This artical reviews the etiology, diagnosis and treatment of oral malodor from a periodontal perspective. The connections among periodontal pathogenic microorganisms, periodontal disease and oral malodor is probably not caused by periodontal disease, there is ample evidence to suggest that periodontal disease increases the severity of oral malodor.
Oral malodor, also called halitosis or bad breath, is universally experienced condition that has a variety of etiologic factors. Offensive odors emanating from the oral cavity have been attributed to certain odoriferous foods, such as garlic and onion; some medications;1 foreign bodies;2 systemic illnesses;1,3,4 and various infections;5 but they are most commonly attributed to bacteria.6 Several nonoral sites have been linked to oral malodor, including the air passages (nose, sinuses, pharynx and lungs), the gastrointestinal tract, and some solid tissue organs (kidneys and liver).1,3,4 Although numerous nonoral sites and many different causes have been correlated to bad breath, an estimated 80 percent to 90 percent of all bad breath odors originate from the mouth,7 and bacteria are directly responsible for most of the offensive gases.6,8,9
The oral cavity has numerous microenvironments to harbor bacteria and contribute to oral malodor. Intraoral conditions such as poor oral hygiene, a tongue coating, extraction sites, necrotic tissues, extensive caries, open contacts allowing food impaction, prosthetic appliances, illfitting restorations, and inflammatory lesions of gingivitis and periodontitis contribute to oral malodors.1 There is evidence to suggest that oral malodor is caused by the microorganisms that cause gingivitis and periodontitis (i.e., periodontal pathogens).l0,ll This evidence, considered alone, could implicate periodontal disease as a causative factor leading to oral malodor. However, periodontally healthy individuals and those without teeth also experience oral malodor. Is it possible that oral malodor is an entity by itself, occurring independent of periodontal disease, or are the conditions related? Of particular interest is whether periodontal inflammatory diseases play an etiologic role in the production of oral malodor. The purpose of this article is to review the etiology, diagnosis and treatment of oral malodor from a periodontal perspective. The review will be limited to bad breath odors originating within the mouth.
The etiology of oral malodor is multifactorial. In the presence of adequate substrate with appropriate conditions, a sequence of events leads to the release into the oral cavity of pungent gases that pollute exhaled air and are perceived as bad breath. Research has identified several microorganisms that produce these offensive odors and provided a fair explanation of the conditions necessary for their production. In addition to the presence of certain types of bacteria, the type and amount of substrate, and oxygen and pH levels influence the occurrence and severity of oral malodor.
Certain chemical end products of bacterial putrefaction known as volatile sulfur compounds (VSCs) are foul smelling and determined to be responsible for the offensive odor recognized as bad breath.l2-l5 Nonsulfur-containing compounds such as cadaverine, putrescine, indole and skatolel6,l7 have also been implicated in the foul smell of oral malodor, but their contribution is thought to be limited.7 VSCs such as hydrogen sulfide, methyl mercaptan, dimethyl sulfide and dimethyl disulfide make up more than 90 percent of the putrid odors from the mouth.8 Two of these VSCs, hydrogen sulfide and methyl mercaptan, account for approximately 90 percent of the total VSCs identified with putrid odors from the mouth.9,l8
Specific groups of bacteria have been identified with the production of oral malodor. Using in vitro methods, McNamara and colleagues demonstrated that the formation of putrid odors from incubated saliva correlated with a shift in the microbial flora from a predominately gram-positive to a predominately gram-negative anaerobic flora.6 Concomitant with this shift in flora, they observed a depletion of carbohydrates and a rise in the pH level of the stagnant saliva. As the carbohydrates are depleted, the gram-positive acidogenic flora are suppressed and the gram-negative microorganisms, capable of protein metabolism, become progressively more dominant.7 Evaluated individually, none (n=9) of the gram-positive microorganisms produced an unpleasant odor whereas all (n=4) of the gram-negative microorganisms (Fusobacterium polymorphum, Veillonella alcalescens, Bacteroides fundiliformis, Klebsiella pneumoniae) produced a putrid odor.6 In a similar study, Solis-Gaffar and colleagues found that only the gram-negative microorganisms (Veillonella alcalescens, Fusobacterium nucleatum, Bacteroides melanogenicus and Klebsiella pneumoniae) produced VSCs.l9The production of VSCs was accompanied by an unpleasant odor and a rise in the pH level of the saliva mixture. Except for Klebsiella pneumoniae, all gram-negative microorganisms required blood in the mixture to produce VSCs. None (n=8) of the gram-positive microorganisms produced VSCs with or without blood products.l9
Anaerobic conditions, necessary for the production of VSCs, are created in microenvironments. The accumulation of plaque and debris and the stagnation of saliva occur most commonly in areas where tooth and tissue crevices lend themselves to stagnant microenvironments. The most common sites for stagnation, plaque accumulation and production of VSCs are the posterior dorsum tongue, interdental spaces and subgingival areas.l7 Dental plaque progresses from an aerobic, gram-positive colonization to one that is anaerobic, favoring gram-negative growth. As the bacterial plaque matures (0.1-0.2 mm thickness), the oxygen level drops to zero, favoring reduced conditions and the production of odoriferous volatiles.20 Oxygen depletion is attributed to the bacteria that use oxygen to oxidize substrates. Anaerobic bacteria produce foul-smelling VSCs from the sulfur-containing proteins and amino acids found in saliva and crevicular fluid.ll,2l Putrefactive formation of VSCs is favored by an alkaline pH (7.2) and inhibited by an acidic pH (6.5).7 The presence of glucose (0.02 M) also inhibits the formation of VSCs7
Specific sulfur-containing precursors are required for the bacterial production of VSCs. Proteinaceous substrates‹namely exfoliated epithelium, leukocytes, food debris and dead bacteria‹are degraded by proteolysis into peptides. and amino acids. The sulfur-containing amino acids, specifically cysteine and methionine, are further degraded into VSCs. Gas chromatographic studies have identified hydrogen sulfide and methyl mercaptan as the putrefactive end products of cysteine and methionine, respectively.22 Exfoliated epithelial cells and effused leukocytes are the major sources of protein with sulfur-containing amino acids.7,9,27 The severity of oral malodor (VSC level) is influenced by bacterial plaque levels, substrate availability, time of day and oral dryness.5 Oral malodor is worst in the morning, following an extended period of oral dryness and undisturbed bacterial putrefaction.8 Oral malodor improves following oral hygiene procedures.8 There is evidence to suggest that periodontal disease increases the severity of oral malodor.
Patients with chronic periodontitis and pocket formation frequently suffer from unpleasant mouth odor associated with accumulated debris and an increased rate of putrefaction.8,l0,ll,14,l5,23,24 The fetid odor characteristic of acute necrotizing ulcerative gingivitis is an extreme example of malodor from periodontal pathogens.25 Periodontal conditions that favor the bacterial growth and retention of debris contribute to oral malodor. Interproximal spaces and periodontal pockets are conducive to anaerobic growth and microenvironments for the production of VSCs. These subgingival and interproximal periodontal malodors make a significant contribution to overall oral malodor.26,27
In an evaluation of oral malodor in healthy subjects and patients with periodontal disease, Yaegaki and Sanada found that bleeding on probing and periodontal pocket depth positively correlated with the production of VSCs.l5 Deep periodontal pockets (3-5mm) were more likely to harbor and promote the growth of VSC-producing microorganisms. Samples of interdental plaque, obtained with dental floss, demonstrate the production of offensive VSCs.28,29 VSCs, specifically hydrogen sulfide and methyl mercaptan, have been identified in patients with gingivitis and periodontitis.l0,l2,30 In fact, a positive correlation has been reported between the amounts of hydrogen sulfide produced and the depth of periodontal pockets.31 An increase in production of VSCs from periodontal pockets provides a plausible explanation for the intensification of oral malodor observed in patients with periodontal disease.
Periodontal pathogens have been positively correlated with oral malodor.ll-l5 Several periodontal pathogens ‹ including Treponema denticola, Porphymonas gingivalis and Bacteroides forsythus ‹ have been identified, with BANA hydrolysis, on the posterior tongue, contributing to oral malodor.13,32,33 Additional periodontal pathogens, including Fusobacterium nucleatum and Bacteroides melanogenicus have been identified as VSC formers.8,19 These microorganisms produce copious amounts of hydrogen sulfide, methyl mercaptan and dimethyl disulfide.34
Several studies suggest that periodontitis increases the severity of oral malodor.7 One possible explanation is the increased amount of substrate available to be metabolized. In patients with periodontitis, more sulfur-containing protein substrate is available through increased exfoliation of epithelial cells and crevicular effusion of leukocytes.7 Sato and colleagues found that the number of leukocytes increased in the saliva of patients with periodontitis and that the level of methyl mercaptan produced correlated with bleeding on probing,, pocket depth and gingival exudate.23 In another study, the metabolism of methionine to methyl mercaptan was found to be significantly higher in the saliva of patients with periodontitis.11 Together, these findings suggest that inflamed periodontal tissues provide more methionine, which is converted into methyl mercaptan at a higher rate than for healthy gingival tissues. Indeed, methyl mercaptan contributes significantly to the oral malador in patients with periodontal disease.35 The concentration of methyl mercaptan in mouth air correlated with the severity of periodontal disease. The increased gingival crevicular fluid flow in periodontitis may be a continual source of methionine.11
Bacterial samples from the tongue in individuals with severe oral malodor were consistently found to be positive for BANA hydrolysis.l3~33 Subjects with higher oral malodor (organoleptic measurements) and VSC scores had more positive BANA hydrolysis and bleeding on probing than individuals with low scores, suggesting that peri-odontal pathogens and the coexistence of periodontitis played a significant role in those individuals with severe oral malodor.13 The average amount of tongue coating in patients with periodontal disease was six times greater than the amount in healthy indi-viduals.15 The estimated production of VSC from the tongue coating was four times greater in individuals with periodontal dis-ease.1l~ls The greater tongue coating in these periodontal patients comprises ep-ithelial cells, leukocytes and microorganisms released from peri-odontal pockets.11
In contrast to the view that periodontal disease contributes to oral malodor, Bosy and colleagues found that oral hygiene levels and not periodontal pockets were more indicative of oral malodor,36 which supports the concept that oral malodor may be an independent entity. Certainly, some gram-negative anaerobic bacteria, which are not known to be periodontal pathogens (Fusobacterium polymorphum, Veillonella alcalescens, Bacteroides fundiliformis and Klebsiella pneumoniae) have been identified with oral malodor.6,19 The bacteria contributing to oral malodor in healthy individuals are most commonly located on the posterior dorsal tongue surface as opposed to in periodontal locations.17
In addition to being a major contributor to oral malodor, VSCs have been implicated in the disruption of oral mucosa and may contribute to the progression of periodontal disease.37 As currently understood, periodontal disease progression consists of a shift in the bacterial plaque from a gram-positive aerobic flora to a gram-negative anaerobic and motile flora. Some studies suggest that the production of VSCs by these microorganisms may contribute to the progression of periodontal disease via breakdown of the oral mucosa leading to bacterial invasion.38 Ng and Tonzetich found that the permeability of porcine sublingual mucosa increased 75 percent and 103 percent following exposure to hydrogen sulfide and methyl mercaptan, respectively.37 This finding suggests that the VSCs of oral malodor could contribute to the pathogenesis periodontitis.
There are a number of methods, from simple to sophisticated, used to detect or diagnose the presence of oral malodor. These tests can be categorized into self-assessments, subjective mea-surements, objective instrumental analysis and indirect measurements (Table 1). Nearly everyone has attempted the simple self-assessment of blowing into a cupped hand and smelling one's own breath. Studies have demonstrated that oral malodor cannot be accurately diagnosed by the individual being evaluated.39,40 However, partial objectivity can be obtained in the case of self-measurement if the stimulus is removed from the body properly either by allowing a saliva sample to dry outside the mouth and smelling it or by using dental floss to sample and smell interproximal plaque.39
Subjective measurements have been used reliably to evaluate oral malodor.26 Another individual or judge sniffs the expelled mouth air of the patient and scores the offensive level of oral malodor. This method is often referred to as organoleptic. Some individuals have a ³nose² for it and can be calibrated well for repeated measurements. The subjective nature of this method presents some obvious problems in objectivity. Because of the training required for judges, this method is exclusively used for research.
Objective instrumental analysis includes the use of gas chromatography to measure the presence of specific VSCs in expelled mouth air. It is an excellent means of accurately determining the levels of specific compounds. It is so precise that it can be used to measure minute differences in VSC levels before and after mouth rinses or other oral hygiene procedures.26 The disadvantages include high cost, time required, expertise required and lack of portability. For these reasons, gas chromatographic measurements are restricted to studies with small sample populations. The portable sulfide monitor, a more practical VSC measuring device, has recently become available. It accurately measures the total amount of VSCs in a sample of mouth air. Advantages include its portability, low cost, rapid analysis time and the limited training necessary. Measurements with a portable sulfide monitor have been shown to be more accurate than organoleptic measurements.29 The main disadvantages are that it is incapable of distinguishing among individual sulfide compounds and that measurements are not reliable in the presence of alcohol or essential oils. The latter problem precludes the use of portable sulfide monitors in mouthrinse studies.26
Attempts have been made to measure oral malodor using indirect methods such as in vitro incubation of saliva and cultures of bacterial isolates. These methods have been used successfully to study and understand the putrefaction process. However, this data must be interpreted with caution because the intraoral environmental factors cannot be replicated in vitro. Some indirect methods have been employed to evaluate for the presence of known pathogenic bacteria. The specific contribution of bacterial pathogens to oral malodor can be assessed in selected cases or studies using BANA hydrolysis. The use of this high technology test for the detection of oral malodor may be limited because it is an indirect measure used to determine the presence of the periodontal pathogenic microorganisms. It does not measure the malodorous VSCs.
Oral malodor is a multifactorial problem that requires a well-defined approach to diagnosis and treatment. Successful treatment is associated with the ability to identify the major and minor contributing factors and to address them with appropriate and effective therapy. When periodontitis, pathologically deep pockets or heavy deposits are identified in an individual with chronic halitosis, treatment of the periodontal disease and improved oral hygiene can produce excellent clinical outcomes.7 Numerous oral hygiene devices and chemical agents can be implemented to improve plaque control and thus effectively manage oral malodor. Patient education about oral hygiene practices is crucial to the successful treatment of oral malodor associated with periodontitis. Periodontal pockets and defective and overhanging restorations that are difficult or impossible to clean should be treated to improve access and correct defects. The successful treatment of periodontal disease is greatly dependent on the patient's daily practice of good oral hygiene to control bacterial plaque growth and progression. Likewise, the successful treatment of oral malodor is greatly dependent on personal oral hygiene.
The evaluation, diagnosis and treatment of an individual with oral malodor that has a periodontal disease component might follow a diagnosis and treatment algorithm as seen in Figure 1. The patient with concerns about malodor is screened for halitosis by organoleptic or portable sulfide monitor (A). If the patient is positive for oral malodor, a separate screening test is conducted to determine whether the odor is originating from the mouth, nose or both (B). If the source of oral malodor is from the mouth, a complete oral examination is indicated (C). Clinical examination for signs and symptoms of periodontal disease remains the most common method for detection of gingivitis and periodontitis. Observation for clinical signs of erythema in the gingiva are diagnostic for current periodontal inflammation. Measuring probing pocket depths with a periodontal probe detects previous attachment loss, calculus deposits and periodontal pocket formation. Although not predictive of future periodontal breakdown, bleeding/exudate from the periodontal pocket or increased temperature within the pocket can indicate disease activity. Radiographic examination determines the degree of prior bone loss and helps detect areas that are inaccessible to cleaning, such as overhangs, caries and furcations. A diagnosis of periodontitis would lead to a series of steps including oral hygiene instructions (D) specifically directed at the periodontal condition and plaque control, periodontal therapy (E) for pocket reduction, plaque control and calculus removal followed by a re-evaluation (F) to determine disease control. Any poor restorations, overhangs or caries should also be treated and/or corrected. The specific contribution of bacterial pathogens to the oral malodor can be assessed in selected cases via indirect methods such as BANA hydrolysis. (G) However, the BANA hydrolysis test is an indirect measure used to determine the presence of the periodontal pathogenic microorganisms. As mentioned above, these tests do not measure the offending compounds.
The ultimate goal of treatment for oral malodor should be directed at eliminating or at least reducing the causative microorganisms and associated substrates. If the microorganisms' quantity and plaque maturity are controlled, then their capabilities to produce VSCs is greatly reduced. The substrate available for metabolic breakdown should likewise be eliminated or reduced with good oral hygiene and control of periodontal inflammatory disease.
An estimated 80 percent to 90 percent of all bad breath odors originate from the mouth and are caused by bacteria. Anaerobic bacteria, oxygen depletion, alkaline pH and sulfur-containing substrates are some of the requirements for oral malodor to occur. The accumulation of plaque and debris and the stagnation of saliva occur most commonly in areas where tooth and tissue crevices lend themselves to stagnant microenvironments. The most common sites for the production of VSCs (hydrogen sulfide and methyl mercaptan) are the posterior dorsum tongue, interdental spaces and subgingival areas.
The association among periodontal pathogenic microorganisms, periodontal disease and oral malodor has been strongly implicated but not proved. A1though oral malodor is probably not caused by periodontal disease, there is ample evidence to suggest that periodontal disease increases the severity of oral malodor. Periodontitis worsens the severity of oral malodor by providing additional sites of VSC production (interdental and subgingival), an increased availability of sulfur-containing substrate (exfoliated epithelial cells and leukocytes) and an increased rate of methionine metabolism (precursor to methyl mercaptan). Periodontitis contributes to an increased tongue coating with higher VSC production. There is evidence to suggest that VSCs, i.e., oral malodor, may contribute to the progression and pathogenesis of periodontal disease via increased mucosal permeability. Treatment for oral malodor should be directed at eliminating or at least reducing the causative microorganisms and the associated substrates with diligent oral hygiene procedures. It is essential to diag nose and control any periodontal disease that may coexist and worsen the severity of oral malodor.
Author, Perry R. Klokkevold, DDS, MS, is an adjunct assistant professor and clinical director at the University of California at Los Angeles School of Dentistry in the Section of Periodontics.
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For printed copies of this article, please contact: Perry R. Klokkevold, DDS, MS, UCLA School of Dentistry. Section of Periodontics, 63-022A CHS Dental, Los Angeles, CA 90095-1668
This article has been printed with the consent of the California Dental Association
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