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Table of Contents

1. A quantitative approach to the effectiveness of ozone against microbiota organisms colonizing

toothbrushes.................................................................................................................................................... 1

Bibliography...................................................................................................................................................... 9

23 February 2013 ii ProQuest



Document 1 of 1

A quantitative approach to the effectiveness of ozone against microbiota organisms colonizing

toothbrushes

Author: Bezirtzoglou, Eugenia; Cretoiu, Silvia-Mariana; Moldoveanu, Mirela; Alexopoulos, Athanasios; Lazar,

Veronica; Nakou, Mela

Publication info: Journal of Dentistry 36. 8 (Aug 2008): 600-605.

ProQuest document link

Abstract: Toothbrushes are rapidly contaminated with different microorganisms, which colonize the oral cavity

and interdental spaces. This can represent a possible cause of infection or reinfection. In this study, the ozone

experimental effect upon toothbrushes microflora was estimated microbiologically before and after saturation

with ozone gas. Fifty used toothbrushes coming from children and adults were entered our study.

Microorganisms were enumerated and identified. Bristles from each brush were soaked in ozone saturated PBS

solution for 5, 10, 15, 20 and 30min and the total microbial population was reassessed. Counts of

microorganisms isolated per brush varied between 102 and 107 CFU. Candida albicans was present in used

toothbrushes. No obligate anaerobes were isolated. Members of Streptococcaceae family were regularly found

(65.2%) belonging to the following species: Streptococcus pyogenes , S. mutans , S. mitis , S. oralis , S.

sobrinus , S. viridans , S. salivarius , S. sanguis , Aerococcus viridans . A. viridans and S. mutans were more

frequently isolated on children toothbrushes while Staphylococcus aureus and S. epidermidis were found on

adults brushes. Escherichia coli, Pseudomonas sp. and Enterococcus sp., were also recovered. We found that

the ozone treatment decreased gradually the microbial load. However, a bacterial re-growth was effective

following short ozonation period. Decontamination was complete after an extended exposure to ozone for

30min. Ozone application was found to remove the toothbrushes bristles microbiota following conventional

brushing. Maximum decontamination efficacy of ozone treatment was observed after 30min while exposure for

short time periods seems to be inefficient which probably reflect the low dose of ozone used in this study.

Full Text:

Species Prevalence (%) Significance (p )

Children group Adult group Total

Streptococcus pyogenes 28 12

20 0.289 Streptococcus mutans

40 44 42

1.000 Streptococcus mitis 8

20 14 0.417

Streptococcus oralisa

60 20

40 0.008 Streptococcus sobrinusa

56 16 36

0.007 Streptococcus viridansa

36

68 52 0.046

Streptococcus salivarius 20 32

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Table 1 - Prevalence of the normal microbiota organisms found in used toothbrushes originated from children (n

: 25, mean age: 8 years) and adults (n : 25, mean age: 40 years) 1 Introduction Toothbrushing is the most

common method of personal hygiene for removal of dental plaque and promoting oral health. The prevention of

caries and the control of the oral hygiene, focus mainly on the mechanical and/or chemical biofilm removal.1

Toothbrushes upon use, rapidly become contaminated by a plethora of oral microorganisms including bacteria,viruses and fungi.

1,2Bacteria isolated from conventional brushes showed increasing rates when compared to

antibacterial brushes used by the same individuals. However, not statistically significant difference was

demonstrated.1-3

The majority of general dental practitioners together with manufacturing companies

recommend to their patients to replace their toothbrushes every 2-3 months. The inference of these

recommendations is that a toothbrush used for such a period, may be less effective in plaque removal than a

brand new brush.4

The toothbrushes are considered to be potential sources of oral, blood and systemic

infection or reinfection.1,5,6

They may act as a reservoir of opportunistic pathogens including Staphylococcus

and Pseudomonas -like organisms.1

Staphylococci, among other potentially oral pathogens, may be transient

members of the oral microbiota and the importance of toothbrushes as a potential source of staphylococcal

infection has not been extensively explored.6,7

Staphylococci were isolated from the floor of the palate, tongue

and crevicular fluid of patients with periodontal disease as well as from healthy controls.6-8

Their numbers are

usually low in healthy individuals oral microbiota.6,7

Staphylococci found on toothbrushes, may originate not

only from the oral cavity but also from the environment where brushes are stored.8

Indeed, toothbrushes may

harbour pathogens from patients having infections which may therefore serve as vehicles for reinfection by

these organisms. Moreover, toothbrushes may harbour pathogens from the external environment which may

cause infection. This contamination presents the possibility of reinfection of a patient by used toothbrushes

harbouring the pathogenic microorganisms. Aware of the possible hazards for a mouth infection with bacteria

originated from a toothbrush, dentists often recommend various methods for sanitizing brushes. Soaking in

alcohol was the first recommended procedure for toothbrush disinfection in 1920s.10 Other methods for

sanitation were proposed such as exposing toothbrushes to sunlight, salt, formaldehyde gas, ultraviolet light,

spraying with antimicrobial solutions, use of a microwave oven and washing of the toothbrush in a dishwater.

26 0.520 Streptococcus sanguisa

8 36 22

0.037 Aerococcus viridansa

68

24 46 0.004

E. faecalis, E. faecium 0 8

4 0.489 Staphylococcus aureusa

16 56 36

0.007 Staphylococcus epidermidisa

24

60 42 0.020

Lactobacillus sp. 40 44

42 1.000 Esherichia coli

8 20 14

0.417 Pseudomonas aeruginosaa

4

28 16 0.048

Candida albicans 52 36




1,9,10Some authors investigated the impact of the accumulated toothpaste debris on toothbrush's microbial

contamination, while the efficacy of the incorporation of an antimicrobial substance in the toothbrush to avoid

bacterial contamination was assessed in other studies.11,12

Bacteria isolated from conventional brushes

showed increasing colonization rates when compared to antibacterial brushes used by the same individuals.

However, non-statistically significant difference was demonstrated.1-3

Ozone (O3) on microorganisms acts

against different cellular substances including proteins lipids, peptidoglycans, enzymes and virus capsids,13

but

effective microbial inactivation seems to be dependent on several environmental factors.14,15

The oxidizing

mechanisms of ozone may involve direct reactions of molecular ozone and free radical-mediated destruction.

The main advantage of ozone usage consists of its superiority compared to other disinfectants like chlorine, for

three main reasons; firstly, is reporting to be 1.5 times stronger than chlorine and acting 3000 times faster

without producing harmful decomposition products.16

In 1995, ozone was declared as Generally Recognized

as Safe (GRAS) by the FDA for treatment of bottled water. Finally, its application was extended as GRAS to

food processing a few years later.17

In dentistry, the efficacy of ozone on oral sanitation procedures or as a

given therapy on a multispecies oral biofilm has been tested in vitro , with promising results.13,18

The aim of

this study was to evaluate the microbial contamination of used toothbrushes and the susceptibility of the

detached microbial load harboured on these brushes to ozone. 2 Materials and methods 2.1 Sampling

preparation Fifty manual toothbrushes were investigated in this study. Toothbrushes were used by the owners

for a period of 1 to over 3 months and none of them were sanitized in any way or had any antibacterial

properties. Brushes were divided in two major groups: those used by children (7-10 years of age) and those by

adults (20-70 years of age). Volunteers were asked to bring their brushes to the laboratory in plastic sterilized

bags and they had their teeth brushed by means of the classic mechanical technique. After use, each

toothbrush was rinsed under running tap water and processed immediately. The bristles from each brush were

aseptically trimmed off and transferred into a tube with 9ml sterile Phosphate Buffered Saline (PBS) solution.

The content was vigorously vortexed for 3min in order for the non-strongly adherent cells to be detached.

Afterwards, this same content was vigorously shaken in a cold bath for 10min,in order for the sessille cells to be

detached.19

Moreover, serial tenfold dilutions in PBS were prepared for microbiological evaluation. 2.2

Microbiological analysis One hundred microliters from each dilution were plated onto different selective and

non-selective growth media as follows: Mannitol salt agar (Oxoid Ltd., Basingstoke, Hampshire, UK) was used

to quantitatively detect Staphylococcus sp. Representative colonies were picked and subjected to Gram-stain,

catalase and coagulase tests (Staphylex, Oxoid Ltd.). MacConkey agar (Oxoid Ltd.) was used to enumerate

presumptively Enterobacteriaceae. Characteristic colonies appeared within 24h were confirmed by the IMVC

test (Indole, Methyl Red, Voges-Proskauer, Citrate). Moreover, the following media were used: MRS agar

(Oxoid Ltd.) for the recovery of Lactobacillus, Mitis salivarius agar (Becton Dickinson Co., USA) for total

Streptococci and Columbia agar supplemented with blood (5%) for the aerobes and facultative anaerobes.Finally, Sabouraud Dextrose agar (Oxoid Ltd.) was used for cultivation of yeasts and moulds. Incubation of the

plates was performed accordingly to the involved medium aerobically for 24h at 37°C or anaerobically for at

least 5 days at 37°C. Identification of the strains was based upon their colony and cell morphology, respiration

requirements and biochemical characteristics. These included microscopic examination of Gram-stained cells;

motility, catalase and oxidase reaction and growth in anaerobic conditions. Finally, biochemical tests by the aid

of commercial kits (API from BioMérieux S.A., Marcy l'Etoile, France and Microgen ID from Microgen

Bioproducts Ltd., UK), were performed for further identification of the isolates to the species level. 2.3 Ozone

sanitation trials In the second phase of the study, the decimal dilutions of our samples (T : 20°C) were ozone

saturated by using a commercial ozone gas generator (Air &Water System PC1325, USA) through a sterilized

microdiffuser and samples for microbiological analysis were drawn after 5, 10, 15, 20 and 30min. 100μl from the

ozonated suspensions were plated on all previous growth media and incubated accordingly. A quantitative

evaluation of the microbial growth achieved by inoculation of 10-1

to 10-7

serial dilutions from each sample




onto Columbia blood agar. Ozone concentrations were estimated photometricaly with the indigo method by

using a commercially available kit (Hach Co., Loveland Co., USA). Final ozone concentration succeeded is

reported to 3-3.5ppm. A quantitative evaluation of the microbial growth was achieved after the end of the

ozonation. The re-growth profile of bacteria was estimated by total counting of the recovered bacteria (CFU/ml).

2.4 Statistical analysis Differences in the occurrence of microbial species between each age group were

examined by using Fisher's exact test. Differences in microbial counts before and after ozonation were

estimated with Mann-Whitney z -test after logarithmic transformation of counts. Linear regression models for the

inactivation of microbes over time were also estimated. All statistical analyses were performed with the SPSS

v13 statistical software package (SPSS Inc., USA) at 95% level of significance. 3 Results The results of the

microbiota's qualitative assessment from all samples are shown in Table 1. A total of 16 different species of

bacteria were identified from adults and children toothbrushes. Overall, most abundant were the Streptococcus

genus with an occurrence of 31.5%, (average count: 4.5log CFU) equally distributed among children (32%) and

adults (31%) and with typical representatives Streptococcus pyogenes , S. mutans , S. mitis , S. oralis , S.

sobrinus , S. viridans , S. salivarius and S. sanguis . From the above strains, S. oralis and S. viridans were

those mostly isolated (60% and 68%, respectively) from our samples. In children, except Streptococcus sp.,

Aerococcus viridans (68%), Candida albicans (52%) and Lactobacillus sp. (40%) were also recovered, while

Staphylococci (S. aureus and S. epidermidis ) were dominant over the adult group. Less abundant species were

Escherichia coli , S. faecalis , S. faecium and Pseudomonas aeruginosa (average count less than 3logs) and

particularly in children's brushes. The quantitative evaluation of the microbiota revealed that the total number of

microorganisms ranged between 102

and 106

CFU per toothbrush. The most evident bacterial growth was

observed on Columbia blood agar with the maximum growth estimated on 6.9×107

for the children and 6.7×107

for adults, indicating no actual differences. Total counts for C. albicans on Sabouraud Dextrose media was

1.87×102

for the children and 1.12×102

for adults. A 48% from children brushes and 64% from adults was free

from C. albicans colonization. Fisher's exact test revealed statistical significant differences regarding the

occurrence of the various species between the two groups in almost half of the verified strains. As can be seen

from Table 1, three of those species (S. oralis , S. sobrinus and A. viridans ) were more frequent in children

while, five species (S. viridans , S. sanguis , S. aureus , S. epidermidis and P. aeruginosa ) were more frequent

in adults, indicating a variable pattern of microflora between the two groups. Concerning the ozone experiments,

in both age groups, only after 10min of ozonation (and in the consequent exposures) statistical significant

differences with the initial microbial concentrations were observed (Mann-Whitney z : -4.77 and -4.96, p <0.05).

After 5min of exposure a slightly and insignificant decrease of 0.5logs was recorded. A full sanitation efficiency

was observed after 30min of ozonation, since no viable counts were observed for those samples. Linear fitted

models for both groups indicated a decrease in total counts by -0.17 to -0.18logs for every 5min of ozonation

(Fig. 1). This similarity of slopes did not disrupted when controlling for the age of the subjects, or the period thetoothbrushes were used. 4 Discussion Based on our results, used toothbrushes harbouring an increased

number of aerobic and facultative anaerobic bacterial species. This finding is in accordance with the results of

previous studies1,3,6-8

and indicates that an actual risk of recolonization exists after each brushing. That risk is

of particular importance for periodontal patients under therapy.3

The profile of total microbiota isolated and

identified in our samples included the species: Streptococcus sp., Aerococcus sp., Enterococcus sp.,

Staphylococcus sp., Lactobacillus sp., Pseudomonas sp., E. coli , and Candida . It was observed that the most

abundant strains were those of the Streptococcus genre like S. pyogenes , S. mutans , S. mitis , S. oralis , S.

sobrinus , S. viridans , S. salivarius , S. sanguis and A. viridans . A part of those species isolated both from

children and adults and their occurrence probably resulted by disruption of bacterial plaque after tooth brushing.

From Micrococacceae family, two species were identified: S. aureus and S. epidermidis usual commensals on

skin, known as potential pathogens and capable of biofilm formation.12,13

Both isolated species of E. faecium

and E. faecalis were recovered from adult's brushes and thus, indicating a dental superinfection, especially




associated with elderly people. A. viridans and some of the Streptococcus sp., were more frequently isolated

from children brushes in contrast to S. aureus and S. epidermidis originating from adult's brushes. The

contamination with those non-fastidious bacteria has its' origin in the oral cavity as S. aureus is frequently

isolated from periodontal patients but also from manual handling of the toothbrushes. In general, the oral

Streptococci group was significantly present in the microbiota isolated from all toothbrushes. P. aeruginosa and

E. coli were present on both groups, probably as the result of the storage conditions (bathrooms with increased

humidity, increased temperature and/or untreated tap water). S. mutans and species from Lactobacillus genre

were present on different frequencies in children brushes and in adults; which indicates somewhat different

dental conditions. No periodontopathogens like A. actinomycetemcomitans , P. gingivalis or F. nucleatum were

recovered, meaning that among our subjects none with apparent oral infection occurred. However, bacterial

variability of potential pathogens recovered on toothbrushes was considerable. Results from ozone sanitation

experiments showed that exposure of the brushes bristles to ozonated Phosphate Buffered Saline solution for 5,

10, 15 and 20min did not result in a radical effect, as slight microbial re-growth afterwards was evident. Only

after 30min of exposure a complete sanitation was observed. A possible explanation is the effect of ozone upon

formed microbial assemblage on brushes. It is known the fact that many bacterial species are responsible of

biofilm formation on different surfaces like toothbrushes and ozone can disrupt the biofilm structure. 16,17,20

Ozone has been used extensively to in vitro experiments for the deactivation of oral microorganisms and dental

plaque treatment17

with remarkable results. However, those investigators reported a complete bactericidal

activity after 10s of exposure to 4mg/l concentrations, which differs substantially from our results of 30min even

thought, in our experiments ozone concentration was slightly lower (3-3.5mg/l). Delayed sanitation times for

toothbrushes, have been reported by other investigators, which experimented with different agents. Caudry et

al.,11

reported a complete disinfection after 20min of soaking in antiseptic, while Nelson et al.,20

after 20h. It is

assumed that this delayed effect on toothbrushes decontamination could be the result of a stiffer biofilm formed

on the bristles by the microbes, in combination with a protective coating offered to them by the accumulated

toothpaste debris. Furthermore, our results also showed a quantitative stimulation (rebound) effect of bacterial

growth after exposure to the ozone for short time periods (i.e. after 5min) and only after the biofilm is already

detached and viability of the cells is affected (i.e. after 30min exposure) no microbial growth was observed.

Another possible explanation should be the early bacteriostatic effect of ozone upon microorganisms growth.

Extensive ozonation for more than 30min results at a relevant bactericidal effect. Comparing to our original

baseline population, we evaluate the qualitative bacterial profile involved in this rebound effect (re-growth),

which collects aerobic or facultative anaerobic bacteria. No strict anaerobic bacteria were found. The direct

oxidative effect of ozone upon the anaerobic microflora is obvious. However, ozone seems like to act as an

oxygen donator for the aerobic and facultative anaerobic bacteria which use it for their re-growth. Extensive

exposure to ozone showed a complete bactericidal effect upon all microorganisms involved. It is of importanceto state here the reductant capacity of the chosen media (as Sodium chloride, Potassium chloride, Disodium

hydrogen phosphate, Potassium dihydrogen phosphate, contained in PBS) in our experimentation to produce

an early redox reaction which will reinforce the global ozone effect upon the microbiota, as we applied only a

low ozone concentration (3-3.5ppm). The redox reaction will occur then in an early stage, before the ozone itself

has time to react directly upon microorganisms. Specifically, ozone diffuses quickly in water and exerts its

bactericidal effect by rupturing microorganisms membranes.16-21

As toothbrushes are a possible source of

microbial contamination, we must advice sanitation of toothbrushes by soaking them in large volumes of

ozonated water which actually could showed a sterilizing effect even with lower ozone concentrations. Usually

the soaking in the ozonated water will be for many hours and even considering the half-life of ozone in water

there could still be some ozone remaining even after 8h. Therefore, the fact that we achieved an excellent result

only after 30min by using a very low ozone concentration could hypothetize that a future study assessing the

ability of much greater ozone concentrations in water should sterilize efficiently toothbrushes for people. The




strategy of managing human infections by ozone application has been used since 1950s.16-22

Indeed, many

scientists have discussed about its role as an alternative agent to chlorine for desinfection of the different water

supplies.15,16

Adverse reactions of ozone were associated with high ozone concentrations.15,16

This is not

the case for ozone used in watery solutions, where the ozone showed high solubility because it dissipates very

quickly in water, especially in elevated concentrations. In this term, the use of ozone in watery ecosystems is

considered quiet safe and a potential toxicity effect should not exclude its use. Last years, ozone seems to

possess an important place as therapeutical agent in dentistry. Ozonated water has been found to act upon

accelerating healing of the oral mucosa following tooth extraction processes or after surgical interventions as it

associate a haemostatic action together with a bactericidal effect. Moreover, ozone was used in dental unit

waterlines22

and in denture cleaning bubbled solutions.22

Recently, ozone was proposed for the management

of primary dental root caries.21,23

For this purpose, ozone was used as a gas directly into the middle of the

lesion21,23

Elevated ozone concentrations, as high as 2.100ppm21

and for extremely short periods of times

(10-20s) are necessary in gas form in order to act directly upon the injured site.24,25

Antimicrobial effect has

been shown especially against cariogenic bacterial species, i.e. S. mutans , Lactobacillus sp. and others.25-27

Hence, some authors by employing high resolution proton nuclear magnetic resonance (NMR) describe that

ozone has the capacity to clinically alleviate oral malodour via the direct oxidative inactivation of VSCs and their

amino acid precurcors.28

In our study, as discussed already limited ozone levels gave an important

disinfenctant effect. However, we must point out here that the exposition to the watery ozone was longer. The

threshold of the ozone efficacy was studied by comparing the initial microbial contamination with that estimated

after every ozone exposure time (Fig. 1). It was observed29

an uncommonly resistance of the uni- and

multispecies biofilms to ozone by comparison with the sensibility of the planktonic cells, where the sterilization

effect was 100%. As our results indicate, an efficient ozone effect was observed after a progressive application

of the ozone, with 5min being the minimum and the 30min the optimum value. This procedure is more efficient

than a unique application at one time. 5 Conclusions Owing to the fact that toothbrushes always are a possible

source of microbial infection and reinfection, the sanitation after each use is advised. Ozone is a strong oxidizer

of cell walls and cytoplasmatic membranes of bacteria and so considered to be a promising bactericidal,

antiviral and antifungal agents. A practical application of the ozone should be the possibility to use it for

prevention from different oral pathogens. It is then conceivable that high dose ozonated water should be tested

directly on contaminated toothbrushes. Acknowledgements The study was sustained by Democritus University

of Thrace, Faculty of Agricultural Development, Department of Food Science and Technology, Laboratory of

Microbiology, Biotechnology and Hygiene and a European ERASMUS Program. References Sammons RL,

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Water and Health 3 423-433, 2005. AuthorAffiliation Athanasios Alexopoulos, Eugenia Bezirtzoglou. Democritus

University of Thrace, Faculty of Agricultural Development, Department of Food Science and Technology,

Laboratory of Microbiology, Biotechnology and Hygiene, GR68200, Orestiada, Greece; Corresponding author .Tel.: +30 2552041149. Silvia-Mariana Cretoiu. National Institute for Research and Development in Microbiology

and Immunology "Cantacuzino" - Molecular Microbiology Laboratory, 050096, Bucharest, Romania Mirela

Moldoveanu. Biology Institute of Romanian Academy, 060031, Bucharest, Romania Veronica Lazar. University

of Bucharest, Faculty of Biology, 76201, Bucharest, Romania Mela Nakou. University of Athens, Dental School,

Oral Microbiological Laboratory, Department of Periodontology, GR11527, Athens, Greece

Subject: Microbiology; Studies; Bacteria; Microorganisms; Free radicals; Drinking water;

Disinfection&disinfectants; Nuclear magnetic resonance--NMR; Organisms; Hygiene; Methods

Identifier / keyword: Oral hygiene, Toothbrush, Microbial contamination, Ozone, Disinfection, Microbiota

Publication title: Journal of Dentistry

Volume: 36




Issue: 8

Pages: 600-605

Publication year: 2008

Publication date: Aug 2008

Year: 2008

Publisher: Elsevier Limited

Place of publication: Oxford

Country of publication: United States

Journal subject: MEDICAL SCIENCES--DENTISTRY

ISSN: 03005712

Source type: Scholarly Journals

Language of publication: English

Document type: EDB, Journal Article

DOI: http://dx.doi.org/10.1016/j.jdent.2008.04.007

ProQuest document ID: 1030081579

Document URL: http://search.proquest.com/docview/1030081579?accountid=17242

Copyright: ©2008 Elsevier Ltd

Last updated: 2012-07-30

Database: ProQuest Nursing&Allied Health Source,ProQuest Research Library


http://dx.doi.org/10.1016/j.jdent.2008.04.007

http://dx.doi.org/10.1016/j.jdent.2008.04.007



BibliographyCitation style: APA 6th - American Psychological Association, 6th Edition

Bezirtzoglou, E., Silvia-Mariana Cretoiu, Moldoveanu, M., Alexopoulos, A., Lazar, V., & Nakou, M. (2008). A

quantitative approach to the effectiveness of ozone against microbiota organisms colonizing toothbrushes.

Journal of Dentistry, 36(8), 600-605. doi: http://dx.doi.org/10.1016/j.jdent.2008.04.007

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