Assessment of periodontal health among the inpatients with schizophrenia

Background/Aim. Many studies on oral health of psychiatric inpatients reported schizophrenia as the most common psychiatric disorder among their sample population. The available evidence suggests the higher prevalence and severity of periodontal disease among the psychiatric inpatients. The aim of this study was to evaluate periodontal health among the inpatients with schizophrenia and to consider possible risk factors for their current periodontal diseases. Methods. This cross-sectional study comprised 190 inpatients with schizophrenia at the Clinic for Psychiatric Disorders “Dr Laza Lazarevic” in Belgrade, and 190 mentally healthy patients at the Clinic for Periodontology and Oral Medicine, Faculty of Dental Medicine, University in Bel-grade. The Community Periodontal Index for Treatment Needs (CPITN) and sociodemographic characteristics were registered in both groups as well as the characteristics of the primary disease among the inpatients with schizophrenia. Results. The patients in the study group had significantly higher scores of the CPITN (2.24 ± 0.98) than the patients in the control group (1.21 ± 1.10). Most of the patients in the study group had supra- , or subgingival calculi (46.8%), in contrast to the control group patients, who had in most cases gingival bleeding (45.8%). The periodontal pockets where detected in 35.8% of schizophrenic inpatients. The linear regression analysis showed that the gender and age were statistically significant predictors of the CPITN value among the inpatients with schizophrenia. Conclusion. The results of this study generally indicate the need for continuous research of psychiatric patients’ oral health, in order to determine the modes of its improvement. Similar studies should elucidate significance of psychiatric patients’ periodontal health and sensitize psychiatrists and psychiatric nurses to the oral problems of their patients.


Introduction
Mental health is a state of well-being in which an individual realizes how can cope with usual life stresses with his or her own abilities, how can work productively and fruitfully, and make a contribution to his or her community 1 . Several studies on oral health of psychiatric inpatients reported schizophrenia as the most common psychiatric disorder among their sample population 2-4 . Schizophrenia is a mental disorder characterized by a disintegration of thinking processes and emotional responsiveness 5 . The disease occurs in 1% of the general population and it is one of ten leading causes of disability in the population between 15 and 44 years of age 6 .
Oral health is a significant part of general health and should not be separated from mental health 7 . The available evidence suggests the higher prevalence and severity of periodontal disease among the psychiatric inpatients 3,[8][9][10][11][12][13] . A bacterial role in the initiation and progression of periodontal disease is essential, but most of the nonbacterial risk factors appear to act as the disease modifiers that may alter the clinical effects of bacterial challenge 14 . There are many factors associated with the poor periodontal status among the psychiatric inpatients: sociodemographic characteristics like age 8,15,16 , gender 10, 15 and educational level 15 ; characteristics of schizophrenia like duration of disease 16 , length of hospitalization 8 and psychotropic medications 15 ; and, the oral health habits like frequency of tooth brushing 10 , tooth brush technique 15 and smoking 10 .
In Serbia, no research has been conducted on periodontal health of this vulnerable group of psychiatric inpatients, although the prevalence of the disease is 1% of the whole population 6 . Therefore, the aim of the present study was to evaluate periodontal health among the inpatients with schizophrenia, and to consider possible risk factors that might contribute to the current periodontal health status of this group of psychiatric inpatients.

Study population
The study was conducted as an observational crosssectional study. It was adjusted to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement for improving the quality of observational studies 17 . The approval for the study was obtained from the Ethics Committee of the Clinic for Psychiatric Disorders "Dr. Laza Lazarević" in Belgrade, Serbia (No. 7221) and the Faculty of Dental Medicine, University of Belgrade, Serbia (No. 36/10). The research was conducted in accordance with the Declaration of Helsinki 18 .
Each subject participated voluntarily and was informed, through a special brochure, of the type of the research and the data collection procedure. The written consent was obtained from all subjects, or their legal representatives to use the personal data for the research purposes.
The study group size was determined according to the prevalence of schizophrenia in the general population in the Republic of Serbia, with 95% confidence level. Consequently, the study group comprised 190 randomly selected inpatients with schizophrenia (95 males and 95 females, aged 19 to 67 years; mean age 43.59 ± 11.96 years) hospitalized at the Clinic for Psychiatric Disorders "Dr. Laza Lazarević" in Belgrade, Serbia. The inclusion criteria for entering the study were that a patient was hospitalized, older than 18 years and diagnosed with schizophrenia (according to the 10th Revision of the International Classification of Diseases) 19 at least two years prior to the study. The exclusion criteria were: a primary diagnosis of another mental disorder, the inpatients diagnosed with schizophrenia in the period shorter than two years from the time of the survey, simultaneous presence of severe somatic illnesses or severe disability, and inability to communicate, or refuse to cooperate.
The control group comprised of 190 patients suffering from localized or generalized chronic periodontitis 20 (95 males and 95 females, aged 19 to 72 years; mean age 43.20 ± 11.89 years), without any psychiatric or somatic illness, who were consecutively recruited from the pool of patients at the Department of Periodontology and Oral Medicine, Faculty of Dental Medicine, University of Belgrade, Serbia. The patients in the control group did not use any medication that could affect oral health 21 . Both, the study and the control groups were age and gender matched.
A questionnaire for both groups was designed in order to record the sociodemographic characteristics (gender, age, educational level, marital status and residence), oral health habits (frequency of brushing teeth and tooth brushing technique) and smoking habits. The data about schizophrenia in the study group were taken from the medical records and included the duration of schizophrenia, number of hospitalizations and current psychotropic medication.

Clinical examination
All patients were subjected to the thorough dental clinical examination in accordance with the criteria recommended by the World Health Organization 22 . The dental clinical examinations were carried out by two trained and calibrated examiners (V.Dj. and M.J.) at the dental office at the Clinic for Psychiatric Disorders "Dr. Laza Lazarević" in Belgrade, Serbia, and the Department of Periodontology and Oral Medicine, Faculty of Dental Medicine, University of Belgrade, Serbia. The examiners were calibrated twice, before and during the study, by assessing the Community Periodontal Index for Treatment Needs (CPITN) 23 , with a degree of agreement with ± 1 mm of 94%. The clinical measurements were performed by using the periodontal probe graded in mm (WHO 621 Trinity probe) on the sextants, scoring on the scale from 0 to 4. In each sextant, all teeth were examined and only the highest value for each sextant was scored and recorded.

Statistical analysis
All collected data were organized and evaluated using the dedicated software (SPSS 17.0 Inc, Chicago, IL, USA) and were analysed by the descriptive statistical parameters and regression models. The descriptive statistical methods were represented by the measures of central tendency (mean and median), measure of variability (standard deviation and var-iation interval) and were expressed in the percentages. The methods for testing the difference of numerical data (age and CPITN) were represented by the t-test of independent groups. For testing the data of different categories (gender, education level, employment status, marital status, residence, smoking, brushing teeth, tooth brush technique), the χ 2 -test was used. The level of significance was set at p ≤ 0.05.

Results
The groups where comparable in terms of age (p = 0.747 for the t-test of independent groups) and gender (p = 1.000 for χ 2 -test). The distribution of sociodemographic characteristics and oral health habits of the enrolled subjects are shown in Table 1. The statistically significant differences between the groups were observed for all sociodemographic characteristics and oral health habits ( Table 1). The educational structure of inpatients with schizophrenia was lower than of the control group patients. Furthermore, the percentage of employees among the inpatients with schizophrenia was significantly lower than in the study group. Most of the patients of the study group were smokers (74.7%) as opposed to the control group patients (39.5%). In the study group, schizophrenia lasted, on average, 14.69 ± 9.61 years (range 2 to 45 years), and the average number of hospitalizations was 8.52 ± 5.71 (range 1 to 30 hospitalizations). The patients were treated with an average of 3.54 ± 0.87 psychotropic medications (range 2 to 6). The characteristics of primary disease in the study group are shown in Table 2.
The patients in the study group mostly did not brush their teeth (54.7%), unlike the patients in the control group. Among the inpatients with schizophrenia, even 72.6% were not familiar with a correct tooth brushing technique, as opposed to the patients in the control group (46.3%).
A statistical significance was observed in the CPITN values between the examined groups ( Table 3). The patients in the study group had the significantly higher scores of the CPITN (2.24 ± 0.98, range 0 to 4) than the patients in the control group (1.21 ± 1.10, range 0 do 4). The patients in the study group had supra-or subgingival calculi more often (46.8%) than the control group patients, who demonstrated gingival bleeding more frequently (45.8%). Moreover, the periodontal pockets where detected in 35.8% of schizo-phrenic inpatients, much more frequently than in the control group patients (13.7%).
Analysing the mean of the CPITN in relation to the sociodemographic characteristics and oral health habits of subjects in both groups (Table 3), a statistically significant difference in the study group was observed in terms of gender, age, and tooth brushing. The older male inpatients with schizophrenia, who did not brush teeth, had the highest value of CPITN. In the control group, a statistically significant difference in the CPITN values was observed in terms of marital status and tooth brush technique ( Table 4). The widowed patients in the control group, who used an incorrect tooth brush technique, had the highest value of CPITN.
In terms of characteristics of the primary disease, a statistically significant difference in the value of CPITN among the study group patients was observed in terms of number of hospitalizations ( Table 5).
The impact of sociodemographic characteristics and oral health habits, as well as the characteristics of the disease, the CPITN values among the inpatients with schizophrenia was examined by the linear regression model (Table 6).   The univariate regression analysis showed a statistical significance of the CPITN among the inpatients with schizophrenia in terms of gender (p = 0.044) and age (p = 0.018), brushing teeth (0.001), a tooth brush technique (p = 0.009), the duration of schizophrenia (p = 0.002), the number of hospitalizations (0.004) and the use of mood stabilizers (p = 0.048).
However, in the multivariate regression analysis, only gender (p = 0.013) and age (p = 0.010) were the statistically significant predictors of the CPITN value among the inpatients with schizophrenia.

Discussion
The presented study was conducted to assess the periodontal health and possible risk factors that might influence periodontal health among the inpatients with schizophrenia. The principal finding in this study was a high prevalence of periodontal disease among the inpatients with schizophrenia. The average value of the CPITN in the inpatients with schizophrenia was a significantly higher than that of the control group, which is in accordance with similar study 15 .
The CPITN revealed poor periodontal health of inpatients with schizophrenia, whereas the healthy periodontium was observed in only 4.7% of subjects, which is even lower in comparison to the previous studies 10,15,[24][25][26] . The presence of calculi (46.8%) was the most common finding in the study group, in contrast to gingival bleeding (45.8%) which was observed in the control group.
Previous studies reported a significantly higher occurrence of calculi in the psychiatric inpatients (range 71.8% to 94.2%) 24,25,27 . The presence of shallow pockets was observed in 24.2% of patients in the study group, much more than in the control group (7.9%). Furthermore, the deep periodontal pockets were detected in 11.1% in the study group, while in the control group they were detected in 5.8% of cases. The occurrence of deep periodontal pockets in the study group is in accordance with previous studies 10,11,16,24 . Higher occurrence of CPITN values among the inpatients with schizophrenia can be explained by several facts. First of all, in the present study, more than one half of inpatients with schizophrenia (54.7%) did not brush their teeth, which is in contrast to previous studies 2, 15,24 . It has been already described that the neglected oral hygiene increases the accumulation of dental plaque, which leads to the gingival inflammation and periodontal disease 28 . The highest value of the CPITN was observed in the patients who did not brush their teeth, compared to those who brushed their teeth once a day, or twice, or more times per day. Likewise, 72.6% of inpatients with schizophrenia did not know how to perform a correct tooth-brushing technique.
In the present study, 74.2% of inpatients with schizophrenia were smokers. It is well-known that stress (like in the people with psychiatric diseases) can cause a behaviour modification, such as smoking, and may have an immunosuppressant effect (decreased leukocyte count, altered helper T1 cell/T2 cell ratio), which can result in more frequent recurrence of periodontal disease 28 . Smoking appear to be a periodontal disease modifier -do not cause periodontal disease, but it can increase the rate of progression of the disease, by determining the age of clinical diagnosis and the severity at given age 14 . The risk for periodontal disease is 2.5 to 7 times higher in smokers than in non-smokers 29 . Smokers have a clinically less pronounced inflammation and less gingival bleeding 29 . Vasoconstriction caused by nicotine reduces blood flow, leading to oedema and clinical signs of inflammation 29 , which may be an explanation for lower rate of bleeding on probing in the study group.
Schizophrenia in the study group lasted 14.69 ± 9.61 years, on average, which is not in line with previous study 30 . The present study showed a large number of hospitalizations per patient (8.52 ± 5.71, range 1-30), which points to the fact that the patients were hospitalized for a proportionally long period of time, which is in accordance with the already published data 2, 4, 10, 11 . The inpatients with schizophrenia were treated by several psychotropic drugs. Previous study 4 reported some oral side-effects of psychotropic drugs on buccal mucosa, and revealed that antipsychotics, benzodiazepines, antidepressants and mood stabilizers were related to xerostomia, because they interfere with the salivary glands' function. Furthermore, another study 26 concluded that xerostomia was recognized as a high risk factor for development of periodontal disease in the patients with schizophrenia due to the decrease in the salivary flow rate. Xerostomia can also increase accumulation of dental plaque 21 , which is one of the important causes of periodontal disease 27 . All these facts may explain the higher CPITN values in the study group.
In the present study, 50% of inpatients with schizophrenia were the females. Therefore, the gender could not influ-ence the difference in the CPITN values between the patients in the study and control groups in this study, although it was noticed that the CPITN values were higher in the males 10,15 , probably due to the observed ignorance toward oral hygiene among the males 31 . Concerning the age, the mean age of patients in the study group was in line with the previous study 8 . The inpatients younger than 30 years had the lower CPITN than the patients older than 50 years of age, which is in accordance with the previous studies 16,24 . The increased severity of periodontal disease in older age is probably related to the length of time of periodontal tissues exposure to dental plaque, which reflects the individual cumulative oral history 32 .
By the stepwise multiple regression analysis, it was demonstrated that the gender and age of inpatients with schizophrenia could influence the CPITN values. The higher CPITN values were observed in the males compared to the females, and in the older compared to the younger inpatients with schizophrenia. This is in accordance with the previous findings 8, 10,15,16,24 . In the present study, the sociodemographic characteristics, oral health habits and medical characteristics did not influence the mean value of the CPITN in the inpatients with schizophrenia, which is not in line with the previous studies 8, 10,15,16 . Our findings suggest that the underlying disease affects oral health indirectly, reducing the patients' motivation for the oral health maintenance.
Certain limitations should be considered when interpreting the results of this study. All subjects in the study group were hospitalized at the Clinic for Psychiatric Disorders, which possesses a dental office enabling dental care within the easy patients' reach. Therefore, it can be assumed that in other psychiatric hospitals, in country, the inpatients with schizophrenia could exhibit even poorer periodontal health. Also, the control group patients were the outpatients coming to the Department of Periodontology and Oral Medicine, Faculty of Dental Medicine, University of Belgrade, Serbia, who were very much familiar with the tooth brushing technique and oral hygiene maintenance. This fact could contribute to the differences between the CPITN values of the study and the control groups in this study.

Conclusion
The high CPITN values of inpatients with schizophrenia indicate a need for continuous considering the treatment needs of their oral and periodontal health improvement, especially during the hospitalization periods. Also, the results of this study indicate the need for a continuous research of psychiatric patients' oral health, in order to determine the modes of its improvement. Similar studies should elucidate a significance of psychiatric patients' periodontal health and sensitize the psychiatrists and psychiatric nurses to the oral problems of their patients.