Association of Khat chewing, smoking, age and sex

Objective: Periodontal diseases are very common dental disease. Many risk factors may play significant role in the periodontal disease initiation and progression. This study was performed to evaluate the effects of khat chewing, smoking, age and gender on periodontal status among Yemeni adults. Material and Methods: This cross-sectional study was performed on 1231 patients attending the outpatient dental polyclinics of University of Science and Technology during the academic years 2017/2018. All completed sheets were collected throughout the year by the supervisors. Data cleaning, descriptive statistics, and inferential statistics were then performed. Results: Khat chewers were more frequent than non-chewers counterparts (60.7% vs. 39.3%). The prevalence of smoking was 25.5% (297 patients). Study results indicated that periodontitis is more associated with female gender and participants aged more than 35 years old. Results also showed that female and age older participants aged more than 35 years were significantly associated with gingival recession. Mean number of the teeth with gingival recession in male patients were higher than in females. Male gender and patients aged more than 35 years old were significantly associated with furcation involvement. Conclusion: The present study has shown females gender and age older than 35 seem to be risk factors of periodontal diseases. Males has more teeth affected by gingival recession and more furcation involvement. RESUMO


INTRODUCTION
T he American academy of periodontology defines periodontal diseases, as a serious infection that if left untreated, can lead to tooth loss. Periodontal diseases involve an inflammation and/or infection that results in the destruction of the supporting tissues of the teeth, including the gingiva, the periodontal ligaments, the cementum, and the alveolar bone [1]. American Academy of Periodontology (AAP) and the European Federation of Periodontology (EFP) workshop presented a new scheme for classification of periodontal and peri-implant diseases and also reorganized the broad spectrum of non-plaque induced gingival diseases and conditions based on primary etiology [2].
Periodontal diagnosis and monitoring rely upon clinical parameters to a large extent. Clinical diagnosis directly affects decisions to initiate therapy and to select methods. Dentists also evaluate the outcome of therapy and attempt long-term prognosis based on clinical parameters. The primary parameters assessed by periodontal probing are probing pocket depth (the distance between the gingival margin and the bottom of the sulcus ⁄ pocket), gingival recession (the distance between the cementoenamel junction and the gingival margin), and clinical attachment level (the distance between the cementoenamel junction and the bottom of the sulcus ⁄ pocket) [3].
Khat (Catha edulis) is a natural stimulant from the Catha edulis plant, found in the flowering evergreen tree which grows mainly in Yemen, Ethiopia, Somalia, Kenya, Saudi Arabia, and at high altitude areas in South Africa and Madagascar. A high proportion of the population habitually chews its fresh leaves and twigs for their amphetamine-like effects [4,5]. The active ingredient of khat responsible for its psychostimulant effect is an alkaloid chemical known as cathinone, which is structurally and chemically similar to damphetamine, and cathine, a milder form of cathinone. Cathinone is a highly potent stimulant, which produces sympathomimetic and central nervous system stimulation analogous to the effect of amphetamine [6].
In Yemen, khat is commonly used for social recreation. Workers such as motor vehicle drivers and truck drivers; building establishment workers also use it under a variety of other conditions. A significant number of students chew khat to be Attentive especially during exams periods. Although largely viewed as a social habit, longterm heavy chewing has been recently reported to cause degree of dependence [7,8].
Khat leaves, which are generally placed in the mouth in the lower distal mucobuccal fold, are usually chewed during sociocultural meetings where the chewing process may take up to 6 hours. Since the process of khat chewing has a drying effect on the oral mucosa, its users tend to consume a great quantity of fluids. Some of the khat users also supplement their chewing practice with smoking habits [9,10]. Khat is usually chewed into a large bolus that is kept in one side of the mouth for several hours, which raises a clinically relevant question about the effect of this habit on periodontal health. Unfortunately, existing literature doesn't provide a clear view on this matter. Comparative cross-sectional clinical studies have reported conflicting results [11][12][13][14][15][16].
While comparisons between chewers and non-chewers indicate that khat chewing is detrimental to the periodontium, some comparisons between khat chewing and nonchewing sides suggest the opposite. Obviously, a sound conclusion cannot be made before controlled, longitudinal in vivo studies are carried out to evaluate the effect of khat chewing on microbial and clinical periodontal parameters. In general, much of the claims about the adverse health effects of khat chewing are either anecdotal or based on inadequate evidence [17,18] With respect to tobacco smoking, there is clear evidence that smoking may negatively affect the results of periodontal treatment. Tobacco smoking is a known risk factor that affects the oral environment and ecology, vascularization of the periodontium, immune and inflammatory responses and the healing potential of the periodontal connective tissues [19,20].
Large epidemiologic surveys reveal a higher prevalence and severity of destructive periodontal disease in men than women [21][22][23]. Gender differences in the development and progression of periodontitis can be attributed to underlying variations in genetic or environmental mechanisms [24,25].
Numerous authors have attributed the higher risk for periodontal breakdown in men to a differential exposure to modifiable environmental risk factors. [26,27] It was asserted that susceptibility to periodontitis increased with age, resulting in tooth loss seen predominantly after 35 years of age. The prevalence of periodontal disease is expected to increase with age as a result of cumulative disease progression over time, not susceptibility [28,29]. The aim of this study was to evaluate the effects of khat chewing, smoking, age and gender on periodontal status among Yemeni adults.

MATERIAL AND METHODS
This cross-sectional study was carried out on patients recruited from the outpatient dental polyclinics at the department of periodontology, Faculty of Dentistry, University of Science and Technology (UST). Preformed case sheets, approved from the department, were used as tools of data collection in the clinical sessions. All patients attended those sessions during the academic years 2017, 2018 were surveyed. The data sheet contained four main parts; personal and demographic data, medical and dental history of the patient, gingival and periodontal scoring indices and diagnosis, and the last part contained questions related to khat chewing ("Yes" or "No"), and smoking ("Yes" or "No"). All data concerning this study were revised carefully by the supervisors during data collection.
The sample population were all the outpatient attended the dental polyclinics at the department of periodontology, diagnosed as having gingivitis or periodontitis and were free or controlled systemic conditions were included in the study. Patients were diagnosed as having gingivitis or periodontitis according to 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions [30] where patients diagnosed having gingivitis if they had the classical signs of gingivitis i.e. erythema, edema, bleeding and tenderness without clinical attachment loss. Gingiva surrounding the tooth divided into 4 scoring units-mesio-facial papilla, facial marginal gingiva, disto-facial papilla and lingual marginal gingiva [31,32]. Periodontitis was considered if there was clinical attachment loss (Periodontal pockets, gingival recession and furcation involvement) [33]. Gingival recession was considered as the distance from the cemento-enamel junction to the free gingival margin and was measured using a Michigan O periodontal probe with William's markings. All measurements were made in millimeters and were rounded to the lower whole millimeter. All permanent, fully erupted teeth, excluding third molars, were examined [34]. Gingival recession was considered on the basis of its presence or absence. Also, the number of teeth affected with gingival recession for each patient. Similarly, furcation involvement was recorded as present or absent.
Participants were considered Khat chewers if they had a history of chewing khat for more than 3 years, not less than 4 days per week and not less than 4 hours per day [7]. All completed sheets were collected throughout the year by the supervisors, then the data were managed using SPSS® statistical package version 20. Descriptive statistics were performed in terms of means, frequencies, and percentages. Chi-square test was utilized for inferential statistics along with odds ratio and 95% confidence interval with P value < 0.05 as a significant level for all tests.

RESULTS
The overall study sample was consisted of 1231 dental outpatients, (Male= 493 (40.0%); Female= 738 (60.0%). Their age ranged from 17 to 81 years (mean age was 35.1 years; SD ± 13.8). Khat chewers were higher among the study sample than non-chewers counterparts (60.7% vs. 39.3%). Regarding smoking, prevalence of smoking among the study sample was 25.5% (297 patients). As seen from the Table 1, analysis of the risk factors with periodontitis among the study sample showed that khat chewing was associated with periodontitis with 78.3% prevalence in comparison to 21.7% although data did not show significant difference between khat chewers and non-chewers regarding this point. Similarly, data showed that 79.5% of smokers had periodontitis and 20.5% had not with no significant difference between both groups. Regarding gender, females showed more prevalence for periodontitis than males with significant difference (OR= 1.64; P= 0.003). Patients with age > 35 years had much higher prevalence of periodontitis with 91.6% compared to 68.5% among patients with age ≤ 35 years with highly significant difference (OR= 5.01; P< 0.001). These results indicated that periodontitis are more associated female gender and age older than 35 years old with highly significant difference. While khat chewers and smokers had high rates of association with periodontitis but with no significant difference than khat non-chewers and non-smokers.

Comparison between mean of teeth with gingival recession between khat chewers and non-chewers is shown in
Furcation involvement appeared to be more prevalent in khat chewers in comparison with non-chewers (15.8% compared to 9.3%) but with no significant difference (OR= 0.79; P= 0.257). Regarding smoking, also no significant difference was found between smokers and non-smokers (17.5% and 11.6%, respectively) (OR= 0.81; P= 0.305). Males showed more furcation involvement than females with significant difference (17.4% and 10.7%, respectively). Similarly, age > 35 years old had more furcation involvement than patient with age ≤ 35 years old with highly significant difference (P< 0.001). Accordingly, male gender and patients aged more than 35 years old were significantly associated with furcation involvement (Table  4).

DISCUSSION
Periodontal diseases are inflammatory diseases that have two main forms. Gingivitis which is reversible with oral care and individual's motivation and limited to the gingiva, and periodontitis which affect the supporting tissues of teeth causing destruction of periodontal ligaments and alveolar bone leading to clinical attachment loss by specific microorganisms [1]. This cross-sectional study examined the association of periodontal status with main risk factors such as Khat chewing, smoking, age and gender among a large sample of Yemeni patients.
Khat chewing is considered as a risk factor of periodontal diseases. An exploring the association between periodontal diseases and Khat habit showed a higher periodontitis among khat chewing sides compared to non-chewing sides [35]. According to Al-hebshi and Al-akhali, comparisons between chewers and non-chewers indicate that khat chewing is harmful to the periodontium, but conversely comparisons between khat chewing and non-chewing sides suggest the opposite [36]. The results of this study showed that female and age more than 35 are significant determinants of periodontitis. Khat chewers and smokers had high rates of periodontitis although these results don't show significant differences than non-khat-chewers and non-smokers, but this can be explained that this is a cross-sectional study and other risk factors for periodontitis didn't excluded. This is in agreement with, a cross-sectional hospital study among Yemeni khat and non khat-chewers which revealed that khat chewing caused many lesions to the supporting structures of the teeth, namely gingivitis, periodontal pocket formation, gingival recession, tooth mobility and tooth mortality [11]. On the other hand, other studies reported a positive effect of khat chewing as anti-plaque, showed a higher probing pocket depth among non-chewing sides compared to chewing side and did not show any significant differences of periodontal status between Khat chewers and non -chewers. Another study considered the khat chewing has no negative effect [7,36,37].
Many researchers have evaluated the relationship between habitual khat chewing and its adverse effect on periodontal tissues, which is still controversy issue. However, continuing mechanical movement is considered as causative factor of gingival recession in many studies, another researcher documented that as mechanical cleaner or anti-plaque [38]. As gingival recession is considered an important parameter for periodontitis, we assessed gingival recession with association with risk factors. In this study, female gender and age more than 35 showed more prevalence for gingival recession. Results showed no significant difference between khat chewers and non-chewers also smokers and non-smokers, but as we said before for periodontitis, there is no exclusion for other factors which may lead for recession. So, other case control studies are recommended to assess the effects of these factors. In the same context, in a study conducted on Khat chewers, the clinical attachment loss was significantly higher among the chewers where 37.9% of daily khat chewers had higher probing pocket depth in contrary to 18.6% of once weekly habit chewers [39].
In this study, the number of teeth with gingival recession was higher in Khat chewers compared to non-chewers. These results are consistent with Amran et al. who found that khat chewing is considered as a risk factor of gingival recession with 60.5% of people had gingival recession and 42.5% of them had GR > 4 mm. The authors referred that to continuous mechanical forces on the chewing side of khat as well as the chemical contents of Khat plant [40]. Another risk factor of periodontal diseases and tooth loss is smoking habit. Previous study documented that the Yemeni smokers had higher mean tooth loss compared to non-smokers groups [41]. The results of the present study showed no significant differences among the smokers compared to non-smokers regarding gingivitis, periodontitis and gingival recession which revealed inconsistent to previous studies that showed highly significant of gingival recession , most likely to have clinical attachment loss 1.17 times related to smokers compared to none [40,42].
Regarding age, the data of the present study showed that the prevalence of periodontitis, and gingival recession were significantly more among the age group older than 35 years old which is agreed with another study conducted by Al-Sharabi AK, et al. [35]. This also was in agreement with Hill and Gibson who observed that effects on oral and dental tissue among Yemeni males with an average age of 35 years who chewed khat for of 20 years increased periodontal pocket depth on the khat-chewing side compared with the non-khat chewing side [12]. Regarding gender, the results of present study showed that the number of teeth with gingival recession among male more than female group. This may be due to this social habit are more common in males than females and high proportion of Khat chewers are male compared to female [35,42].
In a surprising topic, our results showed that the female group had more periodontitis and gingival recession compared to male group which may be seemed unlogical and inconsistent with previous studies [42,43]. This surprisingly data can be explained that females have more motivation toward oral care and follow up in dental clinics especially that our sample was from Yemeni dental patients not Yemeni whole population. This explanation is supported by the results of this study which showed that the number of teeth with gingival recession among male more than female group males for each case. In addition that males usually have more advanced periodontitis and more advanced other miller classes II, III, and IV which may indicated for extraction as published in other studies due to their more habitual khat chewing [40]. Furcation involvement also considered as important indicator for periodontitis, so, in this study, the results showed that the furcation involvement was higher among khat chewers, smokers, males and patients aged more than 35 years compared to other subdivided groups, but khat chewing and smoking showed no significant difference. This agreed with Al-Sharabi et al.
who documented that habitual khat chewing as independent risk factor of periodontitis that caused by mechanical trauma in the posterior vestibule which leading to furcation involvement [35].
As a limitation of this study, there is no valid and reproducible tool to record Khat chewing and smoking status regarding the binary level (Yes-No), hours or number of cigarettes, onset and duration of these habits. Despite of that, the researchers used easy, valid, and non-time-consuming indices to diagnose and evaluate the prevalence of the periodontal diseases among the sample. Also, we compare the effects of smoking and khat chewing on periodontal status without excluding some other risk factors. So, we recommended that other studies should be done with exclusion of these factors. Also use more precise parameters such as miller classification in evaluation of gingival recession.

CONCLUSIONS
Within the limitation of this study, it can be concluded that: 1-Periodontitis are significantly associated female gender and age older than 35 years old.
2-Male gender and age older than 35 years are significantly associated furcation involvement.
3-Females has more prevalence for gingival recession and periodontitis but males have more teeth affected by gingival recession. Also, males have more association with furcation involvement.