|Year : 2015 | Volume
| Issue : 1 | Page : 3-9
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
|Date of Web Publication||2-Feb-2015|
Omar Hamad Alkadhi
P.O. Box 84891, Riyadh 11681
Source of Support: None, Conflict of Interest: None
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 evidence for each treatment modality of halitosis. Electronic databases were searched in a systematic method according to preferred reporting items for systematic reviews and meta-analyses 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 evidence 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 evidence 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.
Keywords: Dentifrices, halitosis, mouthwashes, systematic review
|How to cite this article:|
Alkadhi OH. The management of physiological halitosis: A 20-year systematic review of the literature. Saudi J Oral Sci 2015;2:3-9
|How to cite this URL:|
Alkadhi OH. The management of physiological halitosis: A 20-year systematic review of the literature. Saudi J Oral Sci [serial online] 2015 [cited 2019 Jan 21];2:3-9. Available from: http://www.saudijos.org/text.asp?2015/2/1/3/150579
| 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.  It has been reported that halitosis decreases self-confidence and leads to insecure social relations, to the extent of avoiding social interactions. 
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. , While 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. , 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. ,, 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 evidence present for each method of treatment. The aim of this systematic review is to document the level of evidence available for the use of different modalities in the management of halitosis.
| Materials and Methods|| |
The search was conducted electronically in PubMed from 1999 to 2014. 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].
|Figure 1: Preferred reporinng items for systematic reviews and meta-analyses protocol used in this study|
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The levels of evidence were assigned using the criteria put forth by the center for evidence based medicine [Table 1]. 
| 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:
- Chemical compounds in mouthwashes.
- Chemical compounds in dentifrices.
- Chemical compounds in other products.
- Herbal products.
- 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].
|Table 2: Studies on the addition of chemical compounds to mouthrinses to combat halitosis|
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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].
|Table 3: Studies on the addition of chemicals to dentifrices to prevent oral malodor|
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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].
|Table 4: Studies on alternative delivery systems for chemicals used to treat oral malodor|
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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].
|Table 5: Studies using herbal derived products for the management of halitosis|
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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].
|Table 6: Studies on the efficacy of modified mechanical methods on oral malodor|
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| Discussion|| |
The results of this systematic review suggest that despite the several different approaches used in the 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 III 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, ,, Triclosan and cetylpyridinium chloride are all significantly better than EO mouthwashes at reducing oral malodor.  While there was some initial support for the use of CD in the management of halitosis,  there is an inadequate level I or level II evidence 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 II evidence. Level I evidence existed for Zn lactate to conventional mouthwashes can enhance the masking and therapeutic effect of mouthrinses on oral malodor.  However, Quirynen et al., in a study with level II evidence 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. 
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.  Similarly level II evidence 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 enough evidence to show that that there is a difference in efficacy between ASF with Zn lactate and CHX with cetylpyridinium chloride in reducing oral malodor. , There is, however, level II evidence to suggest that cetylpyridinium chloride is significantly better than EOs or CD with Zn (CD/Zn) in the reduction of oral malodor. 
The brushing of teeth has always been seen as an effective method of reducing halitosis, however few studies with the level I or level II evidence were found in the literature.
Among dentifrices too, there existed a level I and level II evidence 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.  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. 
Among fluoridated toothpastes, it has been shown that stannous fluoride was able to reduce VSC better than sodium fluoride. , Triclosan is a compound that is often added to toothpastes for its effect in preventing the formation of calculus. ,, Sharma et al. have shown that triclosan can produce better breath odor scores 12 h after use in comparison to control.  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.  However, there is no level I or level II evidence in support of triclosan as an agent to fight halitosis. The same holds true for the effect of the addition of EO to dentifrices. 
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 evidence 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.  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. 
Level II evidence existed for products such as hinokitiol.  Abrasive microcapsules (Breezy candy)  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;  while Nohno et al. showed that candy tablets containing protease and actinidine showed a significant reduction in VSC.  Zhu et al. showed that salivary anaerobes were significantly lower in subjects who chewed gum that contained cinnamic aldehyde.  While Iwamoto et al. showed a significant reduction in halitosis parameters in those subjects using lactobacillus salivarius with xylitol tablets  for 2 weeks. Greenstein et al. showed that oxidizing lozenges showed a significant reduction in malodor  of the dorsal surface of the tongue. However, it must be remembered that all these products had only level III evidence and no randomized control studies exist to support their efficacy.
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 evidence of efficacy. Tanaka et al. showed that that eucalyptus-extract chewing gum was able to produce significant reductions in organoleptic and tongue-coating scores at 4, 8, 12, and 14 weeks. 
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. 
Level III evidence was found for the use of echinacea lavandula pistacia in the form of a mucoadhesive tablet,  while level IV evidence was found for the use of curcuma zedoaria and camellia sinensis mouthwash in the reduction of oral malodor. 
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 evidence. The fact that no randomized control trials with a large multicenter sample (level I evidence) were found in this systematic review is an interesting finding; however, there were several studies with level II. Of the different methods that have been studied there have been many that have focused on the use of modifications of tongue scraping.
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  while Erovic-Ademovski et al. showed that organoleptic scores were significantly lower following active rinse combined with tongue scraping compared to rinsing alone.  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.  The above control studies support the initial findings of Seeman et al. who showed tongue cleaning was effective in reducing organoleptic scores.  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;  however, it must be noted that this was not a randomized control study.
There have been several studies that have provided level III evidence 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.  Asokan et al., showed that oil pulling was as effective as CHX mouthwash in the reduction of organoleptic scores. 
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. 
| 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. There is currently insufficient amount of level I evidence 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.
| References|| |
Lee SS, Zhang W, Li Y. Halitosis update: A review of causes, diagnoses, and treatments. J Calif Dent Assoc 2007;35:258-60, 62, 64.
McKeown L. Social relations and breath odour. Int J Dent Hyg 2003;1:213-7.
Erovic Ademovski S, Lingström P, Winkel E, Tangerman A, Persson GR, Renvert S. Comparison of different treatment modalities for oral halitosis. Acta Odontol Scand 2012;70:224-33.
Farina VH, Lima AP, Balducci I, Brandão AA. Effects of the medicinal plants Curcuma zedoaria and Camellia sinensis
on halitosis control. Braz Oral Res 2012;26:523-9.
Masuo Y, Suzuki N, Yoneda M, Naito T, Hirofuji T. Salivary β-galactosidase activity affects physiological oral malodour. Arch Oral Biol 2012;57:87-93.
Scully C. Halitosis. Clin Evid (Online) 2014;9:1305.
Brunner F, Kurmann M, Filippi A. The correlation of organoleptic and instrumental halitosis measurements. Schweiz Monatsschr Zahnmed 2010;120:402-8.
Tamaki N, Kasuyama K, Esaki M, Toshikawa T, Honda S, Ekuni D, et al.
A new portable monitor for measuring odorous compounds in oral, exhaled and nasal air. BMC Oral Health 2011;11:15.
Tsai CC, Chou HH, Wu TL, Yang YH, Ho KY, Wu YM, et al.
The levels of volatile sulfur compounds in mouth air from patients with chronic periodontitis. J Periodontal Res 2008;43:186-93.
Dadamio J, Van Tournout M, Teughels W, Dekeyser C, Coucke W, Quirynen M. Efficacy of different mouthrinse formulations in reducing oral malodour: A randomized clinical trial. J Clin Periodontol 2013;40:505-13.
Malhotra S, Yeltiwar RK. Evaluation of two mouth rinses in reduction of oral malodor using a spectrophotometric technique. J Indian Soc Periodontol 2011;15:250-4.
Thaweboon S, Thaweboon B. Effect of an essential oil-containing mouth rinse on VSC-producing bacteria on the tongue. Southeast Asian J Trop Med Public Health 2011;42:456-62.
Wilhelm D, Gysen K, Himmelmann A, Krause C, Wilhelm KP. Short-term effect of a new mouthrinse formulation on oral malodour after single use in vivo
: A comparative, randomized, single-blind, parallel-group clinical study. J Breath Res 2010;4:036002.
Wigger-Alberti W, Gysen K, Axmann EM, Wilhelm KP. Efficacy of a new mouthrinse formulation on the reduction of oral malodour in vivo
. A randomized, double-blind, placebo-controlled, 3 week clinical study. J Breath Res 2010;4:017102.
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.
Winkel EG, Roldán S, Van Winkelhoff AJ, Herrera D, Sanz M. Clinical effects of a new mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc-lactate on oral halitosis. A dual-center, double-blind placebo-controlled study. J Clin Periodontol 2003;30:300-6.
Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, Coucke W, et al.
The efficacy of amine fluoride/stannous fluoride in the suppression of morning breath odour. J Clin Periodontol 2002;29:944-54.
Borden LC, Chaves ES, Bowman JP, Fath BM, Hollar GL. The effect of four mouthrinses on oral malodor. Compend Contin Educ Dent 2002;23:531-6, 38, 40.
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.
Frascella J, Gilbert RD, Fernandez P, Hendler J. Efficacy of a chlorine dioxide-containing mouthrinse in oral malodor. Compend Contin Educ Dent 2000;21:241-4, 46, 48.
Frascella J, Gilbert R, Fernandez P. Odor reduction potential of a chlorine dioxide mouthrinse. J Clin Dent 1998;9:39-42.
Kozlovsky A, Goldberg S, Natour I, Rogatky-Gat A, Gelernter I, Rosenberg M. Efficacy of a 2-phase oil: Water mouthrinse in controlling oral malodor, gingivitis, and plaque. J Periodontol 1996;67:577-82.
Young A, Jonski G. Effect of a single brushing with two Zn-containing toothpastes on VSC in morning breath: A 12 h, randomized, double-blind, cross-over clinical study. J Breath Res 2011;5:046012.
Payne D, Gordon JJ, Nisbet S, Karwal R, Bosma ML. A randomised clinical trial to assess control of oral malodour by a novel dentifrice containing 0.1%w/w o-cymen-5-ol, 0.6%w/w zinc chloride. Int Dent J 2011;61 Suppl 3:60-6.
Chen X, He T, Sun L, Zhang Y, Feng X. A randomized cross-over clinical trial to evaluate the effect of a 0.454% stannous fluoride dentifrice on the reduction of oral malodor. Am J Dent 2010;23:175-8.
Hu D, Zhang YP, DeVizio W, Proskin HM. A clinical investigation of the efficacy of two dentifrices for controlling oral malodor and plaque microflora overnight. J Clin Dent 2008;19:106-10.
Farrell S, Barker ML, Gerlach RW. Overnight malodor effect with a 0.454% stabilized stannous fluoride sodium hexametaphosphate dentifrice. Compend Contin Educ Dent 2007;28:658-61.
Sharma NC, Galustians HJ, Qaqish J, Galustians A, Rustogi K, Petrone ME, et al.
Clinical effectiveness of a dentifrice containing triclosan and a copolymer for controlling breath odor. Am J Dent 2007;20:79-82.
Olshan AM, Kohut BE, Vincent JW, Borden LC, Delgado N, Qaqish J, et al
. Clinical effectiveness of essential oil-containing dentifrices in controlling oral malodor. Am J Dent 2000;13:18C-22.
Suzuki N, Yoneda M, Tanabe K, Fujimoto A, Iha K, Seno K, et al.
Lactobacillus salivarius WB21 - containing tablets for the treatment of oral malodor: A double-blind, randomized, placebo-controlled crossover trial. Oral Surg Oral Med Oral Pathol Oral Radiol 2014;117:462-70.
Iha K, Suzuki N, Yoneda M, Takeshita T, Hirofuji T. Effect of mouth cleaning with hinokitiol-containing gel on oral malodor: A randomized, open-label pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol 2013;116:433-9.
Tian M, Hanley AB, Dodds MW, Yaegaki K. Chewing gum containing allyl isothiocyanate from mustard seed extract is effective in reducing volatile sulfur compounds responsible for oral malodor. Am J Dent 2013;26:180-4.
Porciani PF, Grandini S. The effect of zinc acetate and magnolia bark extract added to chewing gum on volatile sulfur-containing compounds in the oral cavity. J Clin Dent 2012;23:76-9.
Nohno K, Yamaga T, Kaneko N, Miyazaki H. Tablets containing a cysteine protease, actinidine, reduce oral malodor: A crossover study. J Breath Res 2012;6:017107.
Barak S, Katz J. The effect of Breezy candy on halitosis: A double-blind, controlled, and randomized study. Quintessence Int 2012;43:313-7.
Shin K, Yaegaki K, Murata T, Ii H, Tanaka T, Aoyama I, 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. Clin Oral Investig 2011;15:485-93.
Zhu M, Carvalho R, Scher A, Wu CD. Short-term germ-killing effect of sugar-sweetened cinnamon chewing gum on salivary anaerobes associated with halitosis. J Clin Dent 2011;22:23-6.
Iwamoto T, Suzuki N, Tanabe K, Takeshita T, Hirofuji T. Effects of probiotic Lactobacillus salivarius WB21 on halitosis and oral health: An open-label pilot trial. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:201-8.
Greenstein RB, Goldberg S, Marku-Cohen S, Sterer N, Rosenberg M. Reduction of oral malodor by oxidizing lozenges. J Periodontol 1997;68:1176-81.
Sterer N, Ovadia O, Weiss EI, Perez Davidi M. Day-long reduction of oral malodor by a palatal mucoadhesive tablet containing herbal formulation. J Breath Res 2013;7:026004.
Tanaka M, Toe M, Nagata H, Ojima M, Kuboniwa M, Shimizu K, et al.
Effect of eucalyptus-extract chewing gum on oral malodor: A double-masked, randomized trial. J Periodontol 2010;81:1564-71.
Rassameemasmaung S, Sirikulsathean A, Amornchat C, Hirunrat K, Rojanapanthu P, Gritsanapan W. Effects of herbal mouthwash containing the pericarp extract of Garcinia mangostana
L on halitosis, plaque and papillary bleeding index. J Int Acad Periodontol 2007;9:19-25.
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.
Haas AN, Silveira EM, Rösing CK. Effect of tongue cleansing on morning oral malodour in periodontally healthy individuals. Oral Health Prev Dent 2007;5:89-94.
Asokan S, Kumar RS, Emmadi P, Raghuraman R, Sivakumar N. Effect of oil pulling on halitosis and microorganisms causing halitosis: A randomized controlled pilot trial. J Indian Soc Pedod Prev Dent 2011;29:90-4.
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.
De Luca-Monasterios F, Chimenos-Küstner E, López-López J. Effect of chewing gum on halitosis. Med Clin (Barc) 2014;143:64-7.
Wilhelm D, Himmelmann A, Axmann EM, Wilhelm KP. Clinical efficacy of a new tooth and tongue gel applied with a tongue cleaner in reducing oral halitosis. Quintessence Int 2012;43:709-18.
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.
Wilhelm D, Himmelmann A, Krause C, Wilhelm KP. Short term clinical efficacy of new meridol HALITOSIS tooth & tongue gel in combination with a tongue cleaner to reduce oral malodor. J Clin Dent 2013;24:12-9.
Tian M, 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 Breath Res 2013;7:026001.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]