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. 2020 Mar 6;33(1):34–38. doi: 10.1016/j.sdentj.2020.02.005

The association between periodontal diseases and halitosis among Saudi patients

Hamad Alzoman 1,⁎
PMCID: PMC7801244  PMID: 33473240

Abstract

Objectives

To assess the relationship between the presence of periodontal disease and halitosis.

Methods

A total of 120 patients were enrolled and divided into 2 groups, 60 patients with probing depth (PD) > 3.0 mm (group 1) and 60 patients with PD ≤ 3.0 mm (group 2). Clinical parameters including, plaque index (PI), bleeding index (BI), and PD were obtained. Breath samples were collected and analyzed using a portable gas chromatograph to measure the concentration of volatile sulfur compounds (VSC).

Results

Halitosis was found to affect 58.3% of the total patients. The means of PI, BI, and VSC were significantly higher in group 1 (PD > 3.0 mm) than in group 2 (PD ≤ 3 mm).

Conclusions

The percentage of patients suffering from halitosis in the Saudi population are comparatively high. In addition, there was a positive association between periodontal disease and halitosis.

Keywords: Oral malodor, Periodontitis, Volatile sulfur compounds, Oral chroma

1. Introduction

Halitosis or oral malodor are common terms used to define a hostile or unpleasant odor emitted from the oral cavity. It can cause both health and social dilemmas that affect the life of subjects who suffer from this condition (Silva et al., 2020, De Jongh et al., 2016, De Jongh et al., 2014, De Jongh et al., 2013, Zalewska et al., 2012). The cause of halitosis is connected to both systemic and oral disorders. Several studies demonstrate that the oral cavity is one of the important sources for halitosis (Scully and Greenman, 2012). Through an analysis of 491 subjects with oral malodor, Delanghe et al. (1999) demonstrated that approximately 87% originated primarily from the oral cavity, while 5–8% of halitosis were related to ear, nose, and throat (ENT) problems. Another report specified that 90% of halitosis cases were initiated by sources from the oral cavity (Tonzetich, 1977).

There are certain oral diseases and disorders which are connected with oral halitosis, such as gingivitis, periodontitis (De Geest et al., 2016, John and Vandana, 2006, Liu et al., 2004, Morita and Wang, 2001a), and acute herpetic gingivostomatitis (Kolokotronis and Doumas, 2006). In addition, other oral conditions could be connected with oral malodor, such as dental abscesses, aphthous ulcers, oral cancer, and xerostomia (Nachnani, 2011, Al Buquerque et al., 2010, Nally, 1990).

Volatile sulfur compounds (VSC) have been deliberated as the primary gases responsible for causing halitosis. VSC are generated as a result of protein putrefaction by gram-negative bacteria (Nakano et al., 2002). There are several VSC associated with halitosis, such as hydrogen sulfide.(H2S), methyl mercaptan.(CH3SH), dimethyl sulfide.(CH3SCH3), phenol, and pyridine. Numerous studies have confirmed that oral halitosis is caused mainly due to the presence of H2S, CH3SH, and CH3SCH3 in the exhaled breath (De Boever et al., 1994, Volozhin et al., 2001, Huang et al., 2002).

Periodontitis is reported as one of the important etiological factors of halitosis (Alshehri, 2016). Previous studies demonstrated that the occurrence of oral malodor is considerably greater in periodontal patients when compared to healthy persons. They further stated that there was positive correlation between oral malodor and the presence of sites with pockets of 5 mm or more (Bolepalli et al., 2015, Huang et al., 2002). Figueiredo et al. (2002) reported in their study that the relationship of periodontitis with oral malodor and VSC level was significantly higher in subjects with probing depth > 3 mm; further, they also observed that gingival inflammation contributes the intensity of oral malodour (Aizawa et al., 2005). The aim of this present study was to evaluate the relationship between the presence of periodontal disease and halitosis.

2. Materials and Methods

2.1. Patients and study design

This study was conducted among a total of 120 patients at a single center in Riyadh, Saudi Arabia. The protocol of the study was approved by the Ethical Review Committee of the College of Dentistry Research Center (CDRC), at King Saud University (IR 0028). Informed consent was obtained by all study participants.

A total of 120 systemically healthy patients with and without chronic periodontitis were selected from the outpatient. clinic of the College of Dentistry, King Saud University, Riyadh, Saudi Arabia. The inclusion criteria were (i) no periodontal therapy in the previous 3 months, (ii) systemically healthy, and (iii) 18 years old and older. Patients were excluded if (i) they smoked, (ii) had<12 teeth, or (iii) had received antibiotics within 3 months preceding the study.

The patients that met the inclusion criteria were assigned into 2 groups based on their periodontal condition: group 1 patients with periodontal disease with probing depth (PD) > 3 mm or group 2 (control) periodontally healthy patients with PD ≤ 3 mm.

2.2. Periodontal examination

The clinical periodontal parameters including PD and bleeding on probing (BOP) were assessed in all subjects using a periodontal probe at 6 points around all teeth. Moreover, the plaque index (Pl) was used to calculate adherent dental plaque score.

2.3. Oral malodour assessment

Three hours before oral breath assessment, all subjects were asked to avoid eating, drinking, chewing, brushing, and using mouthwash. The VSC concentrations in their oral cavity were examined using a portable gas chromatograph (OralChroma™, Kyoto, Japan) equipped with a flame photometric detector. A breath sample (1 ml) was taken using a gas-tight plastic syringe, then injected into the gas chromatography column at 70 °C. The concentrations of Hydrogen sulphide, Methyl mercaptan, and Dimethyl sulfide were determined. Halitosis was defined when the VSC of the breath sample was greater than or equal to the cognitive threshold as follows: H2S ≥ 112 PPB, CH3SH ≥ 26 PPB and CH3SCH3 ≥ 8 PPB (Aizawa et al., 2005).

3. Results

A total of 120 patients (60 men and 60 women) participated in this study with a mean age of 27.19 years (±6.3). Halitosis was found among 58.3% (n = 70) of the patients (Fig. 1).

Fig. 1.

Fig. 1

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Presence of Halitosis.

Halitosis was significantly more prevalent among the group 1 (PD > 3 mm) patients, 81.7% (n = 49), versus 35 % (n = 21) in group 2 (PD ≤ 3 mm) patients Table 1. Clinical parameters showed a higher mean score for PI, BI, and PD in group 1 compared to group 2 (Table 1).

Table 1.

Periodontal diseases and gender wise presence of halitosis.

Negative
 Positive
 Total
% N % N
Group 1
(PD > 3 mm Periodontitis)		 18.3 11 81.7 49 60
Group 2
(PD ≤ 3 mm Healthy)		 65.0 39 35.0 21 60
Total 41.7 50 58.3 70 120
p value 0.0001



Negative Positive
% N % N Total
Male 21.1 11 78.9 41 52
Female 58.0 39 42.6 29 68
Total 41.7 50 58.3 70 120.0
p value 0.001
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Fig. 2 shows the VSC scores of the study population. The VSC mean scores were found to be significantly higher among patients with periodontitis (group 1) compared to healthy patients (group 2).

Fig. 2.

Fig. 2

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Measurement of Volatile Sulfur Compounds.

Table 2 shows the clinical measurements of the study population. Comparing group 1 to group 2 patients, significant results were obtained in the clinical parameters of PD (p = 0.0001), BOP (p = 0.001) and PD (p = 0.001).

Table 2.

Clinical measurement of the study population.

Clinical measurement Group 1 Group 2
Mean SD Mean SD p value
Plaque index 69.6 21.5 28.2 34.2 0.000
Bleeding index 32.9 18.5 19.8 18.1 0.001
Probing depth 4.19 3.5 2.2 0.471 0.001
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4. Discussion

Earlier studies have reported that the important VSC that are related to halitosis are: H2S, CH3SH, and CH3SCH3 (Coli and Tonzetich, 1992, De Boever et al., 1994, Schmidt et al., 1978). Another study reported that VSC are the end result of bacterial putrefaction of proteins found in saliva, blood, and gingival crevicular fluid (Kleinberg and Westbay, 1992). Further, the amino acids comprising the sulfur compound leads to the formation of VSC (Waler, 1997, Yano et al., 2009).

In the present study, breath samples were taken from 120 patients to estimate the relationship between the presence of periodontal disease and halitosis using gas chromatography to identify the level of VSC. Gas chromatography is regarded as a reliable method to detect oral gases; it is specific and sensitive for all three VSC i.e. H2S, CH3SH, and CH3SCH3 (Tonzetich et al., 1991, Tangerman and Winkel, 2008, Murata et al., 2006), and is thus recognized as the gold standard for measuring VSC levels in the oral cavity (Tangerman and Winkel, 2008, Yaegaki et al., 2012).

In the present study, 58.3% of the patients were diagnosed with halitosis. This finding is consistent with a previously reported self-assessment of halitosis among Saudi patients, wherein 52% of were aware of having halitosis (Ashri, 2007). In addition, Al-Zahrani et al. (2011) reported self-reported halitosis to be 42.1% among patients with type 2 diabetes. In contrast to the above findings, Al Sadhan (2016) stated the prevalence of self-perceived halitosis to be 22.8% among adults living in Riyadh. This difference in prevalence of this study could be attributed to halitosis being assessed using a survey questionnaire without clinical assessment or breath examination. This asserts the magnitude of the problem that sensitivity of self-diagnosed halitosis is low, which therefore has a social impact (Bornstein et al., 2009a, Bornstein et al., 2009b). Pham et al., 2012a, Pham et al., 2012b compared self-perceived halitosis with the actual clinical diagnosis of 565 patients using both the organoleptic test and Oral Chroma and revealed that patients were incapable of precisely perceiving their own oral malodour. In their study, they reported that 52.6% of patients failed to recognize that they had halitosis (Pham et al., 2012a). They further reported that there are several factors that might affect self-perception of oral halitosis, such as occupation, level of education, knowledge of the self-definition of halitosis, and sensitivity of the nose to their own halitosis.

In this present study, the percentage of patients identified with halitosis in group 1 (PD > 3 mm) was 81.7%, whereas in group 2 (PD ≤ 3 mm) it was 35%, indicating a statistically significant difference between the two groups (p < 0.05). Further, this shows a high relationship between the presence of periodontal disease and halitosis. The result of this study coincides with an earlier report conducted by Morita and Wang, 2001a, Morita and Wang, 2001b which revealed that VSC increased significantly with an increase in the amount of bone loss, and were highly associated with other clinical parameters such as PD, clinical attachment level, and BOP (Morita and Wang, 2001b). Other studies reported a strong relationship between periodontal inflammation and halitosis (Figueiredo et al., 2002). In addition, Figueiredo et al. (2002)reported direct correlation of the severity of halitosis with periodontal disease. In patients with periodontal disease, the mouth harbors anaerobic bacteria such as T. denticola, P. gingivalis, B. forsythus. These bacteria are adept at producing VSC, which may lead to halitosis (Loesche, 2003, Yasukawa et al., 2010, Kato et al., 2005). Further development of periodontal disease has been connected to the hastening in the fabrication of VSC (Pham et al., 2012b, Takeuchi et al., 2010). Non-surgical treatments have proven to be an effective method in improving the periodontal clinical status of a person, as well as reducing halitosis (Silveira et al., 2017, Soares et al., 2015, Pham et al., 2011).

5. Conclusion

Within the limitations of this study, it could be concluded that the percentage of patients suffering from halitosis among the Saudi population are relatively high and there is a strong association between the presence of periodontal disease and halitosis.

6. Funding

This study was funded by King Abdulaziz City for Science and Technology, Riyadh, Kingdom of Saudi Arabia (Grant no. LGP-36-237).

7. Ethical statement

This study was conducted in accordance with the declaration of Helsink and study the protocol of the study was approved by the Ethical Review Committee of the College of Dentistry Research Center (CDRC), King Saud University, Riyadh, Saudi Arabia (IR 0028).

CRediT authorship contribution statement

Hamad Alzoman: Conceptualization, Methodology, Software, Data curation, Writing - original draft.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

I thank all the participants of the study.

Footnotes

Peer review under responsibility of King Saud University.

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.sdentj.2020.02.005.

Appendix A. Supplementary material

The following are the Supplementary data to this article:

Supplementary data 1
mmc1.pdf (294.3KB, pdf)

References

  1. Alshehri F.A. Knowledge and attitude of Saudi individuals toward self-perceived halitosis., Saudi. J. Dent. Res. 2016;7:91–95. [Google Scholar]
  2. Aizawa F., Kishi M., Moriya T., Takahashi M., Inaba D., Yonemitsu M. The analysis of characteristics of elderly people with high VSC level. Oral. Dis. 2005;11(Suppl 1):80–82. doi: 10.1111/j.1601-0825.2005.01099.x. [DOI] [PubMed] [Google Scholar]
  3. Al-Zahrani M.S., Zawawi K.H., Austah O.N., Al-Ghamdi H.S. Self reported halitosis in relation to glycated hemoglobin level in diabetic patients. Open. Dent. J. 2011;5:154–157. doi: 10.2174/1874210601105010154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Al Buquerque D.F., De Souza Tolentino E., Amado F.M., Araka W.A.C., Chinellato L.E. Evaluation of halitosis and sialometry in patients submitted to head and neck radiotherapy. Med. Oral. Patol. Oral. Cir. Bucal. 2010;15:e850–e854. doi: 10.4317/medoral.15.e850. [DOI] [PubMed] [Google Scholar]
  5. Al Sadhan S.A. Self-perceived halitosis and related factors among adults residing in Riyadh, Saudi Arabia. A cross sectional study. Saudi Dent. J. 2016;28:118–123. doi: 10.1016/j.sdentj.2016.06.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ashri N. Self-assessment of halitosis among diabetic Saudi Female Patients. Egyptian Dent. J. 2007:53. [Google Scholar]
  7. Bolepalli A.C., Munireddy C., Peruka S., Polepalle T., Choudary Alluri L.S., Mishaeel S. Determining the association between oral malodor and periodontal disease: a case control study. J. Int. Soc. Prev. Community. Dent. 2015;5(5):413–418. doi: 10.4103/2231-0762.165929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bornstein M.M., Kislig K., Hoti B.B., Seemann R., Lussi A. Prevalence of halitosis in the population of the city of Bern, Switzerland: a study comparing self-reported and clinical data. Eur. J. Oral. Sci. 2009;117:261–267. doi: 10.1111/j.1600-0722.2009.00630.x. [DOI] [PubMed] [Google Scholar]
  9. Bornstein M.M., Stocker B.L., Seemann R., Burgin W.B., Lussi A. Prevalence of halitosis in young male adults: a study in swiss army recruits comparing self-reported and clinical data. J. Periodontol. 2009;80:24–31. doi: 10.1902/jop.2009.080310. [DOI] [PubMed] [Google Scholar]
  10. Coli J.M., Tonzetich J. Characterization of volatile sulphur compounds production at individual gingival crevicular sites in humans. J. Clin. Dent. 1992;3:97–103. [PubMed] [Google Scholar]
  11. De Boever E.H., De Uzeda M., Loesche W.J. Relationship between volatile sulfur compounds, BANA-hydrolyzing bacteria and gingival health in patients with and without complaints of oral malodor. J. Clin. Dent. 1994;4:114–119. [PubMed] [Google Scholar]
  12. De Geest S., Laleman I., Teughels W., Dekeyser C., Quirynen M. Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists. Periodontol. 2016;2000(71):213–227. doi: 10.1111/prd.12111. [DOI] [PubMed] [Google Scholar]
  13. De Jongh A., De Baat C., Horstman M., Van Wijk A.J. Self-perceived oral odour and social interaction. Ned. Tijdschr. Tandheelkd. 2013;120:194–198. doi: 10.5177/ntvt.2013.04.12198. [DOI] [PubMed] [Google Scholar]
  14. De Jongh A., Van Wijk A.J., Horstman M., De Baat C. Attitudes towards individuals with halitosis: an online cross sectional survey of the Dutch general population. Br. Dent. J. 2014;216:E8. doi: 10.1038/sj.bdj.2014.101. [DOI] [PubMed] [Google Scholar]
  15. De Jongh A., Van Wijk A.J., Horstman M., De Baat C. Self-perceived halitosis influences social interactions. BMC. Oral. Health. 2016;16:31. doi: 10.1186/s12903-016-0189-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Delanghe G., Bollen C., Desloovere C. Halitosis–foetor ex ore. Laryngorhinootologie. 1999;78:521–524. doi: 10.1055/s-2007-996920. [DOI] [PubMed] [Google Scholar]
  17. Figueiredo L.C., Rosetti E.P., Marcantonio E., Jr., Marcantonio R.A., Salvador S.L. The relationship of oral malodor in patients with or without periodontal disease. J. Periodontol. 2002;73:1338–1342. doi: 10.1902/jop.2002.73.11.1338. [DOI] [PubMed] [Google Scholar]
  18. Huang X., Li X., Fan X., Liu H. Levels of volatile sulfur compounds and the analysis of related factors in oral cavities of 384 health subjects in Chengdu. Hua Xi Kou Qiang Yi Xue Za Zhi. 2002;20:380–382. [PubMed] [Google Scholar]
  19. John M., Vandana K.L. Detection and measurement of oral malodour in periodontitis patients. Indian. J. Dent. Res. 2006;17:2–6. doi: 10.4103/0970-9290.29899. [DOI] [PubMed] [Google Scholar]
  20. Kato H., Yoshida A., Awano S., Ansai T., Takehara T. Quantitative detection of volatile sulfur compound- producing microorganisms in oral specimens using real-time PCR. Oral. Dis. 2005;11(Suppl 1):67–71. doi: 10.1111/j.1601-0825.2005.01096.x. [DOI] [PubMed] [Google Scholar]
  21. Kleinberg I., Westbay G. Salivary and metabolic factors involved in oral malodor formation. J. Periodontol. 1992;63:768–775. doi: 10.1902/jop.1992.63.9.768. [DOI] [PubMed] [Google Scholar]
  22. Kolokotronis A., Doumas S. Herpes simplex virus infection, with particular reference to the progression and complications of primary herpetic gingivostomatitis. Clin. Microbiol. Infect. 2006;12:202–211. doi: 10.1111/j.1469-0691.2005.01336.x. [DOI] [PubMed] [Google Scholar]
  23. Liu Y., Huang H.Y., Zhang J.C., Wang S.L. The study of the relationship of malodor and microbial composition of interdental and subgingival plaques in periodontitis patients. Hua Xi Kou Qiang Yi Xue Za Zhi. 2004;22:466–470. [PubMed] [Google Scholar]
  24. Loesche W.J. Microbiology and Treatment of Halitosis. Curr. Infect. Dis. Rep. 2003;5:220–226. doi: 10.1007/s11908-003-0077-8. [DOI] [PubMed] [Google Scholar]
  25. Morita M., Wang H.L. Association between oral malodor and adult periodontitis: a review. J. Clin. Periodontol. 2001;28:813–819. doi: 10.1034/j.1600-051x.2001.028009813.x. [DOI] [PubMed] [Google Scholar]
  26. Morita M., Wang H.L. Relationship between sulcular sulfide level and oral malodor in subjects with periodontal disease. J. Periodontol. 2001;72:79–84. doi: 10.1902/jop.2001.72.1.79. [DOI] [PubMed] [Google Scholar]
  27. Murata T., Rahardjo A., Fujiyama Y., Yamaga T., Hanada M., Yaegaki K., Miyazaki H. Development of a compact and simple gas chromatography for oral malodor measurement. J. Periodontol. 2006;77:1142–1147. doi: 10.1902/jop.2006.050388. [DOI] [PubMed] [Google Scholar]
  28. Nachnani, S., 2011. Oral malodor: causes, assessment, and treatment. Compend Contin Educ Dent. 32, 22-24, 26-28, 30-31; quiz 32, 34. [PubMed]
  29. Nakano Y., Yoshimura M., Koga T. Methyl mercaptan production by periodontal bacteria. Int. Dent. J. 2002;52(Suppl 3):217–220. doi: 10.1002/j.1875-595x.2002.tb00928.x. [DOI] [PubMed] [Google Scholar]
  30. Nally F. Dry mouth and halitosis. Practitioner. 1990;234:603. [PubMed] [Google Scholar]
  31. Pham T.A., Ueno M., Shinada K., Kawaguchi Y. Comparison between self-perceived and clinical oral malodor. Oral. Surg. Oral. Med. Oral. Pathol. Oral. Radiol. 2012;113:70–80. doi: 10.1016/j.tripleo.2011.08.012. [DOI] [PubMed] [Google Scholar]
  32. Pham T.A., Ueno M., Shinada K., Kawaguchi Y. Factors affecting oral malodor in periodontitis and gingivitis patients. J. Investig. Clin. Dent. 2012;3:284–290. doi: 10.1111/j.2041-1626.2012.00155.x. [DOI] [PubMed] [Google Scholar]
  33. Pham T.A., Ueno M., Zaitsu T., Takehara S., Shinada K., Lam P.H., Kawaguchi Y. Clinical trial of oral malodor treatment in patients with periodontal diseases. J. Periodontal. Res. 2011;46:722–729. doi: 10.1111/j.1600-0765.2011.01395.x. [DOI] [PubMed] [Google Scholar]
  34. Schmidt N.F., Missan S.R., Tarbet W.J. The correlation between organoleptic mouth-odor ratings and levels of volatile sulfur compounds. Oral. Surg. Oral. Med. Oral. Pathol. 1978;45:560–567. doi: 10.1016/0030-4220(78)90037-3. [DOI] [PubMed] [Google Scholar]
  35. Scully C., Greenman J. Halitology (breath odour: aetiopathogenesis and management) Oral. Dis. 2012;18:333–345. doi: 10.1111/j.1601-0825.2011.01890.x. [DOI] [PubMed] [Google Scholar]
  36. Soares L.G., Castagna L., Weyne S.C., Silva D.G., Falabella M.E., Tinoco E.M. Effectiveness of full- and partial-mouth disinfection on halitosis in periodontal patients. J. Oral. Sci. 2015;57:1–6. doi: 10.2334/josnusd.57.1. [DOI] [PubMed] [Google Scholar]
  37. Silva M.F., Nascimento G.G., Leite F.R.M., Horta B.L., Demarco F.F. Periodontitis and self-reported halitosis among young adults from the 1982 Pelotas Birth Cohort. Oral. Dis. 2020;2020 doi: 10.1111/odi.13286. [DOI] [PubMed] [Google Scholar]
  38. Silveira J.O., Costa F.O., Oliveira P.A., Dutra B.C., Cortelli S.C., Cortelli J.R., Cota L.O., Oliveira A.M. Effect of non-surgical periodontal treatment by full-mouth disinfection or scaling and root planing per quadrant in halitosis-a randomized controlled clinical trial. Clin. Oral. Investig. 2017;21:1545–1552. doi: 10.1007/s00784-016-1959-0. [DOI] [PubMed] [Google Scholar]
  39. Takeuchi H., Machigashira M., Yamashita D., Kozono S., Nakajima Y., Miyamoto M., Takeuchi N., Setoguchi T., Noguchi K. The association of periodontal disease with oral malodour in a Japanese population. Oral. Dis. 2010;16:702–706. doi: 10.1111/j.1601-0825.2010.01685.x. [DOI] [PubMed] [Google Scholar]
  40. Tangerman A., Winkel E.G. The portable gas chromatograph OralChroma: a method of choice to detect oral and extra-oral halitosis. J. Breath. Res. 2008;2 doi: 10.1088/1752-7155/2/1/017010. [DOI] [PubMed] [Google Scholar]
  41. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J. Periodontol. 1977;48:13–20. doi: 10.1902/jop.1977.48.1.13. [DOI] [PubMed] [Google Scholar]
  42. Tonzetich J., Coil J.M., Ng W. Gas chromatographic method for trapping and detection of volatile organic compounds from human mouth air. J. Clin. Dent. 1991;2:79–82. [PubMed] [Google Scholar]
  43. Volozhin A.I., Petrovich I., Filatova E.S., Barer G.M., Fomina O.L., Kreĭt K., Volozhina S.A., Dieva S.V. Volatile compounds in air and oral saliva in healthy people, and in periodontitis and gingivitis patients. Stomatologiia (Mosk) 2001;80:9–12. [PubMed] [Google Scholar]
  44. Waler S.M. On the transformation of sulfur-containing amino acids and peptides to volatile sulfur compounds (VSC) in the human mouth. Eur. J. Oral. Sci. 1997;105:534–537. doi: 10.1111/j.1600-0722.1997.tb00241.x. [DOI] [PubMed] [Google Scholar]
  45. Yaegaki K., Brunette D.M., Tangerman A., Choe Y.S., Winkel E.G., Ito S., Kitano T., Ii H., Calenic B., Ishkitiev N., Imai T. Standardization of clinical protocols in oral malodor research. J. Breath. Res. 2012;6 doi: 10.1088/1752-7155/6/1/017101. [DOI] [PubMed] [Google Scholar]
  46. Yano T., Fukamachi H., Yamamoto M., Igarashi T. Characterization of L-cysteine desulfhydrase from Prevotella intermedia. Oral. Microbiol. Immunol. 2009;24:485–492. doi: 10.1111/j.1399-302X.2009.00546.x. [DOI] [PubMed] [Google Scholar]
  47. Yasukawa T., Ohmori M., Sato S. The relationship between physiologic halitosis and periodontopathic bacteria of the tongue and gingival sulcus. Odontology. 2010;98:44–51. doi: 10.1007/s10266-009-0114-7. [DOI] [PubMed] [Google Scholar]
  48. Zalewska A., Zatonski M., Jablonka-Strom A., Paradowska A., Kawala B., Litwin A. Halitosis–a common medical and social problem. a review on pathology, diagnosis and treatment. Acta Gastroenterol. Belg. 2012;75:300–309. [PubMed] [Google Scholar]

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Supplementary Materials

Supplementary data 1
mmc1.pdf (294.3KB, pdf)

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