Continuing Education Activity

Halitosis is a term coined from the merger of the Latin halitus (breath) and Greek osis (pathological process) to describe a condition that meant an unpleasant odor from the mouth or “bad breath,” as we commonly call it. It is a serious concern for the patient as it could lead to social embarrassment and leave the individual reclusive or occasionally even stigmatized. It is sometimes discovered by the dental practitioner or primary care clinician during a routine examination, and the individual may have been unaware. As social awareness of dental hygiene continues to rise, more people seek medical guidance to help cure this distressing ailment. This activity explains when this condition should be considered in a differential diagnosis, articulates how to evaluate for this condition properly, and highlights the role of the interprofessional team in caring for patients with this condition.

Objectives:

• Review the common causes of halitosis.
• Outline the evaluation of a patient with halitosis.
• Identify treatment options available for a patient with halitosis.
• Explain when halitosis should be considered on a differential diagnosis, articulate how to evaluate for this condition properly, and highlight the role of the interprofessional team in caring for patients with this condition.

Introduction

Halitosis is a term coined from the merger of the Latin halitus (breath) and Greek osis (pathological process) to describe a condition that meant an unpleasant odor from the mouth or “bad breath,” as we commonly call it. Understandably so, it is a serious concern for the patient as it could lead to social embarrassment and leave the individual reclusive or occasionally even stigmatized. It is sometimes discovered by the dental practitioner or primary care physician during a routine examination, and the individual may have been unaware. As social awareness of dental hygiene continues to rise, more people seek medical guidance to help cure this distressing ailment.[1][2]

Etiology

Halitosis is classified into 2 groups: genuine and delusional halitosis.

Delusional or Imaginary Halitosis

• Pseudo halitosis: Here, the patient complains of having oral malodor, which others do not experience, including the clinician.[3] In recent years, clinicians have observed an increasing trend in this group of patients. The cause of this could be attributed to a plethora of products pertaining to oral hygiene and teeth beautification advertised everywhere.[4]
• Halitophobia: In this condition, the patient fears that his breath will be considered malodorous by everyone around him and will remain so despite treatment. This is a cause of great anxiety.[5][6] This pathology affects about 0.5% to 1% of the adult population.[1] Often, it requires intensive counseling after ruling out other organic causes. The olfactory reference syndrome deserves a special mention here. The patient believes that besides foul breath, other body parts like armpits and feet, among others, are malodorous.[7][8]

Genuine Halitosis

• Physiological halitosis
• Pathological halitosis

Intraoral Causes

These account for nearly 80% to 85% of all halitosis cases.[9][10] Gingival and periodontal diseases (acute necrotizing ulcerative gingivitis, herpetic gingivitis, periodontitis, pericoronitis, periodontal abscess), Sjogren syndrome, cancer treatment, and bone pathologies like alveolitis and osteomyelitis attribute to halitosis. Contributing factors are deep carious lesions and large interdental areas where retention of food debris could occur, malaligned teeth, exposed necrotic pulp, ill-fitting dentures and orthodontic appliances, tongue biofilm, and candidiasis.[5] Intraoral neoplastic lesions like malignancies of the tongue or cheeks and mucosal pathologies like tuberculosis and syphilis can cause a buildup of microorganisms and cause halitosis.[1][11]

A drop in the oxygen saturation of saliva results in a lowering of the pH of saliva, causing diamines to form, resulting in malodor.[1]

Extraoral Causes

Respiratory system: The nose, sinuses, tonsils, and upper respiratory system, including the pharynx and larynx, can be the focus of halitosis. Foreign bodies in the nose form a nidus for bacteria to thrive.[3] Klebsiella ozaenae can cause atrophic rhinitis, Streptococcus species is responsible for acute pharyngitis and sinusitis, and nasopharyngeal abscesses and laryngeal carcinoma can cause halitosis. Acute and chronic tonsillitis and tonsilloliths contribute to halitosis as the tonsils, like the surface of the tongue, have crypts that house bacteria producing volatile sulfur compounds (VSCs) and, consequently, malodor.[12] Pneumonia, chronic bronchitis, lung abscess, cystic fibrosis, and bronchiectasis can also cause malodor. Pseudomonas aeruginosa in certain respiratory system diseases excretes 2-amino acetophenone, which causes halitosis.[5]

Gastrointestinal system: Gastrointestinal (GI) causes account for most of the extraoral causes of halitosis.[13] GI reflux, gastric and peptic ulcers, congenital broncho-esophageal fistula, Zenker’s diverticulum, carcinoma of the stomach, hiatus hernia, pyloric stenosis, duodenal obstruction, and steatorrhoea are the other causes of halitosis.[14][15][16] Both Enterococcus faecalis and Helicobacter pylori have been found in periodontal spaces and can cause halitosis.[5]

Systemic/metabolic/endocrine disorders: Certain endocrinological and metabolic disorders like diabetes mellitus render a fruity or acetone-like odor to the breath, while in uremia, the breath gets an ammoniacal odor. Likewise, some other medical disorders altering the odor of the breath are listed below. 

• Acute febrile illness
• Upper respiratory tract infection
• Cystic fibrosis
• Diabetes mellitus
• Leukemia
• Hepatic failure
• Renal failure 
• Menstruation                                            

Drug-related halitosis: Certain drugs like chloral hydrate, disulfiram, acetaminophen, phenothiazines, antihistaminics, ethyl alcohol, griseofulvin, amphetamines, arsenic salts, bisphosphonates, chemotherapeutic agents, among others, cause oral malodor.[17]

Epidemiology

The quantum of data available on halitosis is fairly insufficient as there are no distinct criteria to define a bad odor and its extent for an individual. Hence, a lack of social and ethnic standardization of malodor is the main hindrance for carrying out scientific studies. Willing enrollment in clinical trials would again be questionable because of the sensitive nature of the affliction socially.[1]

Exact documentation of prevalence rates is difficult owing to the nonspecificity in defining a halitosis patient. Certain studies have shown the prevalence of halitosis up to 50%. Differences in prevalence values, however, would vary nationwide or community-wide due to differences in the method of the study.[18]

Certain studies have shown a prevalence of 6 to 23% in China, 50% in the United States, and 21.7% and 35.3% for male and female Indian dental students, respectively.[19][20][21][22] One study has linked the rising incidence of halitosis with age.[16] Halitosis is the third most common cause of referral to dentists after dental caries and periodontal diseases.[5] According to one study, halitosis is amongst the top 100 most distressful diseases in humans.[1]

Pathophysiology

Fetor ex-ore, fetor oris, oral malodor are terms that refer to repelling odors in the air of expiration.[23] It also involves ozostomia, stomatodysodia, halitosis, and fetor community-wide without showing the exact cause.[24]

The gases emanating from the mouth that cause oral malodor are the volatile sulfur compounds (VSCs). These include hydrogen sulfide, methyl mercaptan, and dimethyl sulfide. Gram-negative and anaerobic bacteria from periodontal infections generate these compounds.[25] The intraoral milieu contributes to 80% to 85% of cases of halitosis, where decarboxylation of amino acids such as acetic acid and propionic acid leads to malodorous amines like putrescine and cadaverine and other volatile aromatic compounds like indole and skatole.[9]

In physiological halitosis, which occurs on waking, the cause is putrefaction of entrapped food particles and desquamated epithelial cells by bacteria.[9] The surface of the tongue has desquamated epithelial cells, leucocytes from periodontal pockets, food residues, and bacteria. The depth of the tongue papillae affects the biofilm coating on top, which prevents the cleansing action of saliva and promotes the growth of anaerobic bacteria, giving rise to halitosis. This occurs even in individuals with healthy periodontal tissues and good dental hygiene.[26][14][15][16][27][28]

Contributing factors in the diet include the consumption of volatile foods like onions, garlic, spices, pickles, radish, condiments, betelnut tobacco, and alcohol resulting in malodor. Garlic and onions have a high sulfur concentration in their composition, which on degradation through the gastrointestinal tract, emits the characteristic odor which lasts for hours after consumption.[29][30]

Histopathology

In individuals with halitosis, the posterior dorsum of the tongue is the main source of malodor. Smears taken from this biofilm or scrapings would show desquamated epithelial cells, leucocytes from periodontal pockets, blood metabolites, different food residues, and bacteria. Some bacteria associated with this condition are:

• Oral cavity: Gram-negative and anaerobic bacteria 
• Nasal mucosa: K. ozaenae
• Pharynx, sinuses: Streptococcus species
• Respiratory system (bronchitis, bronchiectasis, lung diseases): P. aeruginosa 
• Stomach: H. pylori
• GI tract: E. faecalis[5]

History and Physical

In a patient who complains of halitosis, a thorough history is important. Clinicians should try and rule out physiological and transient causes of halitosis. A detailed history should include a complete dietary history and habits like smoking, tobacco, and medications. The clinician should obtain a history of past and present illnesses, including symptoms suggesting upper and lower respiratory infections and gastrointestinal causes like cold and cough, fever, weight loss, dyspepsia, or heartburn. A family history of chronic illnesses like hypertension and diabetes mellitus is to be elicited.[4] After a complete history, thorough periodontal screening is required. If there is suspicion of any extraoral cause, more investigations are necessary. The methods of clinical periodontal screening could be direct or indirect.

Evaluation

Assessment methods discriminate between pseudo-halitosis and halitophobia. Diagnostic tests include organoleptic measurement, gas chromatography, sulfide monitoring, the BANA test, quantifying β-galactosidase activity, salivary incubation test, ammonia monitoring, or ninhydrin method.

Direct Methods of Screening

Organoleptic Method

This is by far the commonest method used and the most effective in the clinical scenario. A plastic tube is placed in the patient’s mouth, and the clinician tests the odor from the other end of the tube as the patient exhales into one end of the tube, grading it between 0 and 5:

• Grade 0: No odor detectable
• Grade 1: Malodor is hardly detectable
• Grade 2: Odor slightly exceeding the threshold of malodor recognition
• Grade 3: Most certainly identifiable malodor
• Grade 4: Strong malodor
• Grade 5: Very strong malodor.[31]

The test is easy, inexpensive, and does not require specialized tools but could get a little uncomfortable for the clinician.

Gas Chromatography

With gas chromatography (GC), a quantitative analysis of VSCs like dimethyl sulfide, methyl mercaptan, and hydrogen sulfide can be carried out even at minuscule concentrations from saliva, tongue debris, or any other oral fluid. It is a highly reliable test; the only drawbacks are expense, it is nontransportable, and requires specialized trained personnel for its usage. This test is only for academic and research purposes. Its inability to detect non-sulfur-containing odoriferous molecules is another disadvantage to its use.[32][33]

Portable Sulfide Monitor

The portable sulfide monitor is a portable device. In this test, a single-use tube is inserted into the patient’s mouth, which is closed for 5 minutes, while the patient breathes through his nose. The device detects sulfur-containing molecules in the breath, and this is reflected in the readings. It cannot detect non-sulfur containing molecules.[34][35]

Indirect Methods of Screening

Benzoyl-DL-Arginine-Alpha-Naphthylamide (BANA)

This user-friendly and quick test detects certain gram-negative proteolytic obligate anaerobes like Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia, which form a red complex when treated with BANA, a synthetic trypsin substrate. This provides proof for the presence of these bacteria, which are often present on the dorsum of the tongue and sublingual plaques and cause halitosis.[36]

Ammonia Monitoring

This method uses a pump and disposable tube that measures the ammonia produced orally in a patient with halitosis and measures the reading quantitively.[37][38]

Ninhydrin Technique

This technique is user-friendly. It requires the addition of isopropanol to the patient’s sample to detect amines and polyamines, which contribute to the malodor.[39]

Salivary Incubation Test

This test is more sensitive than the organoleptic test but is more time-consuming. It involves incubation of the patient’s saliva at 37 C under anaerobic conditions for a few hours, after which the odor is detected.[32]

Darkfield/Phase Contrast Microscopy

Quantifying Beta-Galactosidase Activity

The enzyme beta-galactosidase is directly associated with oral malodor and forms the basis for this test. The saliva is placed on a paper disc used for the test, which gives quantitative results in terms of color change.[40][32]

Polymerase Chain Reaction

Today, many prefer polymerase chain reaction (PCR), which is sensitive, specific, and quick to detect VSCs from any sample taken from the oral cavity.[41]

Treatment / Management

Supportive and Sympathetic Reassurance 

The primary step after ruling out physiological halitosis is a thorough examination of the oral cavity to know whether it is tongue biofilm, deep carious lesions or large interdental areas with entrapped necrotic food debris, exposed necrotic pulp, ill-fitted prosthesis or dentures, mucosal lesions like tuberculosis, syphilis or even malignancies like carcinoma of the cheek or tongue, and treat accordingly.

Mechanical Debridement of Tongue Biofilm

The commonest cause of halitosis is poor dental hygiene. Hence, it is imperative to educate the patient about the importance of removing the tongue biofilm, which is the source of malodor generating bacteria and plaque control.[42][43]

This is best done by tongue scrapers than toothbrushes. Flossing teeth is also very important to keep the interdental spaces free of plaque and food debris, thereby controlling halitosis.[44]

Mouth Rinses

For effective control of halitosis, antibacterial agents such as chlorhexidine, zinc, triclosan, and cetylpyridinium chloride are recommended for usage. These have different mechanisms of action. Although chlorhexidine is undoubtedly the best for inhibition of the production of VSCs, it may have an unpleasant side effect of the unsightly staining of teeth.[3] A combination of these agents, along with essential oils, is incorporated in several commercially available preparations.[45]

Other Ancillary Measures

• Tea tree oil has been used effectively to control malodor caused by the bacterium Solobacterium moorei strain, according to one study.[46]
• The reduction of VSCs has been noted in certain cases by the usage of photodynamic waves from a photosensitizer.[47]
• Masking agents like mint or fluoride in toothpaste or flavored chewing gum can be recommended, but it has only a brief effect.[48]
• Lifestyle modifications including avoidance of smoking, tobacco, alcohol, cutting down onions, garlic, and spices in the diet are recommended.
• Patients should be encouraged to increase their fluid intake.

Extraoral causes of halitosis are to be investigated in the absence of intraoral pathology, in consultation with the concerned faculty and treated accordingly. Antibiotics for respiratory infections, antacids for gastroesophageal reflux disease (GERD), or surgical intervention if adenoids are enlarged and infected.

Differential Diagnosis

• Diabetes mellitus

• Fever
• Dehydration

• Internal hemorrhage

• Liver failure

• Renal failure

• Tuberculosis

Deterrence and Patient Education

It is important to educate the patient about the need for good dental hygiene. While most people would associate bad dental hygiene and resulting halitosis with toothaches and unsightly stains, a major deterrent would be to emphasize the links between bad oral hygiene and serious medical issues like cardiovascular diseases, including myocardial infarction, stroke, or endocarditis which are precipitated by periodontitis, or periodontitis. Other problems linked to gum disease include respiratory infections like pneumonia or chronic obstructive pulmonary disease (COPD), preterm births or intrauterine growth retardation, erectile dysfunction, complications of diabetes, kidney diseases, infertility, or even pancreatic cancer.

Enhancing Healthcare Team Outcomes

A multipronged, interprofessional approach involving a physician, otorhinolaryngology surgeon, gastroenterologist, surgeon, and psychologist is recommended.

Since patients with halitosis are generally psychologically depressed, diffident, or even socially isolated, they should be offered mental health counseling. To help get rid of halitosis, an aggressive approach is necessary to make the diagnosis so that treatment can be effective and durable.

Halitosis is an embarrassing medical issue that concerns a vast majority of people that can, apart from a host of medical complications, affect a person’s life and interactions with other members of society. It could lead to depression and even a sociocultural boycott of sorts in extreme cases, hence the need to tackle the issue judiciously and with extreme sensitivity. An empathetic approach by the clinician is of prime importance in handling a patient with halitosis. It would be helpful if one involves a nutritionist and psychologist in the treatment protocol to prevent recurrences and to keep halitosis at bay forever.[49]