Relationship Between Undernutrition and Periodontal Diseases Among Yemen Population: a Cross-sectional Study

Background: Undernutrition is an inadequate supply of energy and nutrients. Periodontal diseases (PDs) dened as a broad form of chronic inammatory diseases of the gingiva, bone and ligaments supporting the teeth. This study aimed to reveal the effect of undernutrition, using body mass index (BMI) and serum albumin level (Alb) on PDs and other risk factors as age, smoking and khat chewing. Methods: This was a cross-sectional study conducted at the faculty of dentistry, Sana’a University. Of 1920 patients attended to clinics, only 229 matched the study criteria. Oral examination was performed to assess the periodontal clinical parameters measurements. BMI and Alb was measured. Statistical analysis was used to present the association between categorical variables was assessed using Chi square test and Fisher-Exact test. ANOVA was used to assess the differences in the mean values of the quantitative outcomes. Chi square test was used to evaluate the association between BMI and age, gender, occupation, education level, smoking, khat chewing as well as BMI with PDs. Results: Most of participants (58.5%) were males and most of the study sample (91.3%) was at the age group of (18-35). Among all subjects, (81.2%) of cases were diagnosed with gingivitis. (60.7%) of study participants were mildly undernourished according to BMI. (93%) of participants showed normal Alb level. Regarding to habits, only (18.2%) of patients were smokers and more than half of participants (59.4%) were khat chewers. Conclusion: There was a relationship between PDs and undernutrition which was obviously seen between gingivitis and mild undernutrition.

The undernourished patients' weights were measured in Kilograms by using a mechanical scale while participants wore light clothes and without shoes. Moreover, the height of the participants was measured in Centimeters by using a measuring tape while a hard ruler was positioned horizontally over the head of the participant to ensure a stable base. BMI was calculated by using the following formula: BMI=weight (Kg)/height (m²). Blood samples were taken from each participant by a laboratory technician on the day of evaluation; samples were placed in special container then sent to the laboratory to measure Alb level. Standard Alb is from 3.5 to 5.5 gram per deciliter (g/dl).

Statistical analysis:
A power calculation was used to determine the minimum sample size required to establish signi cance. Sample size was calculated by using OpenEpi Info software, version 3, with con dence level 95% and an estimated error 5%. Data Analysis was undertaken using the Statistical Package for Social Science (SPSS version 16). Statistical analysis was used to present the demographic data of the study sample and diagnostic variables (IBM, Albumin level, and periodontal diseases) by frequencies and percentages. Association between categorical variables was assessed using Chi square test. Furthermore, Fisher Exact test was used when the assumptions of Chi square test couldn't not meet. Analysis of variance test (ANOVA) was used to assess the difference in the mean values of the quantitative outcomes (CAL). Chi square test was used to evaluate the association between BMI and age, gender, occupation, education level, smoking, khat chewing, as well as BMI with PDs. The signi cant level was set at P <0.05. Figures (Bar charts) were used to present the descriptive data graphically.

Results:
Of 1920 patients who attended oral medicine, diagnosis and periodontology clinic, Sana'a University, only 229 patients matched with the study criteria.
The present study showed that most of cases had a mild undernutrition (60.7%) and normal albumin level (93%). Regarding the periodontal diagnosis, most of the patients were diagnosed with gingivitis (81.2%), as shown in table (2).
In both groups, variables such as age of the patients, smoking, khat chewing and PDs were non-signi cantly associated with BMI, as presented in table (4).
Mild malnutrition was the most frequent category in the patients diagnosed with gingivitis. On the other hand, mild malnutrition was the least frequent category in patients diagnosed with aggressive periodontitis, as shown in gure (1).

Discussion:
This study aimed to evaluate the association between PDs and undernutrition in Yemeni population and the correlation between undernutrition and other risk factors including age, gender, level of education and habits as smoking and khat chewing.
The results showed that there were non-statistically signi cant association between PDs and undernutrition participants. Mild undernutrition was found in (60.7%) of study participants and gingivitis was diagnosed in (81.2%) of study participants. This association may reveal that the reason of gingivitis presence in most of the study sample was the presence of mild undernutrition that may cause a little effect on the immune response.
BMI is the most common non-invasive tests to assess malnutrition [33]. Alb is also a well-known marker of nutritional status [34]. Low BMI and Alb in both genders were not signi cantly associated with PDs. The literature has reported that the severity of undernutrition has massive effects on the immune system which plays a role in progression of immunode ciency [35]. There are many studies which clari ed that the pathogenesis of periodontitis is signi cantly related to the host response with microbial factors [30,[36][37][38] . The Cytokines, which are chemical mediators of in ammatory response, can be in uenced by nutrition as a related factor [39]. People with severe undernutrition are more susceptible to many microbial opportunistic infections [40]. Therefore, this may clarify why low BMI and Alb is not signi cantly associated with PDs as most of the participants were in a mild undernutrition conditions. Rodrigues et al., (2014) [41] published a positive correlation between hypoalbuminemia and periodontitis. A meta-analysis of 63 studies (2125 patients) discussed the effect of starvation on Alb and noti ed that the level of Alb remains normal before the patients reach the ultimate stage of starvation where undernutrition became physically evident [42]. In other words, hypoalbuminemia requires a more destructive in ammation and severe undernutrition to occur. Therefore, this may explain the non-signi cant relation between low BMI and Alb with PDs.
The present study showed that most of participants are between late adolescence and early adult and the majority of the samples were males (58.5%) similar to Degarage et al., 2015 [43]. This can be explained by the neglect behavior and the inability of males to take care of themselves specially those who are studying away from their families and cannot cook food. Regarding the occupation, most of participants were students (60.3%) and most of their education level was bachelor degree (49.8%). Among males group, age, education level and smoking were signi cantly associated with PDs (P=0.001, P=0.004, P=0.002; respectively). There is a high prevalence of khat chewing in Yemen 43.27% [44]. Khat chewing habits promote the development of other habits like cigarette smoking [45][46]. smoking is considered as one of the most or signi cant life style factors that is associated or linked to PDs. It is considered as a detrimental factor that in uence the occurrence and progression of periodontitis [47][48]. This can be explained by the Yemeni society lifestyle of chewing khat which is a common practice among high schools, colleges and university students, since it is considered as a mild stimulant that promote energy during working or studying [49]. Most chewers get a good degree of concentration and raise energy levels and awareness, promote imaginative ability and capacity to incorporate ideas, and enhance the ability to communicate especially among Yemeni males [50]. khat chewing caused obvious CNS symptoms such as loss of appetite (anorexia) and may be associated with the mixed effect of the central amphetamine-like with delaying of gastric empty and insomnia that leads to late waking up in the morning and a reduced activity performance caused by the central release of noradrenergic neurotransmitters [51][52]. Moreover, cathinone promotes or elevates the sympathomimetic activity that results in a late discharge of food from stomach [53]. This may explain why khat chewing can lead to malnutrition.
Poor oral hygiene among males is another risk factor of gingivitis. This can be due to the masculinity behavior of thinking that oral hygiene is not connected to men strength [54]. In contrast, chronic periodontitis presented in the older age [55] and persons of age 40 and above were four times more probably to have periodontitis than younger ages [56]. This may explain why the majority of the sample was diagnosed with gingivitis.
Among females group; age, level of education, smoking and khat chewing were signi cantly associated with the PDs (P=0.014, P=0.000, P=0.002, P=0.000; respectively) due to the previous reasons that explained in males group.
Limitation was the lack of knowledge of patient about the importance of BMI and Alb in diagnosing undernutrition which was an obstacle during conducting sample.

Conclusions:
In conclusion, the relationship between PDs and undernutrition was proven between gingivitis and mild undernutrition. There was a slight relationship between periodontitis and mild undernutrition. Khat chewing habit showed to be the most probable cause of undernutrition in Yemen. Author's contribution MA and MA conceived and designed the study, analyzed the data and drafted the manuscript. SA contributed to drafting the manuscript. All authors have read, reviewed and approved the manuscript.

Funding
There was no fund

Availability of data and materials
The datasets generated during and/or analyzed during the current study are not publicly available due to ethical reasons, but are available from the corresponding author on reasonable request.

Ethics approval and consent to participate
This study was approved by Ethical approval of the Human Ethics Committee of the medical faculty and health sciences of Sana'a University, Yemen was obtained. All subjects in this study provided written informed consent to participate.

Consent for publication
Not applicable.

Competing interests
The authors declare no competing interests.