Prevalence of self-reported halitosis and associated factors in 15 years old male students in Karbala City-Iraq

Background ׃ Halitosis is a common condition and is most often caused by a buildup of bacteria in the mouth because of gum disease, food, or plaque. It can result in anxiety among those affected, it is also associated with depression and symptoms of obsessive-compulsive disorder. This study aims to assess the prevalence of self-reported halitosis and associated factors (dental plaque, gingival condition and dental caries) in 15 years old male students in Karbala city in Iraq. Additionally, we studied adolescents’ concern with their own breath and whether anyone had ever told them that they had halitosis. Methods׃ A cross-sectional observational survey was conducted to15 years old high school students from public and private schools in the city of Karbala, Iraq. The random sample consisted of 400 adolescents from 44 schools. An interview with a structured questionnaire was administered along with measurement of oral parameters (PI, GI, DMF). Results׃ The prevalence of self-reported halitosis was 48.50% according to question one. The prevalence of halitosis according to the total score of the questionnaire was 86.5%. 13.5% reported that they didn’t have halitosis. It is concluded that there is a high prevalence of self-reported halitosis, which is associated with a socio-economic pattern. Most adolescents report a concern with their own breath. Dental plaque and gingival status are associated significantly with self-reported halitosis. The high prevalence of self-reported halitosis according to the questionnaire among the students may be due to the consumption of garlic or spicy food, besides, dental plaque, gingivitis and dental caries cause an increase in volatile silver compound level which cause an increase in halitosis. Conclusion׃ Self-reported halitosis is a prevalent situation in about 50% of adolescents in Karbala city. Patients’ self-reported halitosis is found to be associated with dental plaque, gingivitis and dental caries. Keywords׃ Halitosis; adolescent; prevalence. (Received: 15/1/2021, Accepted: 24/2/2021)


INTRODUCTION
Halitosis is a state in which respired air is offensively changed both for patients and for people with whom they communicate (1) . It distresses millions of people around the world, although its prevalence fluctuates, seemingly elicited by the shortage of oral hygiene and a disorganized lifestyle. It can cause social restrictions, interfere in the quality of life, and maybe a gauge of important systemic diseases. In most societies where halitosis is prevalent, people look for solutions, usually due to the discomfort or embarrassment to which they are subjected (2) . One of the aims for studying halitosis is its social impact as a result of patients feeling unconfident in social, professional and family contacts. It may also affect the quality of life and cause embarrassment to people relating to the individual with bad breath. The measurement of volatile sulfur compound (VSC) concentrations in the exhaled air to assess halitosis is the only method used in some studies.
The results of these surveys have a different meaning from studies that determine the percentage of people who report having halitosis by a questionnaire (1) . Both conclusions are meaningful to understanding the issue, but observation through VSC monitors is considered a surrogate conclusion (measure the disease route, and in general it is therapy centred) (3) , whereas self-reported awareness of halitosis is documented as a true outcome. Epidemiological observation taking into consideration both types of outcomes provides important information and allows broader acceptance of the issue (1) . Adolescence is the evolution period between childhood and adulthood and is categorized by several changes in biological, psychological and social development (4) . Adolescents are subject to several health linked signs, including halitosis, which exceeds the biological scope, affecting the social scope and possibly hurting the physical and psychological health of affected individuals (5) . Furthermore, the presence of halitosis may indicate incidence of important systemic diseases requiring crucial diagnosis and treatment. Nevertheless, in Iraq there are limited papers on adolescents, and still fewer on adolescent halitosis.

MATERIALS AND METHODS Study design/study setting
This study was a cross-sectional study that was carried out during the period between December 2019 and February 2020. The survey was conducted among secondary schools in Karbala City-Iraq. The age was taken according to the criteria of the World Health Organization (1997) and according to the last birthday. The size of the sample composed of 400 students who were randomly selected from 5477. ❖ (The students with the systemic disease were excluded, besides, students in the study were free of: a) Medical history of infectious diseases. b) Malocclusion and draining fistulas associated with chronic alveolar abscesses. c) Usage of any chemical form of plaque control. d) Presence of crowding/overlapping of teeth. ❖ The children were examined by the single calibrated examiner for the following clinical parameters: 1. Self-reported halitosis by questionnaire.

Questionnaire
A well-made format (questionnaire) was designed from previous studies (2,8,9,10) and administered to the students who meet the criteria The questionnaire was tested in a pilot study on 100 male students and validity and reliability was adopted, the questionnaire was adjusted in the light of pilot responses. The questionnaire was anonymous (no identification of an individual was possible). The questionnaire originally formulated in English, subsequently translated into Arabic and then retranslated into English, and ethical approval was achieved from the ethical committee in the college of dentistry and from the psychological department of the Faculty of Arts in Baghdad University.

Statistical analysis
Data were translated into a computerized database structure. An expert statistical counsel was sought.

RESULTS
The prevalence of halitosis among 400 students aged 15 years of male's secondary schools in Karbala city/Iraq was 48.50% according to question one, as seen in the table (1). Regarding question one of the self-reported questionnaire of halitosis, as illustrated in Table 2, the mean value of plaque index and gingival index among students with halitosis is higher than those with no halitosis, which was statistically significant, (P<0.001). The findings of plaque index regarding the selfreported questionnaire of halitosis were illustrated in Table (3), the mean values of plaque index among students with halitosis were higher than those without halitosis, the higher mean value was recorded in question (4), which was asking the students if their breath interfered with social life. These findings were statistically significant, (P<0.001).
Similarly, the mean value of the gingival index among students regarding the self-reported questionnaire of halitosis, was seemed to be higher in students with halitosis than without halitosis, ( Table 4). The higher mean value was recorded in question (3), which was asking the students about receiving any professional treatment for halitosis. This finding were statistically significant, (P<0.001). However, the last question (Q7), which asked the students If they take any measures against halitosis, the difference observed failed to reach the level of statistical significance (P>0.05).

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Vol. 33(1), March 2021 Prevalence of self-reported , similarly the mean differences of DS were statistically significant concerning questions (4,5,6), likewise the FS mean differences were statistically significant concerning question (5), and the mean differences of DMFS were statistically significant concerning question (5,6,7) (P< 0.001). On the other hand, other findings were statistically not significant (P> 0.05).

DISCUSSION
In the present study, 400 students of 5477 aged 15 years old were selected randomly from 44 males' secondary schools in Karbala city/Iraq, to measure the prevalence of self-perceived halitosis in secondary schools' students aged 15 years, as no previous Iraqi study on halitosis was done in this area for this age. The selected student was interviewed in an isolated room in each school to ensure privacy and to avoid embarrassment while answering the questionnaire, and all the oral parameters including dental plaque, gingival condition and dental caries. Plaque Index of Silness and Löe (1964) (6) and Gingival Index of Löe and Silness (1963) (7) were used to assess dental plaque and gingival health condition, respectively. These indices were used due to their flexibility, which provides the possibility of selection of index teeth for examination rather than the whole dentition and keeps the duration of examination to a minimum; in addition to their ease of application (11). The age and gender were stationary, as age was not a risk factor for the increase in the level of VSCs (12) . Multiple regression analysis revealed that male gender was the only variable showing a significant relationship with higher questionnaire scores. These findings corroborate previous studies showing the predominance of halitosis in male children aged 6-9 years, 6 -16 years (13) , and 7 -15 years (14) . However, a study carried out in Israel (15) , showed no difference between the sexes in the 5 -14 age group, nor was there a difference in the adult population (9) . However, some studies have found a higher prevalence of halitosis in women (16) . It is difficult to determine the actual influence of factors such as age and gender on halitosis, since breath odor may be influenced by many factors such as periodontal and dental status, dental hygiene, tongue coating, smoking, nutrition, level of education, and medication (17) . Self-assessment or self-perception of halitosis is a highly relevant outcome since it involves the individual in the process and makes him/her understand the importance of the condition (18) . it is safe to assume self-perception as a true patientcentered outcome, which is highly recommended in present research in the health field 6 . In the present study the overall prevalence of halitosis according to the questionnaire (depending on the answer of question one which inquired the students if they have had bad breath to assess the awareness of the students about halitosis), the result was approaching fifty percent, this was almost similar to the results reported in Qassim, Saudi Arabia (19) , which is also lower in comparison to a study done in Kinondoni (2013), but at the same time is higher J Bagh College Dentistry Vol. 33(1), March 2021 Prevalence of self-reported than the findings reported in other populations especially Brazil (8) , USA (1996) (20) . In these studies, the gender had no statistically significant association to the outcome with similar methodology (8) , so the result of the current study could be compared with these studies. The prevalence of halitosis according to total score of the questionnaire was 86.5% higher than the prevalence of halitosis in Jordanian population which was 78% (10) , this may be due to the overall poorer oral hygiene, or the assumption by other authors that halitosis might be an underestimated oral health problem in the general population may be true (21) , or living in low-middle income countries (22) . The high prevalence of periodontal diseases in low-middle income countries might cause the greater prevalence of halitosis, in addition the intake of volatile foods such as spices and garlic may lead to change in breath odor, and consequently halitosis, another cause for the great prevalence of halitosis is the dryness of the mouth which plays an important role in the formation and perpetuation of halitosis (23) .
Plaque, composed of bacteria and salivary proteins, is one sulfur source in the oral cavity. In an epidemiological study conducted among the 2000 Chinese population, plaque index is significantly correlated with VSC values (12) . This finding was agreed with the data presented in this study, in which the plaque index was associated   (24) , this was inconsistent with the findings of Liu et al. (2006) and  (plaque index). Gingivitis is reversible and infrequently developed to periodontitis in children and adolescent except in special circumstances like aggressive periodontitis and periodontitis associated with systemic diseases (25) . In the current study the finding is consistent with Liu et al. (2006) (12) , Kara et al. (2006) (26) , P. S.   (27) , Al-Saidy (2013) (28) , Ziaei N (2019) (29) and Alzoman H. (2020) (30) . Although halitosis is possibly not caused by periodontal disease, there is ample proof to suggest that periodontal disease increases the severity of halitosis with higher production of volatile sulphur compounds (27) . This can be explained as periodontal conditions favour bacterial growth and retention of debris, besides, the blood decomposition products can themselves produce Sulphur containing peptides and amino acids that are the source of volatile Sulphur compounds. However,   (31) reported no association between halitosis and periodontal condition. In the present study, there was a highly significant association between dental caries experience represented via DMF index and self-reported halitosis, which was in agreement with CM Kayombo (2017) (20) . The findings were opposing with those of Miyazaki et al. (1995) (32) ,   (31) and Liu et al. (2006) (12) . Glucose

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Vol. 33(1), March 2021 Prevalence of self-reported and sucrose can constrain the enzymee activity of salivary peptides by making an acidic environment (33) . Therefore, an acidic condition created by dental plaque may destroy VSC production. However, Nalcaci et al. (2008) (34) found that the prevalence and severity of dental caries had a significant role in halitosis, as an increase in DMFT indicates an increase in caries and a low oral hygiene level, and it seems rational that this may increase the chance of halitosis. Previous studies have shown that this is true (29) , this was a result to increase the incidence of unidentifiable Gram-negative rods, Gram-positive rods and Gram-negative coccobacilli, the increase in species diversity found in halitosis samples proposes that halitosis may be the result of complex collaborations between several bacterial species (35) .

CONCLUSION
Patients' self-reported halitosis was found to be associated with dental plaque, gingivitis and dental caries. The existing findings suggest that a selfreported questionnaire of halitosis can be used to judge one's halitosis.