ozone˚˚ therapy˚˚ in˚˚ dentistry:˚˚ a˚˚ systematic˚˚ review · 268 perform a review...

267

Int. J. Odontostomat.,7(2):267-278, 2013.

Ozone Therapy in Dentistry: A Systematic Review

Ozonoterapia en Odontología: Una Revisión Sistemática

Iris Jasmin Santos German*; Antonio de Castro Rodrigues*; Jesus Carlos Andreo*; Karina Torres Pomini*;Farooque Jamaluddin Ahmed*; Daniela Vieira Buchaim*; Geraldo Marco Rosa Júnior**; Jéssica Barbosa de

Oliveira Gonçalves* & Rogério Leone Buchaim*

GERMAN, I. J. S.; RODRIGUES, A. C.; ANDREO, J. C.; POMINI, K. T.; AHMED, F. J.; BUCHAIM, D. V.; ROSA JÚNIOR,G. M.; GONÇALVES, J. B. O. & BUCHAIM, R. L. Ozone therapy in dentistry: A systematic review. Int. J. Odontostomat.,7(2):267-278, 2013.

ABSTRACT: The purpose of this systematic review was to verify the literature available regarding the effectivenessand the biological effects of ozone therapy in periodontics, orthodontics and dental implants. Studies were searched inSeptember 2012. Analyzed sources included the databases PubMed, Lilacs and SciELO, through a combination of keywords, dental implants, periodontics, orthodontics, therapeutics. Studies between 2002 and 2012 were included. In vitroand in vivo studies English and Spanish language publications, excluding posters, letters to the editors and conferences. InVitro and in Vivo studies showed the inactivation of the major periodontal pathogens by ozone. There were divergent resultsand lack of evidence for the activity of ozone on adhesion of orthodontic brackets, in implantology and orthodontics. Ozonecould be considered as a promissory alternative therapy in dentistry. However, well-designed studies are needed to assessthe application of ozone in order to evaluate its clinical effectiveness in the field of dentistry.

KEY WORDS: dental implants, periodontics, orthodontics, therapeutics.

INTRODUCTION

Ozone is a gas with the chemical formula O3,

and is the third most powerful oxidant. Medical ozoneis produced by oxygen and its passage through avoltage gradient, using ozone generators that react todioxygen molecules, forming ozone (O

2 + O→O

3)

(Ripamonti et al., 2011; Bocci, 2006; Swilling, 2004).

Several biological actions (Fig. 1) of medicalozone include the increase in the synthesis ofbiologically active substances such as interleukins,leukotrienes and prostaglandins that are beneficial inthe reduction of inflammation and in cicatrization, theactivation of aerobic processes (glycolysis, Krebs cycle,beta-oxidation of fatty acids), secretion of vasodilators(e.g. nitric oxide-NO), activation of the mechanism ofprotein synthesis and increase in the quantity ofribosome and mitochondria in the cells, thus raisingthe functional and potential activity of tissueregeneration (Seidler et al., 2008).

The ozone oxidant potential induces thedestruction of cellular walls and cytoplasmatic

membranes of bacteria (Thanomsub et al., 2002). Thegas was named ozone (a Greek word that means"smell") by the German chemist Christian FrederickSchonbein of the University of Basel in Switzerland1840 (Seidler et al.; Veranes et al., 1999).

During the First World War, ozone gas was usedfor the treatment of post-traumatic gangrene, infectedwounds, burns and fistulas and other anaerobicinfections, putrefied wounds, suppurations of bone frac-tures and various inflammations in German soldiers(Azarpazhooh & Limeback, 2008). By the middle of 1932, German dentist Edward A. Fisch, perceived thetherapeutic possibilities of using ozone as a medicaltherapy (Altman, 2007; Bocci, 2005).

Currently, there are divergences in thedeveloped studies regarding ozone therapy action.Therefore, the studies available in the literature mustbe reviewed in order to evaluate the obtained resultsand estimate the effectiveness of ozone therapy andthe methods used. The purpose of this study was to

* Department of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Bauru, Brazil.** University of Sacred Heart, Bauru, São Paulo, Brazil.

268

perform a review regarding the effectiveness of ozonetherapy in the area of dentistry, with emphasis on thecurrent uses, focusing on the areas of periodontics,orthodontics and dental implants. The authors aimedat answering the following questions: “What is theaction of ozone on periodontal pathogens?” “What arethe effects of ozone on the adhesion of brackets todental enamel?” “How does ozone act in the boneintegration of dental implants?”

These questions are important for future studiesin order to understand the properties of ozone and itscontribution in clinical uses.

MATERIAL AND METHOD

Data sources. The literature review included studiesavailable in the databases, PubMed, LILACS andSciELO, utilizing the following descriptors: ozone,dentistry, periodontics, orthodontics and dentalimplants. Studies published between the years 2002and 2012 were included. A combination of the keywords was used, which helped to identify studiesrelated to ozone therapy in dentistry. Booksregarding ozone therapy were also referred to inorder to obtain more information on the theme

Fig. 1. Major biological effects of ozone therapy.

GERMAN, I. J. S.; RODRIGUES, A. C.; ANDREO, J. C.; POMINI, K. T.; AHMED, F. J.; BUCHAIM, D. V.; ROSA JÚNIOR, G. M.; GONÇALVES, J. B. O. & BUCHAIM, R. L. Ozonetherapy in dentistry: A systematic review. Int. J. Odontostomat., 7(2):267-278, 2013.

269

(Altman; Bocci, 2002, 2005). The search was limitedto studies written in English and Spanish. Both in

vitro and in vivo studies regarding ozone therapy indentistry were selected (Fig. 2).

Fig. 2. Search strategy for literature review on the use of ozone therapy in dentistry.


270

Study selection. Letters to the editor, abstracts,conferences, comments, books and panels were notincluded; however all of them were reviewed in orderto identify possible important data that could contributeto the development of this review. Data extraction. After reviewing the titles of theresearched studies, seven pertinent studies were foundrelated to the study objectives (accessed on September26, 2012). Several studies stemming from the searchwere read with the purpose of identifying relevantinformation on the theme in question.

RESULTS

Results are presented in three sectionsaccording to the purposes of the study. Action of ozone on periodontal pathogens. Threein vivo (Kshitish & Laxman, 2010; Martinez Abreu &Abreu Sardinas, 2005; de Ramon et al., 2004) and onein vitro study (Huth et al., 2011) evaluating the actionof ozone on periodontal microbiota were found.

In 2004, de Ramon et al., (Table IA) analyzedthe periodontal responses in terms of the clinical,microbiological and immunologic aspects in patientswith moderate and severe periodontal pockets,comparing the technique of scaling and root planning(control group) with the application of ozone (experi-mental group).

After 30 days, the average clinical evaluationshowed the following data: in the experimental group,initial periodontal index (Russell’s Index) was 5.72 andthe final index was 5.59. Initial supragingival plaqueindex was 31.30 and the final index was 49.99. Initialgingival bleeding index was 62.43 and the final 26.29.

In the experimental group the microbiologicalanalysis the reduction of periodontal pathogens(Aggregatibacter actinomycetencomitans (Aa),Bacteroides forsythus (Bf), and Porphyromonasgingivalis (Pg) was about 50%). In the immunologicanalysis, the initial TNF-a was 101.23 and at the end itdecreased to 36.01. Initial IL-1b also reported adecrease from an initial period of 96.12 to 34.28 after30 days of treatment.

Martínez Abreu & Abreu Sardiñas (Table IA)developed a randomized controlled clinical study. The

study was divided into two groups: the control (treatedwith 0.2% chlorhexidine) and the experimental group(treated with the ozonated oil Oleozon). Amicrobiological analysis was performed on the gingivaof the teeth with periodontitis after 21, 90 and 180 daysrespectively, during a nine-month postoperative period.

The microbiological and clinical evaluation wasdetermined to be:

Satisfactory: Absence or lack of gram-negativemicroorganisms.Unsatisfactory: Abundant presence or prevalence ofgram-negative microorganisms.

After the postoperative period of 180 days,microbiological results were satisfactory in 98% of thepatients in the experimental group and 78% in the con-trol group. Regarding the clinical evaluation,satisfactory results after 180 days were present in 98%of the patients in the experimental group and 95% inthe control group.

In 2010, Kshitish & Laxman (Table IB) developeda double-blind randomized study regarding the use ofozonated water in the treatment of periodontitis. Thecontrol group was irrigated with 0.2% chlorhexidine.Clinical parameters such as gingival index and gingivalbleeding index were analyzed, in addition to the ozoneactivity on oral microorganisms: Aggregatibacteractinomycetemcomitans (Aa), Porphyromonasgengivalis (Pg), Tannerella forsythensis (Tf), HerpesSimplex virus (HSV-1 and HSV-2), Epstein Barr virus(EBV) human cytomegalovirus (HCMV) and Candidaalbicans.

Results of the ozone irrigations showed 12% ofreduction of the plaque index. The gingival indexdecreased 29% and bleeding index 26%. After sevendays, ozone showed presence of Aa in 25%, Pg 50%,Tf 25%, HSV-1 62.5%, HSV-2 0%, HCMV 25%, EBV37.5% and Candida albicans 12.5% of the cases.

In an in vitro study, Huth et al. (2011) (Table IB)determined the efficacy of the use of gaseous/aqueousozone in the reduction of several periodontal pathogens(Aa, Pg, Tannerella forsythia (Tf) and Parvimonas mi-cra (Pm) in both planktonic state and biofilm. Aqueousozone in a concentration of 20 mg ml-1 resulted in thereduction of approximately 99% of the total A.actinomycetencomitans in planktonic state, and 70%in biofilm. Gaseous ozone (concentration of 1, 2, 4, 8,16 g m-3) was capable of reducing this pathogen by


271

Tabl

e IA

. Ozo

ne th

erap

y in

per

iodo

ntic

s.


Aut

hor

(dat

e)P

urpo

seM

etho

dolo

gyR

esul

tsC

oncl

usio

nSt

udy

limit

atio

ns

Ebe

nsb

erg

er e

t al

.(2

002)

To

inve

stig

ate

the

effe

cts

of

irri

gati

ng

ozo

nate

dw

ater

on

the

prol

ifer

atio

nof

cel

ls i

n th

e pe

riod

onta

lli

gam

ent

atta

ched

to

root

sof

ex

trac

ted

hum

an te

eth

.

23

thir

d cu

spid

te

eth

w

ere

extr

acte

d fr

om

pati

ents

ag

edbe

twee

n 2

0-35

yea

rs.

Ozo

nate

dw

ate

r w

as

irri

gate

d

for

2m

inut

es

(Ozo

ne

gene

rato

rpr

otot

ype

Sir

ona

MI,

S

iron

a,B

ensh

eim

, G

erm

any

, in

conc

entr

atio

n of

2.5

-3-5

µg

ml-

1 )

and

the

expr

essi

on

of

the

mar

ker

of

Pro

life

rati

ng

Cel

lN

ucle

ar

Ant

igen

(P

CN

A)

was

eval

uate

d.

The

n

umbe

r o

f po

sitiv

e ce

llsco

mpa

red

to t

he t

otal

num

ber

ofce

lls

was

7.

8% a

fter

ir

riga

tion

wit

h oz

one

and

6.6

%

afte

rir

riga

tion

with

sa

lin

e so

luti

on.

Aqu

eous

oz

one

did

no

t h

ave

neg

ativ

e ef

fect

s on

the

cel

ls o

fth

e pe

riod

onti

um.

Posi

tive

mar

ker

cells

w

ere

foun

d al

one

or

in g

rou

ps i

n th

e ce

men

t or

in

the

rem

nan

t pe

riod

onta

lli

gam

ent.

Irri

gatio

n w

ith

ozon

ated

wat

er

show

ed

high

ra

tes

of c

ells

in

com

pari

son

tosa

line

so

lutio

n (c

ontr

olgr

oup)

, b

ut

with

n

osi

gnif

ican

t di

ffer

ence

s.T

here

wer

e no

dif

fere

nce

sin

th

e nu

mbe

r an

ddi

stri

buti

on

of

posi

tive

PC

NA

cel

ls i

n th

e co

rona

lan

d ap

ical

p

art

of

the

root

s of

the

cu

spid

teet

h.

In

situ

, th

e te

eth

wou

ld

be

subm

itte

dto

fu

ncti

onal

st

ress

,w

hich

cou

ld a

lter

the

expr

essi

on

offi

bro

blas

ts

and

the

DN

A s

ynth

esis

.

de

Ram

on e

t al

.(2

004)

To

anal

yze

the

clin

ical

,m

icro

biol

ogic

al

an

dim

mun

olog

ical

re

spon

ses

in

pati

ents

w

ith

mod

erat

e/se

vere

peri

odon

tal

pock

ets

usin

goz

one

ther

apy.

72

max

illa

ry

hem

iarc

hes

w

ere

anal

yzed

with

at

leas

t 4

teet

han

d 6

m

m

of

pro

bing

de

pth.

One

hem

iarc

h w

as t

reat

ed

wit

hoz

one

and

the

oth

er w

ith s

calin

gan

d

root

p

lani

ng

(Co

ntro

lgr

oup)

.

Init

ial

peri

odon

tal

inde

x(R

usse

ll)

was

5.7

2 an

d th

e fi

nal

was

5.5

9.

Initi

al

supr

agin

giva

lp

laq

ue i

ndex

was

31.

30

and

the

fina

l in

dex

wa

s 49

.99.

In

itial

gin

giva

l bl

eedi

ng

inde

x w

as6

2.43

and

the

fin

al

was

26.

29.

Init

ial T

NF-

α w

as 1

01.2

3 an

d at

the

end

it de

crea

sed

to 3

6.01

.

Ozo

ne h

ad n

o si

gnif

ican

tef

fect

on

the

re

mov

al

ofsu

prag

ing

ival

pl

aque

, bu

tre

duce

d

the

ging

ival

blee

din

g in

dex,

inc

lud

ing

TN

F-a

lfa

and

IL-1

_.

How

ever

, it

d

id

not

prod

uce

chan

ges

in

the

leve

l of

p

erio

dont

alin

sert

ion

and

p

ock

etde

pth.

The

dos

age

used

was

not r

epor

ted

.

Mar

tín

ez

Abr

eu&

Abr

eu S

ard

iñas

(200

5)

To

eval

uate

the

eff

ects

of

ozon

ated

oil

(O

leo

zon)

in

the

trea

tmen

t of

mod

erat

epe

riod

ontit

is.

App

licat

ion

of

Ole

ozo

n

inpe

riod

onta

l po

cket

s af

ter

21,

90an

d 1

80 d

ays

ove

r a

tota

l pe

riod

of 9

mon

ths.

n=

84 p

atie

nts

.

Mic

robi

olog

ical

ev

alua

tion

show

ed,

over

the

per

iod

of 1

80d

ays,

sca

rcity

or

lack

of

gram

-n

egat

ive

mic

roor

gani

sms:

98

%fo

r th

e ex

peri

men

tal

grou

p an

d7

8%

for

the

cont

rol

gro

up(0

.2%

aqu

eous

chl

orh

exid

ine)

.

Impr

ovem

ent

of t

he s

igns

and

sym

ptom

s w

as f

aste

rin

the

gro

up t

reat

ed w

ithoz

onat

ed

oil

than

in

the

cont

rol

grou

p.

Mic

robi

alle

vels

w

ere

mor

eco

mpa

tib

le

wit

h he

alth

ype

riod

ontiu

m

in

the

ozon

ated

gro

up.

The

do

se

of

ozon

eus

ed a

nd

the

tim

e of

each

app

licat

ion

wer

eno

t rep

orte

d.

Hut

h et

al.

(200

7)T

o in

vest

igat

e th

e ef

fect

sof

aq

ueo

us o

zone

on

the

NF-

kB s

yste

m.

Hum

an o

ral

epith

elia

l ce

lls

and

ging

ival

fi

brob

last

s w

ere

culti

vate

d.

Aqu

eous

ozo

ne w

asap

plie

d

to

the

cells

. A

queo

usoz

one

was

ge

ner

ated

w

ith

gase

ous

ozo

ne,

75µ

g/m

l fo

r 15

min

utes

(O

zono

san

-pho

toni

c)re

sulti

ng

in

the

fina

lco

ncen

trat

ion

of 2

0µg/

ml)

.

The

ac

tivi

ty o

f th

e N

F-k

B

onth

e o

ral

cell

s in

the

ra

dicu

lar

surf

aces

p

erio

dont

ally

com

prom

ised

w

as

inhi

bite

dw

hen

incu

bate

d w

ith

ozon

e, i

nad

ditio

n

IkB

α

pro

teol

ysis

,cy

toki

ne

expr

essi

on

and

kB-

dep

ende

nt

tran

scri

ptio

n w

ere

pre

ven

ted.

Aqu

eous

oz

one

h

adin

hibi

tory

ef

fect

s on

the

NF-

_B s

yste

m,

sugg

estin

git

ha

s an

ti-in

flam

mat

ory

prop

erti

es.

Onl

y o

neco

ncen

trat

ion

of

ozon

e an

d ti

me

ofex

posu

re

wer

e us

ed.

Hig

her

or

low

erco

ncen

trat

ion

an

dti

mes

m

ay

gen

erat

edi

ffer

ent r

esul

ts.

272

Tabl

e IB

. (C

ontin

uatio

n) O

zone

ther

apy

in p

erio

dont

ics.


Aut

hor

(dat

e)P

urpo

seM

eth

odol

ogy

Res

ults

Con

clus

ion

Stu

dy li

mita

tion

s

Ksh

itis

h &

Lax

man

(20

10)

To

eval

uate

and

to

com

pare

the

effe

cts

of

irri

gatin

goz

onat

ed w

ater

(0.

082

mg/

hfo

r 5-

10 m

inut

es)

and

0.2%

chlo

rhex

idin

e

(Con

trol

grou

p) i

n cl

inic

al p

aram

eter

ssu

ch

as

ging

ival

in

dex

and

ging

ival

b

leed

ing

inde

x,

inad

diti

on

to

the

acti

on

ofoz

one

on

oral

mic

roor

gani

sms.

16

patie

nts

wit

h ch

roni

cge

nera

lize

d pe

riodo

ntit

is.

Stud

y pe

riod

w

as

for

18da

ys.

Irri

gat

ions

of

aqu

eous

ozon

e an

d ch

lorh

exid

ine

wer

e ra

ndom

ized

. A

nev

alua

tion

of

th

e cl

inic

alpa

ram

eter

s an

d or

alm

icro

orga

nism

s w

aspe

rfor

med

.

Ozo

nate

d w

ater

re

duce

dpl

aque

in

dex

in

12%

,gi

ngiv

al

inde

x in

29

% a

ndbl

eedi

ng

inde

x in

26

%

ofca

ses.

Aft

er 7

day

s th

e oz

one

gro

up

show

ed

pres

ence

of

Aa

in 2

5%,

Pg 5

0%,

Tf

25%

,H

SV

-1

62.5

%,

HS

V-2

0%

,H

CM

V

25%

, E

BV

37

.5%

and

Can

dida

alb

ican

s 1

2.5%

of c

ases

.

Red

ucti

on

of

the

ging

ival

inde

x an

d bl

eedi

ng i

ndex

in

the

ozon

e gr

oup

was

sig

nific

ant

in c

ompa

riso

n to

chlo

rhex

idin

e.

Ozo

ne

is

apo

wer

ful

agen

t in

th

ein

acti

vati

on

of

mic

roor

gani

sms

asso

ciat

edto

per

iodo

ntit

is.

Stu

dy p

erio

d w

as to

o sh

ort.

Sku

rska

et a

l. (

2010

)A

com

pari

son

of t

he c

lini

cal

cond

ition

and

sal

ivar

y le

vels

of

MM

P(M

atri

x m

etal

lopr

otei

nase

)af

ter

scal

ing

and

root

pla

ning

or o

zone

the

rapy

in

pati

ents

with

ag

gres

sive

or

chr

onic

peri

odon

titi

s.

52 p

atie

nts

wit

h ch

roni

c or

aggr

essi

ve

peri

odon

titis

,ag

ed

betw

een

25-6

8 ye

ars,

wer

e di

vide

d in

to 3

gro

ups:

a) C

P-S

: pa

tien

ts

wit

hch

roni

c pe

riod

ontit

issu

bmitt

ed t

o ro

ot s

calin

g. b

)C

P-O

: pa

tient

s w

ith c

hron

icpe

riod

onti

tis

treat

ed

wit

hsc

alin

g an

d ro

ot p

lani

ng a

ndoz

one

ther

apy.

c)

A

P:

pati

ents

wit

h ag

gres

sive

peri

odon

titi

s tre

ated

w

ith

root

sc

alin

g an

d oz

one

ther

apy.

Ozo

ne w

as a

ppli

ed3

tim

es

ever

y 2

days

(1

min

ute,

42.

2 µg

ozo

ne/m

l of

oxyg

en).

Aft

er 2

m

onth

s th

e hi

ghes

tsc

ores

in

de

ntal

pl

aque

redu

ctio

n w

ere

foun

d in

gro

up

AP

(A

PI-3

1.04

. PI

-0.

47).

T

he

low

est

wer

e in

gro

up C

P-S

(57

.77,

PI-

0.78

).L

evel

s of

MM

P-1

incr

ease

din

CP

-O a

nd A

P g

roup

. T

hehi

ghes

t le

vel

of M

MP

-1w

asfo

und

in

grou

p C

P-O

(0.1

85),

whe

rea

s C

P-S

decr

ease

d fr

om

0.17

5 to

0.10

7. T

he l

evel

s of

MM

P-8

decr

ease

d in

all

gro

ups,

but

gro

ups

CP

-O

and

AP

wer

ehi

gher

st

atis

tical

ly

than

in

the

cont

rol g

roup

.

The

sca

ling

and

roo

t pl

anin

g(S

RP

) co

mbi

ned

wit

hoz

onet

hera

py

does

no

tco

ntri

bute

to

fu

rthe

rim

prov

emen

t in

cl

inic

alpe

riodo

ntal

pa

ram

eter

s in

pati

ents

wit

h ag

gres

sive

and

chro

nic

peri

odon

titis

.O

zone

ther

apy

com

bine

dw

ith

SRP

lea

ds t

o a

decr

ease

of s

aliv

a M

MP

con

cent

rati

onin

pa

tien

ts

with

ag

gres

sive

perio

dont

itis

.

A

vacu

um

mou

ld

shou

ldha

ve b

een

used

not

onl

y to

avoi

d to

xici

ty

but

also

to

prov

ide

safe

ty

whe

n th

eco

ncen

trat

ion

used

w

asap

plie

d in

the

mou

th.

Hut

h et

al.

(201

1)T

o in

vest

igat

e th

ean

timic

robi

al

effe

ctiv

enes

sof

aq

ueou

s an

d ga

seou

soz

one

in c

ompa

riso

n to

the

antis

eptic

ch

lorh

exid

ine

digl

ucon

ate

on

peri

odon

tal

mic

roor

gani

sms

inpl

ankt

onic

st

ate

and

inbi

ofil

m.

The

m

icro

orga

nism

s w

ere

cult

ivat

ed a

nd s

ubm

erge

d in

10

ml

of

Bra

in

Hea

rtIn

fusi

on

(BH

I)

at

37ºC

for

48

hour

s.

The

oz

one

was

used

in

conc

entr

atio

n of

1-5

3gm

-3

for

one

min

ute.

T

heco

mbi

natio

n of

ga

seou

sA

queo

us o

zone

was

pre

par

edw

ith

bidi

stil

led

wat

er

and

gase

ous

ozon

e (7

5 µg

m

l-1

for

15 m

inut

es),

res

ulti

ng i

na

fina

l oz

one

conc

entr

atio

nof

20

µg

ml-1

.

Aqu

eous

ozo

ne r

educ

ed 9

9%of

th

e

tota

l A

.ac

tinom

ycet

emco

mita

ns

inpl

ankt

onic

sta

te a

nd 7

0% i

nbi

ofilm

. G

aseo

us o

zone

(1,

-16

g

m-3

) re

duce

dA

ggre

gatib

acte

rac

tinom

ycet

emco

mita

ns(A

.a)

99.7

% i

n is

olat

ed s

tate

and

70%

in

biof

ilm

(53

g m

-

3 ).

Gas

eous

oz

one

pre

sent

edgr

eate

r an

tim

icro

bial

act

ivit

yag

ains

t A

ggre

gat

ibac

ter

acti

nom

ycet

emco

mita

ns.

Ch

lorh

exid

ine,

aq

ueou

s an

dga

seou

s oz

one

show

ed d

ose-

depe

nden

t ef

fect

iven

ess;

how

ever

, th

ere

was

gre

ater

effi

cacy

in

pl

ankt

onic

bact

eria

than

in b

iofi

lm.

Ant

imic

robi

al

agen

ts

wer

ete

sted

on

bio

film

s w

ith o

nly

one

type

of

ba

cter

ia.

Incl

inic

al

cond

ition

s,

biof

ilm

sco

mpo

se

mul

tisp

ecie

s th

atco

uld

prod

uce

chan

ges

in th

eho

st a

nd l

ead

to c

hang

es i

nth

e en

viro

nmen

t.

273

99.7% in isolated state, and by approximately 70% inbiofilm at a concentration of 53 g m-3.

The complete elimination of P. gingivalis and T.forsythia in planktonic state was obtained through theconcentrations of gaseous ozone of 8 and 16 g m-3

and 2% chlorhexidine; in biofilm gaseous ozone of 53g m-3 and 2% chlorhexidine showed effectiveness of100%. Even in low concentrations (1, 2 and 4 g m-3),gaseous ozone reduced the levels of these pathogensby 99.7% in planktonic state.

Parvimonas micron, in isolated state, was totallyeliminated by all agents, with the exception of lowconcentrations of aqueous ozone at 1.25 mg ml-1(reduction of 78% in planktonic state). However, inbiofilm, P. micra presented greater susceptibility toozone gas (53 g m -3) and 2% chlorhexidine. Ozone effects on the adhesion of brackets to den-tal enamel. Two in vitro studies evaluating the effectsof ozone application on the adhesion of orthodonticbrackets were found.

In a randomized in vitro study, Cehreli et al.,(2010) (Table II) evaluated prophylactic pretreatmentwith ozone, applying shear tension to the bonding oforthodontic brackets. Moreover, it analyzed the bondingfailures in the interface using the modified adhesiveremnant index (ARI).

Vertical force was applied to the bracket base(1N/mm2=1MPa) at a speed of 1mm/min. Each toothwas washed, and polished with pumice and rubber cupsfor 10 seconds. The results of the shear bond strengthwere: Group 1: 10.48 MPa; Group 2: 8.89 MPa; Group3: 9.41MPa; Group 4: 9.82 MPa.

The results of modified adhesive remnant indexARI (0-3) were: Group 1: 2.38; Group 2: 1.31; Group3: 3.00; Group 4: 1.92.

Groups that were pretreated with ozone showedgreater shear strength over the bracket. The lowestshear strength was obtained in Group 2. Pretreatmentwith ozone in the enamel did not affect the adhesivesystem used to attach the brackets. Pithon & dos Santos (2010) (Table II)determined whether aqueous ozone reduces the bondstrength of orthodontic adhesives. In total, 120 bovinemandibular incisor teeth were selected randomly anddivided into 4 groups. Groups 1 and 3 were cleaned

with pumice and washed with water; groups 2 and 4were washed with ozonated water before adhesion tostainless orthodontic brackets with resin Transbond XT,3M Unitek, Monrovia, CA, USA (Group 1 and 2;) and amodified resin of glass ionometer cement (Groups 3and 4; Fuji Ortho LC, Japan).

Results showed, on average, shear bondstrength (SBS) of 22.07 Mpa for Group 1; 20.21 Mpain Group 2; approximately 20.06 Mpa in Group 3 andover 18.73 Mpa in Group 4. In terms of the adhesiveremnant index ARI (0-3), results showed: Absence ofadhesive remnant in the tooth (0): Group 1=3, Group2=9, Group 3=0, Group 4=0; less than half of theadhesive remnant in the tooth (1): Group 1=3, Group2=6, Group 3=3, Group 4=12; more than half of theadhesive remnant in the tooth (2): Group 1=15, Group2=12, Group 3=15, Group 4=18; total presence ofadhesive in the tooth (3): Group 1=9, Group 2=3, Group3=12, Group 4=0. Results showed that the SBS of thegroups washed with ozone (Group 2 and 4) wereslightly less than the brackets washed with tap water(Group 1 and 3) but with no significant differencesrelated to the shear bond strength in both groups.Ozone did alter the sites of the resin fracture whenFuji Ortho LC was used. The adhesive remnant index(ARI) in Groups 2 and 3 was significantly different fromGroups 3 and 4. Ozone did not reduce the shearstrength in orthodontic bracket debonding. Ozone action on the bone integration of dentalimplants. The search method used allowed us to findone in vivo study regarding the effects of ozonated oilon the bone integration of implants:

El Hadary et al. (2011) (Table III) evaluatedozonated oil (sunflower oil, 0.55 ml) under the influenceof cyclosporine A in the bone integration of dentalimplants. In total, 20 adult New Zealand rabbits aged9-12 months and weighing between 3 and 3.5 kg, wereadministered a subcutaneous daily dose of 10 mg ofcyclosporine per kg for a period of fourteen days.

Two groups were formed: Group A: ozonatedand Group B: non-ozonated (Control group). After eightweeks, in the ozonated group (A) the microscopic examshowed organization of the mature bone with intimatecontact between the implant surface and new bonewith numerous haversian systems. In group A, bonedensity values (± SD) was initially 126.7 ± 3.3; andafter eight weeks bone density was 134.1 ± 5.0; forGroup B (non-ozonated) bone density was initially117.7 ± 8.4; after eight weeks bone density was 124.0


274

Aut

hor

(dat

e)P

urpo

seM

etho

dolo

gyR

esul

tsC

oncl

usio

nSt

udy

lim

itat

ions

Kro

nenb

erg

et a

l. (

2009

)E

valu

atin

g w

heth

er

ther

e is

no d

iffe

renc

e in

the

ant

icar

ies

prot

ectio

n of

oz

one

and

cerv

itec

/flu

orin

e ar

ound

th

ebr

acke

ts,

in a

dditi

on t

o as

sess

whe

ther

Dia

gnod

ent

and

the

quan

tity

of i

nduc

edfl

uore

scen

t li

ght

are

not

supe

rior

to

th

e vi

sual

eval

uati

on

of

initi

al

cari

ous

lesi

ons.

20 r

ight

-han

ded

pati

ents

wit

hpe

rman

ent

dent

itio

n an

dde

fici

ent

oral

hyg

iene

(pl

aque

inde

x >

40%

) w

ho n

eede

d an

orth

odon

tic

appl

ianc

e w

ere

anal

yzed

fo

r 26

mon

ths.

All

quad

rant

s w

ere

trea

ted

wit

hoz

one

(2’1

00 ±

10%

for

30

seco

nds

ppm

) an

d th

e ot

her

grou

p w

ith

Cer

vite

c/fl

uori

ne(2

50 p

pm).

Vis

ible

pl

aque

in

dex

(VP

I)

in

all

quad

rant

s w

as

55.6

%.

Am

ong

the

quad

rant

s tr

eate

d w

ith

ozon

e, 3

.2%

dev

elop

ed n

ew a

reas

of

whi

te p

oint

sw

hile

in

th

e gr

oup

trea

ted

wit

hC

ervi

tec/

fluo

rine

pr

otec

tor

was

0.7%

of

the

area

s.

The

ant

icar

ies

prot

ecti

ve e

ffec

tof

Cer

vite

c/F

luor

ine

duri

ng t

hepl

acem

ent

of

the

orth

odon

tic

appl

ianc

e w

as

supe

rior

to

ozon

e.

Lac

k o

fco

mpa

risi

on

wit

hot

her

conc

entra

tion

san

d ti

mes

of

appl

icat

ion

Ceh

reli

et a

l. (2

010)

To

dete

rmin

e th

e ef

fect

of

pret

reat

men

t pr

ophy

lact

icoz

one

appl

ying

she

ar t

ensi

onto

the

bon

ding

of

orth

odon

tic

brac

kets

, as

wel

l as

eva

luat

ing

link

age

flaw

s in

the

int

erfa

ceus

ing

a m

odif

ied

adhe

sive

rem

nan

t ind

ex (

AR

I).

52 b

icus

pid

rand

omiz

ed t

eeth

wer

e us

ed a

nd d

ivid

ed i

nto

4gr

oups

(13

eac

h).

Eac

h to

oth

was

w

ashe

d,

and

then

polis

hed

wit

h pu

mic

e an

dru

bber

cu

ps

for

10

seco

nds.

For

li

ght

curi

ng,

a ha

loge

nla

mp

was

use

d fo

r 20

sec

onds

on t

he m

esia

l an

d di

stal

are

aof

eac

h to

oth.

She

ar s

tren

gth

resu

lts

wer

e: G

roup

1: 1

0.48

MP

a; G

roup

2:

8.89

MP

a;G

roup

3:

9.41

MP

a; G

roup

4:

9.82

MP

a.

P=0.

05

The

re

sults

of

th

em

odif

ied

adhe

sive

re

mna

nt

inde

xIA

R (

0-3)

wer

e:(0

) G

roup

1 =

3,

grou

p 2

= 9

, gr

oup

3 =

0; G

roup

4 =

0(1

) G

roup

1 =

3,

grou

p 2

= 6

, gr

oup

3 =

3, g

roup

4 =

12

(2)

Gro

up 1

= 1

5, g

roup

2

= 1

2,gr

oup

3 =

15,

gro

up 4

= 1

8(3

) G

roup

1 =

9,

grou

p 2

= 3

, gr

oup

3 =

12, g

roup

4 =

0.

Gro

ups

that

w

ere

pret

reat

edw

ith

ozon

e sh

owed

g

reat

ersh

ear

stren

gth

. T

he

low

est

stre

ngth

was

obt

aine

d in

gro

up2.

Pre

trea

tmen

t w

ith o

zone

on

the

enam

el d

id

not

affe

ct t

hesh

ear

stre

ngth

.

The

oz

one

conc

entra

tion

used

w

as

not

men

tion

ed.

Pit

hon

& d

os S

anto

s (2

010)

To

dete

rmin

e if

aq

ueou

soz

one

redu

ces

resi

stan

ce

toth

e fi

xati

on

of

orth

odon

tic

adhe

sive

s.

120

bovi

ne

m

andi

bula

rin

ciso

r te

eth

wer

e r

ando

mly

divi

ded

into

4 g

roup

s. G

roup

s1

and

3

wer

e cl

eane

d w

ithpu

mic

e an

d w

ashe

d w

ithw

ater

; gr

oups

2 a

nd 4

wer

ew

ashe

d w

ith

ozon

ated

wat

er(0

.6 m

g/L

).

Res

ults

sho

wed

mea

n sh

ear

stre

ngth

(Mpa

) fo

r gr

oup

1 of

22

.07

Mpa

;gr

oup

2:

20

.21

Mpa

; gr

oup

3:ap

prox

imat

ely

20.0

6 M

pa a

nd g

roup

4 ov

er 1

8.73

Mpa

.

The

re

wer

e no

si

gnif

ican

tdi

ffer

ence

s in

the

she

ar s

tren

gth

of b

rack

ets

debo

ndin

g fr

om t

heen

amel

and

was

hed

with

ozo

neor

tap

wat

er.

Adh

esiv

e re

mna

ntin

dex

(AR

I) i

n g

roup

s 2

and

3w

ere

sign

ific

ant

diff

eren

t fr

omgr

oups

3 a

nd 4

.

A

sing

le

ozon

eco

ncen

trati

on w

asus

ed.

Hig

her

orlo

wer

conc

entra

tion

sm

ay

gene

rate

diff

eren

t re

sults

.

Dhi

ngra

& V

anda

na (

2011

)T

o ev

alua

te

the

clin

ical

effe

cts

of a

sin

gle

subg

ingi

val

irrig

atio

n w

ith o

zona

ted

wat

erin

pat

ient

s w

ith g

ingi

vitis

and

fixe

d or

thod

onti

c ap

plia

nces

and

also

to

co

rrel

ate

the

clin

ical

ef

fect

s w

ith

the

lact

ate

dehy

drog

enas

e (L

DH

)ac

tivity

in

ging

ival

cre

vicu

lar

flui

d.

Sin

gle-

blin

d cl

inic

al

stud

yw

ith

15

subj

ects

ag

ing

17ye

ars

and

usin

g or

thod

onti

cap

plia

nce

and

pres

entin

g 50

%of

site

s w

ith

ging

ival

ble

edin

gan

d 50

% d

icho

tom

ous

plaq

uesc

ore.

Aft

er

28

days

pl

aque

in

dex

decr

ease

d fr

om 1

.93

± 0.

22 to

0.8

9 ±

0.24

. G

ingi

val

blee

ding

in

dex

redu

ced

from

87.

1 ±

6.2%

to

30.9

±4.

5%.

Poc

ket

dep

th

show

edre

duct

ion

from

3.1

0 ±0

.12

to 2

.92

±0.

10.

The

ac

tivi

ty

of

lact

ate

deh

ydro

gena

se

dec

reas

ed

fro

m10

2.7

± 5

9.2

to 1

8.9

± 5.

9 af

ter

28da

ys.

A s

ingl

e irr

igat

ion

wit

hoz

onat

ed

wat

er

in

aco

ncen

trat

ion

of

0.01

m

g l-1

sign

ific

antly

re

duce

d

all

clin

ical

pa

ram

eter

s af

ter

from

base

line

to

28

days

an

dsi

gnif

ican

tly

dec

reas

ed

th

eac

tivity

of

lact

ate

dehy

drog

enas

e in

th

e gi

ngiv

alcr

evic

ular

flu

id.

Abs

ence

of

cont

rol

grou

p.

Tabl

e II.

Ozo

ne th

erap

y in

ort

hodo

ntic

s.


275

± 5.6. The studydemonstrated that theapplication of cyclosporine forshort term in combination withthe topical application ofozonated oil may significantlyinfluence bone density andbone integration qualityaround dental implants. Nostatistically significantdifferences were found relatedto bone density in bothgroups.

DISCUSSION The present literature reviewanalyzed the effects of ozoneon periodontal pathogens,bone integration of dentalimplants and adhesion oforthodontic brackets. The literature available relatedto ozone therapy in dentistryshowed relevance in terms ofthe properties of ozonetherapy, namely: therapeuticaction through the distributionof oxygen, expression ofgrowth factors and cytokinesand reduction of oxidativestress and acting as modifierof the biological response(Seidler et al.; Bocci, 2006;Estrela et al., 2006; Valacchiet al., 2002). Only one in vivo study(Martínez Abreu & AbreuSardiñas) regarding the actionof ozone against periodontalpathogens was performed fora larger period (six months),which represents a fragility ofthe studies alreadydeveloped. Additionally, theresults of this article alsoshowed reduction of 98% ofg r a m - n e g a t i v emicroorganisms in the grouptreated with ozone.A

utho

r (d

ate)

Pur

pose

Met

hodo

logy

Res

ults

Con

clus

ion

Stu

dy li

mit

atio

ns

El H

adar

y et

al.

(20

11)

To

eval

uate

the

eff

ects

of

ozo

nate

d oi

l un

der

the

infl

uenc

e of

Cy

clos

pori

neA

in

bone

int

egra

tion

of

den

tal i

mpl

ants

.

Tw

enty

whi

te a

dul

t m

ale

New

Z

eala

nd

ra

bbits

agin

g 9-

12

mon

ths

and

wei

ghin

g be

twee

n 3

-3.5

kg

w

ere

test

ed.

Dai

lysu

bcut

aneo

us d

ose

of

10m

g of

C

yclo

spor

ine

per

kg

fo

r 14

da

ys

was

adm

inis

trat

ed.

Gro

up

A:

trea

ted

with

oz

onat

ed

oil

(sun

flow

er o

il)

0.55

0 m

lin

gel

ap

plie

d to

fil

l ea

cho

steo

tom

y

site

fo

r th

eim

plan

t.

Gro

up

B:

non-

ozo

nate

d (C

ont

rol g

roup

).

In g

roup

s A

and

B

, th

ein

itia

l bo

ne

dens

ity

was

126.

7 ±

3.3

and

117

.7 ±

8.4

resp

ectiv

ely;

it

was

134.

1 ±

5.0

and

124

.0 ±

5.6

afte

r 2

mon

ths.

The

ligh

t

mic

rosc

opi

cex

amin

atio

nde

mon

stra

ted

evid

ence

of

new

ly

form

ed

mat

ure

bone

w

as

obse

rved

in

grou

p

B,

wh

erea

s in

cont

rol

grou

p

the

spec

imen

s de

mon

stra

ted

the

form

atio

n of

pri

mar

yos

teon

s.

The

ad

min

istr

atio

n

ofsh

ort-

term

cy

clos

pori

neto

geth

er

wit

h th

e to

pica

lap

plic

atio

n of

o

zona

ted

oil

m

ay

infl

uenc

e bo

ned

ensi

ty.

Ozo

ne c

onc

entr

atio

n w

asn

ot r

epor

ted

.

Hau

ser-

Ger

spac

h et

al

.(2

012)

To

in

vest

igat

e th

ean

timic

robi

al

effi

cacy

of

gas

eous

ozo

ne o

n ba

cter

iaad

here

d

to

seve

ral

surf

aces

of

titan

ium

an

dzi

rco

nium

, an

d al

so

toev

alua

te

the

adhe

sion

of

ost

eobl

ast-

like

MG

-63

cell

s to

sur

face

s th

at w

ere

trea

ted

with

ozo

ne.

Tit

aniu

m

and

zirc

oni

umd

isks

(5.

0 m

m

diam

eter

)w

ith

2 ty

pes

of

surf

aces

wer

e st

erili

zed

by

gam

ma

irra

diat

ion

and

incu

bate

din

a

solu

tion

of

ster

ile

saliv

a se

rum

fo

r 15

min

utes

at

35°C

, an

d us

edin

th

e m

icro

biol

ogi

cal

expe

rim

ent.

O

zone

trea

tmen

t w

as c

arri

ed o

utw

ith a

n O

zoto

p un

it, 1

40p

pm;

2L

/min

ute

fo

r 6-

24

seco

nds.

P.

Gin

giva

lis

was

elim

inat

ed i

n 2

4 se

cond

sw

ith o

zone

(>

99.9

4% o

fre

duct

ion)

. S.

sa

ngu

inis

was

m

ore

resi

stan

t an

dsh

owed

gre

ater

red

uctio

nin

zi

rcon

ium

su

bstr

ates

(>90

% re

duc

tion

).

Ozo

ne

did

not

affe

ct t

hesu

rfac

e st

ruct

ure

s of

the

test

sp

ecim

ens

and

did

not

inf

luen

ce o

steo

blas

tic

cell

s

pro

life

ratio

nn

egat

ivel

y.

Po

lishe

dti

tan

ium

an

d zi

rcon

ium

(aci

d

etch

ed

and

pol

ishe

d) p

rese

nted

low

erb

acte

rial

col

oniz

atio

n.

The

stu

dy d

id n

ot i

nclu

deas

pect

s of

th

ed

iffe

rent

iati

on

ofex

trac

ellu

lar

mat

rix

mat

urat

ion,

re

leas

e o

fg

row

th

fact

ors

and

expr

essi

on

of

spec

ific

ost

eobl

astic

mar

ker

s.

Tabl

e III

. Ozo

ne th

erap

y in

den

tal i

mpl

ants

.


276

There was remarkable inactivation of the majorperiodontal pathogens, in both the analyzed in vivo andin vitro studies. The results obtained by de Ramon etal., confirm the effective action of ozone on gingivalbleeding, with a decrease of over 50% of the mainperiodontal pathogens: Aggregatibacteractinomycetencomitans, Bacteroides forsythus andPorphyromonas gingivalis. It showed a significantreduction of TNF-a and IL-1b. Furthermore, there wasno variation in the pocket depth, or the level ofperiodontal insertion, which reinforces the need formechanical removal of plaque for gingival control andperiodontal maintenance (Müller et al., 2007; Lindhe& Nyman, 1975).

Nevertheless, ozone had significantlyeffectiveness in eliminating gram-negativemicroorganisms, reducing periodontal pathogens,bleeding on probing (Kshitish & Laxman).

In one study (de Ramon et al.), ozone reducedplaque index over 25%. However in another article(Kshitish & Laxman) results demonstrated that dentalplaque was reduced by 12%.

Although therapeutic ozone is applied in severalforms, including aqueous, gaseous and oil, there isevidence of better biocompatibility in the cell with theuse of aqueous ozone (Huth et al., 2006). Ozone gashad greater antimicrobial activity in terms of the totalelimination of pathogens (Aa, Pg, Tf and Pm) inplanktonic state than in biofilm.

Regarding the effects of ozone therapy on theadhesion of orthodontic brackets, the results of thestudy of Cehreli et al., demonstrated that groupspretreated with ozone presented greater shear

strength. Although Pithon and dos Santos found thatthe shear bond strength of the brackets washed withozone were slightly less than the brackets washed withtap water after debonding but with no significantdifferences. According to the search strategy used, the only studyfound about ozone activity on bone integration of den-tal implants (El Hadary et al.) demonstrated an increasein bone density around dental implants in the ozonatedgroup, but no significant differences regarding the non-ozonated group were noticed. Nevertheless, the studywas carried out only for two months, under the influenceof an immunosuppressive drug and it also did not reportthe concentration and time of application of ozone,which renders the research irreproducible. Ozone’s biological and stimulatory effects couldbe useful in periodontal therapeutics, in orthodonticsand dental implants.

In conclusion, the studies analyzed showedseveral biological properties of ozone and could beconsidered as a promising therapy. Further studies areneeded for the analysis of the application of ozone indentistry, in order to assess its clinical effectiveness inthe field of dentistry.

ACKNOWLEDGEMENTS

The authors express their thanks to the AnatomyDepartment of the University of São Paulo (USP),Bauru, São Paulo, Brazil, for the additional informationoffered for the development of this review. The authorsreceived no financial support and declare no conflictsof interest related to the authorship of this study.

GERMAN, I. J. S.; RODRIGUES, A. C.; ANDREO, J. C.; POMINI, K. T.; AHMED, F. J.; BUCHAIM, D. V.; ROSA JÚNIOR,G. M.; GONÇALVES, J. B. O. & BUCHAIM, R. L. J. Ozonoterapia en Odontologia: una revisión sistemática. Int. J.Odontostomat., 7(2):267-278, 2013.

RESUMEN: El objetivo de esta revisión sistemática fue verificar la literatura disponible relacionada a la efectividad yefectos biológicos de la ozonoterapia en periodoncia, ortodoncia e implantes dentales. Se realizó una revisión sistemáticaen septiembre del 2012 en las bases de datos PubMed, LILACS and SciELO por medio de la combinación de las palabrasclave dental implants, periodontics, orthodontics, therapeutics. Se evaluaron los artículos publicados entre los años 2002 y2012. Fueron incluidos estudios In vitro e in vivo y publicaciones en Inglés y Español, excluyendo pósters, carta al editor yconferencias. Estudios in vitro e in vivo mostraron inactivación de los principales patógenos periodontais con el uso delozono. Hubo resultados contradictorios y falta de evidencia sobre la acción del ozono en la adhesión de los bracketsortodónticos, así como también en la osteointegración de los implantes dentales. El ozono puede ser considerado comouna terapia alternativa promisoria en la Odontología. Sin embargo, es necesaria la realización de estudios bien diseñadospara, de ese modo, evaluar la aplicación del ozono y su efectividad clínica en el campo de la Odontología.

PALABRAS CLAVE: implantes dentales, periodoncia, ortodoncia, terapéutica.


277

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Correspondence to:Iris Jasmin Santos GermanDepartment of Biological Sciences (Anatomy)Bauru School of DentistryAl. Dr. Octávio Pinheiro Brisola, 9-75Postal code: 17012-901University of São PauloFOB-USPBauru - BRAZIL Phone: +55 14 3235-8226Fax: +55 14 3235-8223

Email: [email protected]

Received: 27-04-2013Accepted: 15-06-2013


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