’Original article Oral health in patients with liver cirrhosis Lea L. Grønkjær and Hendrik Vilstrup Objective The aim of this study was to describe the oral care habits and self-perceived oral health in patients with liver cirrhosis, as well as to evaluate the impact of oral health on well-being and the relation to nutritional status. Participants and methods From October 2012 to May 2013, we carried out a prospective study on patients with liver cirrhosis. Questions on oral care habits and self-perceived oral health were answered, and the Oral Health Impact Profile questionnaire (OHIP-14) provided information on oral conditions. The findings were compared with The Danish Institute for Health Services Research report on the Danish population’s dental status. Results One hundred and seven patients participated. Their oral care habits and self-perceived oral health were poorer than the Danish population; the patients had fewer teeth (on average 19 vs. 26, P = 0.0001), attended the dentist less frequently (P = 0.001), more rarely brushed teeth (P = 0.001) and had problems with oral dryness (68 vs. 14%, P = 0.0001). The patients’ mean OHIP score was 5.21 ± 7.2, with the most commonly reported problems being related to taste and food intake. An association was observed between the OHIP score and the patients’ nutritional risk score (P = 0.01). Conclusion Our results showed that cirrhosis patients cared less for oral health than the background population. Their resulting problems may be contributing factors to their nutritional risk and decreased well-being. Oral health problems may thus have adverse prognostic importance. Our results emphasize the need for measures to protect and improve the oral health of cirrhosis patients. Eur J Gastroenterol Hepatol 27:834–839 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
Participants and methods
Patients with liver cirrhosis have a high incidence of periodontal disease such as gingival inflammation, periodontitis and candidiasis [1,2]. This is not a trivial problem because it predisposes to systemic infections and malnutrition, leading to more frequent and prolonged hospitalizations and increased morbidity and mortality [3]. Periodontal disease may be because of oral neglect and poor oral health [4,5], yet, so far, no study has examined oral care habits and self-perceived oral health of cirrhosis patients. Oral problems in themselves may contribute toward decreased quality of life because of mouth pain and reduced social interactions [6,7]. Furthermore, the oral health status of cirrhosis patients may also be important for their very frequent dysnutrition that is associated with reduced survival and quality of life [8]. The aim of the present study, therefore, was to describe oral care habits and self-perceived oral health in a representative cohort of patients with liver cirrhosis as well as to evaluate the impacts of their oral health on general wellbeing and nutritional risk.
Study design and population
European Journal of Gastroenterology & Hepatology 2015, 27:834–839 Keywords: liver cirrhosis, nutritional risk, oral health impact profile, oral health status Department of Hepatology and Gastroenterology, Aarhus University Hospital, Aarhus C, Denmark Correspondence to Lea L. Grønkjær, RN, MSN, Department of Hepatology and Gastroenterology, Aarhus University Hospital, 44 Noerrebrogade, 8000 Aarhus C, Denmark Tel: + 45 26 66 81 84; fax: + 45 78 46 28 53; e-mail: [email protected] Received 13 January 2015 Accepted 3 March 2015
A prospective descriptive study was carried out between October 2012 and May 2013 at Aarhus University Hospital, Denmark. The participants were consecutively recruited from the Department of Gastroenterology and Hepatology, which has a large local catchments population and receives referred patients. All patients had an established diagnosis of liver cirrhosis for which they were receiving treatment and being monitored. Patients with acute conditions such as sepsis or gastrointestinal bleeding and those unable to communicate were excluded. The minimum sample size was calculated taking into account a two-sided significance level of 5% and a 95% power to significantly detect a difference of four teeth because the mean number of teeth is reported to be 26 [9] in the Danish population and 22 [3] among cirrhosis patients. The sample size was calculated to 88 and it was increased to a minimum of 100 to compensate for dropouts and to improve the precision of our findings. Danish population reference
The Danish Institute for Health Services Research has published a report on the Danish population’s dental status and oral health [9] on the basis of more than 4000 interviews. We had access to the original data that provided adjusted reference values for oral care habits and self-perceived oral health of our patient sample (Table 1). Data collection
Oral health-related quality of life was measured using the Danish version of the Oral Health Impact Profile
0954-691X Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/MEG.0000000000000356 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Oral health in patients with liver cirrhosis Grønkjær and Vilstrup
Table 1. Measure of comparison between liver cirrhosis participants and the Danish population Cirrhosis participants (n = 107) Oral care habits
Self-perceived oral health
Danish population (n = 4240)
Dental status (number of teeth) Oral hygiene (brushing frequency) Dental attendance (frequency of dental visits) Experience of oral dryness
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Pearson r2 correlation coefficients or Spearman’s ρ correlation coefficient were used to assess the association between variables. A level of P less than 0.05 was considered to be statistically significant. The data were analysed using Stata version 12.0 (Stata Corp LP, College Station, Texas, USA). Results
Experience of oral pain
questionnaire (OHIP-14) [10]. The OHIP-14 is derived from the original 49 items [11] on the basis of a model developed by the WHO [12] and adapted for oral health by Locker [13]. The 14-item questionnaire OHIP-14 has proved to be reliable [14], sensitive to change [15] and has adequate cross-cultural consistency [16]. The OHIP-14 questions are organized into seven domains: functional limitation, physical pain, psychological discomfort, physical disability, psychological disability and social disability and handicap. Each one of the questions identifies the presence of a functional or a psychosocial impact in the preceding three months in relation to teeth, mouth or dentures; this is based on a Likert-type response scale coded as never = 0, rarely = 1, sometimes = 2, very often = 3 and always = 4. The total OHIP-14 score is the sum of the points for each question, that is maximum 14 × 4 = 56 points. A high score indicates a negative influence on quality of life in the domain in question and the total score indicates the overall impact of oral health on quality of life. The questions that we used on oral care habits and selfperceived oral health were identical to those in the report quoted [9] and were included in the same booklet as the OHIP-14 questionnaire. Initially, demographic variables and questions on smoking and alcohol exposure and disease characteristics were asked or collected from the medical charts of the patients. Furthermore, the patients’ nutritional risks were assessed using a standardized screening tool [17]. The risk was graded on a scale from 0 to 7 on the basis of patients’ age, nutritional status assessed from recent weight loss, food intake and BMI, and severity of disease on the basis of the increased nutritional requirements. A score of 3 or above indicates high nutritional risk and the need for targeted nutritional therapy [17]. Ethics
All patients were informed of the aims of the study and its voluntary nature. The study was approved by The Central Denmark Region Committees on Health Research Ethics. Data analysis
Student’s t-test, the analysis of variance test, the Kruskal–Wallis test and the Mann–Whitney U-test were used for the statistical comparison of the averages of results; the χ2-test was used for comparisons of proportions. The linear regression analysis was used to assess the association between the total OHIP scores and the nutritional risk scores. The requirements for linear regression were fulfilled by a model check of the residuals; the
One hundred and ten patients were asked to participate and three declined. Of the 107 participating patients, 64.5% were men and 35.5% women. Their age mean and range was 58 and 19–82 years. Their demographic and clinical characteristics are presented in Table 2. Dental status
The mean number of teeth of the cirrhosis patients was 19 ± 10.43 (range 0–32), which was lower than the Danish population, with a mean number of 26 ± 4.75 teeth (range 0–32) (P = 0.0001). The number of teeth among cirrhosis patients did not differ with aetiology, Child–Pugh score, sex or smoking habits, but decreased with age (r2 = − 0.39, P = 0.001). The decreased number of teeth was evident from the age of 25 years and older and was significant for each age group older than 45 years (Fig. 1). Oral hygiene
Brushing teeth twice a day was routine for only 52% of the cirrhosis patients compared with 81% of the Danish population (P = 0.001), the difference mostly being because of patients with alcoholic cirrhosis brushed teeth less than those with nonalcoholic cirrhosis (P = 0.03) as there was no clear difference for the patients with nonalcoholic cirrhosis and the Danish population (P = 0.1). Fewer smoking cirrhosis patients brushed teeth twice a day compared with nonsmokers (P = 0.001), but the nonsmoking patients still brushed teeth less frequently than the Danish population (P = 0.01). We found a positive association between the number of teeth and the frequency of brushing teeth (r2 = 0.21, P = 0.02) (Table 3). Dental attendance
The proportion of patients who had attended a dentist a least once a year was 44 versus 89% among the Danish population (P = 0.001). Twenty-seven per cent of the cirrhotic patients had not visited a dentist for more than 5 years versus only 1% in the population. The patients with alcoholic cirrhosis visited the dentist less frequently than patients with nonalcoholic cirrhosis (P = 0.01) (Table 3), but a difference in frequency was still found between patients with nonalcoholic cirrhosis and the background population (P = 0.01). The same was true for the smoking cirrhosis patients who attended the dentist less than the nonsmokers (P = 0.003), but again, even the nonsmokers did so less frequently than the background population (P = 0.006). Oral dryness (xerostomia)
Oral dryness was a common complaint and much more so among the cirrhosis patients: 61% versus 14% in the population (P = 0.001) (Table 3). The patients treated with
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Table 2. Clinical and demographical characteristics of liver cirrhosis patients (n = 107) Variables Age (years) Mean ± SD > 40 40–50 51–60 < 60 Sex Male Female Marital status Single/divorced/widower Married/cohabiting Career Employed/student Unemployed Disability pensioner Retired Smoker status Current smoker Nonsmoker Alcohol consumption Current alcohol use No alcohol use Comorbidity (Charlson’s score) 3+ 2 1 0 Aetiology of disease Alcoholic cirrhosis Cryptogenic cirrhosis Autoimmune hepatitis Cholestastic cirrhosis Viral B and/or C cirrhosis Child–Pugh class Class A Class B Class C Complications of cirrhosis Ascites Variceal bleeding Hepatic encephalopathy BMI Mean ± SD Nutritional risk score 3+ 2 1 Blood samples (mean ± SD) Alanine transaminase (U/l) Alkaline phosphatase (U/l) Bilirubin (μmol/l) Coagulation factors 2, 7, 10 Albumin (g/l) Sodium (mmol/l)
however, were not more frequent than in the background population (26%) (Table 3).
n (%)
Prevalence of oral problems 58 ± 10.58 5 (4.7) 17 (15.9) 45 (42.1) 40 (37.4) 69 (64.5) 38 (35.5) 55 (51.4) 52 (48.6) 19 10 43 35
(17.8) (9.3) (40.2) (32.7)
50 (46.7) 57 (53.3) 39 (36.4) 68 (63.6) 5 6 29 67
(4.7) (5.5) (27.1) (62.6)
73 16 2 9 7
(68.2) (15.0) (1.9) (8.4) (6.5)
22 (20.6) 53 (49.5) 32 (29.9) 57 (53.3) 31 (29.0) 30 (28.0) 25.55 ± 4.75 58 (54.2) 41 (38.3) 8 (7.5) 59.02 ± 100.57 162.79 ± 88.93 57.97 ± 89.86 0.53 ± 0.21 28.31 ± 6.67 134.76 ± 5.99
diuretics were slightly more likely to experience oral dryness (52% vs. 48%, P = 0.05). The cirrhosis patients with oral dryness had a total OHIP score of 7.2 ± 8.34 compared with 2.1 ± 2.8 for those without (P = 0.001). Furthermore, the patients with dry mouth had a higher risk of a high risk nutritional score (65% vs. 38%, P = 0.01). Oral pain
Twenty-eight per cent of the patients had experienced oral pain in the last 3 months. These patients had a higher total OHIP score than those without oral pain (11.5 ± 9.2 vs. 2.8 ± 4.2, P = 0.001). The patients’ complaints of oral pain,
Seventy-two per cent of the cirrhosis participants reported at least one problem because of oral conditions and their mean total OHIP score was 5.21 ± 7.2 (range 0–40, maximum possible 56). Figure 2 shows the mean score of each question and the total OHIP score. The most commonly reported problems were for taste and food intake. We found an association between the total OHIP score and the nutritional risk score (r2 = 0.25, P = 0.01). The patients reporting problems of worsening in taste (P = 0.01), dissatisfaction with diet (P = 0.0001) and interruptions of meals (P = 0.003) were more likely to have a high nutritional risk score. The oral health items that resulted in few reported problems were those related to the daily tasks performed by the participants (OHIP questions number 12 and 14, Fig. 2). Discussion
This is the first study to systematically describe oral care habits, self-perceived oral health and the importance of oral health on quality of life and nutritional status in patients with liver cirrhosis. Our results clearly indicate that the patients’ attitude towards oral hygiene was poor; they had fewer teeth, attended the dentist less frequently, more rarely brushed teeth, had more problems with oral dryness and more frequently had problems with taste and food intake than the Danish population. These subjective complaints were of clinical consequence as they predicted a high nutritional risk score. The mean number of 19 teeth in cirrhotic patients corresponds to earlier reports from Scandinavian and other countries [3,4], and was markedly lower than in the population. The loss of teeth probably reflects the patients’ negligent attitude towards dental hygiene as documented in detail in our results. These are consistent with the reported high frequency of periodontal disease and poor oral health status in patients awaiting liver transplantation [18,19]. Many factors can influence the evolution of poor oral health such as cognitive function, depression, disease and alcoholism [20]. Among our patients, those with alcoholic cirrhosis had distinctly worse oral health status than those with nonalcoholic cirrhosis. This is consistent with the findings reported by Helenius-Hietala et al. [18] and Novacek et al. [5], who consider nonalcoholic cirrhosis patients to be more health conscious than those with alcoholic cirrhosis. Still, and in contrast to the studies quoted, we did not find a lower number of teeth in alcoholic cirrhosis patients compared with nonalcoholic cirrhosis patients; thus, it remains unclear whether the loss of teeth is attitude or disease dependent. Smoking is noxious to the oral cavity [2] and in our study, the smokers also attended the dentist less often and brushed more rarely than the nonsmokers. In the Danish population, more smokers than nonsmokers have fewer than 20 teeth [9]. Still, our smoking cirrhosis patients did not have fewer teeth. We do not have an explanation for this seeming inconsistency, but most likely, the cirrhosis
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Oral health in patients with liver cirrhosis Grønkjær and Vilstrup
30
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NS
NS NS
P < 0.05
25
837
P < 0.0001 P < 0.0001 P < 0.01
20
15
10
5
0
18 − 24 25 − 34 35 − 44 45 − 54 55 − 64 65 − 74 years years years years years years
75+ years
Cirrhosis patients Mean number of teeth
32
25
26
23
19
14
7
Danish population Mean number of teeth
29
29
28
27
26
24
21
Fig. 1. Mean number of teeth divided into groups.
Table 3. Oral health status and self-perceived oral health in patients with liver cirrhosis and the Danish population
Dental status Number of teeth (mean ± SD) Dentate (%) Edentulous (%) Brushing frequency (%) 2 + times/day < 2 times/day Frequency of dental visits (%) 1 + times/year < 1 times/year Oral dryness (%) Yes Oral pain (%) Yes
Alcoholic cirrhosis (n = 73)
Nonalcoholic cirrhosis (n = 34)
P value
Cirrhosis participant (n = 107)
Danish population (n = 4240)
P value
20.3 ± 9.84
17.1 ± 11.43
0.27
19.27 ± 10.43
26.64 ± 4.75
0.0001
93.2 6.8
91.2 8.8
0.71
95.5 7.5
99.3 0.7
0.84
45.2 54.8
67.6 32.4
0.03
52.3 47.7
80.8 19.2
0.001
35.6 64.4
61.8 38.2
0.01
43.9 56.1
88.6 11.4
0.001
63.0
55.9
0.53
60.7
14.4
0.001
28.8
26.5
1.0
28.0
25.7
0.60
patients already have a strongly reduced number of teeth so that any effect of smoking is not evident. Oral dryness was a very common complaint in the patients and much more so than in the population. It may well be related to the use of diuretics, as also suggested earlier, but may also be because of disease, dehydration or lifestyle [21]. Oral dryness is unpleasant and increases the risk of caries and oral infections, and it impairs general well-being. Signs and symptoms of dry mouth are often overlooked in the broad spectrum of cirrhosis-related problems including side effects to medication, but our results indicate that the patients may benefit from a higher level of attention and treatment for this problem [22]. The OHIP-14 questionnaire measures the oral health impact on the quality of life and its score was increased in our cirrhosis patients. This was because of both the complaints of oral dryness mentioned above and also oral pain and a nutritional risk score above 3.
However, the most commonly reported oral health problems were related to taste and the ingestion of food. These results are in agreement with those of the study of Linsen et al. [23], in which most oral health problems were associated with feeding behaviour. Dysnutrition is a major and partly unexplained complication of cirrhosis, and it contributes towards higher mortality and morbidity [24,25]. Decreased food intake is the most obvious source of malnutrition in cirrhosis [26], and this may likely be partly because of poor oral health. The patients’ anorexia is sometimes related to their changes in dietary and taste preferences. Our study seems to confirm the cirrhosis-related taste deviations and it is possible that these, to some extent, are ascribable to the patients’ unpleasant oral experiences with some food constituents. It remains partly unexplained why even vigorous nutritional therapy is often unsuccessful, and our results may point to the ultimate part of food intake, the
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European Journal of Gastroenterology & Hepatology
6.00 5.21
4.00 3.00 2.00 0.15 0.1
bi lit y di sa
co re
bi lit y
So ci al
isa ol og ic a
ld
di sa Ps yc h
Ph ys ic
al
isc
bi lit y
om fo rt
in ld ol og ic a
Ps yc h
Ph ys ic
al
pa
tio n l li m ita io na ct Fu n
0.15 0.09
IP -s
0.32 0.23
0.00
p
0.63 0.58
0.4 0.21
lO H
0.78
di ca
0.49
To ta
0.76 0.33
an
1.00
H
Mean scores
5.00
OHIP-1: Trouble pronouncing words Functional limitation OHIP-2: Felt sense of taste worsened OHIP-3: Painful aching in mouth Physical pain OHIP-4: Uncomfortable eating OHIP-5: Feeling self-conscious Psychological discomfort OHIP-6: Felt tense OHIP-7: Diet been unsatisfactory Physical disability OHIP-8: Interrupting meals OHIP-9: Difficult to relax Psychological disability OHIP-10: Been a bit embarrassed OHIP-11: Irritable with other people Social disability OHIP-12: Difficulty doing usual jobs OHIP-13: Found life less satisfying Handicap OHIP-14: Been totally unable to function Fig. 2. Mean impact score of the oral health impact profile questionnaire according to its domains and the total OHIP score among the cirrhosis patients. Each domain consists of two questions.
transit of food from the plate to the swallowing. Thus, the poor oral status probably negatively influences the patients’ nutritional intake and eventually is co-responsible for their malnutrition. This has not been studied previously in patients with liver cirrhosis, but is consistent with studies of other patient groups [27]. There are limitations to this study. First, its descriptive design provides information only on associations among the study variables and not on causality. In addition, we do not have information from the patients on why they had negligent oral care habits, but this information might be important for the interpretation of our data. Second, the cohort was from one department and although sensibly large, it may not represent all patients with liver cirrhosis. This does not affect the internal study validity, but the results may not be fully generalized. Third, the reference values from the Danish authorities’ report on the population’s oral status do not take into account sex, smoking habits, socioeconomic status or the level of education, which may all influence oral hygiene. Also, they presented no references for the OHIP questionnaire. A matched
sick–control group could have reduced this bias, but is not readily available and would not have influenced the clinical message of our study. Furthermore, most of the information in our study was collected by self-reported questionnaires, the answers to which may be subject to recall bias and the participants providing socially acceptable responses [28]. However, despite the exploratory nature of our study, we believe that its results add useful information to the sparse knowledge on patients’ attitude towards oral health, and they may motivate and indicate further studies in this field. This study indicates that although there has been an overall improvement in oral health over the last decade [29], patients with cirrhosis have poorer oral health than the general population. The patients and their caregivers need to be better educated on the importance of oral health for their nutritional status and overall general health. In conclusion, this study indicates that patients with liver cirrhosis have poorer oral care habits and selfperceived oral health than the general population, and that adverse effects on oral health may lead to inappropriate
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Oral health in patients with liver cirrhosis Grønkjær and Vilstrup
food ingestion, negatively influencing the well-being of the patients and the clinical course of their cirrhosis. Further research is required to directly establish the impact of oral health on the nutritional status of cirrhotic patients. However, if confirmed, this link would have important clinical implications by directing increased attention towards oral health in the care and treatment of patients with liver cirrhosis.
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9
10 11 12
Acknowledgements
13
The authors thank Nils-Erik Fiehn, Department of International Health, Immunology and Microbiology and Lisa Bøge Christensen, Department of Odontology, Faculty of Health Sciences, University of Copenhagen, for making the reference values from the report on Danish population’s dental status and oral health available to us. H.V and L.L.G designed the study. L.L.G included patients and collected data. L.L.G carried out the statistical analysis. H.V provided supervision throughout the study execution. L.L.G drafted the manuscript. L.L.G and H.V contributed to the final manuscript. This work was supported by grants from Aarhus University Hospital and Central Denmark Region, Foundation for Health Research.
14 15
16 17
18
19
20
Conflicts of interest
There are no conflicts of interest.
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Silva Santos PS, Fernandes KS, Gallottini MH. Assessment and management of oral health in liver transplant candidates. J Appl Oral Sci 2012; 20:241–245. Guggenheimer J, Eghtesad B, Close JM, Shay C, Fung JJ. Dental health status of liver transplant candidates. Liver Transpl 2007; 13:280–286. Aberg F, Helenius-Hietala J, Meurman J, Isoniemi H. Association between dental infections and the clinical course of chronic liver disease. Hepatol Res 2014; 44:349–353. Movin S. Relationship between periodontal disease and cirrhosis of the liver in humans. J Clin Periodontol 1981; 8:450–458. Novacek G, Plachetzky U, Pötzi R, Lentner S, Slavicek R, Gangl A, Ferenci P. Dental and periodontal disease in patients with cirrhosis – role of etiology of liver disease. J Hepatol 1995; 22:576–582. Hollister MC, Weintraub JA. The association of oral status with systemic health, quality of life, and economic productivity. J Dent Educ 1993; 57:901–912. Locker D, Matear D, Stephens M, Jokovic A. Oral health-related quality of life of a population of medically compromised elderly people. Community Dent Health 2002; 19:90–97.
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Eghtesad S, Poustchi H, Malekzadeh R. Malnutrition in liver cirrhosis: the influence of protein and sodium. Middle East J Dig Dis 2013; 5:65–75. Cortsen B. Dental status – oral health objective and subjective evaluated [in Danish]. Copenhagen: The Danish Institute for Health Services Research; 2012. Gjørup H, Svensson P. OHIP- (D), a Danish version of the Oral Health Impact Profile [in Danish]. Danish Dent J 2006; 110:304–311. Slade GD, Spencer AJ. Development and evaluation of the Oral Health Impact Profile. Community Dent Health 1994; 11:3–11. World Health Organisation. International classification of impairments, disabilities and handicaps. Geneva: WHO; 1980. Locker D. Measuring oral health: a conceptual framework. Community Dent Health 1988; 5:3–18. Slade GD. Derivation and validation of a short-form oral health impact profile. Community Dent Oral Epidemiol 1997; 25:284–290. Locker D, Jokovic A, Clarke M. Assessing the responsiveness of measures of oral health-related quality of life. Community Dent Oral Epidemiol 2004; 32:10–18. Allison P, Locker D, Jokovic A, Slade G. A cross-cultural study of oral health values. J Dent Res 1999; 78:643–649. The Danish National Board of Health. A guide for doctors, nurses, healthcare assistants, auxiliary nurses and clinical dietitians Screening and treatment of patients at nutritional risk. Denmark: The Danish National Board of Health; 2008. Helenius-Hietala J, Meurman JH, Höckerstedt K, Lindqvist C, Isoniemi H. Effect of the aetiology and severity of liver disease on oral health and dental treatment prior to transplantation. Transpl Int 2012; 25:158–165. Lins L, Bittencourt PL, Evangelista MA, Lins R, Codes L, Cavalcanti AR, et al. Oral health profile of cirrhotic patients awaiting liver transplantation in the Brazilian Northeast. Transplant Proc 2011; 43:1319–1321. Dasanayake AP, Warnakulasuriya S, Harris CK, Cooper DJ, Peters TJ, Gelbier S. Tooth decay in alcohol abusers compared to alcohol and drug abusers. Int J Dent 2010; 2010:786503. Guggenheimer J, Moore PA. Xerostomia: etiology, recognition and treatment. J Am Dent Assoc 2003; 134:61–69. quiz 118–119. Dodds MW, Johnson DA, Yeh CK. Health benefits of saliva: a review. J Dent 2005; 33:223–233. Linsen S, Schmidt-Beer U, Fimmers R, Grüner M, Koeck B. Craniomandibular pain, bite force, and oral health-related quality of life in patients with jaw resection. J Pain Symptom Manage 2009; 37:94–106. Johnson TM, Overgard EB, Cohen AE, DiBaise JK. Nutrition assessment and management in advanced liver disease. Nutr Clin Pract 2013; 28:15–29. Plauth M, Cabré E, Riggio O, Assis-Camilo M, Pirlich M, Kondrup J, et al. DGEM (German Society for Nutritional Medicine); ESPEN (European Society for Parenteral and Enteral Nutrition). ESPEN Guidelines on Enteral Nutrition: liver disease. Clin Nutr 2006; 25:285–294. Campillo B, Richardet JP, Scherman E, Bories PN. Evaluation of nutritional practice in hospitalized cirrhotic patients: results of a prospective study. Nutrition 2003; 19:515–521. Barrios R, Tsakos G, García-Medina B, Martínez-Lara I, Bravo M. Oral health-related quality of life and malnutrition in patients treated for oral cancer. Support Care Cancer 2014; 22:2927–2933. Allen PF. Assessment of oral health related quality of life. Health Qual Life Outcomes 2003; 1:40–43. Sheiham A, Netuveli GS. Periodontal diseases in Europe. Periodontol 2000 2002; 29:104–121.
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Introduction
Participants and methods
Patients with liver cirrhosis have a high incidence of periodontal disease such as gingival inflammation, periodontitis and candidiasis [1,2]. This is not a trivial problem because it predisposes to systemic infections and malnutrition, leading to more frequent and prolonged hospitalizations and increased morbidity and mortality [3]. Periodontal disease may be because of oral neglect and poor oral health [4,5], yet, so far, no study has examined oral care habits and self-perceived oral health of cirrhosis patients. Oral problems in themselves may contribute toward decreased quality of life because of mouth pain and reduced social interactions [6,7]. Furthermore, the oral health status of cirrhosis patients may also be important for their very frequent dysnutrition that is associated with reduced survival and quality of life [8]. The aim of the present study, therefore, was to describe oral care habits and self-perceived oral health in a representative cohort of patients with liver cirrhosis as well as to evaluate the impacts of their oral health on general wellbeing and nutritional risk.
Study design and population
European Journal of Gastroenterology & Hepatology 2015, 27:834–839 Keywords: liver cirrhosis, nutritional risk, oral health impact profile, oral health status Department of Hepatology and Gastroenterology, Aarhus University Hospital, Aarhus C, Denmark Correspondence to Lea L. Grønkjær, RN, MSN, Department of Hepatology and Gastroenterology, Aarhus University Hospital, 44 Noerrebrogade, 8000 Aarhus C, Denmark Tel: + 45 26 66 81 84; fax: + 45 78 46 28 53; e-mail: [email protected] Received 13 January 2015 Accepted 3 March 2015
A prospective descriptive study was carried out between October 2012 and May 2013 at Aarhus University Hospital, Denmark. The participants were consecutively recruited from the Department of Gastroenterology and Hepatology, which has a large local catchments population and receives referred patients. All patients had an established diagnosis of liver cirrhosis for which they were receiving treatment and being monitored. Patients with acute conditions such as sepsis or gastrointestinal bleeding and those unable to communicate were excluded. The minimum sample size was calculated taking into account a two-sided significance level of 5% and a 95% power to significantly detect a difference of four teeth because the mean number of teeth is reported to be 26 [9] in the Danish population and 22 [3] among cirrhosis patients. The sample size was calculated to 88 and it was increased to a minimum of 100 to compensate for dropouts and to improve the precision of our findings. Danish population reference
The Danish Institute for Health Services Research has published a report on the Danish population’s dental status and oral health [9] on the basis of more than 4000 interviews. We had access to the original data that provided adjusted reference values for oral care habits and self-perceived oral health of our patient sample (Table 1). Data collection
Oral health-related quality of life was measured using the Danish version of the Oral Health Impact Profile
0954-691X Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/MEG.0000000000000356 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
834
Oral health in patients with liver cirrhosis Grønkjær and Vilstrup
Table 1. Measure of comparison between liver cirrhosis participants and the Danish population Cirrhosis participants (n = 107) Oral care habits
Self-perceived oral health
Danish population (n = 4240)
Dental status (number of teeth) Oral hygiene (brushing frequency) Dental attendance (frequency of dental visits) Experience of oral dryness
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Pearson r2 correlation coefficients or Spearman’s ρ correlation coefficient were used to assess the association between variables. A level of P less than 0.05 was considered to be statistically significant. The data were analysed using Stata version 12.0 (Stata Corp LP, College Station, Texas, USA). Results
Experience of oral pain
questionnaire (OHIP-14) [10]. The OHIP-14 is derived from the original 49 items [11] on the basis of a model developed by the WHO [12] and adapted for oral health by Locker [13]. The 14-item questionnaire OHIP-14 has proved to be reliable [14], sensitive to change [15] and has adequate cross-cultural consistency [16]. The OHIP-14 questions are organized into seven domains: functional limitation, physical pain, psychological discomfort, physical disability, psychological disability and social disability and handicap. Each one of the questions identifies the presence of a functional or a psychosocial impact in the preceding three months in relation to teeth, mouth or dentures; this is based on a Likert-type response scale coded as never = 0, rarely = 1, sometimes = 2, very often = 3 and always = 4. The total OHIP-14 score is the sum of the points for each question, that is maximum 14 × 4 = 56 points. A high score indicates a negative influence on quality of life in the domain in question and the total score indicates the overall impact of oral health on quality of life. The questions that we used on oral care habits and selfperceived oral health were identical to those in the report quoted [9] and were included in the same booklet as the OHIP-14 questionnaire. Initially, demographic variables and questions on smoking and alcohol exposure and disease characteristics were asked or collected from the medical charts of the patients. Furthermore, the patients’ nutritional risks were assessed using a standardized screening tool [17]. The risk was graded on a scale from 0 to 7 on the basis of patients’ age, nutritional status assessed from recent weight loss, food intake and BMI, and severity of disease on the basis of the increased nutritional requirements. A score of 3 or above indicates high nutritional risk and the need for targeted nutritional therapy [17]. Ethics
All patients were informed of the aims of the study and its voluntary nature. The study was approved by The Central Denmark Region Committees on Health Research Ethics. Data analysis
Student’s t-test, the analysis of variance test, the Kruskal–Wallis test and the Mann–Whitney U-test were used for the statistical comparison of the averages of results; the χ2-test was used for comparisons of proportions. The linear regression analysis was used to assess the association between the total OHIP scores and the nutritional risk scores. The requirements for linear regression were fulfilled by a model check of the residuals; the
One hundred and ten patients were asked to participate and three declined. Of the 107 participating patients, 64.5% were men and 35.5% women. Their age mean and range was 58 and 19–82 years. Their demographic and clinical characteristics are presented in Table 2. Dental status
The mean number of teeth of the cirrhosis patients was 19 ± 10.43 (range 0–32), which was lower than the Danish population, with a mean number of 26 ± 4.75 teeth (range 0–32) (P = 0.0001). The number of teeth among cirrhosis patients did not differ with aetiology, Child–Pugh score, sex or smoking habits, but decreased with age (r2 = − 0.39, P = 0.001). The decreased number of teeth was evident from the age of 25 years and older and was significant for each age group older than 45 years (Fig. 1). Oral hygiene
Brushing teeth twice a day was routine for only 52% of the cirrhosis patients compared with 81% of the Danish population (P = 0.001), the difference mostly being because of patients with alcoholic cirrhosis brushed teeth less than those with nonalcoholic cirrhosis (P = 0.03) as there was no clear difference for the patients with nonalcoholic cirrhosis and the Danish population (P = 0.1). Fewer smoking cirrhosis patients brushed teeth twice a day compared with nonsmokers (P = 0.001), but the nonsmoking patients still brushed teeth less frequently than the Danish population (P = 0.01). We found a positive association between the number of teeth and the frequency of brushing teeth (r2 = 0.21, P = 0.02) (Table 3). Dental attendance
The proportion of patients who had attended a dentist a least once a year was 44 versus 89% among the Danish population (P = 0.001). Twenty-seven per cent of the cirrhotic patients had not visited a dentist for more than 5 years versus only 1% in the population. The patients with alcoholic cirrhosis visited the dentist less frequently than patients with nonalcoholic cirrhosis (P = 0.01) (Table 3), but a difference in frequency was still found between patients with nonalcoholic cirrhosis and the background population (P = 0.01). The same was true for the smoking cirrhosis patients who attended the dentist less than the nonsmokers (P = 0.003), but again, even the nonsmokers did so less frequently than the background population (P = 0.006). Oral dryness (xerostomia)
Oral dryness was a common complaint and much more so among the cirrhosis patients: 61% versus 14% in the population (P = 0.001) (Table 3). The patients treated with
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Table 2. Clinical and demographical characteristics of liver cirrhosis patients (n = 107) Variables Age (years) Mean ± SD > 40 40–50 51–60 < 60 Sex Male Female Marital status Single/divorced/widower Married/cohabiting Career Employed/student Unemployed Disability pensioner Retired Smoker status Current smoker Nonsmoker Alcohol consumption Current alcohol use No alcohol use Comorbidity (Charlson’s score) 3+ 2 1 0 Aetiology of disease Alcoholic cirrhosis Cryptogenic cirrhosis Autoimmune hepatitis Cholestastic cirrhosis Viral B and/or C cirrhosis Child–Pugh class Class A Class B Class C Complications of cirrhosis Ascites Variceal bleeding Hepatic encephalopathy BMI Mean ± SD Nutritional risk score 3+ 2 1 Blood samples (mean ± SD) Alanine transaminase (U/l) Alkaline phosphatase (U/l) Bilirubin (μmol/l) Coagulation factors 2, 7, 10 Albumin (g/l) Sodium (mmol/l)
however, were not more frequent than in the background population (26%) (Table 3).
n (%)
Prevalence of oral problems 58 ± 10.58 5 (4.7) 17 (15.9) 45 (42.1) 40 (37.4) 69 (64.5) 38 (35.5) 55 (51.4) 52 (48.6) 19 10 43 35
(17.8) (9.3) (40.2) (32.7)
50 (46.7) 57 (53.3) 39 (36.4) 68 (63.6) 5 6 29 67
(4.7) (5.5) (27.1) (62.6)
73 16 2 9 7
(68.2) (15.0) (1.9) (8.4) (6.5)
22 (20.6) 53 (49.5) 32 (29.9) 57 (53.3) 31 (29.0) 30 (28.0) 25.55 ± 4.75 58 (54.2) 41 (38.3) 8 (7.5) 59.02 ± 100.57 162.79 ± 88.93 57.97 ± 89.86 0.53 ± 0.21 28.31 ± 6.67 134.76 ± 5.99
diuretics were slightly more likely to experience oral dryness (52% vs. 48%, P = 0.05). The cirrhosis patients with oral dryness had a total OHIP score of 7.2 ± 8.34 compared with 2.1 ± 2.8 for those without (P = 0.001). Furthermore, the patients with dry mouth had a higher risk of a high risk nutritional score (65% vs. 38%, P = 0.01). Oral pain
Twenty-eight per cent of the patients had experienced oral pain in the last 3 months. These patients had a higher total OHIP score than those without oral pain (11.5 ± 9.2 vs. 2.8 ± 4.2, P = 0.001). The patients’ complaints of oral pain,
Seventy-two per cent of the cirrhosis participants reported at least one problem because of oral conditions and their mean total OHIP score was 5.21 ± 7.2 (range 0–40, maximum possible 56). Figure 2 shows the mean score of each question and the total OHIP score. The most commonly reported problems were for taste and food intake. We found an association between the total OHIP score and the nutritional risk score (r2 = 0.25, P = 0.01). The patients reporting problems of worsening in taste (P = 0.01), dissatisfaction with diet (P = 0.0001) and interruptions of meals (P = 0.003) were more likely to have a high nutritional risk score. The oral health items that resulted in few reported problems were those related to the daily tasks performed by the participants (OHIP questions number 12 and 14, Fig. 2). Discussion
This is the first study to systematically describe oral care habits, self-perceived oral health and the importance of oral health on quality of life and nutritional status in patients with liver cirrhosis. Our results clearly indicate that the patients’ attitude towards oral hygiene was poor; they had fewer teeth, attended the dentist less frequently, more rarely brushed teeth, had more problems with oral dryness and more frequently had problems with taste and food intake than the Danish population. These subjective complaints were of clinical consequence as they predicted a high nutritional risk score. The mean number of 19 teeth in cirrhotic patients corresponds to earlier reports from Scandinavian and other countries [3,4], and was markedly lower than in the population. The loss of teeth probably reflects the patients’ negligent attitude towards dental hygiene as documented in detail in our results. These are consistent with the reported high frequency of periodontal disease and poor oral health status in patients awaiting liver transplantation [18,19]. Many factors can influence the evolution of poor oral health such as cognitive function, depression, disease and alcoholism [20]. Among our patients, those with alcoholic cirrhosis had distinctly worse oral health status than those with nonalcoholic cirrhosis. This is consistent with the findings reported by Helenius-Hietala et al. [18] and Novacek et al. [5], who consider nonalcoholic cirrhosis patients to be more health conscious than those with alcoholic cirrhosis. Still, and in contrast to the studies quoted, we did not find a lower number of teeth in alcoholic cirrhosis patients compared with nonalcoholic cirrhosis patients; thus, it remains unclear whether the loss of teeth is attitude or disease dependent. Smoking is noxious to the oral cavity [2] and in our study, the smokers also attended the dentist less often and brushed more rarely than the nonsmokers. In the Danish population, more smokers than nonsmokers have fewer than 20 teeth [9]. Still, our smoking cirrhosis patients did not have fewer teeth. We do not have an explanation for this seeming inconsistency, but most likely, the cirrhosis
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Oral health in patients with liver cirrhosis Grønkjær and Vilstrup
30
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NS
NS NS
P < 0.05
25
837
P < 0.0001 P < 0.0001 P < 0.01
20
15
10
5
0
18 − 24 25 − 34 35 − 44 45 − 54 55 − 64 65 − 74 years years years years years years
75+ years
Cirrhosis patients Mean number of teeth
32
25
26
23
19
14
7
Danish population Mean number of teeth
29
29
28
27
26
24
21
Fig. 1. Mean number of teeth divided into groups.
Table 3. Oral health status and self-perceived oral health in patients with liver cirrhosis and the Danish population
Dental status Number of teeth (mean ± SD) Dentate (%) Edentulous (%) Brushing frequency (%) 2 + times/day < 2 times/day Frequency of dental visits (%) 1 + times/year < 1 times/year Oral dryness (%) Yes Oral pain (%) Yes
Alcoholic cirrhosis (n = 73)
Nonalcoholic cirrhosis (n = 34)
P value
Cirrhosis participant (n = 107)
Danish population (n = 4240)
P value
20.3 ± 9.84
17.1 ± 11.43
0.27
19.27 ± 10.43
26.64 ± 4.75
0.0001
93.2 6.8
91.2 8.8
0.71
95.5 7.5
99.3 0.7
0.84
45.2 54.8
67.6 32.4
0.03
52.3 47.7
80.8 19.2
0.001
35.6 64.4
61.8 38.2
0.01
43.9 56.1
88.6 11.4
0.001
63.0
55.9
0.53
60.7
14.4
0.001
28.8
26.5
1.0
28.0
25.7
0.60
patients already have a strongly reduced number of teeth so that any effect of smoking is not evident. Oral dryness was a very common complaint in the patients and much more so than in the population. It may well be related to the use of diuretics, as also suggested earlier, but may also be because of disease, dehydration or lifestyle [21]. Oral dryness is unpleasant and increases the risk of caries and oral infections, and it impairs general well-being. Signs and symptoms of dry mouth are often overlooked in the broad spectrum of cirrhosis-related problems including side effects to medication, but our results indicate that the patients may benefit from a higher level of attention and treatment for this problem [22]. The OHIP-14 questionnaire measures the oral health impact on the quality of life and its score was increased in our cirrhosis patients. This was because of both the complaints of oral dryness mentioned above and also oral pain and a nutritional risk score above 3.
However, the most commonly reported oral health problems were related to taste and the ingestion of food. These results are in agreement with those of the study of Linsen et al. [23], in which most oral health problems were associated with feeding behaviour. Dysnutrition is a major and partly unexplained complication of cirrhosis, and it contributes towards higher mortality and morbidity [24,25]. Decreased food intake is the most obvious source of malnutrition in cirrhosis [26], and this may likely be partly because of poor oral health. The patients’ anorexia is sometimes related to their changes in dietary and taste preferences. Our study seems to confirm the cirrhosis-related taste deviations and it is possible that these, to some extent, are ascribable to the patients’ unpleasant oral experiences with some food constituents. It remains partly unexplained why even vigorous nutritional therapy is often unsuccessful, and our results may point to the ultimate part of food intake, the
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European Journal of Gastroenterology & Hepatology
6.00 5.21
4.00 3.00 2.00 0.15 0.1
bi lit y di sa
co re
bi lit y
So ci al
isa ol og ic a
ld
di sa Ps yc h
Ph ys ic
al
isc
bi lit y
om fo rt
in ld ol og ic a
Ps yc h
Ph ys ic
al
pa
tio n l li m ita io na ct Fu n
0.15 0.09
IP -s
0.32 0.23
0.00
p
0.63 0.58
0.4 0.21
lO H
0.78
di ca
0.49
To ta
0.76 0.33
an
1.00
H
Mean scores
5.00
OHIP-1: Trouble pronouncing words Functional limitation OHIP-2: Felt sense of taste worsened OHIP-3: Painful aching in mouth Physical pain OHIP-4: Uncomfortable eating OHIP-5: Feeling self-conscious Psychological discomfort OHIP-6: Felt tense OHIP-7: Diet been unsatisfactory Physical disability OHIP-8: Interrupting meals OHIP-9: Difficult to relax Psychological disability OHIP-10: Been a bit embarrassed OHIP-11: Irritable with other people Social disability OHIP-12: Difficulty doing usual jobs OHIP-13: Found life less satisfying Handicap OHIP-14: Been totally unable to function Fig. 2. Mean impact score of the oral health impact profile questionnaire according to its domains and the total OHIP score among the cirrhosis patients. Each domain consists of two questions.
transit of food from the plate to the swallowing. Thus, the poor oral status probably negatively influences the patients’ nutritional intake and eventually is co-responsible for their malnutrition. This has not been studied previously in patients with liver cirrhosis, but is consistent with studies of other patient groups [27]. There are limitations to this study. First, its descriptive design provides information only on associations among the study variables and not on causality. In addition, we do not have information from the patients on why they had negligent oral care habits, but this information might be important for the interpretation of our data. Second, the cohort was from one department and although sensibly large, it may not represent all patients with liver cirrhosis. This does not affect the internal study validity, but the results may not be fully generalized. Third, the reference values from the Danish authorities’ report on the population’s oral status do not take into account sex, smoking habits, socioeconomic status or the level of education, which may all influence oral hygiene. Also, they presented no references for the OHIP questionnaire. A matched
sick–control group could have reduced this bias, but is not readily available and would not have influenced the clinical message of our study. Furthermore, most of the information in our study was collected by self-reported questionnaires, the answers to which may be subject to recall bias and the participants providing socially acceptable responses [28]. However, despite the exploratory nature of our study, we believe that its results add useful information to the sparse knowledge on patients’ attitude towards oral health, and they may motivate and indicate further studies in this field. This study indicates that although there has been an overall improvement in oral health over the last decade [29], patients with cirrhosis have poorer oral health than the general population. The patients and their caregivers need to be better educated on the importance of oral health for their nutritional status and overall general health. In conclusion, this study indicates that patients with liver cirrhosis have poorer oral care habits and selfperceived oral health than the general population, and that adverse effects on oral health may lead to inappropriate
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Oral health in patients with liver cirrhosis Grønkjær and Vilstrup
food ingestion, negatively influencing the well-being of the patients and the clinical course of their cirrhosis. Further research is required to directly establish the impact of oral health on the nutritional status of cirrhotic patients. However, if confirmed, this link would have important clinical implications by directing increased attention towards oral health in the care and treatment of patients with liver cirrhosis.
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8
9
10 11 12
Acknowledgements
13
The authors thank Nils-Erik Fiehn, Department of International Health, Immunology and Microbiology and Lisa Bøge Christensen, Department of Odontology, Faculty of Health Sciences, University of Copenhagen, for making the reference values from the report on Danish population’s dental status and oral health available to us. H.V and L.L.G designed the study. L.L.G included patients and collected data. L.L.G carried out the statistical analysis. H.V provided supervision throughout the study execution. L.L.G drafted the manuscript. L.L.G and H.V contributed to the final manuscript. This work was supported by grants from Aarhus University Hospital and Central Denmark Region, Foundation for Health Research.
14 15
16 17
18
19
20
Conflicts of interest
There are no conflicts of interest.
21 22
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