Oral Health Group
Feature

Pipelines for Halitosis

October 1, 2011
by Getulio Nogueira, DDS


WHAT IS IT? 
Halitosis or bad breath, oral malodor, foetor oris, or foetor ex ore, refers to the sense of an unpleasant smell in someone’s breath. Halitosis is not necessarily a disease but a sign indicating that something may be wrong in the body. Equally so it could be physiological or caused by poor oral hygiene. Making an analogy with the fever, bad breath may represent a warning or a breakdown of homeostasis.

In general, halitosis can be distinguished by three main types: (i) True halitosis, (ii) Pseudo-halitosis and (iii) Halitophobia. The term true or real halitosis is used when bad breath that can be diagnosed organoleptically or by means of analytical methods. Pseudo-halitosis is when the patient is convinced that he/she has bad breath but no obvious odor can be detected. Halitophobia is when, after successful treatment of true halitosis or in the case of pseudo-halitosis, the patient remains convinced that they suffer from bad breath (Yaegaki & Coil, 2000).

Advertisement






Bad breath can originate from sources other than the mouth. Several pathological conditions have been related to oral malodor, including respiratory tract infection, sinus infections, several pathological entities of the gastrointestinal tract and some metabolic diseases. However, clinical surveys have shown that over 90% of all bad breath odor originates in the mouth (van Steenberghe, 2004).

Halitosis is characterized primarily by the emanation of foul odors from the mouth, and thus is characterized as a human condition of public interest. It affects a large segment of the population and can lead to the development of neuroses, social isolation, divorce and suicide (Rosenberg, 1992). In spite of its consequences, it is still rarely addressed in the field of scientific research, in contrast to great public interest on the subject (Kazor & Loesche, 2002).

WHAT ARE THE CAUSES?
In the morning, on waking up, the breath is usually stronger and unpleasant due to a drastic reduction in the salivary flow during sleep associated with the accumulation and decay of oral squamous cells, food debris and saliva especially on tongue surface and mucosa. Then, this accumulation forms a whitish layer on the tongue, especially in the posterior third, called the tongue coating (TC). The epithelial cells contained in TC are composed of proteins rich sulfur-containing amino acids, and due to a biochemical process that occurs in the presence of some bacterial species in the oral cavity, these compounds are released as gases, causing the mouth bad odor. It is important that people realize that morning breath is physiological and a proper oral hygiene routine can eliminate it.

Persistent oral malodor though is due to the formation of a series of volatile chemicals, of which the sulfur compounds are the most studied. The volatile substances derived from sulfur, known generically as volatile sulfur compounds (VSC) include hydrogen sulfide (H2S), methyl mercaptan (CH3SH), dimethyl sulfide (CH3) 2S and dimethyl trisulfide (CH3) 2S3, which are often produced in the oral environment by metabolizing protein substrates by some members of the oral microbiota (Tonzetich, 1977). Other odorous substances such as indole, skatole, cadaverine, putrescine and short-chain fatty acids contribute less to oral malodor, because, although present and smelly, they are insufficiently volatile in the oral environment due to the high molecular weight and salivary pH (Tonzetich, 1967).

As a matter of fact, the presence of low concentrations of oxygen and the salivary proteolytic anaerobic microorganisms contribute even more to halitosis as bacteria proliferate intensely in the tongue fissures, and villous surface irregularities of lingual tonsils (Yaegaki & Sanada, 1992; Bosy et al, 1994). Thus, the presence of TC is considered the second major cause of halitosis (36% of cases), while the major cause, according to several studies (van Steenberghe, 2004, Delangue et al, 1997), is still attributed to periodontal diseases i.e. gingivitis (27%) and periodontitis (24%). Studies suggest that most cases of halitosis are related to the metabolic activity of bacteria, especially those living on the surface of the tongue and dental biofilms (see Table 1).

WHAT IS THE RELATIONSHIP WITH PERIODONTICS?
Dental sciences have ignored the problem of bad mouth odor and failed to recognize it as a clinical entity that needs further attention. Almost three decades have passed since Tonzetich’s (1977) description of the biological basis of halitosis but the scientific interest in this area is relatively recent. The specialty of periodontics took up leadership in this area of research because the high prevalence of periodontal diseases in the adult population and the potential of bad breath to serve as a diagnostic marker of periodontal disease. Although still scarcely used, several studies introduced the notion of ‘periodontal halitosis’ (Loesche et al. 1983; Faveri et al., 2006, Cortelli et al., 2008).

Using the experimental gingivitis model, Kostel et al. (1984) -‚ by means of gas chromatography and Nogueira-Filho et al. (2002) – by means of halimeter measurements, both demonstrated that the production of sulfhydryl groups increase in saliva of subjects with gingivitis and then decrease upon return to in gingival health. Significant associations between the severity of periodontal disease and oral malodor has been demonstrated in subjects with poor oral hygiene habits or in individuals who develop substantial amount of biofilm (Yaegaki & Sanada, 1992; De Boever et al., 1994, Miyazaki et al, 1995, Söder et al, 2000, Figueiredo et al., 2002; Nogueira-Filho et al, 2008).

On the other hand, evidence supporting the contribution of known periodontal pathogens in halitosis is indirect and based on the ability of the subgingival bacterial biofilm containing periodontal putative bacteria to produce VSC (F.nucleatum, T.denticola, P.intermedia, P. gingivalis, T.forsythia, Eubacterium sp). These bacteria, among other species that colonize the subgingival environment, can produce large amounts of hydrogen sulfide and methylmercaptan from methionine, cysteine or serum proteins and develop true halitosis related to periodontal diseases (Persson et al, 1989, Persson et al, 1990). These studies also indicated that periodontal microbiota is involved in the formation of oral malodor, as they have the necessary enzymes in vivo and have access to amino acids and peptides present in the fluid and gingival bleeding (Morita et al, 2001).

Yaegaki and Sanada (1992) described the effect of removing the tongue coating by scraping or tongue brushing to reduce halitosis in patients with signs of adult periodontitis. Also, the authors observed higher concentrations of VSC in the breath of patients with periodontal pockets greater than or equal to 4mm in depth when compared to patients who had less than 4mm pockets. They suspected that high concentrations of VSC, especially methylmercaptan, could preclude or indicate progression of periodontal attachment loss.

The epidemiological study by Miyazaki et al. (1995), with 2,672 Japanese workers, revealed that the presence of TC in patients with periodontal health, assessed by the Community Index of Periodontal Treatment Needs (CPITN), were statistically associated with levels of VSC. The authors suggest that in young individuals, the cause of oral malodor was most strongly related to the presence of TC, whereas in the elderly it is related to the association between the presence of TC and periodontal disease.

Studies have shown that bacterial species involved in the etiology of periodontal disease, such as Spirochetes ssp, Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans can colonize the tongue surface that acts as microbial reservoir in the oral environment (Goodson 1994, Quirynen et al., 2001). These authors suggest the cleaning of TC and the use of topical antimicrobial agents on tongue surfac
e should be an integral component of periodontal treatment.

HOW TO DIAGNOSE?
The techniques and strategies for diagnosis and treatment of halitosis are based on research methods (Tonzetich, 1977; Yaegaki & Coil, 2000). However, clearly defined and easily quantifiable clinical protocols for the diagnosis of halitosis are lacking.

The examiner can check the breath by smelling the exhaust air through the mouth of the patient and classify it according to a scale (as organoleptic). This technique is considered the gold standard for diagnosis of halitosis in daily clinical practice. For the organoleptic evaluation, the patient is instructed to close his/her mouth for one minute and then to slowly exhale the air through the mouth at a distance of 10cm from the examiner’s nose, which uses a scale of 0 to 5 (see table 2) to assign a score to the patient’s breath (Yaegaki & Coil, 2000).

VSC portable monitors, for example, the Halimeter® (Interscan Corporation-USA) are devices that are available worldwide. The Halimeter® has been used both in research and in clinical practice as this instrument is easy to use and can detect VSC in parts per billion (ppb); its results are expressed as the total concentration of the oral VSC (Yaegaki & Sanada 1992, Bosy et al., 1994, Rosenberg et al., 1991 a, b). The Halimeter® has a high sensitivity to hydrogen sulfide, but lower sensitivity to methylmercaptan. Despite the fact that this instrument is easy to handle at a low cost, the Halimeter®, cannot be used in the presence of high levels of alcohol and/or after eating certain foods like garlic or onions. Therefore interpretation of the results with these instruments requires a degree of training.

Therefore, methods of diagnosis other than organoleptic chairside assessment and portable monitor of halitosis (Halimeter®) all additional methods are still high-cost procedures that are justified and practical only for scientific use (gas chromatography – GC, gas chromatography mass spectrometry – GCMS and the biochemical and microbiological analysis of saliva).

WHAT TO DO TO PREVENT BAD BREATH? 
Simple and daily practices can prevent halitosis arising from non-pathological origins: i) drink water regularly, ii) a balanced diet including fibers, iii) cleaning the tongue, iv) avoiding excessive consumption of foods with odors like garlic, peppers or onions, v) having small meals every three to four hours, vi) avoid alcohol and smoking, vii) maintain high quality personal oral hygiene, including the use of dental floss and cleaning of the tongue; viii) regular visits to the dentist to prevent cavities and periodontal disease (gingivitis and periodontitis).

WHAT TO DO TO TREAT HALITOSIS? 
The treatment of halitosis should aim at the elimination of its the cause. Hence, the first step is to identify the etiology. Since diagnosis is imprecise and the vast majority of cases of halitosis are of oral origin (Delangue et al, 1997), elimination of the most prevalent intraoral causes makes therapeutic sense. The therapy of halitosis should be tailored according to the individual needs of each patient. Common therapeutic approaches should be considered: a) reduction of intra-oral bacterial load, b) reducing the availability of protein nutrients for bacteria, since the microbes responsible for converting VSC are proteolytic, c) removal of the tongue coating, and d) periodontal assessment and treatment.

Whereas the dorsal surface of the tongue and the dental biofilm are the main reservoirs of bacteria that produce VSC, periodontal treatment procedures, and an effective control of bacterial biofilms associated with the hygiene of the dorsal surface of the tongue are measures of fundamental importance. In cases of patients with special needs, where the ability of performing oral hygiene procedures is compromised, assisted oral hygiene measures have to be delivered by family or attending staff. Instructions for mechanical removal of dental plaque (toothbrushing, dental flossing) must be provided and individually adapted. Devices of tongue cleaning, prescription of antimicrobial toothpastes and mouthwashes should be integral part of regular professional dental checkups.

The use of alcohol-free mouthwashes can help in tackling the “cosmetic” bad mouth odor, but should not be considered as the sole treatment. The use of antiseptics, for the most part, does not treat halitosis effectively; rather serve to “mask” it and provide a more pleasant breath while the product is active in the oral cavity. Antiseptics, however, can help to reduce halitosis (e.g. chlorhexidine gluconate or zinc chloride in the formulations). Chlorhexidine has the ability to remain active in the oral cavity up to 12 hours due to its ability to adsorb to mucosal and dental surfaces, albeit its side effects of staining of teeth and tongue requires professional prophylaxis performed by a dentist or dental hygienist. Oral mouthwashes containing zinc have also been listed as VSC reducers with duration of three hours (Yaegaki & Suetaka, 1989; Rosing et al, 2002). In addition to mouthwashes, several toothpastes have demonstrated antimicrobial and anti-halitosis effectiveness even with the use of regular commercial toothpastes (Nogueira-Filho et al, 2000, Nogueira-Filho et al, 2002, Nogueira-Filho et al, 2008; Peruzzo et al, 2007; Peruzzo et al, 2008, a, b).

FINAL THOUGHTS
• Halitosis affects a large proportion of the population with a significant impact on the social behavior of the affected subjects.

• The diagnostic methods are imprecise and rather arbitrary. If oral malodor persists after elimination of the most common intra-oral causes of bad breath differential diagnosis may require a medical evaluation involving other health care professionals.

• The use of portable monitors in the dental office is useful but requires careful interpretation. In reality, dentists should use the organoleptic evaluation of breath as their primary diagnostic method.

• Periodontal treatment and maintenance are key factors in the prevention and treatment of halitosis. Emphasis should be placed on personal oral hygiene habits in addition to professional prophylaxis and periodontal treatment.

• More studies are needed to evaluate the effectiveness of antimicrobial agents as adjuncts to prevent and treat halitosis.OH

Dr. Getulio Nogueira is Assistant Professor, Department of Preventive Dentistry, Faculty of Dentistry, University of Toronto, Canada.

Oral Health welcomes this original article.

REFERENCES
1. Bosy A, Kulkarni GV, Rosenberg M, Mcculloch CAG. Relationship of oral malodor to Periodontitis: evidence of independence in discrete subpopulations. J periodontal. 1994; 65(1): 37-46.
2. Cortelli JM, Aquino DR, Cortelli SC, Franco GC, Fernandes CB, Roman-Torres CV, Costa FO. Detection of periodontal pathogens in oral mucous membranes of edentulous individuals. J. Periodontol. 2008; 79(10): 1962- 65.
3. De Boever EH, Uzeda M, Loesche WJ. Relationship between volatile sulfur coumpounds, BANA hydrolysing bacteria and gengival health in patients with or without complaints of oral malodor. J Clin Dent. 1994; 4: 114-19.
4. Delanghe G, Ghyselen J, van Steenberghe D, Feenstra L. Multidisciplinary breath-odour clinic.
5. Lancet. 1997 Jul 19;350(9072):187.
6. Faveri M, Feres M, Shibli JA, Hayacibara RF, Hayacibara MM, Figueiredo LC. Microbiota on the dorsum of the tongue after plaque accumulation: an experimental study in humans. J Periodontol. 2006; 77: 1539-46.
7. Figueiredo LC, Roseti EP, Marcantonio Jr E, Marcantonio AC, Salvador, SL. The relationship of oral malodor in patients with or without periodontal disease. J Periodontol. 2002; 73: 1338-42.
8. Goodson JM. Antimicrobial strategies for treatment of periodontal disease. P
eriodontol 2000. 1994; 5: 142-68.
9. Kostelc JG, Preti G, Zelson PR, Brauner L, Baehni P;. Oral odors in early experimental gingivitis. J Periodontal Res. 1984; 19: 303-12.
10. Loesche WJ, Gusberti F, Mettraux G, Higgins T, Syed S. Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infect Immun 1983; 42: 659-67.
11. Loesche WJ, Kazor C. Microbiology and treatment of halitosis. Periodontol 2000. 2002; 28: 256-79.
12. Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation between volatile sulphur compounds and certain oral health measurements in the general population. J Periodontol. 1995; 66: 679-84.
13. Morita M, Wang HL. Relationship of sulcular sulfide level to severity of periodontal disease and BANA test. J Periodontol. 2001; 72: 74-78.
14. Nogueira-filho GR, Duarte PM, Toledo S, Tabchoury CP, Cury JA. Effect of triclosan dentifrices on mouth volatile sulphur compounds and dental plaque trypsin-like activity during experimental gingivitis development. J Clin Periodontol. 2002; 29(12): 1059-64.
15. Nogueira-filho GR, Peruzzo DC, Sallum AW. Relationship between the formation of volatile sulfur compounds (VSC) and the severity of the periodontal disease: a pilot study. J Breath Res, 2 (4pp) 017005. doi:10.1088/1752-7155/2/1/017005. 2008
16. Nogueira-filho GR, Toledo S, Cury JA. Effect of 3 dentifrices containing triclosan and various additives. An experimental gingivitis study. J Clin Periodontol. 2000; 27(7): 494-98.
17. Persson S, Claesson R, Carlsson J. The capacity of subgengival species to produce volatile sulfur compounds in human serum. Oral Microbiol Immunol. 1989; 4: 169-72.
18. Persson S, Edlund M-B, Claesson R, Carlsson J. The formation of hydrogen sulfide and methyl-mercaptan by oral bacteria. Oral Microbiol Immunol. 1990; 5: 195-201.
19. Peruzzo DC, Jandiroba PF, Nogueira-Filho GR. Use of 0.1% chlorine dioxide to inhibit the formation of morning volatile sulphur compounds (VSC). Braz Oral Res. 2007; 21(1): 70-74.
20. Peruzzo DC, Salvador SL, Sallum AW, Nogueira-Filho GR. Flavoring agents present in a dentifrice can modify volatile sulphur compounds (VSC) formation in morning bad breath. Braz Oral Res. 2008; 22(3): 252-57.
21. Peruzzo DC, Salvador SL, Sallum AW, Nogueira-Filho GR. Effects of sodium lauryl sulphate (SLS) present in dentifrice on volatile sulphur compound (VSC) formation in morning bad breath. J Int Acad Periodontol. 2008; 10(4): 130-36.
22. Quirynen M, De Soete M, Dierickx K, Van Steenberghe D. The intra-oral translocation of periodontopathogens jeopardises the outcome of periodontal therapy. J Cin Periodontol. 2001; 28: 499-507.
23. Richter JL. Diagnosis and treatment of halitosis. Compend Contin Educ Dent. 1996; 17(4): 370-76.
24. Rosenberg M, Kulkarni GV, Bosy A, McCulloch CA. Reproducibility and sensitivity of oral malodor measurements with a portable sulfide monitor. J Dent Res. 1991; 70: 1436-40.
25. Rosenberg M, Septon I, Eli I, Bar-Ness R, Gelernter I, Brenner S, Gabbay J. Halitosis measurement by an industrial sulfide monitor. J Periodontal. 1991; 62: 487-89.
26. Rosenberg M. Measurement of oral malodor: current methods and future prospects. J Periodontal 1992; 63(1): 776-82.
27. Rosing CK, Jonski G, Rolla G. Comparative analysis of some mouthrinses on the production of volatile sulfur-containing compounds. Acta Odonto Scand 2020; 60: 10-12.
28. Schmidt NF, Tarbet WJ. The effect of oral rinses on organoleptic mouth odour ratings and levels of volatile sulfur compounds. Oral Surg Oral Med Oral Pathol. 1978; 45: 560-67.
29. Söder B, Johansson B, Söder PO. The relationship between foetor ex ore, oral hygiene and periodontal disease. Swed Dent J. 2000; 24: 73-82.
30. Tonzetich J. Oral malodor: an indicator of heath status and oral cleanliness. Int Dent J. 1978; 28: 308-19.
31. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol. 1977; 48: 13-20.
32. Tonzetich J. Volatility as a factor in the inability of certain amines and indoles to increase the odor of saliva. Arch Oral Biol. 1967; 12: 1167 – 75.
33. van Steenberghe D. Causes of breath malodor. In: van Steenberghe D, ed. Breath Malodor a step-by-step approach. Copenhagen: Quintessence Publishing, 2004; 18- 31.
34. Yaegaki K, Coil JM. Examination, classification and treatment of halitosis; clinical perspectives. J Can Dent Assoc. 2000; 66: 257-61.
35. Yaegaki K, Sanada K. Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodontol Res 1992; 27: 233-38.
36. Yaegaki K, Suetaka T. The effect of zinc chloride mouthwash on the production of malodour, the degradations of cellular elements and proteins. J Dent Health. 1989; 9: 377-86.