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J Am Dent Assoc, Vol 135, No 8, 1133-1141.
© 2004 American Dental Association
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RESEARCH

The antimicrobial potential of 14 natural herbal dentifrices

Results of an in vitro diffusion method study



SEAN S. LEE, D.D.S., WU ZHANG, M.D. and YIMING LI, D.D.S., M.S.D., Ph.D.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background. Increasing numbers of Americans are using natural herbal products for general and oral health care. Few of these products, however, have undergone rigorous testing, as evidenced by the limited amount of information on their safety and efficacy in the literature. The authors conducted an in vitro study to evaluate the antimicrobial potential of 14 natural herbal dentifrices.

Methods. The authors used a diffusion method to evaluate the antimicrobial effectiveness of 14 natural herbal dentifrices against four microorganisms: Streptococcus mutans, Streptococcus sanguis, Actinomyces viscosus and Candida albicans. Colgate Total (Colgate-Palmolive, New York City) and sterile pyrogen-free water served as the positive and negative controls, respectively. The authors tested the natural herbal dentifrices at full strength and at 1:1 dilution. They measured the zones of inhibition at 24 and 48 hours to evaluate the antimicrobial potential of the dentifrices.

Results. Six herbal dentifrices were effective in inhibiting the growth of all four microorganisms. The positive control produced significantly sized inhibition zones with all four microorganisms, while the negative control produced no observable zones. Six herbal dentifrices produced larger inhibition zones with A. viscosus than did the positive control. Six herbal dentifrices were inhibitory against C. albicans at full strength, but at 1:1 dilution, only three had such inhibitory effect. One herbal dentifrice produced microbial growth around and over the samples, indicating possible microbial contamination of the toothpaste. Only one herbal dentifrice showed consistent antimicrobial activity against all four microorganisms.

Conclusions. The variation in antimicrobial inhibition among the herbal dentifrices indicates that more research is needed to validate their effectiveness claims.

Clinical Implications. This study provides practitioners with insight into the claims of natural herbal dentifrices’ antimicrobial effects.

An estimated one-third to one-half of all Americans practice some form of alternative medicine,1–4 including use of natural or herbal health care products. The use of these products, including dentifrices, has increased significantly in the last decade.5–8 American consumers who gravitate toward using herbal products often view these products as being safer than products that contain chemicals.9 Dentifrices labeled as "natural" typically do not include ingredients such as synthetic sweeteners, artificial colors, preservatives, additives, or synthetic flavors and fragrances.10 The term "herbal" on the label implies that most of a dentifrice’s active ingredients are plant-based.

Only one herbal dentifrice showed consistent antimicrobial activity.

Consumers of these natural health care products typically are well-educated and have above-median incomes.11 However, they tend to conceal their outside-the-mainstream practices from their health care professionals to avoid ridicule.12

As the popularity of natural medicines and dentifrices continues to rise,13 dental professionals are in a position to provide information to patients about these products’ safety and efficacy. This can be difficult, however, owing to a lack of professional consensus on the subject. To date, an insufficient amount of clinical research on herbal-based mouthrinses and dentifrices has been reported,14–19 in contrast with a plethora of such research for conventional oral care products.20–22 A lack of scientific studies on natural and herbal products in the peer-reviewed dental literature poses a conundrum for health care professionals when dealing with these products. While some of these natural products could be just as safe as conventional dentifrices, others may pose various risks if used incorrectly. 4,13,23 In addition, as only a limited number of in vivo studies on herbal dentifrices have been published, it has not been determined whether they are superior, equivalent or substandard to conventional dentifrices in reducing plaque, for example.17,24 Furthermore, few research efforts have been directed toward addressing the potency or quality of herbal ingredients used in these dental products. It generally is agreed that with the exclusion of fluoride from most natural herbal dentifrices, these dentifrices usually forfeit caries-preventive benefits.25

The antimicrobial activity the authors observed varied greatly among the 14 herbal dentifrices tested.

While many herbal dentifrices claim to have antimicrobial properties, very little research has been conducted to investigate these claims. Therefore, we formed a team of investigators affiliated with Loma Linda University School of Dentistry (Loma Linda, Calif.) to conduct an in vitro study to assess the antimicrobial potential of 14 over-the-counter natural or herbal dentifrices using a standard diffusion method.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
We purchased 14 natural herbal dentifrices (one powder and 13 pastes) from retail health food stores in Southern California (Table 1Go). Colgate Total (Colgate-Palmolive, New York City) served as the positive control, and we used sterile pyrogen-free water (Milli-Q system, filtered with Millipak Gamma Gold Filters, Sterile Vented Filter Unit 0.22 µm, Millipore, Bedford, Mass.) as the negative control. We obtained four oral microorganisms from American Type Culture Collection, or ATCC (Manassas, Va.). They were Streptococcus mutans (ATCC 25175), Streptococcus sanguis (ATCC 10556), Actinomyces viscosus (ATCC 43146) and Candida albicans (ATCC 18804). We tested the dentifrices at full strength and at 1:1 dilution with the sterile pyrogen-free water using a standard diffusion technique.26 We placed dentifrice samples of approximately 50 milligrams on sterile filter disks (Millipak-40, Millipore) and positioned the disks on the surfaces of tryptic soy agar that we inoculated with the test microorganisms. We then incubated the agar plates with dentifrice samples at 37 C. If antimicrobial activity was present on the plates, it was indicated by an inhibition zone surrounding the filter disk containing the test material. We measured the diameter of the inhibition zones in millimeters at 24 and 48 hours. We conducted the experiments in triplicate at full strength and at 1:1 dilution for each test dentifrice and the controls. For each dentifrice, we calculated the mean and standard deviation of the diameters of inhibition zones. We analyzed the data using one-way analysis of variance, or ANOVA. Null hypothesis was rejected. Therefore, we used a multiple comparison procedure known as Student-Newman-Keuls test to determine the significance of differences among the means at the significance level of P = .05.


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  		TABLE 1 DENTIFRICES TESTED FOR ANTIMICROBIAL POTENTIAL.

 

   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The antimicrobial activity we observed on the agar plates varied greatly among the 14 herbal dentifrices tested. The positive control produced significantly sized inhibition zones for all four microorganisms. The negative control produced no observable inhibitory effect.

Among the 14 test dentifrices, we observed most of the antimicrobial activity at 24 hours; we detected little additional inhibition at 48 hours (Table 2Go, page 1136). When we tested the 14 dentifrices at full strength, nine, 11 and 10 of the 14 test dentifrices produced zones of inhibition against S. mutans, S. sanguis and A. viscosus, respectively. When we tested them at a 1:1 dilution, nine, nine and 10 of the 14 test dentifrices exhibited various activities of inhibiting the growth of S. mutans, S. sanguis and A. viscosus, respectively. Dental Herb (Franklin Botanical Laboratory, Northridge, Calif.), Herbal Brite (GS America, Los Angeles), Peelu (Peelu, Fargo, N.D.) and Pink Toothpaste With Myrrh (Weleda, Congers, N.Y.) had no inhibitory effect on S. mutans, even at full strength, while Dental Gel (NutriBiotic, Lakeport, Calif.) produced a significantly larger inhibition zone than the positive control.


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  		TABLE 2 MEAN DIAMETER OF INHIBITION ZONES INDUCED BY 14 HERBAL DENTIFRICES WITH FOUR ORAL MICROORGANISMS.

 
At 1:1 dilution, the differences among the 10 test dentifrices shown to inhibit the growth of microorganisms at full strength became less evident. We observed these phenomena in the positive control as well. In plates with S. sanguis, Dental Gel and Dental Herb at full strength were more effective than the positive control, but Nature’s Gate Natural Toothpaste (Levlad, Chatsworth, Calif.) at 1:1 dilution produced larger inhibition zones than did the positive control.

Two and four test dentifrices (Dental Herb, Nutrismile C [Jason Natural Cosmetics, Los Angeles], Peelu and Pink Toothpaste With Myrrh) showed no inhibitory effect against the growth of S. sanguis at full strength and 1:1 dilution, respectively. The full strength of Dental Gel, Acu-Herb (Murphy’s Import, Los Angeles), Healthy Mouth (Jason Natural Cosmetics), Auromere Herbal Toothpaste (Balsara International, Mumbai, India), Nature’s Gate Natural Toothpaste and Tom’s of Maine Natural Tooth-paste (Tom’s of Maine, Kennebunk, Maine) induced larger inhibition zones than the positive control in plates with A. viscosus; however, only Dental Gel was more effective than the positive control at the 1:1 dilution.

In plates of C. albicans, Dental Gel and Nutrismile C were more effective than other herbal dentifrices when tested at full strength. At 1:1 dilution, these two dentifrices, as well as Healthy Mouth, also were more effective than the positive control. Dental Gel, Nutrismile C, Healthy Mouth, Sea Fresh (Jason Natural Cosmetics), Tom’s of Maine Natural Toothpaste and Nature’s Gate Natural Toothpaste tested at full strength had an inhibitory effect against C. albicans. At 1:1 dilution, 11 of the 14 herbal dentifrices tested and the positive control had negligible antimicrobial effect on C. albicans. Dental Gel, Nutrismile C and Healthy Mouth were the three dentifrices that did produce inhibition zones.

Among the herbal dentifrices tested, Dental Gel (Figure 1Go) was the only one that showed consistent antimicrobial activity against all four oral microorganisms. Dentifrico de Echinacea (Bio-force AG, Roggwil, Switzerland) (Figure 2Go) had no inhibitory effect against any of the four microorganisms. Instead, we observed growth of unidentified microorganisms over and around the samples in all test plates. To rule out investigator-induced variations, we tested Dentifrico de Echinacea two additional times, and our previous results were confirmed. Therefore, the results for this dentifrice indicate possible microbial contamination of the original product.



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  		Figure 1. Antimicrobial activity of Dental Gel (NutriBiotic, Lakeport, Calif.) against Actinomyces viscosus. Colgate Total is manufactured by Colgate-Palmolive, New York City. PFW: Pyrogen-free water.

 


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  		Figure 2. Antimicrobial activity of Dentifrico de Echinacea (Bioforce AG, Roggwil, Switzerland) against Actinomyces viscosus. Colgate Total is manufactured by Colgate-Palmolive, New York City. PFW: Pyrogen-free water.

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
We chose S. mutans, A. viscosus and C. albicans as test microorganisms for our study because they have been implicated in oral diseases. We also chose S. sanguis as a test microorganism for our study. While it is considered to be an opportunistic bacterium in the oral cavity, it may induce significant health risks if it enters any sites in which abscesses can develop, such as the brain and the heart. It is believed that the viridans streptococci such as S. sanguis, which can enter the bloodstream through an oral infection wound or an extraction site, cause between 40 and 50 percent of cases of endocarditis,27 for which patients with damaged heart valves or other cardiac abnormalities are at risk of developing. Of the Candida species, C. albicans is the most common yeast isolated from the oral cavity, and it is associated with fungal oral infection, endocarditis and septicemia.27 The results of this study, which measured dentifrices’ ability to inhibit these microorganisms, provides significant information for dental professionals. For example, after considering our study’s results and consulting other sources, a practitioner may recommend a dentifrice that has good inhibition properties against C. albicans for a patient who is susceptible to oral fungal infections.

Limitations. There are limitations associated with our study. Bacterial and fungal pathogenicity is a multifactorial process, involving microbial virulence and host response, along with genetic and environmental factors such as saliva buffering and diet.27 Some researchers have looked at whether detrimental shifts in periodontopathic, cariogenic or opportunistic flora and increases in resistant strains have resulted from antibacterial ingredients in regular dentifrices.28 It is known that a balance exists in each person’s oral microbial population. If that balance is lost, opportunistic microorganisms can proliferate, enabling the initiation of disease processes. Therefore, the dentifrice we identified as having the largest microbial inhibition zone—and thus probably the strongest antibacterial and antifungal properties—may not be necessarily superior to those found to have smaller-diameter inhibition zones.

Because a dentifrice used in vivo likely is diluted by saliva, the level to which antimicrobial properties are buffered or lost in dilution in vitro is of interest. In 1:1 dilutions tested at 24 hours on the agar plates inoculated with C. albicans, we observed areas of partial inhibition for three test dentifrices. This finding indicates that the antimicrobial efficacy of these dentifrices against C. albicans may be compromised when diluted. As measured by a dilution procedure, the diameter of a zone of inhibition is indirectly proportional to the minimum inhibitory concentration.26

The mean standard deviation for three observations of each dentifrice is, at most, a nonparametric statistical analysis for comparisons among dentifrices. In addition, dentists should keep in mind that the mean average inhibition zone of one dentifrice may not be directly comparable with that of another dentifrice because dentifrices may diffuse at different rates.

Our testing method also functioned as a screening method, and it may not have been able to detect the effects of a chemical that does not diffuse through the agar matrix. More importantly, we conducted the test in vitro, so it cannot be assumed that the results of antimicrobial efficacy could be proportional or transferable to the oral cavity and translated into clinical effectiveness. Research has demonstrated that bacteria in biofilm forms such as plaque have decreased sensitivity to antibacterial agents. Moreover, formulations for topical antimicrobial oral use, such as mouthrinses and dentifrices, must be able to penetrate the biofilm matrix and deliver the active agents quickly because exposure times are limited under actual use conditions. Nevertheless, the in vitro method is a well-established technique that commonly is used in screening the antimicrobial efficacy of chemicals before in vivo testing.

Labeling. The packaging of the herbal dentifrices we tested listed numerous natural substances, plant extracts and other ingredients that the manufacturers claim to have beneficial properties (Table 3Go)2,4,6,8 that have been subjected to some laboratory and human testing. The ingredients included echinacea,29,30 seaweed derivatives such as carageenan,29 ginger,31–34 bee propolis,35 baking soda,36 myrrh,24 sage oil,14 fennel,6 rosemary,6 golden seal,32 aloe vera,32 juniper extract,31,37 grapefruit seed extract,32 green tea bioflavonoids,33,34,38,39 cinnamon6 and sanguinarine.6,38 The products that contain these substances and make antibacterial claims often do so under the guise of "killing germs that cause bad breath" or "reducing gingivitis." To validate such claims, however, researchers must evaluate and determine the level of antimicrobial activity.40 Investigators who have conducted in vivo and in vitro studies have found potential oral side effects from these products—especially those containing botanicals41—such as tongue numbness (echinacea) and increased bleeding (ginger).5 While usually transient, some of these side effects can cause significant discomfort, and the use of these substances is contraindicated with the presence of certain conditions, diseases and pharmaceuticals.


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  		TABLE 3 EXAMPLES OF BENEFICIAL PROPERTIES CLAIMED BY HERBAL OR NATURAL INGREDIENTS IN HERBAL TOOTHPASTES.*{dagger}

 
Government regulations. Owing to the increased public popularity of herbal products, the Dietary Supplement Health Education Act, or DSHEA, was enacted in 1994.42 Herbal products that are not approved by the U.S. Food and Drug Administration, or FDA, and are without specific therapeutic claims can continue to be sold. However, the FDA issued a new regulatory framework for the safety and labeling requirements.43 New labels provide details on the quantity of each ingredient, as well as which part of the plant has been used in the herbal product. The labels can contain a structural claim, functional claim or both, but they must include a disclaimer stating that the FDA has not evaluated the product’s claims and that the product is not intended to diagnose, prevent or cure any disease.

Herbal dental products are not covered by the DSHEA, and at present, there are no established regulations for herbal dentifrices. According to the FDA, a product claiming therapeutic effects is a drug.43 Dental caries and gingivitis are oral diseases. Therefore, products claiming to have anti-caries properties, antigingivitis properties or both are considered drugs, which are regulated by the FDA. So far, the FDA has not approved any herbal dentifrices; however, many herbal dentifrices on the market claim to have anticaries and antigingivitis properties. It is important that dental professionals and the public be educated adequately about the safe and effective use of herbal dentifrices.

Risks. It has been established that medicinal plants can be contaminated with microorganisms.31 For example, the growth of unidentified microorganisms around and over the samples of Dentifrico de Echinacea in our study raised the possibility that the product was contamination by microbes, which could have exposed consumers to uncertain risks. Dentists need to recognize this potential danger that is associated with herbal ingredients in dentifrices, for which there are no defined requirements and regulations. The ADA Seal of Acceptance is an important part of this process, as it indicates that an oral care product has demonstrated adequate evidence of safety and efficacy.44 We found that Tom’s of Maine Natural Toothpaste—the only herbal dentifrice in our study that has the ADA Seal of Acceptance—showed consistent antimicrobial activity and no microbial contaminations, thus confirming its potential efficacy.

Another potential risk associated with the herbal dentifrices we tested was that there was no batch number, expiration date or both for some of the products (Table 1Go). Although a tube of toothpaste or a bottle of tooth powder may have a long shelf life, it is not known how its expiration date affects its efficacy and safety. It is possible that the contaminated toothpaste had expired when we tested it. Expiration dates and shelf life can affect stability, and this information would be a valid consideration for consumers when purchasing natural herbal products. The inability to judge stability limited our ability to make comparisons among the dentifrices.


   CONCLUSIONS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
After conducting our study, we came to the following conclusions:

– the antimicrobial properties of herbal dentifrices vary greatly;
– some of the herbal dentifrices had no antimicrobial potential against one or more of the four oral microorganisms: S. mutans, S. sanguis, A. viscosus and C. albicans;
– microbial contamination of herbal dentifrices may exist, exposing consumers to health risks;
– herbal dentifrices that have been evaluated adequately, particularly those that have received the ADA Seal of Acceptance, can be recommended;
– further research efforts are needed to help establish guidelines to ensure the efficacy and safety of natural oral care products such as herbal dentifrices and mouthrinses.



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  		Dr. Lee is an assistant professor, Department of Restorative Dentistry, Loma Linda University School of Dentistry, Loma Linda, Calif. 92350, e-mail "seanlee{at}sd.llu.edu". Address reprint requests to Dr. Lee.

 


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  		Dr. Zhang is an assistant professor, Department of Dental Educational Services, Loma Linda University School of Dentistry, Loma Linda, Calif.

 


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  		Dr. Li is a professor, Department of Restorative Dentistry, Loma Linda University School of Dentistry, and a professor, Department of Microbiology and Molecular Genetics, Loma Linda University School of Medicine, Loma Linda, Calif.

 


   FOOTNOTES
 

The authors thank Jason Li and Christopher Lee for their computer artwork assistance in preparing the manuscript.


   REFERENCES
TOP
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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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