The management of physiological halitosis: A 20-year systematic review of the literature

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1 REVIEW ARTICLE Saudi Journal of Oral Sciences The management of physiological halitosis: A 20-year systematic review of the literature Omar Hamad Alkadhi Department of Preventive Dentistry, Riyadh Colleges of Dentistry and Pharmacy, Riyadh, Saudi Arabia Abstract Halitosis is a common problem. There are many assessment methods in the literature as well as treatment modalities. The objective of this systematic review is to evaluate the level of for each treatment modality of halitosis. Electronic databases were searched in a systematic method according to preferred reporting items for systematic reviews and metaanalyses guidelines. The review included human clinical trials with or without randomization and excluded case reports and case series. Only articles written in English were included in the review. Forty-three articles were included in this review. It was found that treatment modalities can be classified into chemical compounds in mouthwashes, chemical compounds in dentifrices, chemical compounds in other products, herbal products and combinations of chemical and physical methods. The level of ranged from I to IV for each class. This review suggests that mouthwashes and dentifrices are the best ways to combat halitosis. There is currently insufficient amount of level I to support the efficacy of herbal products or mechanical modifications to oral hygiene practices and there is a need for a greater number of randomized controlled trials to study the efficacy of these methods. Key words: Dentifrices, halitosis, mouthwashes, systematic review Introduction Halitosis is a problem that has been reported to be a cause of embarrassment among individuals, and it has been reported that Americans spend up to 3 billion dollars a year on gum, mints and breath fresheners. [1] It has been reported that halitosis decreases self-confidence and leads to insecure social relations, to the extent of avoiding social interactions. [2] There are many causes of halitosis including tongue coating, periodontal disease, peri-implant disease, deep carious lesions, exposed necrotic tooth pulps, pericoronitis, mucosal ulcerations, impacted food or debris, imperfect dental restorations, unclean dentures, xerostomia and endodontic lesions. [3,4] While Quick Response Code: Access this article online Website: DOI: / several pathological conditions such as oral cancer or candidiasis in immuno-compromised patients can result in halitosis, the term physiological halitosis, or physiological malodor is used to describe halitosis in individuals where no underlying systemic cause is detectable. [5,6] Halitosis has been attributed to the presence of volatile sulfur compounds (VSCs) such as hydrogen sulfide (H 2 S), methyl mercaptan and dimethyl sulfide. These compounds may be measured using gas chromatography, organoleptic test, sulfide monitoring, quantifying β-galactosidase, salivary incubation, ammonia monitoring, and polymerase chain reaction DNA testing. [7-9] While there are several studies on the efficacy of different measures available to combat halitosis, there has been little attempt in the literature to quantify the level of present for each method of treatment. The aim of this systematic review is to document the level of available for the use of different modalities in the management of halitosis. Address for correspondence: Dr. Omar Hamad Alkadhi, P.O. Box 84891, Riyadh 11681, Saudi Arabia. omar.alkadhi@riyadh.edu.sa S J Oral Sci Vol 2 No 1 3 January 2015

2 Materials and Methods The search was conducted electronically in PubMed from 1999 to The keywords used were Halitosis and Oral and Malodor/Malodour. The studies included human clinical trials with or without randomization and excluded case reports and case series. Only articles written in English were included in the review. A total of 897 articles were identified. Of these, 204 articles were screened. 58 full-text articles were then assessed for eligibility. 16 articles were then excluded since they did not meet the inclusion criteria. Finally, 42 articles were included in the qualitative synthesis in this review, which were then subjected to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines for systematic reviews [Figure 1]. The levels of were assigned using the criteria put forth by the center for based medicine [Table 1]. [3] Results Of the 42 articles that were found to be suitable for inclusion in the review, it was found that the articles could be broadly classified based on the approach used toward halitosis. These were: 1. Chemical compounds in mouthwashes. 2. Chemical compounds in dentifrices. 3. Chemical compounds in other products. 4. Herbal products. 5. Combinations of chemical and physical methods. Chemical compounds in mouthwashes There have been several attempts made over the past two decades to study the effect of adding chemicals such as zinc (Zn), cetylpyridium chloride and chlorine dioxide (CD) to existing essential oil (EO) mouthwashes or chlorhexidine (CHX) rinses. There have also been attempts made to assess and compare the efficacy of anti-bacterial products such as triclosan and sodium fluoride. A total of 12 studies met the inclusion criteria set by the PRISMA guideline. The results of these studies are summarized in Table 2. Chemicals added to dentifrices Toothpastes with chemical additives to specifically prevent the malodor have been studied in detail over the past two decades. However, only eight studies met the inclusion criteria of this systematic review; these articles are summarized in Table 3. Chemical compounds in other products There have been attempts to reduce oral malodor by adding specific chemicals to products such as tablets, gels, candies, chewing gum and lozenges. The search using the PRISMA criteria yielded 10 results, which are summarized in Table 4. Herbal products The past two decades has seen a slew of herbal products in the market. However, we were only able to find four studies that met the inclusion criteria of this review. These articles are summarized in Table 5. Evaluations of modified mechanical methods There have been studies on the efficacy of modified mechanical methods, particularly tongue cleansing, on the reduction of organoleptic scores in patients complaining of halitosis. The search using our criteria yielded eight results. These are summarized in Table 6. Discussion Mouthwashes The results of this systematic review suggest that despite the several different approaches used in the Figure 1: Preferred reporting items for systematic reviews and meta-analyses protocol used in this study Table 1: Levels of Level of I I IV V Explanation High-quality, multi-centered or single-centered, randomized controlled trial with adequate power; or systematic review of these studies Lesser-quality, randomized controlled trial; prospective cohort study; or systematic review of these studies Retrospective comparative study; case-control study; or systematic review of these studies Case series Expert opinion; case report or clinical example; or based on physiology, bench research or first principles S J Oral Sci Vol 2 No 1 4 January 2015

3 Table 2: Studies on the addition of chemical compounds to mouthrinses to combat halitosis Author Sample Chemical used Conclusion Level of Dadamio et al. [10] 54 Addition of zinc lactate to conventional Addition of zinc produces better masking and therapeutic effects I mouthwashes Malhotra and % CHX rinse compared to an EO CHX rinse produces significantly greater reduction in VSCs Yeltiwar [11] mouth rinse Thaweboon and 36 EO-containing mouth rinse compared The mean VSC-producing bacteria in subjects using the EO mouth rinse I Thawaboon [12] with water were significantly lower than those using the control rinse twice daily Wilhelm et al. [13] 42 CHX-free mouthrinse containing ASF No significant difference between amine/stannous fluoride and CHX in I against a benchmark containing CHX reducing oral malodor Wigger-Alberti 174 ASF with 0.2% zinc lactate, compared No significant difference between ASF with zinc lactate and CHX with I et al. [14] with 0.05% CHX, 0.05% cetylpyridinium chloride, 0.14% zinc lactate cetylpyridinium chloride in reducing oral malodor Both groups significantly better than plain CHX or water Carvalho et al. [15] % triclosan, 0.12% CHX gluconate, VSC formation was inhibited in descending order, by positive control 0.05% cetylpyridinium chloride and EOs (0.2% CHX), 0.12% CHX, triclosan and EOs and cetylpyridinium chloride Winkel et al. [16] 40 CHX, cetylpyridinium chloride and Significant reduction in OLSs in comparison to placebo (P < 0.05) I zinc-lactate Quirynen % CHX compared to cetylpyridinium No significant difference between mouthwashes but all the et al. [17] with zinc lactate and an amine fluoride mouth rinse mouthwashes were successful in reducing malodor Borden et al. [18] 99 EOs or CD/Zn compared to Only cetylpyridinium chloride produced significant reduction in oral mal I cetylpyridinium chloride Van % CHX-Alc; 0.12% CHX with 0.05% CHX-Alc and CHX-CPC-Zn, showed significant reductions in both aerobic Steenberghe et al. [19] NaF; CHX with CHX-CPC-Zn and anaerobic CFU/ml were noticed in comparison with baseline data for both tongue coating and saliva samples Frascella et al. [20] 31 CD CD produced a significant reduction in oral malodor compared to the control Frascella et al. [21] 12 CD CD produced a significant reduction in oral malodor compared to the control I Kozlovsky et al. [22] 50 2-phase oil: Water mouthrinse The two phase oil water mouthrinse produced a significantly greater reduction in malodor than water I VSC: Volatile sulfur compound, ASF: Amine fluoride/stannous fluoride, CFU: Colony forming units, CPC-Zn: Cetylpyridium chloride and zinc, EO: Essential oils, CD/Zn: Chlorine dioxide with zinc, CHX: Chlorhexidine, CHX-Alc: Chlorhexidine with alcohol, OLS: Organoleptic scores Table 3: Studies on the addition of chemicals to dentifrices to prevent oral malodor Author Sample Chemical used Conclusion Level of Young and Jonski [23] 28 Zn citrate with PVM/MA copolymer Significant reduction in volatile sulfide compounds compared to control Payne et al. [24] % w/w o-cymen-5-ol with 0.6% w/w Significant reduction in volatile sulfide compounds compared to sodium I zinc chloride/sodium fluoride dentifrice fluoride control Chen et al. [25] % stannous fluoride Significantly lower adjusted mean VSC level compared to NaF Hu et al. [26] 81 Dentifrice containing 0.3% triclosan/2.0% PVM/MA copolymer/0.243% sodium fluoride in a 17% dual silica base Significant 28.4% reduction in oral malodor scores compared to the control fluoridated dentifrice I Farrell et al. [27] % stabilized stannous fluoride sodium hexametaphosphate dentifrice Statistically significant reduction of overnight VSC (P < 0.03) and the overnight hedonic scores (P < 0.02) relative to the negative control after 1-day of product use Sharma et al. [28] 76 Triclosan with a co-polymer Significantly better breath odor score at 12 h compared to control I Olshan et al. [29] 170 EO EO dentifrices were significantly more effective (P 0.033) than the I control in reducing intrinsic oral malodor from 90 to 120 min VSC: Volatile sulfur compound, PVM/MA: Polyvinylmethyl ether/maleic acid, EO: Essential oil I management of halitosis, mouthwashes still remain the mainstay of halitosis management. Essential oil mouthwashes are often referred to as cosmetic mouthwashes and have been the most commonly prescribed over the counter medications for halitosis. While there have been level I studies that show that EO mouthwashes are better than water, almost all other chemical mouthwashes have been documented to have a greater reduction in malodor. Studies show that CHX, [11,15,19] Triclosan and cetylpyridinium chloride are all significantly better than EO mouthwashes at reducing oral malodor. [15] While there was some initial support for the use of CD in the management of halitosis, [20] there is an inadequate level I or level to support the use of CD as an agent against halitosis. Of the many different additions to mouthwashes, the addition of Zn compounds seemed to have the greatest number of studies with the level I or level. S J Oral Sci Vol 2 No 1 5 January 2015

4 Table 4: Studies on alternative delivery systems for chemicals used to treat oral malodor Author(s) Sample size Product(s) used Method of delivery Conclusion Level of Suzuki et al. [30] 26 Lactobaccilus Salivarius WB21 Tablets Daily consumption of tablets decreased malodor I Iha et al. [31] 18 Hinokitiol Gel Significant reduction in malodor and plaque scores Tian et al. [32] 15 Allyl-isocyanate combined with Chewing gum 89% reduction in VSC after chewing I zinc salts Porciani and 123 Zinc acetate with magnolia Chewing gum Significant reduction in VSC after 1 h of chewing I Grandini [33] extract Nohno et al. [34] 14 Protease and actinidine Candy tablets Significant reduction in VSC I Barak and Katz [35] 75 Zinc gluconate 0.5%, propolis Abrasive microcapsules Abrasive microcapsules are an effective means of 2%, and a combination of both (Breezy candy) controlling halitosis Shin et al. [36] 15 Bovine lactoferrin and Tablets Significantly greater number of patients with acceptable lactoperoxidase CH 3 SH scores when compared to control group Zhu et al. [37] 15 Cinnamic aldehyde Sugared chewing gum Significant reductions in salivary anerobes I Iwamoto et al. [38] 20 Lactobacillus Salivarius with Tablet Significant reduction in oral hygiene parameters I xylitol Greenstein et al. [39] 123 Oxidizing agents Lozenges Full-strength oxidizing lozenge significantly reduced tongue dorsum malodor, as determined by the spoon test I VSC: Volatile sulfur compound, CH 3 SH: Methyl mercaptan Table 5: Studies using herbal derived products for the management of halitosis Author(s) Sample size Active ingredient(s) Sterer et al. [40] 40 Echinacea Lavandula Pistacia Method of delivery Mucoadhesive tablets Conclusion The herbal mucoadhesive tablet caused a significant reduction in malodor scores (P=0.004), VSC levels (P=0.002) and beta-galactosidase assay (P=0.02) Tanaka et al. [41] 97 Eucalyptus-extract Chewing gum Significant reductions in clinical parameters, including organoleptic I and tongue-coating scores in the high-and/or low-concentration groups, occurred at 4, 8, 12, and 14 weeks (P<0.05) Rassameemasmaung 60 Pericarp extract of Mouthwash VSC were significantly different at day 15 (P<0.05) et al. [42] Garcinia mangostana L. Farina et al. [4] 30 Curcuma zedoaria and Camellia sinensis Mouthwash Some effect in reducing malodor IV VSC: Volatile sulfur compound Table 6: Studies on the efficacy of modified mechanical methods on oral malodor Level of Author(s) Sample size Method used Conclusion Level of Oliveira-Neto et al. [43] 20 Tongue scraper attached to The toothbrush s tongue scraper was able to toothbrush significantly reduce bad breath for up to 2 h Erovic Ademovski 21 Mouth rinse with and without Significantly lower OLS following active rinse et al. [3] adjunct tongue scraping combined with tongue scraping Haas et al. [44] 10 Tongue scraper No significant changes in OLSs I Asokan et al. [45] 20 Oil pulling Oil pulling was as effective as CHX mouthwash I in reducing OLS Faveri et al. [46] 19 Tongue scraping and dental flossing Significantly higher OLS in groups that did not perform tongue scraping De Luca-Monasterios 98 Chewing gum Chewing gum without any chemical additives I et al. [47] produced a significant reduction in OLSs Wilhelm et al. [48] 54 Tongue cleaner with gel application Significant reduction in OLS I Seemann et al. [49] 30 Mechanical tongue cleaning Significant reduction in OLS scores I OLS: Organoleptic score, CHX: Chlorhexidine I Level I existed for Zn lactate to conventional mouthwashes can enhance the masking and therapeutic effect of mouthrinses on oral malodor. [10] However, Quirynen et al., in a study with level showed that the reduction of halitosis produced by Zn lactate, though significant was not significantly better than 0.2% CHX nor to amine fluoride/stannous fluoride (ASF) mouthwashes. [17] There have been several studies comparing CHX to ASF mouthwashes. Wilhelm et al. showed that there was no significant difference between CHX-free mouthrinses containing ASF and CHX mouthwashes. [50] Similarly level suggests that while addition of compounds such as Zn lactate to ASF or cetylpyridinium of CHX improves the efficacy of these mouthwashes when compared to plain CHX or water, there is not S J Oral Sci Vol 2 No 1 6 January 2015

5 enough to show that that there is a difference in efficacy between ASF with Zn lactate and CHX with cetylpyridinium chloride in reducing oral malodor. [14,16] There is, however, level to suggest that cetylpyridinium chloride is significantly better than EOs or CD with Zn (CD/Zn) in the reduction of oral malodor. [18] Dentifrices The brushing of teeth has always been seen as an effective method of reducing halitosis, however few studies with the level I or level were found in the literature. Among dentifrices too, there existed a level I and level that the addition of Zn or zinc derived compounds offered a significant reduction in halitosis scores. Payne et al. showed that 0.1% w/w o-cymen- 5-ol/0.6% w/w Zn chloride/sodium fluoride dentifrice was able to reduce volatile sulfide better than a sodium fluoride dentifrice. [24] Young and Janski showed a significant reduction in volatile sulfide when using Zn toothpaste and an experimental toothpaste (Zn citrate + polyvinylmethyl ether/maleic acid [PVM/MA] copolymer) compared to a control toothpaste without Zn. [23] Among fluoridated toothpastes, it has been shown that stannous fluoride was able to reduce VSC better than sodium fluoride. [25,27] Triclosan is a compound that is often added to toothpastes for its effect in preventing the formation of calculus. [30-32] Sharma et al. have shown that triclosan can produce better breath odor scores 12 h after use in comparison to control. [28] This is also supported by the findings of Hu et al. who showed that 0.3% triclosan/2.0% PVM/MA copolymer/0.243% sodium fluoride in a 17% dual silica base can reduce oral malodor 28.4% better than the control fluoridated toothpaste. [26] However, there is no level I or level in support of triclosan as an agent to fight halitosis. The same holds true for the effect of the addition of EO to dentifrices. [29] Use of alternative products as vehicles The third category examined included studies that introduced chemical compounds through products other than mouthwashes or dentifrices. Level I studies included the findings of Suzuki et al., who concluded that the daily consumptions of tablets containing lactobacillus salivations WB-21 could reduce oral malodor. [30] Porciani et al. in their randomized control trial showed that Zn acetate and magnolia bark extract containing chewing gum could significantly reduce the oral VSC levels for more than 1 h compared to control. [33] Level existed for products such as hinokitiol. [31] Abrasive microcapsules (Breezy candy) [35] and tablets containing bovine lactoferrin and lactoperoxidase. Tablets and candies with other products have also been documented. Tian et al. showed that allyl-isocyanate combined with Zn salts chewing gum was found to reduce VSC by 89% after chewing; [51] while Nohno et al. showed that candy tablets containing protease and actinidine showed a significant reduction in VSC. [34] Zhu et al. showed that salivary anaerobes were significantly lower in subjects who chewed gum that contained cinnamic aldehyde. [37] While Iwamoto et al. showed a significant reduction in halitosis parameters in those subjects using lactobacillus salivarius with xylitol tablets [38] for 2 weeks. Greenstein et al. showed that oxidizing lozenges showed a significant reduction in malodor [39] of the dorsal surface of the tongue. However, it must be remembered that all these products had only level I and no randomized control studies exist to support their efficacy. Herbal products While there is a slew of herbal remedies available over the counter that claim to control halitosis, this review was able to find only one study with level I of efficacy. Tanaka et al. showed that that eucalyptusextract chewing gum was able to produce significant reductions in organoleptic and tongue-coating scores at 4, 8, 12, and 14 weeks. [41] Rassameemasmaung et al. in their case control study used the pericarp extract of Garcia mangostana L. in the form of a mouthwash to reduce VSC significantly at day 15 compared to control. [42] Level I was found for the use of echinacea lavandula pistacia in the form of a mucoadhesive tablet, [42] while level IV was found for the use of curcuma zedoaria and camellia sinensis mouthwash in the reduction of oral malodor. [4] Modifications to mechanical methods While mechanical methods form the backbone of oral hygiene, the modification of mechanical methods specifically for combating malodor remains a debated field with little detailed. The fact that no randomized control trials with a large multicenter sample (level I ) were found in this systematic review is an interesting finding; however, there were several studies with level. Of the different methods that have been studied there have been many that have focused on the use of modifications of tongue scraping. S J Oral Sci Vol 2 No 1 7 January 2015

6 Olivier-Neto et al. showed that a tongue scraper attached to the back of a toothbrush was able to significantly reduce bad breath for up to 2 h [43] while Erovic-Ademovski et al. showed that organoleptic scores were significantly lower following active rinse combined with tongue scraping compared to rinsing alone. [3] Faveri et al. showed that tongue scraping was the most effective method of reducing organoleptic scores compared to other oral hygiene methods without tongue scraping. [46] The above control studies support the initial findings of Seeman et al. who showed tongue cleaning was effective in reducing organoleptic scores. [49] These studies are in contrast to the findings of Haas et al. who showed that there was no effect of tongue scraping on organoleptic scores; [44] however, it must be noted that this was not a randomized control study. There have been several studies that have provided level I for the use of different mechanical methods. Oil pulling, a method by which sesame or mustard oil is kept in the mouth and swished has been used traditionally in India to achieve oral hygiene. [47] Asokan et al., showed that oil pulling was as effective as CHX mouthwash in the reduction of organoleptic scores. [45] While attempts to introduce several chemicals using chewing gum as a vehicle have been discussed earlier; De Luca-Monasterios et al. studied the effect of chewing gum without any active ingredients. They were able to demonstrate that chewing gum, when used as a purely mechanical method showed a significant effect on the reduction of oral malodor. [47] Conclusions The results of this systematic review suggest that while there are several physical and chemical methods available to combat oral halitosis, the use of mouthwashes and dentifrices remain the mainstay of halitosis management. 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