|Year : 2013 | Volume
| Issue : 6 | Page : 757-761
How to deal with morning bad breath: A randomized, crossover clinical trial
Jeronimo M Oliveira-Neto, Sandra Sato, Vinicius Pedrazzi
Department of Dental Materials and Prosthodontics, Faculty of Dentistry of Ribeirão Preto, University of São Paulo USP, Ribeirão Preto, Brazil
|Date of Submission||23-Jan-2013|
|Date of Acceptance||18-Jul-2013|
|Date of Web Publication||7-Jan-2014|
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Context: The absence of a protocol for the treatment of halitosis has led us to compare mouthrinses with mechanical oral hygiene procedures for treating morning breath by employing a hand-held sulfide monitor. Aims: To compare the efficacy of five modalities of treatment for controlling morning halitosis in subjects with no dental or periodontal disease. Settings and Design: This is a five-period, randomized, crossover clinical trial. Materials and Methods: Twenty volunteers were randomly assigned to the trial. Testing involved the use of a conventional tongue scraper, a tongue scraper joined to the back of a toothbrush's head, two mouthrinses (0.05% cetylpyridinium chloride and 0.12% chlorhexidine digluconate) and a soft-bristled toothbrush and fluoride toothpaste for practicing oral hygiene. Statistical Analysis Used: Data analysis was performed using SPSS version 17 for Windows and NCSS 2007 software (P < 0.05). The products and the periods were compared with each other using the Friedman's test. When significant differences (P < 0.05) were determined, the products and periods were compared in pairs by using the Wilcoxon's test and by adjusting the original significance level (0.05) for multiple comparisons by using the Bonferroni's method. Results: The toothbrush's tongue scraper was able to significantly reduce bad breath for up to 2 h. Chlorhexidine reduced bad breath only at the end of the second hour, an effect that lasted for 3 h. Conclusions: Mechanical tongue cleaning was able to immediately reduce bad breath for a short period, whereas chlorhexidine and mechanical oral hygiene reduced bad breath for longer periods, achieving the best results against morning breath.
Keywords: Halitosis, mouthwashes, tongue scraper, sulfide monitor
|How to cite this article:|
Oliveira-Neto JM, Sato S, Pedrazzi V. How to deal with morning bad breath: A randomized, crossover clinical trial. J Indian Soc Periodontol 2013;17:757-61
|How to cite this URL:|
Oliveira-Neto JM, Sato S, Pedrazzi V. How to deal with morning bad breath: A randomized, crossover clinical trial. J Indian Soc Periodontol [serial online] 2013 [cited 2019 Jul 18];17:757-61. Available from: http://www.jisponline.com/text.asp?2013/17/6/757/124497
| Introduction|| |
Currently, there are no standard or accepted protocols for the treatment of halitosis.  Different treatment strategies, including mechanical debridement of the tongue and rinsing with antimicrobial agents, have been proposed for the management of intra-oral halitosis.  Both tongue brushing and tongue scraping , have been advocated for removing the tongue coating responsible for emitting volatile sulfur compounds (VSCs). 
However, cleansing the tongue can be uncomfortable and may cause gag reflex. For this reason, the easier use of generally accepted mouthrinses has led to the development of a large number of commercially available products as a popular way of dealing with bad breath. ,
Although there are a large number of studies evaluating the effect of these products on halitosis, there is still plenty of disagreement among the results and their real effectiveness.
As there are no clinical trials comparing the effects of antimicrobial products of oral health care with the effect of mechanical reduction of bacteria and substrates,  the premise of this study was to evaluate, in vivo, both methods and to compare them with oral hygiene for morning breath control.
| Materials and Methods|| |
Twenty adults (six men, 14 women; mean age 35.9 years, range 18-50 years) of good general health and from a private dental office volunteered to participate in this randomized, crossover clinical trial. The study was explained to the subjects, who expressed their agreement by signing an informed consent statement approved by the Committee of Ethics in Clinical Research of the Ribeirγo Preto Dental School, University of Sγo Paulo, under process number 2006.1.1408.58.2. The study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2000. All the volunteers were submitted to an anamnesis and an oral clinical exam. Each subject had at least 20 erupted natural teeth, good oral hygiene and no periodontal disease. Exclusion criteria included dental caries, systemic disease, the use of any removable partial or total dentures, antibiotic treatment in the past 3 months, smoking, pregnancy and xerostomia or any other chronic oral inflammatory disease.
This study was based on a randomized, crossover design and a statistical analysis of the masked data clinical trial. It was constructed as a 5 × 5 balanced Latin-square - Williams design with a sample size of 20.  Each of the 20 subjects were randomly allocated by sortition into one of the five following sequences, as described in [Figure 1].
|Figure 1: In each day of interventions, all the products were used by different voluntaries with the intention that at the last day of intervention all the products were used, in an order of five different sequences for use of the products|
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During a 7-day pre-experimental phase, the volunteers were instructed to follow their customary oral hygiene procedures and were given a toothbrush (Professional Extreme - Johnson and Johnson Reach® , Sγo José dos Campos, SP, Brazil) and toothpaste without any antimicrobial agents other than sodium fluoride (Contente® , Suavetex Ind. Com. Ltda., Uberlβndia, MG, Brazil) by the researchers. They were not allowed to use any type of mouthrinse from the week before the first intervention throughout the study period. Dental flossing was not forbidden as individual variables could be compensated due to the crossover design of the study, as previously described. 
To register the baseline levels of VSCs in the morning, volunteers were instructed to remain without any type of oral hygiene (the last tooth brushing should have been performed by 12:00 pm) for 20 h before beginning the experiments. Furthermore, the volunteers were asked to avoid the consumption of foods whose decomposition would produce a strong odor (like garlic, onion, egg or cabbage) as well as the intake of alcoholic beverages. 
The commercial toothbrush, toothpaste, tongue scrapers and mouthrinses used as preventive dental materials are described below and identified by codes in [Table 1] and are also presented in [Figure 2].
|Figure 2: Hand-held sulfide monitor with a disposable straw and the oral hygiene care products used|
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|Table 1: Products tested for their ability to reduce the volatile sulfur compound levels |
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The levels of VSCs were measured by asking the volunteers to expel air through their mouths into a hand-held sulfide monitor, Breath Alert™ (Tanita Corporation® -Japan), according to the manufacturer's instructions [Figure 2], as performed previously in a study by Pedrazzi et al. in 2004. 
On the morning of the appointment, the volunteers were instructed not to practice any oral hygiene and to use one product after breakfast according to the recommendations of the manufacturers. When oral care had to be performed by brushing the teeth with toothpaste, the volunteers were permitted to brush their tongues with the toothbrush's bristles but without using the toothbrush's scraper. Each product was used once for 1 day per week (15 mL for 1 min in the case of the mouthrinses and ten strokes from the back to the tip of the tongue for the tongue scrapers). ,, The breath of each volunteer was examined at the following time intervals:
- T00 = before using the product (baseline data)
- T0 = immediately after rinsing or tongue cleaning or oral hygiene
- T1 = after 1 h
- T2 = after 2 h
- T3 = after 3 h.
After data collection, the volunteers were instructed to make use of only a toothbrush and toothpaste provided by the researchers for another 1-week period (washout). This was performed to avoid interference of the results with those of the next week (carry-over) because of similar studies with chlorhexidine formulations whose effects were found to be more long lasting.  After this period, the levels of VSCs were again measured when the volunteers switched to the next product in accordance with the pre-defined sequence, and so on until the fifth week.
Data analysis was performed using statistical software SPSS version 17 for Windows (SPSS, Chicago, IL, USA) and NCSS 2007 software (NCSS, Kaysville, USA), and the differences were considered to be statistically significant only for P < 0.05.
The five products were compared with each other in each period (Friedman's test), the five periods were compared for each product (Friedman's test) and the five sequences of products used were compared by the Kruskal-Wallis test. When significant differences (P < 0.05) were determined by using the Friedman's test, the products and periods were compared in pairs by using the Wilcoxon's test and by adjusting the original significance level (0.05) for multiple comparisons by using the Bonferroni's method.
With respect to the Kruskal-Wallis's test, when significant differences were found, comparison of the sequences was performed by the Dunn's test, with Bonferroni's adjustment for multiple comparisons.
| Results|| |
All the subjects finished the study. Significant differences in reduction of VSC levels were found only in the T0 period among the different products. The difference was significant among the groups using cetylpyridinium chloride - CPC (A) and both mechanical methods of tongue cleaning: The toothbrush's scraper (C) (P = 0.0004) and a conventional tongue scraper (D) (P = 0.0003). Chlorhexidine - CHX (B) differed from both the mechanical methods, C (P = 0.0003) and D (P = 0.0002) and from the positive control (with oral hygiene - method E) (P = 0.0029).
Although CPC (A) increased the breath scores immediately (P = 0.003), the levels returned to the baseline in the first hour. No significant difference was found after 1, 2 or 3 h when compared to the baseline.
CHX (B) was also able to increase the breath values immediately (P = 0.0005). However, there was a significant reduction in bad breath (compared with the baseline) only at the end of the second (P = 0.004) and third (P = 0.017) hours.
The toothbrush's scraper (C) decreased the breath scores immediately (P = 0.0049), and this decrease continued until the second hour (T1-P = 0.031; T2-P = 0.0008). However, the breath score was not significantly different from the baseline at the end of the third hour.
The conventional tongue scraper Kolbe® (D) showed differences over time when compared simultaneously by using the Friedman's test (P < 0.001). However, no statistically significant differences were found between any of them when comparing the periods in pairs with Wilcoxon's test with Bonferroni's adjustment. It was not possible to detect any difference from the baseline over the time periods of this study.
Using a toothbrush (and toothpaste) with an optional tongue brush reduced the breath scores only at the end of the first hour (P = 0.002). These breath scores reached the lowest value (normal breath) during this period and remained at that value for up to 3 h (T2-P = 0.0008; T3-P = 0.001).
| Discussion|| |
When the breath values at different times were compared with the baseline, the following observations were made:
Immediately (in T0) after the single use of the products, CPC chlorhexidine and the positive control (brushing with toothpaste) were able to raise the breath scores as a side-effect of detachment, disintegration and flotation of desquamated epithelial cells, food waste and defense cells. ,
CPC increased the breath scores immediately but did not reduce bad breath in any of the periods studied (P > 0.05). CHX also increased the scores immediately after use but was able to significantly reduce the breath scores at the end of the second hour; this effect lasted up to the third hour. These results show the superiority of CHX over CPC in reducing bad breath for a longer period.
The inferior performance of CPC in reducing bad breath in this study can be due to the lack of antibacterial activity, , whereas CHX was more effective against VSCs.
The toothbrush's scraper was able to reduce bad breath immediately after its use, an effect that was observed for up to 2 h. The third-hour breath scores did not differ from the baseline. The conventional tongue scraper also reduced bad breath, but not significantly. This demonstrates the superiority of the toothbrush's scraper to reduce bad breath when compared with the conventional scraper, but only for up to 2 h. Tongue scraping appears to be an important hygienic procedure to reduce morning breath in periodontally healthy individuals, and should therefore be incorporated into daily oral hygiene procedures. 
Although mechanical cleaning of the tongue can reduce its bacterial load, this effect is transient. Some authors  report such a decrease to last for up to 100 min, similar to our findings. This could be because the tongue has a large surface area and its papillary structure represents an anaerobic niche in the oral cavity, favoring the accumulation of debris and microorganisms responsible for the formation of VSCs. Mechanical methods show short-term efficacy in improving morning breath in studies on persistent or chronic halitosis. ,
In the present study, the association of tooth brushing (mechanical cleaning) with sodium fluoride toothpaste (mechanical and chemical) in oral hygiene care led to a significant reduction of bad breath in the first hour, and lasted up to the third hour. In this case, the positive control expectedly gave one of the best performances in combating morning halitosis for the first hour. It has been claimed that regular use of a toothbrush for cleaning the tongue is inferior in the removal of tongue debris and microorganisms compared with the use of specific cleansers.  However, it is desirable to use a product that provides the maximum benefit with a minimum number of tongue movements, thereby reducing the gag reflex. 
Masking products are ineffective and antimicrobial agents are only temporarily effective in reducing the levels of microorganisms and their substrates. Good short-term results have been reported with chlorhexidine in studies on real halitosis. 
Studies have shown that brushing the tongue with toothpaste could reduce the levels of VSCs for at least 1 h, and this was more effective than only brushing the teeth. , In our study, the control group had low breath scores for up to 3 h, perhaps due to the restoration of normal microbiota after practicing oral hygiene, which is uncommon in patients with chronic halitosis.
In this study, oral hygiene was effective in reducing bad breath within the first hour, an effect that lasted for up to 3 h. However, it is not possible to say whether this effect was due to tongue cleaning, because it was not considered mandatory and because brushing the tongue with toothpaste is rarely practiced due to discomfort and/or lack of awareness by professionals or patients.  Even so, it can be inferred that this method, which is a combination of a mechanical method (removal of dental and/or tongue biofilm with a toothbrush and toothpaste) and a chemical effect (sodium fluoride) achieved the best results after 1 h. The other effective approach in reducing mouth odor was the use of chlorhexidine. However, this should not be routinely used because of the risk of staining of the teeth and alteration of taste. 
Overall, this study demonstrates the superiority of chlorhexidine over CPC (among the chemical methods) and over mechanical methods (both cleansers) for up to 3 h. However, when compared with the control, the practice of oral hygiene, like CHX, was more effective in the first hour (along with the brush's scraper) until the third hour. 
With these results, we can say that it is evident that morning halitosis in healthy individuals is a cosmetic problem, similar to body odor.  Oral hygiene is sufficient to eliminate the problem, as previously stated by Yaegaki and Coil (2000)  in their discussion of the need to treat morning breath. Tonzetich (1977) and Rosenberg (1990) argue that the best way to treat halitosis is to motivate the patient to practice good oral hygiene and that a gentle but effective deep tongue cleaning should become part of daily oral hygiene. ,
To sum up, methods for the improvement of morning breath should not be applied to chronic halitosis as the results of this study are similar to those of other studies testing methods or products against morning breath ,, but are different from reports in the literature on persistent halitosis. ,
Although there is no consensus on the best treatment for bad breath, the dentist will remain befuddled on the patient needs, while will be available in the market, new, lucrative and growing promises to combat a so common and ancient problem called bad breath.
| Acknowledgment|| |
The authors would like to thank Johnson and Johnson for the generous donation of the toothbrushes, Oral-B for the mouthrinses and they would also like to thank all the volunteers who participated in this project.
| References|| |
|1.||Morita M, Wang HL. Association between oral malodor and adult periodontitis: A review. J Clin Periodontol 2001;28:813-9. |
|2.||Fedorowicz Z, Aljufairi H, Nasser M, Outhouse TL, Pedrazzi V. Mouthrinses for the treatment of halitosis. Cochrane Database Syst Rev 2008;4:1-23. |
|3.||Pedrazzi V, Sato S, de Mattos Mda G, Lara EH, Panzeri H. Tongue-cleaning methods: A comparative clinical trial employing a toothbrush and a tongue scraper. J Periodontol 2004;75:1009-12. |
|4.||Bordas A, McNab R, Staples AM, Bowman J, Kanapka J, Bosma MP. Impact of different tongue cleaning methods on the bacterial load of the tongue dorsum. Arch Oral Biol 2008;53:13-8. |
|5.||Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, van Steenberghe D. Impact of tongue cleansers on microbial load and taste. J Clin Periodontol 2004;3:506-10. |
|6.||Saad S, Greenman J, Shaw H. Comparative effects of various commercially available mouthrinse formulations on oral malodor. Oral Dis 2011;17:180-6. |
|7.||van den Broek AM, Feenstra L, de Baat C. A review of the current literature on management of halitosis. Oral Dis 2008;14:30-9. |
|8.||Newcombe RG, Addy M, McKeown S. Residual effect of chlorhexidine gluconate in 4-day plaque regrowth crossover trials, and its implications for study design. J Periodontal Res 1995;30:319-24. |
|9.||Peruzzo DC, Jandiroba PF, Nogueira Filho Gda R. Use of 0.1% chlorine dioxide to inhibit the formation of morning volatile sulphur compounds (VSC). Braz Oral Res 2007;21:70-4. |
|10.||Rosenberg M, Gelernter I, Barki M, Bar-Ness R. Day-long reduction of oral malodor by a two-phase oil: Water mouthrinse as compared to chlorhexidine and placebo rinses. J Periodontol 1992;63:39-43. |
|11.||Seemann R, Kison A, Bizhang M, Zimmer S. Effectiveness of mechanical tongue cleaning on oral levels of volatile sulfur compounds. J Am Dent Assoc 2001;132:1263-7. |
|12.||Roldan S, Herrera D, Santa-Cruz I, O'Connor A, Gonzalez I, Sanz M. Comparative effects of different chlorhexidine mouth-rinse formulations on volatile sulphur compounds and salivary bacterial counts. J Clin Periodontol 2004;31:1128-34. |
|13.||Kuyama K, Yamamoto H. A study of effects of mouthwash on the human oral mucosae: With special references to sites, sex differences and smoking. J Nihon Univ Sch Dent 1997;39:202-10. |
|14.||Gagari E, Kabani S. Adverse effects of mouthwash use. A review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995;80:432-9. |
|15.||Cortelli JR, Barbosa MD, Westphal MA. Halitosis: A review of associated factors and therapeutic approach. Braz Oral Res 2008;22 Suppl 1:44-54. |
|16.||Young A, Jonski G, Rolla G. Inhibition of orally produced volatile sulfur compounds by zinc, chlorhexidine or cetylpyridinium chloride-effect of concentration. Eur J Oral Sci 2003;111:400-4. |
|17.||Faveri M, Hayacibara MF, Pupio GC, Cury JA, Tsuzuki CO, Hayacibara RM. A cross-over study on the effect of various therapeutic approaches to morning breath odour. J Clin Periodontol 2006;33:555-60. |
|18.||Roldan S, Herrera D, Sanz M. Biofilms and the tongue: Therapeutical approaches for the control of halitosis. Clin Oral Investig 2003;7:189-97. |
|19.||Christensen GJ. Why clean your tongue? J Am Dent Assoc 1998;129:1605-7. |
|20.||Tonzetich J. Oral malodour: An indicator of health status and oral cleanliness. Int Dent J 1978;28:309-19. |
|21.||Yaegaki K, Coil JM, Kamemizu T, Miyazaki H. Tongue brushing and mouth rinsing as basic treatment measures for halitosis. Int Dent J 2002;52:192-6. |
|22.||Carvalho MD, Tabchoury CM, Cury JA, Toledo S, Nogueira-Filho GR. Impact of mouthrinses on morning bad breath in healthy subjects. J Clin Periodontol 2004;31:85-90. |
|23.||Yaegaki K, Coil JM. Examination, classification, and treatment of halitosis; clinical perspectives. J Can Dent Assoc 2000;66:257-61. |
|24.||Tonzetich J. Production and origin of oral malodor: A review of mechanisms and methods of analysis. J Periodontol 1977;48:13-20. |
|25.||Rosenberg M. Bad breath, diagnosis and treatment. Univ Tor Dent J 1990;3:7-11. |
|26.||van Steenberghe D, Avontroodt P, Peeters W, Pauwels M, Coucke W, Lijnen A, et al. Effect of different mouthrinses on morning breath. J Periodontol 2001;72:1183-91. |
|27.||Roldan S, Winkel EG, Herrera D, Sanz M, Van Winkelhoff AJ. The effects of a new mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc lactate on the microflora of oral halitosis patients: A dual-centre, double-blind placebo-controlled study. J Clin Periodontol 2003;30:427-34. |
[Figure 1], [Figure 2]