Int J Stomatol

Int J Stomatol ›› 2021, Vol. 48 ›› Issue (5): 592-599.doi: 10.7518/gjkq.2021069

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Volatile sulfur compounds and its role in the management of intra-oral halitosis

Huang Peiqing(),Peng Xian,Xu Xin()   

  1. State Key Laboratory of Oral Disease & National Clinical Research Center for Oral Diseases & Dept. of Cariology and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China
  • Received:2021-01-03 Revised:2021-04-01 Online:2021-09-01 Published:2021-09-10
  • Contact: Xin Xu E-mail:122659187@qq.com;nixux1982@hotmail.com
  • Supported by:
    General Program of National Natural Science Foundation of China(81771099)

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Abstract:

Intra-oral halitosis is one of the most frequent complaints of patients seeking oral treatment, which is mainly produced due to the breakdown of certain amino acids by anaerobic bacterium, followed by the release of volatile sulfur compounds (VSCs). It is generally considered that VSCs are closely related with tongue coating and periodontitis. This review summarizes the source of VSCs and the progress on the treatments of intra-oral halitosis, which are aimed at controlling dental plaque or reacting directly with VSCs. Research advancement in this field provides not only evidence for halitosis therapy, but new ideas and methods of halitosis treatment.

Key words: intro-oral halitosis, volatile sulfur compounds, oral anaerobic bacteria, dental plaque biofilm

CLC Number: 

  • R781

TrendMD: 
[1] Kandalam U, Ledra N, Laubach H, et al. Inhibition of methionine Gamma lyase deaminase and the grow-th of Porphyromonas gingivalis: a therapeutic target for halitosis/periodontitis[J]. Arch Oral Biol, 2018, 90:27-32.
doi: S0003-9969(18)30056-6 pmid: 29525436
[2] Kapoor U, Sharma G, Juneja M, et al. Halitosis: current concepts on etiology, diagnosis and management[J]. Eur J Dent, 2016, 10(2):292-300.
doi: 10.4103/1305-7456.178294 pmid: 27095913
[3] Nakhleh MK, Quatredeniers M, Haick H. Detection of halitosis in breath: between the past, present, and future[J]. Oral Dis, 2018, 24(5):685-695.
doi: 10.1111/odi.12699 pmid: 28622437
[4] Seerangaiyan K, Jüch F, Winkel EG. Tongue coa-ting: its characteristics and role in intra-oral halitosis and general health-a review[J]. J Breath Res, 2018, 12(3):034001.
doi: 10.1088/1752-7163/aaa3a1
[5] Suzuki N, Yoneda M, Takeshita T, et al. Induction and inhibition of oral malodor[J]. Mol Oral Micro-biol, 2019, 34(3):85-96.
[6] Seerangaiyan K, Maruthamuthu M, van Winkelhoff AJ, et al. Untargeted metabolomics of the bacterial tongue coating of intra-oral halitosis patients[J]. J Breath Res, 2019, 13(4):046010.
doi: 10.1088/1752-7163/ab334e
[7] Oshiro A, Zaitsu T, Ueno M, et al. Characterization of oral bacteria in the tongue coating of patients with halitosis using 16S rRNA analysis[J]. Acta Odontol Scand, 2020, 78(7):541-546.
doi: 10.1080/00016357.2020.1754459
[8] Ye W, Zhang Y, He M, et al. Relationship of tongue coating microbiome on volatile sulfur compounds in healthy and halitosis adults[J]. J Breath Res, 2019, 14(1):016005.
doi: 10.1088/1752-7163/ab47b4
[9] Silveira JO, Costa FO, Oliveira PAD, et al. Effect of non-surgical periodontal treatment by full-mouth disinfection or scaling and root planing per quadrant in halitosis-a randomized controlled clinical trial[J]. Clin Oral Investig, 2017, 21(5):1545-1552.
doi: 10.1007/s00784-016-1959-0
[10] Scully C, Greenman J. Halitology (breath odour: aetiopathogenesis and management)[J]. Oral Dis, 2012, 18(4):333-345.
doi: 10.1111/j.1601-0825.2011.01890.x pmid: 22277019
[11] De Geest S, Laleman I, Teughels W, et al. Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists[J]. Periodontol 2000, 2016, 71(1):213-227.
doi: 10.1111/prd.2016.71.issue-1
[12] Makino Y, Yamaga T, Yoshihara A, et al. Association between volatile sulfur compounds and perio-dontal disease progression in elderly non-smokers[J]. J Periodontol, 2012, 83(5):635-643.
doi: 10.1902/jop.2011.110275 pmid: 21861638
[13] Chen X, Zhang Y, Lu HX, et al. Factors associated with halitosis in white-collar employees in Shanghai, China[J]. PLoS One, 2016, 11(5):e0155592.
doi: 10.1371/journal.pone.0155592
[14] De Geest S, Laleman I, Teughels W, et al. Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists[J]. Periodontol 2000, 2016, 71(1):213-227.
doi: 10.1111/prd.2016.71.issue-1
[15] Boyanova L. Stress hormone epinephrine (adrenaline) and norepinephrine (noradrenaline) effects on the anaerobic bacteria[J]. Anaerobe, 2017, 44:13-19.
doi: 10.1016/j.anaerobe.2017.01.003
[16] Çoban Z, Sönmez I. Halitosis: a review of current literature[J]. Meandros, 2017, 18(3):164-170.
doi: 10.4274/meandros
[17] Washio J, Sato T, Koseki T, et al. Hydrogen sulfide-producing bacteria in tongue biofilm and their relationship with oral malodour[J]. J Med Microbiol, 2005, 54(Pt 9):889-895.
doi: 10.1099/jmm.0.46118-0
[18] Yoo JI, Shin IS, Jeon JG, et al. The effect of probio-tics on halitosis: a systematic review and Meta-analysis[J]. Probiotics Antimicrob Proteins, 2019, 11(1):150-157.
doi: 10.1007/s12602-017-9351-1
[19] Mogilnicka I, Bogucki P, Ufnal M. Microbiota and malodor: etiology and management[J]. Int J Mol Sci, 2020, 21(8):2886.
doi: 10.3390/ijms21082886
[20] De Lima PO, Nani BD, Rolim GS, et al. Effects of academic stress on the levels of oral volatile sulfur compounds, halitosis-related bacteria and stress biomarkers of healthy female undergraduate students[J]. J Breath Res, 2020, 14(3):036005.
doi: 10.1088/1752-7163/ab944d
[21] Yoshimura M, Nakano Y, Yamashita Y, et al. Formation of methyl mercaptan from L-methionine by Porphyromonas gingivalis[J]. Infect Immun, 2000, 68(12):6912-6916.
doi: 10.1128/IAI.68.12.6912-6916.2000 pmid: 11083813
[22] Kleinberg I, Westbay G. Salivary and metabolic factors involved in oral malodor formation[J]. J Perio-dontol, 1992, 63(9):768-775.
[23] Sterer N, Rosenberg M. Streptococcus salivarius promotes mucin putrefaction and malodor production by Porphyromonas gingivalis[J]. J Dent Res, 2006, 85(10):910-914.
pmid: 16998130
[24] Masuo Y, Suzuki N, Yoneda M, et al. Salivary β-galactosidase activity affects physiological oral malodour[J]. Arch Oral Biol, 2012, 57(1):87-93.
doi: 10.1016/j.archoralbio.2011.07.015
[25] Tanabe S, Grenier D. Characterization of volatile sulfur compound production by Solobacterium moo-rei[J]. Arch Oral Biol, 2012, 57(12):1639-1643.
doi: 10.1016/j.archoralbio.2012.09.011
[26] Nani BD, Lima PO, Marcondes FK, et al. Changes in salivary microbiota increase volatile sulfur compounds production in healthy male subjects with a-cademic-related chronic stress[J]. PLoS One, 2017, 12(3):e0173686.
doi: 10.1371/journal.pone.0173686
[27] Wu J, Cannon RD, Ji P, et al. Halitosis: prevalence, risk factors, sources, measurement and treatment-a review of the literature[J]. Aust Dent J, 2020, 65(1):4-11.
doi: 10.1111/adj.12725 pmid: 31610030
[28] Bowen WH, Burne RA, Wu H, et al. Oral biofilms: pathogens, matrix, and polymicrobial interactions in microenvironments[J]. Trends Microbiol, 2018, 26(3):229-242.
doi: 10.1016/j.tim.2017.09.008
[29] Deutscher H, Derman S, Barbe AG, et al. The effect of professional tooth cleaning or non-surgical perio-dontal therapy on oral halitosis in patients with perio-dontal diseases. A systematic review[J]. Int J Dent Hyg, 2018, 16(1):36-47.
doi: 10.1111/idh.12306 pmid: 28836329
[30] Iatropoulos A, Panis V, Mela E, et al. Changes of volatile sulphur compounds during therapy of a case series of patients with chronic periodontitis and halitosis[J]. J Clin Periodontol, 2016, 43(4):359-365.
doi: 10.1111/jcpe.12521 pmid: 26824613
[31] Liu SS, Fu E, Tu HP, et al. Comparison of oral malo-dors before and after nonsurgical periodontal therapy in chronic periodontitis patients[J]. J Dent Sci, 2017, 12(2):156-160.
doi: 10.1016/j.jds.2016.12.004
[32] Acar B, Berker E, Tan Ç, et al. Effects of oral prophylaxis including tongue cleaning on halitosis and gingival inflammation in gingivitis patients-a randomized controlled clinical trial[J]. Clin Oral Investig, 2019, 23(4):1829-1836.
doi: 10.1007/s00784-018-2617-5
[33] Aung EE, Ueno M, Zaitsu T, et al. Effectiveness of three oral hygiene regimens on oral malodor reduction: a randomized clinical trial[J]. Trials, 2015, 16:31.
doi: 10.1186/s13063-015-0549-9 pmid: 25622725
[34] Christensen GJ. Why clean your tongue[J]. J Am Dent Assoc, 1998, 129(11):1605-1607.
pmid: 9818580
[35] Rowley EJ, Schuchman LC, Tishk MN, et al. Tongue brushing versus tongue scraping[J]. Clin Prev Dent, 1987, 9(6):13-16.
pmid: 3505832
[36] Yaegaki K, Coil JM, Kamemizu T, et al. Tongue brushing and mouth rinsing as basic treatment measures for halitosis[J]. Int Dent J, 2002, 52(Suppl 3):192-196.
doi: 10.1002/j.1875-595X.2002.tb00923.x
[37] Matsumura Y, Hinode D, Fukui M, et al. Effectiveness of an oral care tablet containing kiwifruit powder in reducing oral bacteria in tongue coating: a crossover trial[J]. Clin Exp Dent Res, 2020, 6(2):197-206.
doi: 10.1002/cre2.262 pmid: 32250572
[38] Mugita N, Nambu T, Takahashi K, et al. Proteases, actinidin, papain and trypsin reduce oral biofilm on the tongue in elderly subjects and in vitro[J]. Arch Oral Biol, 2017, 82:233-240.
doi: S0003-9969(17)30145-0 pmid: 28662376
[39] Kato K, Tamura K, Shimazaki Y. Oral biofilm uptake of mineral ions released from experimental too-thpaste containing surface pre-reacted glass-ionomer (S-PRG) filler[J]. Arch Oral Biol, 2020, 117:104777.
doi: 10.1016/j.archoralbio.2020.104777
[40] Saku S, Kotake H, Scougall-Vilchis RJ, et al. Antibacterial activity of composite resin with glass-ionomer filler particles[J]. Dent Mater J, 2010, 29(2):193-198.
doi: 10.4012/dmj.2009-050
[41] Suzuki N, Yoneda M, Haruna K, et al. Effects of S-PRG eluate on oral biofilm and oral malodor[J]. Arch Oral Biol, 2014, 59(4):407-413.
doi: 10.1016/j.archoralbio.2014.01.009 pmid: 24530472
[42] Kang JH, Kim DJ, Choi BK, et al. Inhibition of ma-lodorous gas formation by oral bacteria with cetylpyridinium and zinc chloride[J]. Arch Oral Biol, 2017, 84:133-138.
doi: 10.1016/j.archoralbio.2017.09.023
[43] Jervøe-Storm PM, Schulze H, Jepsen S. A randomized cross-over short-term study on the short-term effects of a zinc-lactate containing mouthwash against oral malodour[J]. J Breath Res, 2019, 13(2):026005.
doi: 10.1088/1752-7163/aaf401
[44] Yadav SR, Kini VV, Padhye A. Inhibition of tongue coat and dental plaque formation by stabilized chlorine dioxide vs chlorhexidine mouthrinse: a rando-mized, triple blinded study[J]. J Clin Diagn Res, 2015, 9(9): ZC69-ZC74.
[45] Sreenivasan PK, Gittins E. Effects of low dose chlor-hexidine mouthrinses on oral bacteria and salivary microflora including those producing hydrogen sulfide[J]. Oral Microbiol Immunol, 2004, 19(5):309-313.
doi: 10.1111/omi.2004.19.issue-5
[46] Erovic Ademovski S, Lingström P, Renvert S. The effect of different mouth rinse products on intra-oral halitosis[J]. Int J Dent Hyg, 2016, 14(2):117-123.
doi: 10.1111/idh.12148 pmid: 26031397
[47] Jamali Z, Aminabadi NA, Samiei M, et al. Impact of chlorhexidine pretreatment followed by probiotic Streptococcus salivarius strain K12 on halitosis in children: a randomised controlled clinical trial[J]. Oral Health Prev Dent, 2016, 14(4):305-313.
[48] Lang NP, Catalanotto FA, Knöpfli RU, et al. Quality-specific taste impairment following the application of chlorhexidine digluconate mouthrinses[J]. J Clin Periodontol, 1988, 15(1):43-48.
pmid: 3422243
[49] Supranoto SC, Slot DE, Addy M, et al. The effect of chlorhexidine dentifrice or gel versus chlorhexidine mouthwash on plaque, gingivitis, bleeding and tooth discoloration: a systematic review[J]. Int J Dent Hyg, 2015, 13(2):83-92.
doi: 10.1111/idh.12078 pmid: 25059640
[50] Georgiou AC, Laine ML, Deng DM, et al. Efficacy of probiotics: clinical and microbial parameters of halitosis[J]. J Breath Res, 2018, 12(4):046010.
doi: 10.1088/1752-7163/aacf49
[51] Lee SH, Baek DH. Effects of Streptococcus thermophilus on volatile sulfur compounds produced by Porphyromonas gingivalis[J]. Arch Oral Biol, 2014, 59(11):1205-1210.
doi: 10.1016/j.archoralbio.2014.07.006
[52] Moon JE, Moon YM, Cho JW. The effect of Streptococcus salivarius K12 against Prevotella intermedia on the reduction of oral malodor[J]. Int J Clin Prev Dent, 2016, 12(3):153-161.
doi: 10.15236/ijcpd.2016.12.3.153
[53] Benic GZ, Farella M, Morgan XC, et al. Oral probio-tics reduce halitosis in patients wearing orthodontic braces: a randomized, triple-blind, placebo-controlled trial[J]. J Breath Res, 2019, 13(3):036010.
doi: 10.1088/1752-7163/ab1c81
[54] Pitts G, Pianotti R, Feary TW, et al. The in vivo effects of an antiseptic mouthwash on odor-producing microorganisms[J]. J Dent Res, 1981, 60(11):1891-1896.
pmid: 6945328
[55] Tanabe S, Desjardins J, Bergeron C, et al. Reduction of bacterial volatile sulfur compound production by licoricidin and licorisoflavan A from licorice[J]. J Breath Res, 2012, 6(1):016006.
doi: 10.1088/1752-7155/6/1/016006
[56] Satthanakul P, Taweechaisupapong S, Paphangkora-kit J, et al. Antimicrobial effect of lemongrass oil against oral malodour micro-organisms and the pilot study of safety and efficacy of lemongrass mouthrinse on oral malodour[J]. J Appl Microbiol, 2015, 118(1):11-17.
doi: 10.1111/jam.12667 pmid: 25327222
[57] Veloso DJ, Abrão F, Martins CHG, et al. Potential antibacterial and anti-halitosis activity of medicinal plants against oral bacteria[J]. Arch Oral Biol, 2020, 110:104585.
doi: 10.1016/j.archoralbio.2019.104585
[58] Watanabe K, Hiramine H, Toyama T, et al. Effects of French pine bark extract chewing gum on oral malodor and salivary bacteria[J]. J Nutr Sci Vitami-nol (Tokyo), 2018, 64(3):185-191.
[59] Shin K, Yaegaki K, Murata T, et al. Effects of a composition containing lactoferrin and lactoperoxidase on oral malodor and salivary bacteria: a randomized, double-blind, crossover, placebo-controlled clinical trial[J]. Clin Oral Investig, 2011, 15(4):485-493.
doi: 10.1007/s00784-010-0422-x
[60] Nakano M, Shin K, Wakabayashi H, et al. Inactiva-ting effects of the lactoperoxidase system on bacte-rial lyases involved in oral malodour production[J]. J Med Microbiol, 2015, 64(10):1244-1252.
doi: 10.1099/jmm.0.000150
[61] Nakano M, Shimizu E, Wakabayashi H, et al. A randomized, double-blind, crossover, placebo-controlled clinical trial to assess effects of the single ingestion of a tablet containing lactoferrin, lactoperoxidase, and glucose oxidase on oral malodor[J]. BMC Oral Heal-th, 2016, 16:37.
[62] Sreenivasan PK, Haraszthy VI, Zambon JJ. Antimicrobial efficacy of 0.05% cetylpyridinium chloride mouthrinses[J]. Lett Appl Microbiol, 2013, 56(1):14-20.
doi: 10.1111/lam.12008 pmid: 23039819
[63] Rioboo M, García V, Serrano J, et al. Clinical and microbiological efficacy of an antimicrobial mouth rinse containing 0.05% cetylpyridinium chloride in patients with gingivitis[J]. Int J Dent Hyg, 2012, 10(2):98-106.
doi: 10.1111/j.1601-5037.2011.00523.x pmid: 21831254
[64] Liu J, Ling JQ, Wu CD. Cetylpyridinium chloride suppresses gene expression associated with halitosis[J]. Arch Oral Biol, 2013, 58(11):1686-1691.
doi: 10.1016/j.archoralbio.2013.08.014 pmid: 24112735
[65] Feres M, Figueiredo LC, Faveri M, et al. The efficacy of two oral hygiene regimens in reducing oral malodour: a randomised clinical trial[J]. Int Dent J, 2015, 65(6):292-302.
doi: 10.1111/idj.12183
[66] Hanley AB, Parsley KR, Lewis JA, et al. Chemistry of indole glucosinolates: intermediacy of indol-3-ylmethyl isothiocyanates in the enzymic hydrolysis of indole glucosinolates[J]. J Chem Soc Perkin Trans, 1990(8):2273.
[67] McDanell R, McLean AE, Hanley AB, et al. Chemical and biological properties of indole glucosinolates (glucobrassicins): a review[J]. Food Chem To-xicol, 1988, 26(1):59-70.
[68] McDanell R, McLean AE, Hanley AB, et al. The effect of feeding Brassica vegetables and intact glucosinolates on mixed-function-oxidase activity in the livers and intestines of rats[J]. Food Chem Toxicol, 1989, 27(5):289-293.
pmid: 2473016
[69] Walter W, Bode KD. Syntheses of thiocarbamates[J]. Angew Chem Int Ed Engl, 1967, 6(4):281-293.
doi: 10.1002/(ISSN)1521-3773
[70] Tian MM, Hanley AB, Dodds MW. Allyl isothiocyanate from mustard seed is effective in reducing the levels of volatile sulfur compounds responsible for intrinsic oral malodor[J]. J Breath Res, 2013, 7(2):026001.
doi: 10.1088/1752-7155/7/2/026001
[71] Kim JS, Park JW, Kim DJ, et al. Direct effect of chlorine dioxide, zinc chloride and chlorhexidine solution on the gaseous volatile sulfur compounds[J]. Acta Odontol Scand, 2014, 72(8):645-650.
doi: 10.3109/00016357.2014.887770
[72] Pham TAV, Nguyen NTX. Efficacy of chlorine dio-xide mouthwash in reducing oral malodor: a 2-week randomized, double-blind, crossover study[J]. Clin Exp Dent Res, 2018, 4(5):206-215.
doi: 10.1002/cre2.v4.5
[73] Friedrich CG, Rother D, Bardischewsky F, et al. O-xidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism[J]. Appl Environ Microbiol, 2001, 67(7):2873-2882.
doi: 10.1128/AEM.67.7.2873-2882.2001
[74] Ramadhani A, Kawada-Matsuo M, Komatsuzawa H, et al. Recombinant sox enzymes from Paracoccus pantotrophus degrade hydrogen sulfide, a major component of oral malodor[J]. Microbes Environ, 2017, 32(1):54-60.
doi: 10.1264/jsme2.ME16140 pmid: 28260736
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