Oral malodor and its treatment

The term halitosis is a general term used to describe any disagreeable odor of expired air, regardless of its origin. It is a common problem because of which patients visit the dentist. Historically, it has been known by various names such as halitosis, fetor oris, fetor ex-ore. Since ancient times, people have tried to find out remedies for oral malodor. Greeks and Romans wrote about the remedies of oral malodor. Hippocrates also wrote about the treatment of oral malodor which primarily focused on the treatment of periodontitis. He observed a reduction in the offensive odor from the mouth as the periodontitis was treated and periodontium returned to health. The scientific research on halitosis began in 1960’s when Tonzetich and Richter (1964) 1 reported that volatile sulfur compounds (VSC’s) were primarily responsible for oral malodor. These volatile compounds are the result of the breakdown of cell wall polypeptide chains of amino acids by anaerobic bacteria. Later on, Tonzetich and Richter (1978) 2 found that the offensiveness of oral malodor increased with the increase in periodontal destruction. Other compounds which caused oral malodor were identified by Yaegaki and Sanada (1992) 3, who reported that along with VSC’s, methyl mercaptan and hydrogen sulfide are also responsible for halitosis. They also reported that the concentration of VSC’s, methyl mercaptan and hydrogen sulfide was around eight times more in patients with periodontal diseases as compared to periodontally healthy patients.

Tonzetich and Ng (1976) 4 in their one of the most important contributions to halitosis research showed that hydrogen sulfide and methyl mercaptan affected the permeability of oral mucosa. The gingival sulcular epithelium and junctional epithelium are considered to be weak barriers for the passage of bacterial products. It was demonstrated that VSC’s, methyl mercaptan and hydrogen sulfide increased the permeability of epithelia, allowing the entry of bacterial antigens into the connective tissue 5, 6. Further, it was observed that VSC’s could affect the collagen metabolism and that they may have a potential role in the formation of the initial lesion in periodontal disease 7. Simultaneously, research on saliva demonstrated that saliva provides necessary substrates for degradation by bacteria, including salivary proteins and other metabolic factors 8. Present literature on halitosis, suggests that there are multiple factors that facilitate the development of halitosis, including poor oral hygiene, bacterial infection, periodontal tissue degradation, pH of the oral cavity (alkaline pH favors malodor), salivary proteins, food impaction, faulty restorations and oral habits such as tobacco or alcohol use.

Prevalence of halitosis

Halitosis is a common problem in all parts of the world. In a study done in the United States, the prevalence of halitosis was found to be 10% to 30% 9. Another study done in Japan showed that 28% population under study complained of halitosis 10. Further, it was noted that around 87% of cases with halitosis had oral causes associated with the condition 11. Various studies have been done worldwide to know the prevalence of halitosis in different populations. Some of them have been summarized in the Table 33.1.

Table 33.1 Various studies done worldwide to know the prevalence of halitosis in different populations.

Authors/year
Country
Sampling procedure and number of patients
Measurement of halitosis
Main results
Miyazaki et al., (1995) 10JapanConvenience sample, 2672 government workers, age = 18-64 yearsVSC (Halimeter)Prevalence of moderate halitosis (≥ 75 ppb) = 28%
Loesche et al., (1996) 12USAConvenience sample, 270 adults, age = 60+ yearsSelf-reportPrevalence of self perception = 31% Prevalence of halitosis informed by others = 24%
Söder et al., (2006) 13SwedenRandomized representative sample, 1681 adults, age = 30-40 years,OrganolepticPrevalence of severe halitosis (score 5) = 2.4%
Nadanovsky et al. (2007) 14BrazilRandomized representative sample, 344 individuals, age= 1– 87 yearsSelf-reportPrevalence of persistent oral malodor = 15%
Nalçaci et al., (2008) 15TurkeyConvenience sample, 628 children, age= 7-11 yearsOrganolepticPrevalence of halitosis = 14.5%
Bornstein et al., (2009) 16SwitzerlandRandomized sample, 419 adults, age=18-94 yearsSelf-report, Organoleptic and VSCPrevalence of organoleptic score 3+ = 11.5% Prevalence of self-reported halitosis = 32% Prevalence of VSC 75+ ppb = 28%
Bornstein et al., (2009) 17SwitzerlandConvenience sample, 626 male army recruits, age=18-25 yearsSelf-report and clinical analysisPrevalence of detected chronic halitosis = 20% Prevalence of individuals without halitosis experience = 17%
Yokoyama et al. (2010) 18JapanConvenience sample, 474 senior high school studentsSelf-report and clinical analysisPrevalence of halitosis experience (anxiety or consciousness of the problem at least once) = 42% Prevalence of clinically detectable malodor = 39.6%
Hammad et al. (2014) 19Jordan Random sample, 205 employees from the Jordan University of Science and Technology (JUST), age= 18-68 years Self-reported halitosis and clinical analysis Prevalence of halitosis was 78% with a low rate of awareness (20.5%).

Biochemistry of oral malodor

The degradation of oral tissues by bacteria is the primary cause of oral malodor. The main organisms involved in this process are Gram-negative anaerobic oral bacteria 20. The most important substrates for the production of oral malodor are cysteine, cysteine and methionine 21. Their degradation results in the formation of various VSC’s. VSC’s involved in halitosis are hydrogen sulfide (H2S), methyl mercaptan (CH3SH) and dimethyl sulfide (CH3)2S (Table 33.2). Other molecules involved in oral malodor, but to a lesser extent, are diamines (indole and skatole) or polyamines (cadverin and putrescin). Table 33.3 enumerates various bacteria involved in the formation of VSC’s. Most of the organisms responsible for causing malodor are well established periodontal pathogens. That is why; there is a positive correlation between bad breath and periodontitis 22. When the tongue coating is taken into account, the correlation is even more significant 23, 24. Furthermore, the microbiota identified on the tongue surface seems to be identical to the subgingival plaque 25.

Table 33.2 Volatile sulfur compounds contributing to malodor 21, 25, 26

Volatile sulfur compounds
Compounds
Volatile sulfur compoundsHydrogen sulfide: H2S
Methyl mercaptan: CH3SH
Dimethyl sulfide: (CH3)2S
DiaminesPutrescine: NH2(CH2)4NH2
Cadaverine: NH2(CH2)5NH2
Butyric acid: CH3CH2CH2COOH
Propionic acid: CH3CH2COOH
Valeric acid: C5H10O2
Phenyl compoundsIndole: C8H7N
Skatole: C9H9N
Pyridine: C5H5N
Alcohols1-propoxy-2-propanol
Alkalines2-methy-propane
Nitrogen-containing compoundsUrea: (NH2)2CO
Ammonia NH3
Ketones

Table 33.3 Various volatile sulfur compounds produced by various bacteria and their substrates 27

Volatile sulfur compounds
Substrate
Bacteria
H2SCysteinePeptostreptococcus anaerobius
Micros prevotii
Eubacterium limosum
Bacteroides spp.
Centipedia periodontii
H2SSerum Prevotella intermedia
Prevotella loescheii
Porphyromonas gingivalis (BANA positive)
Treponema denticola (BANA positive)
Selenomonas artermidis
CH3SHMethionineFusobacterium nucleatum
Fusobacterium periodonticum
Eubacterium spp.
Bacteroides spp.
CH3SHSerum Treponema denticola (BANA positive)
Porphyromonas gingivalis (BANA positive) Porphyromonas endodontalis
Other compounds Various substrates Prevotella melaninogenica
Tanerella forsythensis
Eikenella corrodens
Solobacterium moorei
Treponema forsythensis
Centipeda periodontii
Atopobium parvulum

Classification of halitosis

Halitosis can be classified in different ways, depending on its source or oral/non-oral origin.

Miyazaki’s classification:

Miyazaki et al. (1999) 28 classified halitosis into different categories and also elaborated treatment needs for different types of halitosis (Table 33.4). They classified halitosis into following categories,

I. Genuine halitosis

  1. Physiological halitosis
  2. Pathological halitosis

(i) Oral origin

(ii) Systemic origin

II. Pseudo-halitosis

III. Halitophobia

Genuine halitosis originates from the oral cavity and may have physiological or pathological etiology. Genuine physiological halitosis occurs in the absence of any oral or systemic organic disease and is caused by eating or drinking food that results in malodor. The condition is short-lived, temporary and easily reversible. Genuine pathological halitosis results from………

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Pseudo-halitosis refers to a condition where there is no halitosis present, but the patients believe that they have oral malodor. Psychological halitosis, which may result from certain brain dysfunctions may result in delusional cacosmia. In this condition, oral malodor is falsely perceived by  patients who  may have a brain dysfunction or tumor. In the case of intracranial neoplasms, changes in taste and smell sensation may frequently occur.

Halitophobia is characterized by a patient’s persistent belief that he or she has halitosis, despite reassurance, treatment, and counseling. Many of the patients with halitophobia have slight bad breath when they seek treatment, but despite adequate treatment, they still complain of bad breath.

Table 33.4 Classification of halitosis with corresponding treatment needs, Miyazaki et al. (1999) 28

Classification of halitosis with corresponding treatment needs, Miyazaki et al. (1999) 28

Etiology of oral malodor

As already stated there are multiple causes for oral malodor which include both oral and non-oral causes (Table 33.5).

Oral causes of halitosis:

Almost 80-85% of all halitosis cases have the cause/causes of the condition in the oral cavity. In a study where 2000 patients with halitosis were examined, almost 76% of them had oral causes of bad breath including tongue coating (43%), gingivitis/periodontitis (11%) or a combination of the two (18%) 29. So, tongue coating is considered as a major cause of halitosis. Other causes include dental and periodontal infections, mouth breathing, xerostomia etc.

Tongue coating:

 The dorsal surface of the tongue provides a large area for accumulation of microorganisms which significantly contribute to oral malodor 30. The dorsum of the tongue has an average surface area of 25 cm2, which provides an ideal niche for oral bacteria 31. Since tongue surface has embedded in it desquamating epithelial cells, food remnants and components of saliva; bacteria have sufficient substrate. It results in putrefaction of these substrates causing halitosis. Hence, tongue cleaning is an important component of daily oral hygiene procedures. Tongue scrapers are used to remove the coating from the dorsal surface of the tongue. Tongue cleaning also improves the taste sensation.

Periodontal infections:

Gingivitis and periodontitis are two most common periodontal problems which have primary bacterial etiology 32. It has been demonstrated that a positive correlation exists between oral malodor and increasing pocket depth 23. With the improvement of periodontal condition, oral malodor reduces. Severe periodontal infections such as in the case of necrotizing gingivitis or periodontitis cause extremely offensive malodor. This is caused due to excessive periodontal tissue destruction. These conditions are seen in patients with compromised immune system, stress, smoking or insufficient oral hygiene.

Xerostomia:

It is the condition where the salivary flow in the oral cavity is reduced. In these patients, the salivary flow is around 0.15 ml/min instead of 0.25-0.50 ml/min. It results in increased accumulation of plaque on the tooth surfaces and also results in increased tongue coating 33. Saliva has both clearing action on deposits in the oral cavity and buffering action to maintain optimum pH in the oral cavity. It has been observed that in xerostomia there is a microbial shift from Gram-positive to Gram-negative species 34. Decreased salivary flow results in increased……..

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Other oral causes:

There are many other oral causes which may contribute to the development of oral malodor. These include decayed teeth with exposed necrotic pulp, extraction wounds, dry socket and food impaction.  Some less common causes of oral malodor are pericoronitis, peri-implantitis, recurrent oral ulcerations and herpetic gingivitis 39.

Table 33.5: Oral and non-oral causes of halitosis

Oral causes
Non-oral causes
Poor oral hygiene
Tongue coating
Periodontal disease
Dental cavities
Peri-implantitis
Exposed tooth pulp
Healing wounds
Dry socket
Pericoronitis
Interdental food impaction
Oral cancer
Dentures not cleaned
Cyst with fistula
Necrotizing ulcerative gingivitis/periodontitis
Ear, nose and throat origin
• Acute tonsillitis
• Postnasal drip
• Cleft palate
• Antral malignancy
• Atrophic rhinitis
• Sinusitis
Respiratory origin
• Sinusitis
• Tuberculosis
• Emphysema
• Tumors
• Pharyngitis
• Pneumonia
• Bronchitis
• Bronchiectasis
Gastrointestinal tract origin
• Gastroesophageal reflux disease
• H. Pylori infection
• Peptic ulcer disease
• Stomach cancer
• Malabsorption
• Zenker’s diverticulum
Blood born halitosis
• Metabolic disorder (e.g. diabetes)
• Liver pathology (liver failure, liver cirrhosis, gall bladder diseases)
• Renal failure
• Trimethylaminuria (fish odor syndrome)
• Medications
o Amphetamines
o Chloral hydrate
o Cytotoxic agents
o Dimethyl sulphoxide
o Disulfiram
o Nitrates and nitrites
o Phenothiazines
o Solvent abuse
Menstrual cycle

Non-oral causes of halitosis:

Non-oral causes of halitosis are less common than oral causes but must be identified to adequately treat and eliminate oral malodor.

ENT and pulmonary causes:

Ear, nose and throat infections may result in halitosis. Infections related to tonsils, nasal cavity, maxillary sinuses or pulmonary system may cause halitosis.

Tonsillitis:

It has been shown that around 10% of all cases of halitosis originate from ENT infections and 3% out of these are caused by tonsil infection 40. Acute tonsillitis is the most important cause of halitosis from the ENT region. While examination of the oral cavity in a halitosis patient special attention should be given to tonsils. The tonsils should be examined for their size, structure (invaginations, coating, and hyperemia) and the presence of tonsilloliths 41. The most common cause of tonsillitis is infection with streptococci, but viral infections (e.g. Mononucleosis infectiosa) may also cause tonsillitis. Tonsillectomy is the treatment of choice if acute tonsillitis occurs more than three times in a year. The presence of tonsilloliths increases the frequency of oral malodor to upto 10 folds 42. Various bacterial species that have been isolated from tonsilloliths are Eubacterium, Fusobacterium, Porphyromonas, Prevotella, Selenomonas, and Tanerella. All of these species are capable of producing VSC’s 43. Plaut-Vincent angina is another ENT cause of halitosis. The condition is caused by Fusobacterium Plaut Vincenti and Borrelia Vincenti 44.

Nasal cavity:

The most common nasal cause of halitosis is post nasal drip. Anything that causes excess mucus formation can/will result in post-nasal drip. It is commonly caused by cold or allergies (food, pollen, pets, etc.), or bacterial infection. Excess mucus creates an environment ripe for bacteria to multiply, giving the discharge an odor. Post nasal drip contacting the dorsum of the tongue further increases halitosis 45. Another nasal cause for halitosis is atrophic rhinitis with a bacterial infection. It can be caused following surgical resection of the tumor, radiotherapy or excessive consumption of nasal decongestants. Communication of oral and nasal cavity in cleft palate cases may also cause halitosis.

Sinusitis:

Sinusitis is the inflammation of the membranes lining the paranasal sinuses. Most common bacterial species involved in sinusitis are Streptococcus pneumonia, Haemophilus influenza, and Moraxella catarrhalis. The radiographic and CT scan show presence of sinus obliteration. Sinusitis may also be caused by dental infection in one or multiple teeth. In these cases, the bacterial species involved in the infection are Peptostretococcus spp., Fusobacterium spp., Prevotella spp. and Porphyromonas spp. These organisms are capable of producing VSC’s and cause halitosis. It has been observed that 50-70% of patients with chronic sinusitis complain of bad breath 46.

Pulmonary infections:

Most important pulmonary causes of halitosis are bronchiectasis, lung abscesses and necrotizing lung neoplasia 47-51. The odors emitted from patient with respiratory conditions depend on the type of disease. The carcinomas in the upper respiratory tract usually produce normal or branched organic acids, whereas carcinomas of the lung may produce acetones, methylethylketone, n-propanol, aniline and o-toluidine 52. These products result in malodor which can be related to the underlying respiratory cause.

Gastrointestinal causes:

Various gastrointestinal (GI) diseases may result in halitosis, including gastrointestinal reflux, hiatus hernia, stomach cancers, malabsorption etc. After oral origin, patients usually think that the cause of their bad breath is related to gastric reasons. The GI related etiology of halitosis may be related to the esophagus, stomach or intestines.

Esophagus:

The prevalence of esophagus related origin of halitosis is quite less. Certain conditions like the presence of Zenker’s diverticulum gives rise to continuous oral malodor 53. The condition is seen usually in patients above 65 years of age and its incidences are only 0.1%. In the case of severe regurgitation, there may be continuous oral malodor.  Endoscopic investigations may reveal ulcerations in the esophagus.  Esophageal bleeding may also be present, which results in musty odor. If such findings are present, prompt treatment is required because it may transform into carcinoma if not treated.

Stomach:

The most common cause of stomach related oral malodor is infection with Helicobacter pylori. This infection may cause……….

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Intestine:

A documented cause of intestine related oral malodor is intestinal obstruction resulting in fecal mouth odor. The condition was found in two siblings with extrinsic duodenal obstruction caused by congenital peritoneal bands 59. Because of unique kind of oral malodor, the barium meal investigation was done which confirmed duodenal obstruction.

Blood born halitosis:

This type of halitosis is caused by metabolic disorders in which malodorous products circulate in the bloodstream and are exhaled in the breath after the alveolar gas exchange. The volatile sulfur compound dimethylsulfide is the main contributor to extra-oral or blood-borne halitosis 60. Certain medications also result in blood born halitosis because their metabolism in the body results in the formation of malodorous products which circulate in the blood and are exhaled during respiration.

Metabolic causes:

Diabetes mellitus:

Diabetes mellitus is a metabolic disorder characterized by chronic hyperglycemia with disturbances of carbohydrate, fat and protein metabolism, resulting from defects in insulin secretion, insulin action, or both. Patients with uncontrolled diabetes mellitus having diabetic ketoacidoses can emit ketonic breath which is also described as sweet ‘fruity’ smell or rotten apple breath 61 (Table 33.6).

Liver pathologies:

Liver-related pathologies may also result in oral malodor.  Liver is a major site for the metabolism of various ingested food components and medications. The metabolites produced in the liver are either utilized in the body or are excreted as waste products. Reduced liver function results in the incorporation of these metabolites in the blood, which are then eliminated through the lungs resulting in a sweet, excremental odor ‘fetor hepticus’.  Hepatic encephalopathy results in this typical oral malodor 62. Liver failure results in the lack of detoxification of various toxins which results in oral malodor 63. Hereditary disorders like tyrosinemy result in typical ‘cabbage odor’.

Renal disorders:

The kidneys are responsible for filtration of blood. Impaired renal function results in high blood urea nitrogen levels and low salivary flow rates. A typical uremic odor is characteristic of renal failure.

Trimethylaminuria:

This genetic disorder of bowels typically results in ‘fishy odor’. In this disorder a volatile, fish-smelling compound, trimethylamine accumulates in the body and is excreted in the urine. This compound is formed by bacteria in the gut by reduction of compounds, including trimethylamine-N-oxide and choline. This compound is also secreted in sweat and breath which results in this typical odor from the person.  The condition can be diagnosed by estimation of trimethylamine and trimethylamine-N-oxide in urine after the patient is given a diet rich in substrates of these compounds such as a marine fish meal. The management of the condition is done by avoiding a diet rich in precursors of trimethylamine or antibiotics to control bacteria in the gut or using charcoal to sequester trimethylamine 64.

Medications:

There are many medications that can cause reduced salivary flow. Some also have a distinct odor of their own, which enters the breath via the lungs. Some medications such as bisphosphonates can result in necrosis of the tissues. Bisphosphonates associated jaw necrosis is a common problem with their use, which results in filthy odor from oral cavity 65. Other drugs that may cause oral malodor include nitrates, disulfiram, cytotoxic agents, antidepressants etc.

Menstrual cycle:

Hormonal changes during ovulation and menstruation may contribute a “mousy” odor to breath 66, 67. It has been reported that VSC levels in women with periodontitis increased 2.2-fold in the ovulation phase as compared to the follicular phase 68. Furthermore, bleeding on probing along with VSC levels was found to be significantly higher in subjects with periodontitis than in healthy subjects.

Table 33.6 Specific metabolic or endocrinal problems and their associated oral malodor

Metabolic or endocrinal problems
Associated oral malodor
Intestinal obstructionFecal odor
Type-1-diabetes in children
Type-2-diabetes in adults
Alcoholic ketoacidosis
Fruity odor/ ketonic breath/rotten apple odor
Hepatic cirrhosisMusty or mousey odor
Blood dyscrasiasResembling decomposed blood of a healing surgical extraction wound
Renal insufficiency
Trimethylaminuria
Ammonia of fishy odor
PhenylketonuriaMouse odor
Methionine adenosyltransferase (MAT) deficiencyCooked cabbage odor
Isovaleriaan aciditySweating feet odor
Maple syrup urine diseaseBurned sugar odor
HomocystinuriaSweet musty odor
Disease of LignacRotten eggs odor
Wegener's granulomatosisNecrotic, putrefactive odor
Lung abscess, tuberculosis, BronchiectasisFoul, putrefactive odor

Diagnosis of Halitosis

Since, oral malodor is a common problem and is a distressing symptom for patients, the need to diagnose the underlying cause is very important. The diagnostic approach involves questioning about the history of halitosis, dental history, and medical history. It is important to identify the source of oral malodor (oral or non-oral). Furthermore, many patients who complain of bad taste may not have bad breath. The taste disorders may be due to other causes 69. The patient should be asked about frequency and time of occurrence of oral malodor during the day. For example, oral malodor associated with stomach hernia precipitates after meals. The patient should be asked about if he/she is taking any medications and its duration and other symptoms, like dry mouth which is sometimes associated with intake of medication 70. The diagnosis of oral malodor is made by self-examination or professional examination.

Self-diagnosis:

It is the identification of oral malodor by the patient on self-examination. It is useful when the cause of halitosis is intraoral. The patient is treated for the cause and is asked to do monitoring of results of the therapy by self-examination. The following self-testing can be used 70:

  1. Smelling a metallic or non-odorous plastic spoon after scraping the back of the tongue.
  2. Smelling a toothpick after introducing it in an interdental area
  3. Smelling saliva spit in a small cup or spoon.
  4. Licking the wrist and allowing it to dry, followed by smelling the area.

Professional diagnosis:

In persistent oral malodor, specialized professionally used methods are required to diagnose the causes of halitosis. These include direct and indirect methods.

Direct methods:

  1. Organoleptic method (whole-mouth breath test, spoon test, floss odor test, salivary odor test and self-perception of odor)
  2. Gas chromatography
  3. Sulfide monitors
  4. “Electronic nose”

Indirect methods

  1. Bacterial culture and smear
  2. Enzyme assay

Organoleptic method:

It is a subjective test scored on the basis of the examiner’s perception of a subject’s oral malodor. The organoleptic measurement can be carried out by sniffing the patient’s breath and grading the level of halitosis. It is a crude method of oral malodor determination, but is still considered the “gold standard” in the examination of breath malodor. In this method, a trained judge sniffs the expired air and assesses the intensity of malodor. Rosenberg and McCulloch (1992) 71 have proposed following ratings for organoleptic measurement of malodor,

0 = no odor present,

1 = barely noticeable odor,

2 = slight but clearly noticeable odor,

3 = moderate odor,

4 = strong offensive odor, and

5 = extremely foul odor

Before this test is performed, the individual undergoing this test is instructed to refrain from using deodorants or fragrances six hours prior to the visit to the clinic. At least 12 h before the consultation, teeth should not be cleaned or rinsed. Smoking should be stopped at least 24 h before any examination 72.

The examiner conducting the test should have a normal sense of smell. He or she should avoid drinking coffee, tea or alcohol, abstain from smoking and the use of perfumes and scented cosmetics should be strictly avoided. While doing this test, different samples are analyzed from each patient. These include,

Mouth odor test: While performing this test, the patient is asked to keep the mouth closed for two minutes and not to swallow during this period so that reproducible assessment of oral malodor can be made. After two minutes the subject breathes out gently, at a distance of 10 cm from the nose of their counterpart and the organoleptic odors are assessed 71.

Spoon test: 123

Saliva odor test: It can be done in two ways. In one method, the patient is asked to lick the wrist and after 10 s of drying, a score is given to this sample. In another method, the patient is instructed to expectorate about 1-2 ml of saliva into a glass tube. It is then covered and incubated for five minutes at 37⁰C. The glass tube is then held about 4 cm away from the nose for assessing odor.

Tongue coating test: 123

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Interdental ‘floss’ test: Here, after flossing with dental tape, the odor of the floss is scored by holding the floss about 3 cm from the nose.

Nasal odor test: The patient is asked to breathe through the nose and a score is given to the exhaled air.

Prosthesis odor test: In case, the patient is wearing partial or full removable denture, scoring of the odor of this prosthesis is noted.

The organoleptic method of assessing oral malodor is a relatively inexpensive method of diagnosing and rating oral malodor. However, it has the inherent disadvantage of subjective variations. To minimize this variation, assessment of oral halitosis should be carried out on two or three occasions by two or more different examiners. Females have a better olfactory sense and it decreases with age.

Gas chromatography:

Gas chromatography is a highly sensitive technique to assess breath malodor 73. In this technique, measurement of VSC’s is done on samples of saliva, tongue coating or expired breath by producing mass spectra analyzed by a gas chromatograph 1. Along with VSC’s other substances that are associated with oral malodor such as cadaverine, putrescine and skatole can also be detected using this technique. One such device is OralChromaTM (Figure 33.1)portable gas chromatography. The test using this device is performed in three steps,

  1. The device consists of a plastic syringe which is placed deep in the oral cavity and patient is asked to make a tight lip seal around the syringe. The plunger is gently pulled and then pushed back. The procedure is repeated again and the syringe is taken out of the mouth.
  2. The needle is dried on the outer surface and plunger is pushed such that only 0.5 cc of the gaseous contents remains in the syringe.
  3. The remaining gaseous contents of the syringe are injected into an inlet of the main unit of the OralChromaTM.

The main advantage of gas chromatography is that the technique identifies various components in a relatively minute quantity of air. However, the technique requires highly trained personnel.

Figure 33.1 OralChroma TM

Oral Chroma

Sulfide Monitors:

These are portable chair side equipment used to assess oral malodor. The main advantage of these monitors is that they are cost effective and easy to use. The monitor is equipped with a transparent tube that carries the exhaled breath of the patient to a suction pump which in turn carries the air to the monitor. The machine then analyses the sulfur content in the air. However, it cannot differentiate between different sulfur compounds. The results are displayed as parts per billion levels of hydrogen sulfide. The peak value during recordings is considered for oral malodor estimation. Values less than 100 are considered normal; between 100-180 are considered as minor halitosis and greater than 250 are considered as chronic halitosis.

Halimeter® (Figure 33.2), a portable sulfide meter has been widely used over the last few years in oral malodor testing. The device utilizes an electrochemical, voltammetric sensor which generates a signal when it is exposed to sulfur gasses (to be specific, hydrogen sulfide) and measures the concentration of hydrogen sulfide gas in parts per billion. The major advantage of this system is that it does not require highly trained personnel to operate and is easy to use. However, the readings are affected by perfume, hair spray, deodorant, etc. The device is very sensitive to alcohol, so the patient should be restrained from drinking alcohol for at least 12 hours prior to the test. The device is periodically recalibrated to obtain accurate results 71.

Figure 33.2 Halimeter® 

Halimeter

The sulfide monitoring system may show inaccurate results in the presence of high ethanol or essential oil levels in the breath. For this reason, the monitor should be recalibrated periodically to maintain its sensitivity.

Electronic nose:

The electronic nose system has been developed for the automated detection and classification of odors, vapors, and gasses. There are two main components of an electronic nose system: sensing system and pattern recognition system. The system is a hand-held device that rapidly classifies the chemicals in the unidentified vapor. This is a revolutionary technology where the sensor makes unique fingerprints for distinct odors which are then identified when a sample of air is subjected to analyses. The evidence from initial experiments indicates its effective utilization for diagnosis of halitosis.

In a study 74, Quartz Crystal Microbalance (QCM) sensor array combined with a pre-concentrator was used for discriminating VSC’s (hydrogen sulfide, methyl mercaptan, and dimethyl sulfide). Tanaka et al. (2004) 75 analyzed efficacy of the FF-1 electronic nose (composed of a pre-concentrator and an array of 6 MOS sensors) to discriminate the odors present in the human breath of 49 patients complaining of oral malodor and 29 control subjects without halitosis. The experiment was continued by Nonaka et al. (2005) 76, who tried to express clinically, oral malodor intensity as an absolute value.

Bacterial culture and smear:

This is an indirect method for the identification of oral malodor, wherein the samples taken from oral cavity are cultured and the bacterial species present in the sample are identified. Bacterial species which can produce VSC’s can be identified by this method.  Another indirect method is to go for microscopic evaluation of the plaque sample. Dark-field or phase-contrast microscopy is commonly used for this purpose. It has been observed that high proportions of spirochetes in plaque are associated with a specific acidic malodor 70.

BANA test:

The BANA (Benzoyl-DL-arginine-2 naphthylamide) test has been used to detect T. denticola, B. forsythus and P. gingivalis which are capable of producing VSC’s. These organisms are well established periodontal pathogens. BANA test is a rapid chair side test for the evaluation of non-sulfurous malodorous compounds. The test is performed by wiping a cotton swab on the tongue or interdental regions. The sample is placed on the BANA test strip which is then incubated at 55° for 5 minutes. The strip turns blue in the presence of the above organisms. More blue the strip turns, the higher is the concentration and the greater is the number of microorganisms. Patients who have been treated for halitosis can be re-evaluated using this test for the presence of above stated periodontal pathogens. In periodontally healthy patients who have been successfully treated for halitosis, the test should turn negative from positive.

β-galactosidase test:

One study has found that salivary levels of β-galactosidase positively correlated with oral malodor 77.

Treatment of oral malodor

Once the origin of oral malodor (oral or non-oral) has been identified, the treatment is planned accordingly.

Treatment of halitosis with oral origin:

The treatment of halitosis with oral origin is primarily based on reducing bacterial load in the oral cavity and treatment of active dental or periodontal diseases.

Periodontal therapy:

The periodontal treatment is helpful in reducing oral malodor. However, it must be remembered that only periodontal treatment is usually not capable to completely eliminate oral malodor because of multiple sources of malodor. Hence, it must be considered as one of the components of treatment of halitosis. It has been demonstrated that in periodontitis patients, strict supragingival plaque control is able to reduce the VSC’s and organoleptic scores 78. Many other studies have also supported these findings 29, 79. A systematic periodontal treatment significantly improves the periodontal status of the patient thus helping in the reduction of malodor. Mechanical plaque control is the cornerstone of reducing bacterial plaque in the oral cavity.

Along with mechanical plaque control measures, the chemical plaque control measures also helps in reducing bacterial load in the oral cavity. Chlorhexidine (CHX) has been used widely for plaque control. Along with its anti-bacterial activity, CHX is a strong oxidizing agent. It can reduce oral malodor by the oxidation of H2S, CH3SH, cysteine and methionine. A study has reported 29% reduction in odor for 4 hours after CHX application 80. Other chemicals effective in the oral malodor reduction include triclosan, aminefluoride/tinfluoride and H2O2. Triclosan is an effective anti-bacterial agent and has been shown to reduce the production of VSC’s by 84%, 3 hours after its application 81. A combination of aminefluoride and tinfluoride has been shown to cause 83% reduction in the morning halitosis 82. H2O2 is a strong oxidizing agent and has been shown to result in 90% VSC’s reduction, 8 hours after its application at 3% concentration 83. One stage, full mouth disinfection which includes scaling and root planing in combination with chlorhexidine application has been shown to result in significant microbiological improvement up to 2 months along with the reduction of organoleptical scores 84, 85.

Studies have also been done on toothpaste to evaluate their efficacy in reducing oral malodor. It has been shown that toothpaste containing stannous fluoride, zinc or triclosan cause a significant reduction in oral malodor for a limited period of time 86-88. Metal ions that have an affinity to pick up sulfur-containing gasses can be used to reduce halitosis. Metal ions such as zinc, mercury and copper ions can effectively adsorb these compounds, thus reducing their volatilization 89, 90. In a study, it was demonstrated that a combination of 0.005% CHX, 0.05% cetylpyridinium chloride (CPC) and 0.14% zinc lactate was significantly more effective in reducing oral malodor than CHX. It was attributed to the presence of zinc ions in the combination that seems to have a synergistic effect with CHX in reducing halitosis 91. Masking agents can also be used to reduce oral malodor for a limited period of time. Various sprays, mint tablets or chewing gums are available which can mask the VSC’s. These agents increase the salivary secretion, thereby retaining more soluble sulfur containing compounds 92.

Tongue coating:

One of the most important causes of oral malodor is tongue coating. In cases of halitosis with the oral origin, extensive tongue cleaning is extremely important. By scraping the deposits on the dorsal surface of the tongue, the bacterial load on tongue surface is reduced. It significantly reduces oral malodor 93. Tongue cleaning can be done by toothbrush, but a specific tongue scraper should be used for this purpose. Most of the coating is present on the posterior part of the dorsal surface of the tongue, so cleaning the tongue as posterior as possible is advised. There is strong evidence that tongue cleaning causes a significant reduction in oral malodor 94. Furthermore, it also seems to improve the taste sensation 82. Along with tongue scraping, interdental cleaning should be performed to remove any food particles.

Dietary recommendations:

The patient should be advised to drink plenty of liquids and to eat fresh, fibrous vegetables. Mouth rinsing should be done after every meal, especially after taking milk products, fish, and meat. If any known diet related cause of halitosis has been identified, it should be avoided.

Treatment of pathologies associated with teeth:

Open necrotic pulp chambers are one of the sources of oral malodor. Treatment of decayed and endodontically involved tooth/teeth is an important component of treatment of halitosis. Along with this, un-healed extraction sockets and any pus discharging sinuses and fistulas should be treated appropriately because these also contribute to halitosis.

Treatment of halitosis with non-oral origin:

If the origin of the halitosis is non-oral, and systemic cause of halitosis has been identified, the patient should be referred to an appropriate specialist. However, a brief description of the treatment of various systemic diseases relating to halitosis is given here,

The most common reason for non-oral halitosis is ENT or pulmonary infection. Most common ENT infection is pharyngitis which may of viral or bacterial origin. Bacterial pharyngitis is most commonly caused by streptococci. Treatment with antibacterial agents eliminates the infection and also eliminates oral malodor 95. In the case of acute sinusitis, the origin of infection may be dental. Most commonly, endodontic infection of second molars results in sinusitis. The endodontic treatment or extraction of the involved tooth is recommended along with broad spectrum antibiotics. Chronic sinusitis may result from various underlying causes. The treatment should be done depending on the underlying cause. The treatment of chronic tonsillitis involves elimination of deep crypts which harbors micro-organisms. Antibiotic treatment is recommended to eliminate the infection.

A common gastrointestinal cause of oral malodor is gastro-esophageal regurgitation. The treatment includes…….

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Treatment of Halitophobia

 Around 0.5-1% of people among the adult population believe that they have halitosis but actually they don’t have it. The constant feeling that they have bad breath, affects their social life. In spite of adequate counseling and treatment, these patients do not get convinced that they do not have bad breath. For this reason, these patients keep on consulting different oral health care providers for the treatment of this condition. Other than the conversation with the patient, the treatment of this condition is poorly documented in psychiatric literature 97. Cases of halitophobia described in literature resemble the psychiatric syndrome of social phobia 98.

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Pseudo halitosis:

Patients with pseudo halitosis believe that they have bad breath when they actually don’t have it. But, after diagnosis and therapy, they get convinced that they do not have halitosis. These patients often show symptoms of depression 99.

 

Olfactory reference syndrome

It is a mental disorder in which there is a persistent, false belief about and preoccupation with emitting abnormal body odor(s), which are foul and offensive to other individuals 100. These patients misinterpret the normal behavior of other people such as sniffing, touching nose or opening a window, as being referential to a body odor which in reality is non-existent. The disorder is commonly associated with shame, embarrassment, significant distress, avoidance behavior, social phobia and social isolation 101. There is aggrement on the treatment protocol for this condition. However, in most of the cases, antidepressants, antipsychotics, and various psychotherapies have been used 102.

Conclusion

Halitosis affects the social life of an individual and affects his/her personal relationships also. Most commonly, patients suffering from the condition use masking agents to get temporary relief from the problem. However, it does not solve the problem. Oral health professionals are an excellent judge of halitosis and with proper history taking, can identify the exact underlying cause of halitosis. As already stated, around 90% of oral malodor cases have an oral origin, so appropriate dental/periodontal treatment usually eliminates the condition. When the systemic origin of halitosis is anticipated, the patient should be referred to concerned person for treatment of the underlying cause.

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References:

References available in the hard copy of the website

Periobasics: A textbook of periodontics and implantology

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