Halitosis
- Part II
Drs.
Evi Stamou and xxxxxxx Davidovitch
ORAL CAUSES OF MALODOR
Formation of oral malodor Unpleasant oral odor usually results from sulphur containing proteins and peptides being hydrolysed by gram negative bacteria in an alkaline environment. Production and release of volatile compounds, and later detection of these oral malodorous substances, appears to depend on many local factors such as: Salivary pH, reduced ambient oxygen concentration, bacterial population and the substrate available for bacterial metabolism.
Production of putrid odors is associated with oral conditions contributing to a shift from gram positive to gram negative bacteria(10). Conditions that favour the retention of anaerobic G¯ bacteria are thought to contribute to odor production(23,24). This bacterial shift is caused by reduced salivary flow, reduced carbohydrates available as bacterial substrates, and a rise in the oral pH(23).
Tonzetich and Richter were first to report that oral malodor is primarily associated with volatile sulphur compounds (VSC), rather than amines and ammonia. VSC are produced in the oral cavity through the putrefactive action of micro-organisms on exogenous and endogenous proteinaceous substrates, including exfoliated cells, leukocytes, saliva, blood, and food debris (1).
Hydrogen sulfide and methyl mercaptan have been cited as the major gases associated with halitosis (3,6,18,23,25). Since dimethyl sulfide is usually present in trace amounts, hydrogen sulfide and methyl mercaptan are the main constituents of VSC in mouth air (6). Besides the presence in exhaled air of VSC's, oral malodor can also be caused by also short-chain fatty acids, such as butyric, propionic, and valeric acids. In addition, polyamines such as putrescine and cadaverine also contribute to oral malodor. These compounds result from the proteolytic degradation by oral bacteria of sulfur containing peptides and amino acids from the saliva, gingival cervicular fluid, blood, and desquamated epithelial cells (26).
Yaegaki and coworkers showed that hydrogen sulfide is produced largely from the tongue dorsum, and that malodor from periodontal tissues is enriched with methyl mercaptan and dimethyl sulfide(8).
Role of tongue in malodor
In people with rigorous oral hygiene, clean and intact dentition and a healthy periodontium, the source of bad breath is likely to be the posterior aspect of the tongue (5,27). Coating of the tongue has a significant influence on VSC (5,16,18,25) and eventually on odor formation(9,20,28). Organoleptic and VSC values are directly related to this condition(9). The relationship of the tongue to malodor has been reported and confirmed by several investigations (9,18,20,28,29). The amount of tongue odor may be related to the degree of oral malodor(16,20). Tongue coating is a result of epithelial cells from the oral mucosa, microorganisms, and leukocytes from periodontal pockets(18). These compounds are the principal malodorants in halitosis (6).
The surface anatomy of the tongue provides an ideal environment for collection of desquamated cells, food debris and bacterial growth, all of which are capable of causing odors (10). Hairy or fissured tongues are believed to cause malodour as well(14).
Fissures and crypts of the tongue can harbour large quantities of the above mentioned species. Surface irregularities protect the bacteria from the flushing action of saliva and possess low oxygen levels which facilitate their growth. The presence of significant amounts of bacteria on the tongue has also been found to correlate strongly with malodor. In fact, most researchers suggest that the increased microbial density on coated tongues was responsible for malodor. However, this, was not confirmed in the study of Quirynen et.al.(9). The constant desquamation of the tongue mucosa might explain the absence of a relationship between bacterial colonization and odor production (9).
The posterior area of the dorsal surface of the tongue can be assessed by scraping it with a disposable plastic spoon which frequently yields a sample of a yellowish discharge. Although there is no direct evidence, this discharge is probably postnasal drip(27). Postnasal drip is extremely common and may not be indicative of any frank nasal infection or other pathological condition. Although postnasal drip might not be odiferous when initially contacting the tongue (M. Littner, D.M.D., and M. Rosenberg, Ph.D., unpublished data, 1994), it can subsequently be putrified by the abundant tongue microbiota (5).
Yaegaki and Sanada have shown that the tongue is the major contributor in healthy mouths to production of oral malodor. Coating of tongue may be an important factor that accelerates VSC production in subjects with or without periodontitis (28).
The results of a study by Miyazaki et al. suggest, that oral malodor might be caused mainly by tongue coating in younger subjects, and by periodontal diseases together with tongue coating in older individuals in the general population (18).
Furthermore, Yaegaki and Sanada suggested that removal of tongue coating markedly reduced both VSC production and the methyl mercaptan ratio, both in orally healthy subjects and in patients with periodontal disease (28).
Periodontitis and oral malodor
It has been demonstrated that periodontal disease and tongue coating are the major source of VSC, and therefore, the cause of offensive odors (18). The mechanism responsible for this is believed to be the metabolism of colonizing bacteria situated on the tongue dorsum and periodontium and their modulation by salivary flow rate. This latter aspect has been shown to be varied by normal daily the function, as well as food impaction and diet (8).
The association between periodontal disease, tongue coating and bad breath has reported by several researchers (3,6,11,14,16,18,20,25,28,30). Tonzetich observed a positive correlation between the severity of periodontitis and VSC content in the mouth (18). In addition, the existence of active periodontal disease has been associated not only with causing halitosis, but also with its intensification (11). Periodontal pockets are believed to be the main site of VSC production in affected patients (20,28). Furthermore, bleeding pockets contain higher VSC levels than healthy sites(9).
Several factors have been shown to contribute to the malodor produced by periodontitis (9):
a) The shift towards a more Gram
negative microbiota. These produce hydrogen sulfide and methyl mercaptan (9).
Sulfur containing amino acids and peptides serve as a substrate for the G¯ anaerobic
bacteria in their production of VSC (23).
b) Increase in cervicular fluid volume carrying metabolic products(9)
c) Bleeding tendency of the periodontal tissues which provides essential substrates
for odor production(9)
d) Increased salivary putrefaction (9)
e) Significant periodontal pockets which permit the trapping of food (14)
Salivary putrefaction and production of disagreeable odors has been demonstrated to occur more rapidly in patients with periodontal disease (10,31,32). Saliva from periodontally involved individuals contains greater total number and proportion of damaged epithelial cells (11), disintegrated cells (7) and leukocytes than samples collected from essentially healthy mouths (Dreizen, Gilley and Spies, 1956) (11). Almost all of the VSC of saliva is produced from the salivary sediment which is essentially composed of epithelial cells, leukocytes and micro-organisms (11). Blood and cellular elements provide the essential substrates for odor production. Blood provides certain factors, which accelerate bacterial growth, and stimulates proteolysis and odor production of putrescent saliva. Numerous microorganisms indigenous to saliva, dental plaque, gingival crevice and tongue possess marked odor-producing potential (7). Therefore, putrefactive activity in the oral cavity is the principal source of VSC, and, hence oral malodour in periodontally involved subjects (Tonzetich 1971) (11,16).
Yaegaki and Sanada (25,28) have provided evidence that the methyl mercaptan-to-hydrogen sulfide ratio in tongue (WHAT'S THIS "IN TONGUE"), disulfide content and oral malodor changes as a function of the severity of periodontal disease. However, it is unclear whether variation of methyl/mercaptan, hydrogen sulphide can account for a difference in the qualities observed (25). Methyl mercaptan /hydrogen sulfide ratio in patients with a gingival sulcus probing depth of 4mm or more, was much higher than in subjects with healthy periodontium (16,25,?28). This finding was reported to increase in proportion to the bleeding index, reflecting the extent of periodontal disease (25), ie. the intensity of the odor increases with the severity of the disease (16).
However, since disulfide concentration is only in trace amounts, elevated concentration of methyl mercaptan, rather than hydrogen sulfide, may accelerate the progress of periodontal disease because methyl mercaptan is present in high concentrations in patients suffering from this condition (28). Much more VSC, especially methyl mercaptan, was produced by dorsal tongue surfaces in periodontal patients. Whereas, methyl mercaptan is the main component of VSC in patients with periodontal disease, hydrogen sulfide is found in higher concentrations in orally healthy subjects(25). It has been suggested that VSC production (11,29) in periodontal pockets(11), and tongue dorsum in subjects with periodontal disease(16) especially methyl mercaptan(29) accelerate periodontal disease (11,29). The produced mechanism for this is due to the effect of methyl mercaptan increasing the permeability of oral mucosa more so than than a similar concentration of hydrogen sulphide(29). Meaning, that VSC increases the permeability of the oral mucosa, decreases protein and collagen solubility and protein or collagen synthesis, thus VSC's may be considered to be involved in pathogenesis of periodontal disease(25).
Yaegaki and Sanada(28) reported that tongue coating, microrganisms, gingival fluid, as well as plaque in PDL pockets as being one of the main sources of VSC production in periodontal disease patients. In addition, that these play an important role in accelerating methyl mercaptan production in the oral cavity. These results contradict those of Kaizu who suggested that tongue coating in PDL disease can not be a major source of VSC production (28). Furthermore, saliva may make only a minor contribution to pathological odor production (25).
Positive correlations between VSC levels in mouth air as well as in gingival pockets were also reported by Kozlovsky et al.(1), who found that deep and shallow pockets yielded high scores of VSC compounds. Many oral bacteria, including those isolated from deep periodontal pockets, are capable of producing VSC, primarily hydrogen sulfide and methyl mercaptan, from serum and from L-cysteine and L-methionine (Persson et al.,1990).(1). Among the organisms capable of proteolysis and VSC production are pathogenic strains of bacteroides melaninogenicus which have been implicated in the pathogenesis of periodontal disease. Of significance is that these organisms produce copious amounts of hydrogen sulfide, methyl mercaptan and dimethyl sulfide (Tonzetich and McBRide,1977) and are found more frequently in deep than in shallow gingival sulci( Nolte,1973)(11).
In a study by Miyazaki et al. (18), an association between VSC and periodontal conditions was observed in older age groups. These findings coincide with those of Rosenberg et al. This might suggest that for people in the general population with relatively low levels of VSC, oral malodor is caused by a combination of several factors, including periodontal conditions, tongue coating, and/or qualitative salivary characteristics and salivary flow rate (18).
Furthermore, Tonzetich and Spouge (1977)(2) also showed that a positive correlation between the number of periodontal pockets in excess of 3mm depth and the VSC content of mouth air. However, Rosenberg et al. demonstrated only a weak association between the presence of pockets greater than 5mm deep and both organoleptic and VSC measurements.
Hydrogen sulfide can be converted to methyl mercaptan in the oral cavity(25). The levels of 2-ketobutyrate are increased in the oral cavity of patients with periodontal disease, which indicates that the metabolism of methionine to methyl mercaptan is low (25).
Although periodontal pockets are believed to be important sites for VSC production, an association between them and VSC levels or organoleptic scores was not established in the study of Bosy et.al.(1994) and Loeshe et al.(1996). These failed to show any difference between mean values of tongue odor in subjects with or without periodontitis (16). The former study also indicated that the tongue dorsum contributed to the oral malodor and VSC content of total mouth air. Therefore, Bosy et. al. concluded that the tongue is an important site of odor production in periodontally healthy subjects.
Gingival fluid
The concentration of methyl mercaptan in mouth air correlated with the severity of periodontal disease, which increased the gingival crevicular fluid flow rate. The supply of methionine from gingival fluid is greater than that of cysteine or cystine. Metabolism of methionine is accelerated in periodontal pockets. The elevated methyl mercaptan production in periodontal pockets in turn would exacerbate the periodontal disease since methyl mercaptan has been demonstrated to be more cytotoxic than hydrogen sulphide(25).
Oral factors causing halitosis
A recent report by Delanghe et al. (33), in a multidisciplinary Breath Odor Clinic indicated that in 87% of the consulting patients, oral malodor could be related to an oral cause. Poor oral hygiene and the presence of prosthetic appliances contribute to the development of oral candidiasis(10). Dentures particularly if made of vulcanite rather than acrylic resin can cause a type of halitosis referred to as 'denture breath'(14). Unclean removable dental prostheses (i.e. dentures), particularly those worn continuously (3), also contribute to oral malodor(3,5).
Trauma, local infections or neoplasms may cause lip ulcerations (10). Healing of dental extraction sites, necrotic tissues from ulcerations (14), and areas of inflammation/healing harbor gram negative bacteria(10). Susler and others (30) have reported that carious lesions are sites of food retention and putrefaction. Other loci of oral microbial putrefaction include, areas of food impaction, and improper dental restorations (3,5,31). Poorly contoured restorations should be replaced or recontoured(31).
Diseases of dental pulp can provide an environment favourable to noxious gas production (10). Xerostomia (decreased salivary flow)(3,10), can contribute to a reduced cleansing action and a change in the oral flora toward gram-negative organisms responsible for oral malodors. The daily cycle of salivary flow affects bad breath in an inverse relationship (5). Another cause of malodor include abcesses which drain into the oral cavity(5).
The incidence of active dental caries has a marked effect on mouth and breath odors(11,12,18). Carious lesions harbor bacteria and retain food which combine to produce bad breath through putrefaction (18). However, other studies (5,11), claim that the contribution of active carious lesions to bad breath occurs only when the lesions are large enough to entrap food (5,11).
Bacterial dental plaque also possesses a strong potential to form odor from substrates containing cysteine, cystine, methionine, nutrient broth, and salivary sediment to yield similar volatile compounds produced through salivary putrefaction. The capacity of plaque to utilize salivary substrate for odor production was established by the utilization of lyophilised fractions of saliva(7).
Deposits of oral microorganisms of plaque on teeth or in periodontal pockets may contribute to bad breath (20). Eight to fourteen hours maturation are required before plaque deposits produce VSC (16). Protected plaque in interproximal sites produces substantial odors and is associated with overall VSC levels, the observation in this study (WHICH STUDY????) indicated that oral malodor production in healthy individuals may originate from protected interdental sites(16). Bosy et al.(16) and Kozlovsky et al.(1), however did not find a correlation between plaque index and VSC levels. The results might indicate that oral malodor production in healthy individuals may originate from protected interdental sites (16). A weak correlation was found between VSC levels and plaque index by Rosenberg et al. (2), and Miyazaki et al. (18).
Recent studies indicated that in addition to periodontal pockets and dorsal tongue surface, most pathogens colonize other niches of the oral cavity such as mucosal surfaces and the saliva. Quiryen et.al., shed doubt on the role of lingual plaque in the production of malodor since non-microbial elements are reported to predominant (9). The amount and pathogenicity of plaque on intraoral hard surfaces (teeth, dentures, or endosseous implants) was found to correlate positively with the roughness of the area (9).
Gingivitis may give rise to putrefactive odors (11,12,34). There is a marked increase in both general and mouth odor intensities(12). Malodorous sulphur compounds in mouth air were found to increase quantitatively in subjects with gingivitis compared to control subjects(18). Salivary volatile sulphur production increased with deterioration in gingival health and conversely, decreased with maintenance of optimal periodontal conditions(18).
Pyorrhea gives rise to a foul odor that is reflected in both general and mouth odor. Odor intensity with age seems to progress more rapidly in women than in men which may be due to the fact that women mature more rapidly than men (12).
However, this correlation was not found in regards to the mouth odor samples (12). As far as mouth odor in the aging female population is concerned, the increase in its intensity with age was found to be appreciably less in women (12). It would seem that any pathologic condition of the oral cavity contributes to in the problem of mouth and breath odors. Therefore, excellent oral hygiene and timely dental operative procedures may play a definite and constructive part in the alleviation of bad breath arising in the mouth. Mouth conditions that produce breath odors are in order of their importance, pyorrhea, gingivitis, and caries (12).
Secondarily, CPITN, time since latest oral activity, and self-diagnoses were found to have significant influences on VSC (18). Time after meals, gender (12) and age (12,18), were all found to be factors in the production of breath and mouth odors. Malodor is intensified during states of dehydration, overindulgence and retention of aromatic foods in the mouth (Massler, Emslie and Bolden 1951) (11).
Age
As reflected in the literature, age is considered a controversial factor contributing to oral malodor. According to Sulser(12), odor intensity increases with age and odor intensity and bad breath is quite prevalent in older people. Gingival recession, commonly found in the older sector of the population, possibly related to a reduction in the effectiveness of the immune system, provides areas in which food may be trapped/impacted. This acts to make available to the bacterial population nutrients which they metabolize through putrefaction, hence producing mouth malodor. Furthermore, this condition causes a greater tendency toward pyorrhea which would in-and-of-itself cause an increase in odors(12).
Rosenberg et al.(2) also showed an age related increase in both organoleptic and VSC measurements. Miyazaki et al.(18), however, demonstrated that age did not contribute to VSC increase. Miyazaki demonstrated that age was a risk factor for deterioration of periodontal disease and/or tongue coating rather than for VSC increase.
Gender-specific differences in oral malodor
Sulser (12) showed that there is difference in odor intensity between males and females and the difference is related to age. Females exhibit odor intensity more rapidly with age than males, whereas the increase of odor intensity of the mouth odor is appreciably less in females compared to males. According to Sulser et al.(12),the increase in odor intensity with age seems to progress more rapidly in women than in men which may be due to the fact that women mature more rapidly than men. However, at an older age, the increase in odor intensity is less in women probably because women are more concerned about oral hygiene than men(12).
Howeveer, no difference in oral malodor between males and females was demonstrated in the studies by Miyazaki et al.(18) and Rosenberg et al.(2). Rosenberg et al. demonstrated that the age related increase in both organoleptic and VSC measurements were similar in the 2 sexes.
Bacteria
The majority of cases of oral malodor are thought to be due to bacterial activities in the mouth (5,35) but many of the bacterial species responsible have not yet been identified(35). The assimilatory reduction of sulphate to sulphide is carried out by many bacterial groups during the synthesis of sulphur containing amino acids and coenzymes (35).Gram negative anaerobic bacteria have been reported to be positively correlated to odor formation(26,35).
Experimental evidence strongly suggests that putrefaction of sulphur-containing proteinaceous substrates by predominantly gram-negative oral microorganisms is the primary cause of oral malodor(7). Optimum putrefactive activity occurs in a low carbohydrate environment, and under anaerobic conditions (7,16) together with the existence of physiological pH(7). However, Bosy et al. reported that optimum activity for the reduction of oral malodor occurs above a neutral pH. They concluded that no direct association existed between pH and the presence of oral bacteria (16). Salivary sediment containing exfoliated cells is the primary source from which the disulfide substrates are derived as part of the putrification process.
Putrefaction involves a range of gram-negative microorganisms, including species of Fusobacterium(5,25), Haemophilus, Veilonella(5), T. Denticola (5,26) and P. gingivalis(5). Proteolysis and reduction of disulfide bonds precedes the formation of odor. The odor intensity of putrescent saliva and plaque vapor have been correlated with the concentration of volatile sulphur compounds consisting of hydrogen sulphide, methyl mercaptan, and dimethyl sulphide(7).
Although Gram-positive bacteria usually do not produce odor under laboratory conditions, one research group has recently suggested that proteolysis by gram-positive Stomatococcus mulaginus contributes to malodor produced on the dorsum of the tongue(5). Some of these potentially malodorous bacterial species have been isolated from the dorsal surface of the tongue resemble the malodorous microflora found in subgingival plaque (26).
Bacteria associated with gingivitis and/or periodontitis(9) (porhyromonas gingivalis, prevotella intermedia/nigrescens(9,26), Actinobacillus actinomycetemcomitans, Campylobacter rectus (9), Fusobacterium nucleatum (9,26), Peptostreptococcus micros(9), Bacteroides forsythus (9,16,26), Bacteroides melaninogenicus(11), Eubacterium species (9,26), and Spirochetes), are known to produce large amounts of volatile sulfur compounds that create malodor(9).
Other oral Gram-negative microorganisms such as Spirochetes, fusiforms, vibrios, veilonella (16) and other subgingival species (26) have the capacity to produce oral malodor(16) methyl mercaptan and hydrogen sulphide(26), presumably through putrefaction of sulfur-containing protein substrates such as cystine(16), cysteine, methionine(16,26) or serum proteins(26). Regardless of periodontal status, the most objectionable odor is produced when large numbers of disintegrated epithelial cells covered with bacteria are trapped in plaque and in crevices of the tongue dorsum (16).
Willis et al (35), reported that the concentration and activity of sulphate-reducing bacteria were negatively correlated with malodour. Sulphate reducing bacteria have been detected in the mouth of healthy adults (posterior and anterior tongue, sub-and supragingival plaque, mid-buccal mucosa and vestibular mucosa). Sulphate reducing bacteria would be found at sites where the redox potential is low as in subginigival plaque and tongue biofilm samples. Volatile sulphur compounds produced by bacteria have been proposed as major components of oral malodor in healthy individuals. The fact that sulphate reducing bacteria are negatively associated with malodor seems to imply that sulfide produced during dissimilatory sulphate reduction might not make a significant contribution to this condition. This negative association suggests that competition may be occuring between these bacteria and other organisms responsible for the generation of malodour. This may be due to the direct inhibition by sulphate-reducing bacteria or the growth of large numbers of odorigenic bacteria out-competing sulphate centers for key substrates.
Another possible explanation for the different numbers of sulphate-reducing bacteria in individuals may be differences in activity or amount of mucin sulphatases which are responsible for cleavage of sulphate from the glycosylated side-chains of human salivary mucin molecules. Thus, the source of oral malodour remains unclear, but it seems likely that interactions between several groups of organisms in the mouth may be responsible(35). Non-sulphur compounds have also been implicated in halitosis(35).
Halitosis in children
The presence of bad breath in young subjects was reported by Amir(21) who observed children between 5-14 years of age. Significant correlations were observed between whole mouth malodor levels and other odor assessments such as nasal odor, tongue dorsum anterior odor, and tongue dorsum posterior odor. Whole mouth malodor was also significantly associated with other parameters such as plaque index, the oratest and the number of gingival sulcuses which bleed upon being probed (21).
The posterior part of the tongue was significantly associated with a wide range of odor and dental parameters: whole mouth odor, nasal odor, tongue dorsum anterior odor, interdental odor, mouth breathing, regular brushing habits, presence of tongue coating, presence of bleeding on tooth brushing, and presence of food impaction. Anterior tongue dorsum odor appeared to be highly related to a history of throat infection and was also associated with regular brushing habits and bleeding on brushing(21).
Plaque index levels were associated with brushing, bleeding on brushing, tongue coating, food impaction, floss odor, mouth breathing and history of throat infections.
Bad breath in children is generally similar to adults. More significant positive correlations were found in this study between bad breath parameters and dental parameters such as plaque index, number of bleeding sites, food impaction, tongue coating, and regular toothbrushing. The study of Amir et al.(21), underlies the importance of nasal odor in this group and suggests nasal odor and oral parameters. Nasal odor was related to several specific oral odors, particularly with tongue dorsum posterior malodor, the presence of tongue coating, and brushing habits. Oral malodor in many adults is related to tongue odor caused by putrefaction of postnasal drip, which accumulated on the back of the tongue.
The role of tonsils in chronic malodor is unclear. Parents commonly report a transient oral malodor coincident with the onset of sore throat in children(21).
Together, the above mentioned studies suggest that bad breath in children is related to both nasal and oral odor, with posterior tongue odor being of particular significance. Malodor parameters were generally improved by an increased awareness of the importance of oral hygiene(21).
Treatment of halitosis
The treatment of halitosis involves paying attention to oral hygiene, tooth and tongue brushing, dental flossing, and proper management of gingivitis and gum disease(6). Tongue brushing and tooth brushing resulted in reduction of VSC for a period of 2-3 hours (18). Patients with oral malodor are encouraged to reduce smoking, eliminate offending foods, eat at regular intervals, make regular visits to a periodontist, and brush and floss daily as directed(6).
Most successful treatments include mechanical debridement of the tongue surface(6,26), combined with the use of an antimicrobial mouth rinse. Mouth rinses containing zinc chloride were remarkably effective in reducing malodor, as measured by both organoleptic score and by the amounts of methyl mercaptan in exhaled air(26).
Most of the agents that appear to reduce malodour, have antibacterial activity. Mouth rinses containing zinc salts as the active ingredient rely on the strong affinity of zinc ions for thiol groups present in VSC. The binding of zinc would render hydrogen sulphide and methyl mercaptan nonmalodorous by converting them into non-volatile sulfides. This approach treats the symptom(s) of bad breath rather than its etiology(26).
Self Diagnosis of oral malodor Participants are unaware of their objective malodor (17,42). Paradoxically, the breath of those who complain vociferously about its offensive odour usually smells sweet, whereas those with unpleasant breath do not notice it (17).
In a study by Rosenberg et al.(43), it was found that subjects were generally unable to score their own malodor in an objective fashion. It appears that in the general population, those who are not concerned about having bad breath do have some inherent, objective ability to determine its level (43). However, those who are concerned about the problem are largely subjective in their appraisal and are relatively unable to sense improvement (43).
Rosenberg and McCulloch(8) also reported that people possessing foul bad breath are often unaware of it, whereas many individuals who have relatively low malodor levels may be excessively concerned that they have bad breath. Clearly, self diagnosis of bad breath is a subject of considerable public interest.
Conclusion
Both periodontally healthy and diseased individuals can exhibit significant levels of oral malodor levels and VSC. Therefore, oral malodour alone is unlikely to be diagnostic of the presence of periodontitis. It might also be the case that whether periodontal disease is currently active is more significant than the presence of deeper pockets. As etiology of halitosis is multifactorial, careful differential diagnosis should be carried out.
REFERENCES
1 Kozlovsky A., Gordon D., Gelertner I., Loesche W.T., and Rosenberg M.: Correlation between the BANA test and oral malodor parameters. J Dent Res 73: 1036, 1994
2 Rosenberg, M., Kulkarni, G.V., Bosy A., and McCulloch C.A.G.: Reproducibility and sensitivity of oral malodor measurements with a portable sulphide monitor, J Dent Res 70:1436, 1991
3 Rosenberg M., Septon I.,Eli I., Bar-Ness R.,Gelernter I., Brenner S., and Gabbay J.: Halitosis measurement by an industrial sulfide monitor. J Periodontol 62:487,1991
4 Attia EL., Marshall KG.: Halitosis. Can Med Assoc J 126:1281,1982
5 Rosenberg M.: Clinical assessment of bad breath: Current concepts. JADA 127: 475,1996
6 Nachnani S. and Clark G. T.: Halitosis: A Breath of fresh air. CID 25 (Suppl 2):218, 1997
7 Tonzetich J.: Production and origin of oral malodor: A review of mechanisms and methods of analysis, J Periodontol48: 13,1977
8 Rosenberg M. and McCulloch C.A.G.: Measurement of Oral malodor: Current methods and future prospects. J Periodontol 63: 776, 1992.
9 Quirynen M., Mongardini C., and Van Steenberghe D.: The effect of a 1- Stage Full-Mouth disinfection on Oral Malodor and Microbial Colonization of the tongue in periodontitis patients. A pilot study. J Periodontol 69: 374, 1998 1
0 McDowell J., Kassebaum D.: Diagnosing and treating halitosis JADA, 124:55, 1993
11 Tonzetich J.: Oral malodour: an indicator of health status and oral cleanliness. Int Dent J 28:309, 1978
12 Sulser G. F., Brening R. H., and Fosdick L. S.: Some conditions that effect the odor concentration of breath. J Dent Res 18:355, 1939
13 McNamara T.F., Alexander J.F., and Lee M. and Plains M.: The role of microorganisms in the production of oral malodour. Oral Surg.34:41, 1972
14 Lu D.P.: Halitosis: an etiologic classification, a treatment approach, and prevention.Oral Surg Oral Med Oral Patho 54:521, 1982
15 Kleinberg I., Westbay G.: Salivary and metabolic factors involved in oral malodor formation. J Periodontol 63:768, 1992
16 Bosy A., Kulkarni G.V., Rosenberg M., and McCulloch C.A.G.: Relationship of oral malodor to periodontitis: Evidence of independence in discrete subpopulations. J Periodontol, 65:37, 1994.
17 Hawkins C.: Real and imaginary halitosis. Br Med J, 294:200, 1987
18 Miyazaki H., Sakao S., Katoh Y., Takehara T.:Correlation between volatile sulphur compounds and certain oral health measurements in the general polulation. J Periodontol 66:679, 1995
19 Preti G.,Clark L., Cowart B.J., Feldman R.S., Lowry L.D.,Weber E., and Young I. M.: Non-oral etiologies of oral malodor and altered chemosensation. J Periodontol 63:790, 1992
20 Neiders M., Ramos B.: Operation of bad breath clinics Quintessence International, 30:295, 1999
21 Amir E., Shimonov R., Rosenberg M.: Halitosis in children The Journal of Pediatrics, 134:338,1999
22 Malasi T.H., El-Hilu S.R., Mizra I.A. and Fakhr El-Islam M.:Olfactory Delusional Syndrome with various aetiologies. British Journal of Psychiatry 156:256, 1990.
23 Waler S.M.: The effects of some metal ions on volatile sulfur-containing compounds originating from the oral cavity Acta Odontol Scand 55:261, 1997
24 Tonzetich J, Ng SK.: Reduction of malodour by oral cleaning procedures Oral Surg Med Oral Path 42:172,1976.
25 Yaegaki K. and Sanada K.: Biochemical and clinical factors influencing oral malodor in periodontal patients. J Periodontol 63: 783, 1992
26 Loesche W.J.: The effect of antimicrobial mouthrinses on oral malodor and their status relative to US food and drug administration regulations. Quintessence International 30:311,1999
27 Rosenberg M., Leib E.: Experiences of an Israeli malodor clinic. In: Bad breath: Research Perspectives. Ramot publishing, Tel-Aviv University; pp.139, 1997
28 Yaegaki K, Sanada K.: Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease.J Periodont Res 27:233,1992.
29 Miyazaki H, Fujita C, Soh I, Takehara T.: Relationship between volatile sulphur compounds and oral conditions in the general Japanese population.In: van Steenberghe D. Rosenberg M.eds. Bad breath, A Multidisciplinary approach. Leuven: Leuven University Press; 165,1996
30 Rosenberg M., Gelernter I., Barki M., and Bar-Ness R.: Day-long reduction of oral malodor by a two-phase oil: water mouthrinse as compared to chlorehexidine and placebo rinses. J Periodontol 63:39,1992
31 Kostelc JG, Preti G, Zelson NH, Stoller NH, Tonzetich J.: Salivary volatiles as indicators of periodontitis. J Periodont Res 15:185, 1980
32 Crohn BB.: Halitosis in relation to oral diagnosis. Am J Orthodontics Oral Surg 28:109, 1942.
33 Delanghe G, Ghyselen J. Feenstra L. van Steenberghe D.: Experiences of a Belgian multidisciplinary breath odor clinic. In: van Steenberghe D. Rosenberg M, eds. Bad Breath. A multidisciplinary Approach. Leuven: Leuven University Press: 1996; 199
34 Kostelc JG., Preti G., Zelson PR, Brauner L., Baechni P.: Oral odor in early experimental gingivitis. J Periodont Res 19:303,1984
35 Willis C. L., Gibson G.R., Holt J., Allison C.: Negative correlation between oral malodour and numbers and activities of sulphate-reducing bacteria in the human mouth. Archives of Oral Biology 44: 665, 1999
36 Sterer N., Greenstein B.N., Rosenberg M.: ß-Galactosidase activity in saliva is associated with oral malodor. J Dent Res 81:182, 2002
37 Bhide V. M., Smith L., Overall C. M., Birek P., and McCulloch C.A.G.: Use of a flourogenic septapetide matrix metalloproteinase assay to assess responses to periodontal treatment. J of Periodontol, 71:690, 2000
38 Lindhe J.: Textbook of Clinical Periodontology, Pg.76, Fig.2-10a
39 Lindhe J.: Textbook of Clinical Periodontology, Pg.76, Fig.2-9
40 Rosenberg M.: Bad Breath, Research Perspectives, Ramot Publishing, Tel-Aviv University, 3, 1997
40 Zhu W. Sha Y., Chung-Hua Kou Chiangi, Hsuch Tsa Chih.: The relationship between oral malodor, VSCs levels in the mouth air with periodontitis and tongue coating. Chinese Journal of Stomatology 37(4):300,2002
41 Lucas V., Omar J., Vieira A., Roberts G.J.: The relationship between odontogenic bacteremia and orthodontic treatment procedures. EJO 24: 293, 2002.
42 Rosenberg M.,Kozlovsky A., Wind Y., Mindel E.: Self-assessment of oral malodor 1 year following initial consultation. Quintessence International 30:324, 1999