Risk Factors, Diagnosis, and Management of Halitosis in Children: A Comprehensive Review

Prevalence of Halitosis in Children

The prevalence of halitosis among the pediatric population has been investigated worldwide with varying estimations, between 5% and 76.3%,⁵ attributed to differences in factors, such as sample size, diagnostic methods, and age-groups considered.^16–20 A study in Italy by Villa et al. reported a prevalence of 37.6% of halitosis among 101 children of 6 to 16 years of age.¹⁶ Patil et al. conducted a study on 900 Indian children of 7 to 15 years of age and found a prevalence of halitosis in 40.9% with a significant association between age, oral hygiene status, and mouth breathing.¹⁷ While Kanehira et al reported 8% of 119 Japanese children with halitosis wherein mouth breathing was a major contributing factor;¹⁹ on the contrary, Ueno et al. reported 44.9% with halitosis in 768 Japanese children of 6 to 15 years of age, wherein a significant score of tongue coating was considered a contributing factor for halitosis.²⁰ Nalçaci et al. reported a prevalence of 14.5% in 628 Turkish children of 7 to 11 years with halitosis, significantly associated with the severity of dental caries.²¹ Therefore, irrespective of the contributing or associated factors that differed for halitosis among the geographies, its dominant prevalence among the pediatric population was undeniable.

Associated Risk Factors for Halitosis in Children

Numerous studies have evaluated and reported statistically the significant presence of certain oral and extraoral factors with halitosis, which is routinely encountered in the pediatric population. The literature has documented the prevalence of mouth breathing habit among the pediatric population (50–56%)²² and has analyzed the relationship between mouth breathing and halitosis. Mouth-breathing habit as a primary entity leads to the changes in salivary flow patterns and water imbalance, resulting in the surface dryness of the oral mucosa, thereby contributing to halitosis. Further, conditions such as dental caries, periodontal diseases may have a positive association with mouth breathing; chronic allergies, nasal, and throat infections may be associated with mouth breathing, all of which may directly or indirectly contribute to halitosis in their own respective ways.²³ Studies by Motta et al.,¹⁵ Kanehira et al.,¹⁹ and Alqutami et al.²⁴ have reported a significant increase in halitosis among mouth breathers.

Other significant oral contributing factors, such as poor oral hygiene, periodontal diseases,^25–28 tongue coating,^{17,20,26–29} dental caries, and proximal restorations,^25,30,31 pose as a risk factor in the development of halitosis in the pediatric population. Fissured tongue presents as a high risk of bacterial and food lodgment within the fissures and, therefore, enhances the tongue coating.³² Further, Ueno et al. stated in their study that children with 2 or 3 score of tongue-coating thickness were 3.28-fold times more prone to present with halitosis than with score 0 and 1 thickness of tongue coating, which can be considered as a significant risk factor.²⁰

Though studies have reported a positive association between orthodontic appliances and halitosis,^33,34 however, contradicting to former results, Keris et al. reported a negative association of fixed and removable space maintainers with halitosis.³⁵

Dinc et al. investigated the presence of halitosis in 40 children of 5 to 15 years of age diagnosed with adenoid hypertrophy and whether adenoidectomy decreased it. They concluded that there was a significant association between them and treatment did present with an improvement of halitosis. They further suggested that in children with no other oral pathologic etiology for halitosis, adenoid hypertrophy needs to be evaluated.³ Therefore, this helps us to understand the multifactorial origin and association of halitosis with the risk factors evaluated.

Diagnosis of Halitosis in Children

Halitosis assessment methods are crucial as they help to detect its presence, classify the type of halitosis, its severity, and thereby determine the treatment protocol to be followed accordingly.⁶ These diagnostic aids range from simple to complex, being subjective to objective, and used unsophisticated to sophisticated equipment.^6,8,10 Common diagnostic aids, such as organoleptic measurement, sulfide monitoring, gas chromatography, BANA test, and chemical sensors and not so common methods, such as quantifying β-galactosidase activity, salivary incubation test, ammonia monitoring, and ninhydrin method are used in detecting halitosis presence, differentiate pseudohalitosis and halitophobia, and also assess the severity of halitosis.⁶ However, studies on the pediatric population have reported the routine use of organoleptic measurement, sulfide monitoring, and gas chromatography in halitosis assessment.^{17,19,20,25,26,29,31} Another important factor to be noted was the questionnaire assessment on the presence of halitosis in children either by caregivers or self-evaluation, which was an additional factor evaluated commonly in some studies.⁵

Organoleptic assessment, a sensory test,¹³ is defined as a method that can measure the strength of target odors and expresses the value in terms of a point or number with reference to a predefined organoleptic scale. It is the oldest, simplest method where the quality of the mouth and/or nasal air will be assessed organoleptically by a calibrated odor judge,^6,36 from a specific distance and scored on a scale from 0 to 5 points. Though simple test yet faced with low reproducibility, the requirement of trained breath assessor, disease transmission risk, and test specificity are a few of its limitations.^9,11

A sulfide monitor, an objective test, analyzes the total sulfur content of the patients’ mouth air.¹³ Halimeter^® (Interscan, Chatsworth, CA, USA), introduced in the early 1990s, is portable, chair-side equipment, where a reading less than 100 ppb is normal while 100 ppb or more is considered as halitosis. Though it has a relatively cost-effective value,³⁷ it has a high sensitivity for hydrogen sulfide, yet low sensitivity for methyl mercaptan; false-positive readings due to other volatile vapors, such as acetone, ethanol, and methanol, are its limitations.^13,38,39

A gas chromatograph is a sophisticated device that analyzes exhaled breath and can detect a wide range of odorous compounds and is considered by many studies to be the method of choice for differentiating and quantifying major halitosis-associated VSCs.¹¹ The analysis of VSCs by gas chromatography is considered to be the most reliable measurement for the diagnosis of intra- and extraoral halitosis by detecting even low concentrations of VSCs to distinguish the origins of halitosis.^6,11 Conventional gas chromatography is a relatively expensive, massive, and large apparatus that requires trained and experienced technicians and specialists.⁴⁰ A small, portable version of conventional gas chromatography known as OralChroma^™ (Oral Chroma^™, Abimedical, Osaka, Japan) became available in 2003,⁴¹ wherein on evaluation, the concentration of each VSCs appears on the screen and halitosis is considered present if one or more of the VSCs gases exceeded the following cognitive threshold: (H2S) > 112 ppb, (CH₃SH) >26 ppb, and (CH₃SCH₃) >8 ppb.^34,42

Villa et al. assessed halitosis in 101 children with the portable sulfide monitor and Halimeter^®;¹⁶ Guedes et al. considered organoleptic test in his cross-sectional study on 150 children;⁴³ Dinc et al. assessed halitosis in 40 children with adenoid vegetation using the portable gas chromatograph OralChroma;³ Keceli et al. determined halitosis in 151 children using both the organoleptic and sulfide monitoring;²⁹ Motta et al. used the Breath Alert^™ on 55 children to assess halitosis;¹⁵ and Ueno et al. considered organoleptic assessment method for detection of halitosis in 768 children²⁰ and so on. Some studies have even evaluated the differences between the tests for halitosis and their significant relationship in the pediatric population. In a study by Petrini et al., 50 children were assessed for halitosis using organoleptic test and quantification of salivary β-galactosidases, wherein they reported that the salivary β-galactosidases level was significantly related to organoleptic scores along with other clinical evaluated parameters.⁴⁴ Lin et al., compared organoleptic test and Halimeter^® on 30 children, wherein the results were inconsistent. The authors concluded that their results may suggest the involvement of other factors for halitosis in the pediatric population.²⁵ These above-cited studies and more documented in the literature help us to understand the different methods used for the detection of halitosis in children.

Management of Halitosis in Children

Identification of the presence of halitosis, followed by the type and its severity allows for an effective management protocol. The presence of microorganisms in the oral cavity and their role in the etiology of halitosis are well-documented. Also, poor oral hygiene, tongue coating, dental caries, gingivitis, periodontitis, and periodontal abscess wherein the microorganisms’ role is undeniable may contribute to halitosis. Therefore, the primary aim of the management in such a scenario would be mechanically reducing the load of the microbial biofilm by enforcing a good oral hygiene regime, such as routine toothbrushing, flossing, tongue cleaning, and mouth rinses.^9,26–29,45 It is also advisable to inculcate the habit of swishing the mouth after eating in children at a young age as a regular practice that would reduce food lodgment, microbial load, and even halitosis caused due to dietary foods, such as onion, garlic, to name a few. At times, the basic protocol followed as above is mostly successful in reducing halitosis to a greater extent in the pediatric population.

Addressing underlying evident pathology for halitosis follows the next step. Nonsurgical periodontal therapy comprising scaling, restoration of decayed teeth, and periodontal and pharmacological treatment as advised based on the oral examination findings is recommended by the practitioners. This would also aid in the reduction of the oral microbial load responsible for halitosis. In children with mouth breathing, identification of the possible etiological factors such as adenoid hypertrophy would aid in addressing the related halitosis.³

The literature documented that most of the children, who were assessed for halitosis, were of genuine halitosis with predominant oral pathologic causes; however, the severity did vary among them. Amir et al. reported a reduction in halitosis after providing oral hygiene instructions to the 24 children recruited in their study.²⁸ Similar results were recorded by Nalçaci and Sönmez, whereupon improving oral hygiene and controlling gingival diseases in 30 caries-active children, a reduction of halitosis was noted.²¹ Kara et al. reported that the oral hygiene instruction and periodontal scaling were successful in reducing halitosis in 150 Turkish children.²⁷ Keceli et al. reported significant reductions in both the VSC levels and organoleptic scores after instructing tongue brushing and a good oral hygiene in 69 children.²⁹ In a study by Yilmaz et al., the authors reported that H. pylori eradication was beneficial in the treatment of children with a positive H. pylori antigen test and with halitosis.⁴⁶ Similarly, Hoshi et al. and Sayedi et al. reported metronidazole effectiveness in children halitosis.⁴ Recently, AlMadhi et al. investigated the pre- and posteffect of full mouth rehabilitation on 57 children under general anesthesia on halitosis and reported a significant reduction of VSCs level in more than 50% of the sample measured by OralChroma^™.^31,47 Lastly, the importance of providing instructions and counseling to maintain a good oral hygiene to the caregivers and the children cannot be emphasized more, as they are the basic steps in the treatment protocol to be followed in the management of halitosis.