A Narrative Review of the Diagnosis, Etiology, and Treatment of Halitosis Over the Past Three Decades

Stuart J. Froum, DDS; Ye Shi, DDS; Natacha Reis, DDS; and Tanatorn Asvaplungprohm, DDS

The term "halitosis" was coined in 1874 by Dr. Joseph William Howe in his book, The Breath and The Diseases Which Give It a Fetid Odor.¹ "Halitosis" comes from the Latin word "halitus" ("breath") and the Greek suffix "-osis," which means a diseased state.² The Oxford English Dictionary defines halitosis as, "A condition in which the breath smells unpleasant."³

While this condition has been identified for about 150 years, recent interest in halitosis has grown because of the need or even requirement in some locations for people to wear a mask due to the COVID-19 virus. Basically, whenever indoors, whether in supermarkets, on buses or subways, and in offices (except in some instances when the surrounding people have been vaccinated), people have been wearing masks. A television news broadcast in May 2020 aired a segment called, "Bad breath behind the coronavirus mask? 10 reasons and remedies for your halitosis."⁴ A 2021 review article listed halitosis as one of the oral manifestations of COVID-19.⁵

Most people experience oral malodor even occasionally in their lives. According to the National Institute of Dental Research, approximately 65 million Americans have halitosis at some point during their lives. Moreover, at least 50% of the population has persistent effects of oral malodor, and half of these people suffer from a chronic problem. Oral malodor is considered the third cause of dental office visits, behind dental caries and periodontal diseases.⁶

The worldwide prevalence of halitosis ranges from 22% to 50%, with the highest percentage being when self-reported. This wide discrepancy is due to perception, self-perceived, and diagnostic tools influenced by race and cultural differences.^7-9 There is an increase of halitosis associated with age; however, there is no relationship between the severity of halitosis and gender.¹⁰ In addition to a lack of studies on prevalence, the data on prevalence may be inaccurate due to differences in methodologies among studies and to a high number of self-reported cases not considered to be true halitosis.⁶

The recent interest in halitosis due to mask wearing during the pandemic prompted the authors to examine the problem over the past 30 years, focusing on its diagnosis, etiology, and treatment, and whether any or all of these three aspects changed during this time. The purpose of the following narrative review was to examine the published literature concerning halitosis over the past three decades and discuss the diagnosis, etiology, and treatment of the disease.

Material and Methods

An electronic search was performed in PubMed, MedLine and Google Scholar databases using the following keywords: "halitosis" AND/OR "oral malodor" AND "etiology" AND "diagnosis" AND "treatment." A total of 2,083 articles were found. However, the search results were limited to articles published from 1990 to 2021 in the English language only with full-text access. In addition, the search results were restricted to systematic reviews, reviews, meta-analyses, randomized controlled trials, controlled clinical trials, clinical trials, case series, and case reports, only in humans. The inclusion criteria resulted in 136 articles included in this review of the literature, according to their relevance that was decided by authors' agreement (NR and TA).

The review was divided into four parts: diagnosis, method of measurements, etiology, and treatment.

Diagnosis

The diagnosis of halitosis should begin with the recognition of the problem by the patient or a close confidant of the patient. Determining the cause of halitosis requires a rigorous medical history and physical examination and knowledge of the possible etiology. In 1992, three separate diagnostic groups were considered when diagnosing halitosis: non-pathologic causes, pathologic causes, and, lastly, psychiatric conditions and psychosomatic halitosis.¹¹ However, a systematic classification to distinguish and diagnose halitosis was not established until 2000 by Yaegaki and Coil.¹²

This classification of halitosis includes categories of genuine halitosis, pseudo-halitosis, and halitophobia (Table 1).^12,13 Genuine halitosis is defined as obvious malodor beyond socially acceptable levels. It can be perceived by patients and quantified with measuring methods. Genuine halitosis is subclassified into physiologic halitosis and pathologic halitosis. Physiologic halitosis is described as malodor that arises through putrefactive processes within the oral cavity without any related pathologic condition. The origin of physiologic halitosis is mainly the dorsoposterior region of the tongue.¹⁴ Temporary halitosis due to dietary factors is excluded from physiologic halitosis even if there is no pathologic condition observed. Pathologic halitosis is subclassified into oral pathologic halitosis and extraoral pathologic halitosis. True pathologic etiology is found in this type of halitosis. Pseudo-halitosis is the condition in which patients stubbornly complain of the existence of oral malodor, but it is not perceived by others.

Halitophobia is the condition in which patients continue to insist that they have halitosis even after they have been treated for genuine or pseudo-halitosis without any physical or social evidence suggesting the presence of halitosis. The condition of halitophobia was confirmed in a study that showed those with a primary complaint of halitosis have a lower percentage of true halitosis than those with secondary complaints.¹⁵ This classification not only clearly demonstrates the different etiology and origin for each type of halitosis, but also allows the clinician to diagnose a psychological condition that may be present. It still remains the most cited and acknowledged classification.¹²

Measurement

Due to the classification of pseudo-halitosis and halitophobia, the method of measuring halitosis is important for accurate diagnosis and effective management. To date, six major measurements have been used: self-assessment, organoleptic assessment, gas chromatography, sulfide monitor, microbial quantification, and tongue coating status. Each has its own advantages and disadvantages (Table 2).^16-32

Since 2000, another measurement by chemical sensor, called "electronic nose," has been used both clinically and in research. The sensor is integrated into a probe and can perform measurement in periodontal pockets and on the dorsum of the tongue. The probe, which is 0.25" x 0.75" in size, is applied with light pressure at the test sites. Electrochemical voltage from the sulfide sensing monitor of the probe is generated in relation to the amount of sulfide ions. It has demonstrated results very comparable to organoleptic readings and gas chromatography measurements.^17,33-35 Currently, chemical sensor is the most promising alternative method for both research and clinical purposes. In early 2000, another testing method, the cysteine challenge testing, was utilized to test the efficacy of intervention to reduce malodor in multiple studies. Subjects were instructed to rinse with cysteine to create malodor, and interventions were applied to determine which method could reduce the malodor created from cysteine rinse.³⁶ In 2017, another method of measurement using copper or molybdenum oxide sensors, which have a high affinity and sensitivity to hydrogen sulfide, began gaining increased acceptance and use as a diagnostic tool for halitosis.³⁷

Additional indirect methods for measuring halitosis have been proposed and documented such as the BANA test, which detects the presence of proteolytic obligate gram‐negative anaerobes, primarily those that form the red complex.The test strip shows a blue color in 5 minutes if the results are positive. It is user-friendly and can show a strong positive correlation with periodontal disease activity.³⁴ Other tests include quantifying b‐galactosidase activity,³⁸ lead acetate,²² ammonia monitoring,³⁹ ninhydrin method,^39-41 polymerized chain reaction, and more.⁴² These tests have been found to strongly correlate with standard volatile sulfur compound (VSC) and organoleptic scores, suggesting that they can serve as alternatives to other measurements.

Etiology

Halitosis has a multifactorial etiology. Understanding the etiology of halitosis is not only important for diagnosis but also for formulating multidisciplinary treatment. Another classification of halitosis reveals the complex etiologies of this disease, which can be divided into non-pathologic/physiologic causes, pathologic causes, and psychiatric causes (Table 3).^18,43,44

Genuine halitosis can originate either intraorally or extraorally; however, approximately 80% to 90% of malodor cases originate from the oral cavity.^18,43-48 Intraorally caused halitosis can be attributed to three main factors: host (salivary flow, topography of the tongue, external factors such as stress), bacteria, and substrate.¹⁹ Substrate can be exogenous (food) or endogenous (saliva).^19,28,49-52 Saliva plays an important role in halitosis formation. Depending on the oxygen supply, the substrate provided, the flow rate, and the pH level, saliva can inhibit or favor halitosis production.^{28,45,49,50,53} The main cause of halitosis, however, is the accumulation of gram-negative anaerobic bacteria from tongue coating and subgingival plaque, which generate VSCs as microbial degradation products.^43,45 The association between anaerobic bacteria that produce VSCs and halitosis has been well‐documented since the 1990s.^49,54 In the 1990s, the etiology was thought to mainly consist of the three VSCs-hydrogen sulfide, methyl mercaptan, and dimethyl sulfide-with the first two gases contributing to 90% of the VSC in exhaled air.^43,49,50 Since 2000, more compounds have been found to be associated with malodor. These include five groups: volatile aromatic compounds, short-chain fatty acids, alcohols, volatile aliphatic compounds, and aldehydes and ketones. However, hydrogen sulfide has a low threshold and high odor power, so the treatment is usually focused on this gas.^51,52,55

Physiologic halitosis, as a subclassification of genuine halitosis, is so-called foul morning breath, affecting approximately half of adults.^28,56 It is transient, occurs regardless of oral health status, usually is less intense, and can fluctuate at different times of the day.^43,50,53,57 Its origin is mainly the dorsoposterior region of the tongue where the microbial putrefaction of food debris, desquamated cells, saliva, and blood are aggravated by the reduction of salivary flow during sleeping at night.^19,50 The rough surface of the tongue with a complex papillary structure is a reservoir for anaerobic gram-negative bacteria, which are proficient at producing VSCs from food and epithelial debris. Clinically, higher tongue coating scores are strongly associated with more severe halitosis.^18,47,56 Other physiologic causes of halitosis are hormonal changes, especially in women, some types of foods, such as garlic, onions, choline, those containing animal fats, curries, durian, spices, etc., or habits like smoking and drinking alcohol.^18,19,45,50

Pathologic halitosis, as the other subclassification of genuine halitosis, can have both intraoral and extraoral etiologies and is more intense than physiologic halitosis.^43,50 Intraoral halitosis has odor proliferating from only the mouth, while extraoral halitosis has odor coming from both the mouth and nose.^46,47,54

Intraoral sources of halitosis are listed in Table 4.¹³ Many studies have shown periodontal health to have a direct correlation to halitosis.^{8,28,49,56,58,59} Patients with periodontitis are three times more prone to halitosis and have eight times more VSCs and four times more tongue coating.^8,49 The incidence of halitosis in elderly people can be due to higher prevalence and severity of periodontal disease.⁴⁹ Patients with chronic periodontitis and deep periodontal pockets suffer from halitosis due to higher amounts of gram-negative anaerobic bacteria, accumulation of debris, and increased putrefaction. The microbiological link between halitosis and periodontal disease is that the main microbial (anaerobic gram-negative) generating VSCs is present in the latter. In addition, coating of the dorsum of the tongue by subgingival bacteria and gingival fluid are also factors promoting VSCs.^{8,19,28,56,58,60}Other odontogenic conditions associated with halitosis can cause retention of food debris, including deep caries, poor restorations, fixed orthodontic appliances, and overwearing of acrylic dentures at night; conditions that cause wound infection, such as a dry socket or foreign graft material exposure, also are culprits. Additionally, several mucosal lesions are oral sources of the disease.^18,47,48,61 The absence of saliva or hypofunction causing dry mouth (xerostomia) will result in an increased bacteria accumulation and microbial putrefaction, which will increase VSCs.^50,60,62 However, from 2010 on, dry mouth has generally been considered a risk or predisposing factor rather than an etiology of halitosis.⁴⁷

Extraoral sources of halitosis are listed in Table 5.¹³ Although approximately only 10% of halitosis cases have an extraoral origin, it is still important to understand the potential sources to complete a proper diagnosis and treatment plan.⁶³ As most authors in the 1990s suggested, main origins are the ear/nose/throat region, with the most common origin being the tonsils⁶⁴ followed by the pharynx and sinus due to the presence of streptococcal species.⁶⁵ The lower respiratory tract is a source of the problem due to inflammation or infection,⁶⁶ trapped foreign bodies are a less frequent cause, and metabolic or gastric dysfunction is a rare cause.^28,43,45,50 Since 2000, however, more studies have shown the relationship between gastrointestinal disease and halitosis, especially gastroesophageal reflux disease (GERD) and Helicobacter pylori, both of which are common diseases.^19,48 Although much less common, some metabolic disorders also can cause halitosis. In these systemic diseases, odiferous agents circulating in the bloodstream can be exhaled through alveolar gas exchange and cause halitosis. This is also known as blood- borne halitosis. The dimethyl sulfide of the three VSCs is the main contributor to extraoral or blood-borne halitosis.^46,48,62 The systemic diseases inducing halitosis include uncontrolled diabetes, pancreas, liver, and renal dysfunction, and the genetic metabolic disorder trimethylaminuria (fish odor syndrome).^28,66 More rarely, halitosis can arise as a side effect of medications containing a dimethyl sulfide structure that can appear in breath.¹⁸ In 2020, medications causing halitosis were categorized into 10 groups: acid reducers, aminothiols, anticholinergics, antidepressants, antifungals, antihistamines and steroids, antispasmodics, chemotherapeutic agents, dietary supplements, and organosulfur substances.⁶⁷ The malodor varies according to the systemic condition: diabetic ketoacidosis is presented with fruity odor, bowel obstruction produces a fecal odor, chronic renal failure produces an ammonia- or urine-like odor, and hepatic cirrhosis produces a musty odor.^43,45,48,50

Delusional/hallucinatory/imaginary halitosis is caused by psychiatric disorders; it is also known as pseudo-halitosis or halitophobia.^28,62 These patients complain of bad breath, however, after rigorous clinical examination, history taking, and halitosis treatment, the symptoms persist and are not detected by other people.^43,45,47 These types of halitosis can be caused by mineral and vitamin deficiencies changing the person's taste buds and sense of taste, structural anatomical injuries and abnormalities causing taste disorders, neurodegenerative diseases, or exposure to some types of chemicals.⁶² Patients experiencing imaginary halitosis can demonstrate specific behaviors such as covering their mouth and keeping distance from others. However, it is difficult for these patients to accept the relation between their halitosis and their psychological condition. The clinician, therefore, should try to convince the patient, without being argumentative, to see a specialist in psychology.^28,47,48

Treatment

The first step in the treatment of halitosis is to determine the etiology, then treat accordingly.^18,68-70 A thorough medical, dental, and dietary history will help in establishing an accurate diagnosis and effective treatment plan.⁶⁹ Treatment can be specified according to the extraoral or intraoral cause. Halitosis, however, can also have a detrimental effect on a patient's psychological status. Therefore, it is important to include psychological intervention if needed.⁷¹

Since the 1990s, treatments have included dental treatment, mouthrinses, dentifrices, tongue scrapers, masking agents, behavioral modification, and herbal treatments as described in Table 6.^{15,18,35,70-104} The combination of mechanical and chemical modalities, however, is the most effective and potent treatment for halitosis.^105-108

In the late 2000s, the concepts of vaccine therapy and photodynamic therapy (laser) were introduced.¹⁰⁹ However, laser treatment was found to be inferior to regular scaling/root planing treatment for malodor reduction in patients with periodontitis.¹¹⁰ In 2009, an oral function program that included facial and tongue muscle exercises, salivary gland massage, and education about oral anatomy was utilized and proved to effectively reduce halitosis and improve salivary flow and overall speech pronunciation.^111,112 After 2010, newer halitosis treatments included lactoferrin and lactoperoxidase tablets.¹¹³ A review by Scully and Greenman also included metronidazole in the management of persistent halitosis cases.¹³

In a more recent review in 2016, the authors developed a management strategy based on the type of halitosis, as shown in Figure 1.¹¹⁴

Alternatively, oil pulling has been comparatively effective in reducing malodor in many randomized controlled studies. The mechanism behind oil pulling is that microbes with hydrophobic coats adhere to oil droplets and are expectorated along with the oil. Rice bran oil and sesame oil showed effects comparative to chlorhexidine in reducing halitosis.^115-117

The treatment of halitosis has been consistent over the past three decades; only in the last decade has probiotics been advocated as an effective treatment. A recent study indicated that daily consumption of probiotic tablets could help to control halitosis.^118-126 Although probiotics did not create permanent colonization, the lasting effect of probiotics could range from 3 days to 2 weeks.¹¹⁹ In 2019, the concept of prebiotics, carbohydrates in the form of fibers, was used along with probiotics in the treatment of halitosis and was shown to successfully reduce halitosis parameters tested in a study.¹²⁵ Another study used Escherichiacoli to successfully treat gut-caused extraoral halitosis.¹²⁷ Despite probiotics leading to improved halitosis parameters in many studies, different strains and vehicles have been used, contributing to the need for more standardized research regarding the topic.^122,123 In 2018, significant reduction in halitosis parameters was shown after rapid maxillary expansion treatment.¹²⁸ In 2019, ozone was proposed to be delivered in either gas form, water form, or oil form to kill bacterial pathogens contributing to halitosis.¹²⁹

Another emerging trend since 2010 is photodynamic or laser treatment. Laser therapy for halitosis treatment involves light-sensitive dye (photosensitizer), a light source with high power energy, and oxygen. The combination will create reactive oxygen species and result in bacterial cell death. Laser treatment was found to produce short-term resolution of halitosis after a single treatment.^130-136 A systematic review reported that laser therapy can be an effective adjunct to mechanical debridement, but its effectiveness requires further study.¹³⁶

A Cochrane review that included multiple studies mentioned in the present review reported that most studies have a low level of evidence, and, consequently, a conclusion cannot be made as to which intervention is the most effective.¹³⁷

Conclusion

Because of the multifactorial complexity of halitosis, proper diagnosis, identification of the etiology, and timely referrals are important for effective treatment. An interdisciplinary approach in treating halitosis is crucial to prevent misdiagnosis and/or unnecessary treatment. If the etiology is dentally related (eg, caries, periodontal disease, poor oral hygiene), elimination of halitosis can be achieved by correcting these factors, which the patient and dentist may be able to accomplish. However, if systemic factors are contributing to the problem, an interdisciplinary approach is required. Regardless, more controlled studies are needed to determine the most effective treatment of the various types of halitosis.

ABOUT THE AUTHORS

Stuart J. Froum, DDS
Adjunct Clinical Professor and Director of Clinical Research, Ashman Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York; Private Practice, New York, New York

Ye Shi, DDS
Clinical Assistant Professor, Ashman Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York

Natacha Reis, DDS
Fellow at Advanced Program for International Dentists in Implant Dentistry, Ashman Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York; Diplomate, International Congress of Oral Implantologists

Tanatorn Asvaplungprohm, DDS
Fellow at Advanced Program for International Dentists in Implant Dentistry, Ashman Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York; Diplomate, International Congress of Oral Implantologists

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