentage of OHIP-14 answer scores of all AD patients.

Many studies have shown that individuals with AD have more dental decay, worse oral hygiene and fewer teeth [19-21]. The present study evaluated subjects with all the stages of AD using OHIP-14, a precise, valid and reliable instrument for assessing oral health-related quality of life among adult population in all over the world [22,23]. Largely used in Anglophone countries, is being translated in many languages to facilitate the approach with an increasing number of people [24,25]. This Italian version gave good results if compared with similar studies. The low rate of filled teeth and the high percentage of plaque index suggested that the oral hygiene of the sample analyzed was inadequate since before the onset of the AD. The older age (associated with a worse status of AD) and the female gender were strongly related with a greater OHIP value according to Sampogna et al. [26]. Periodontal disease and a fewer number of teeth resulted the two most important factors able to influence negatively the OHIP score. Gingival bleeding and a probing depth > 4 mm were strictly connected with the lowest QoL levels. The mobility grade > 3 were indicated as the main cause of discomfort, associated with the Question n. 5 of the OHIP-14. The choice of food consistency was correlated to dental status [27] while the alimentation status (Questions n. 7-8) was strongly compromised in patients showing less than 5 teeth, according to Suzuki et al [28], suggesting to investigate different options to recover the chewing ability. Concerning the high plaque index detected, we can conclude that the decrease of cognitive functions caused a deterioration of oral hygiene procedures: tooth brushing was irregular in this sample of AD patients, consisting with Hatipoglu et al [29]. The OHIP-14 results not only demonstrated that the patients had an unsatisfactory perception of their oral condition, but also a strong link between the worsening of oral health and AD progression in agreement with previous studies [30,31]. Analyzing the literature, our results were in agreement with other studies, except for DMFT score that resulted lower due to the exclusion of totally edentulous patients. Our study aimed to investigate OHRQoL in relation with periodontal disease and caries in a sample formed exclusively by AD patients without the presence of a control group, and this could be considered a limitation of this research. However, it is important to underline that this paper aimed also to provide an important report about the oral health of AD patients in the south of Italy, were similar data were not collected yet.

The results of the present study showed a correlation between the age and the high index of pathologies analyzed, due to the progressive nature of the disease. The OHIP-14 results showed a significant relation between Alzheimer’s disease and Oral Health Related Quality of life in an elderly population of the south of Italy.

Disclosure of conflict of interest

None.