J Clin Periodontol 2001; 28: 1074–1078 Copyright C Munksgaard 2001

Printed in Denmark . All rights reserved

ISSN 0303-6979

Short Communication
Anton Sculean1,
Effect of an enamel matrix protein Thorsten M. Auschill2,
Nikolaos Donos3, Michel Brecx1 and

derivative (EmdogainA) on ex Nicole B. Arweiler2

1
Department of Periodontology and
Conservative Dentistry, University of
Saarland, Homburg, Germany; 2Department

vivo dental plaque vitality of Operative Dentistry, University of Freiburg,

Germany; 3Department of Periodontology and
Fixed Prosthodontics, University of Berne,
Switzerland

Sculean A, Auschill TM, Donos N, Brecx M, Arweiler NB: Effect of an enamel

matrix protein derivative (EmdogainA) on ex vivo dental plaque vitality. J Clin
Periodontol 2001; 28: 1074–1078. C Munksgaard, 2001.

Abstract
Background: A common clinical observation following surgical periodontal ther-
apy with an enamel matrix derivative (EmdogainA) is the improved healing of the
soft tissues and the limited inflammation of the operated areas. These clinical
observations are empirical and difficult to explain. One of the factors influencing
the early wound healing might be a potential antimicrobial effect of EmdogainA.
Aim: To investigate the effect of EmdogainA on the vitality of ex vivo supragin-
gival dental plaque and to compare this effect to that of a standard 0.2% chlor-
hexidine solution.
Materials and Methods: 24 patients suffering from adult periodontitis were in-
cluded in the study. At the beginning of the experiment, all participants were given
a professional tooth cleaning. For the following 4 days, they had to refrain from
any kind of oral hygiene measures. At day 5, from each of the volunteers, a
voluminous plaque biofilm sample was taken with a sterile curette from the ves-
tibular surfaces of the 1st lower molars and divided into 5 equal parts. Each part
was mounted with 5 ml of the following solutions: (1) NaCl, (2) enamel matrix
derivative dissolved in water (EMD), (3) enamel matrix derivative dissolved in the
vehicle (EmdogainA), (4) vehicle (propylene glycol alginate, PGA), (5) 0.2% chlor-
hexidine digluconate (CHX). After a reaction time of 2 min the test solutions
were sucked off, and subsequently the biofilm was stained with a fluorescence
dye. The vitality of the plaque flora after the treatments was evaluated under
the fluorescence microscope (VF%).
Results: Plaque samples treated with NaCl showed a mean vitality of 76.8∫8%.
The EMD, EmdogainA, PGA and CHX showed VF values of 54.4∫9.2,
21.4∫10.6%, 19.6∫11.6% and 32.3∫11.8%, respectively. EmdogainA, PGA and
CHX showed statistically highly significant reductions (p⬍0.0001) in terms of bac-
teria vitality when compared to water (negative control) and EMD. Both Emdo-
gainA and PGA were found to be statistically significantly different compared
to CHX (p⬍0.001) (positive control).
Key words: dental biofilm; chlorhexidine;
Conclusion: The results of this study indicate that EmdogainA might have an enamel matrix derivative; antibacterial effect
antibacterial effect on the vitality of the ex vivo supragingival dental plaque
flora. Accepted for publication 23 March 2001

Recently, an enamel matrix protein de- et al. 1997, Heijl 1997, Sculean et al. mation of a new periodontal ligament,
rivative (EmdogainA) has been shown 1999a, 2000, Yukna and Mellonig of new cementum with perpendicularly-
to promote periodontal wound healing 2000). Treatment of different types of oriented collagen fibers and of new al-
in animals and humans (Hammarström periodontal defects resulted in the for- veolar bone (Hammarström et al. 1997,

Fig. 1. Representative vital fluorescence staining of a plaque sample
containing mainly living cells (living cells are stained green).
Heijl 1997, Sculean et al. 1999a, 2000,
Yukna and Mellonig 2000). A common
empirical clinical observation following
application of EmdogainA is the im-
proved healing of the soft tissues during
the first post-operative period and the
limited inflammation at the operated
areas (Héden et al. 1999, Pontoriero et
al. 1999, Sculean et al. 1999 a, b, c). A
potential factor influencing the early
wound healing might be an anti-
microbial effect of EmdogainA. To our
knowledge, there is no information con-
cerning the direct antimicrobial effect
of EmdogainA on the vitality of supra-
gingival dental plaque.
Therefore, the aim of the present
study was to investigate the effect of
EmdogainA on the vitality of ex vivo
supragingival dental plaque biofilm and
to compare this effect to that obtained
following the use of the gold standard
0.2% chlorhexidine.
Material and Methods
24 patients suffering from adult peri-
odontitis were included in the study.
Criteria for exclusion were the use of
antibiotics or other antibacterial sub-
stances during the last 6 months that
could have influenced plaque growth.
At the beginning of the experiment,
all participants were given a pro-
fessional tooth cleaning. For the follow-
ing 4 days, they had to refrain from any
kind of oral hygiene measures. At day
5, from each of the volunteers, a vol-
uminous plaque biofilm sample was
taken with a sterile curette from the ves-
tibular surfaces of the first lower molars
and divided into 5 equal parts. Each
part was mounted with 5 ml of the fol-
lowing solutions:
Fig. 2. Representative vital fluorescence staining of a plaque sample
containing mainly dead cells (dead cells are stained red).
1. NaCl-solution (negative control);
2. enamel matrix derivative (Biora,
Malmö, Sweden) dissolved in water
(EMD);
3. enamel matrix derivative dissolved in
the vehicle (EmdogainA, Biora,
Malmö, Sweden);
4. vehicle (propylene glycol alginate,
PGA) (Biora, Malmö, Sweden);
5. chlorhexidine 0.2% (CHX, Corso-
dylA, SB, Bühl, Germany) (positive
control).
EmdogainA consists of the enamel ma-
trix protein derivative (EMD) itself,
and a vehicle solution based on propy-
lene glycol alginate. Before applying to
the plaque specimens, the 2 components
were always freshly mixed according to
the instructions given by the manufac-
turer.
After a reaction time of 2 min the
test solutions were sucked off, and sub-
sequently the treated samples were vital
stained according to the vital fluor-
escence technique as described in detail
elsewhere (Netuschil et al. 1989, Arwei-
ler et al. 2000, 2001). Briefly, the tech-
nique is based on the use of fluoresce-
indiacetate (FDA) and ethidium bro-
mide (EB). FDA, a fluorescent dye, is
not fluorescent but membrane soluble.
In vital cells it is metabolised to fluor-
escein which is green and cannot leave
the cell (Rotmann & Papermaster
1966). Living cells are stained green
(Fig. 1). Dead cells are not able to
metabolise the FDA, so that there is no
staining. A contra-staining with ethidi-
um bromide (EB) binds to the nucleic
acids of dead cells and stains red (Fig.
2). The method allows living and dead
cells to be simultaneously stained.
Thus, a dichotomous decision: living/
dead can be made for each single cell.
EmdogainA and plaque vitality 1075
After a staining reaction of 3 min,
the samples were immediately processed
under the fluorescent microscope (Leitz
DMR B, Leica GmbH, Wetzlar, Ger-
many) to enumerate the % of vital flora
(VF%) using a counting grid (Brecx et
al. 1990).
For each group, the mean values of
VF% were calculated. Data series and
their differences to water were exam-
ined for normal distribution using the
Kolmogorov-Smirnov test. Since data
proved significant, differences between
the controls and the test preparations
were detected using the Student’s paired
t-test. Bonferroni adjustments were not
considered to be necessary (Perneger
1998). With the results and the given
sample size, a power (1-b) of 0.95 was
reached.
Results
The results are summarized in Table 1.
Plaque biofilm treated with the NaCl
solution showed a mean vitality of
76.5∫8.0%. The plaque samples treated
with EMD demonstrated a mean vi-
tality of 54.4∫9.2%. EmdogainA, PGA
and CHX (positive control) showed re-
duced vitality values of 21.4∫10.6%,
19.6∫11.6% and 32.3∫11.8%, respec-
tively. EMD, EmdogainA, PGA and
Table 1. Vitality values and significance level
compared to placebo (by paired t-test)
VF (in %) p
NaCl 76.5∫8.0 n.s.
EMD 54.4∫9.2 ⬍0.0001
EmdogainA 21.4∫10.6 ⬍0.0001
PGA 19.6∫11.6 ⬍0.0001
CHX 32.3∫11.8 ⬍0.0001
1076 Sculean et al.
CHX showed statistically highly sig-
nificant reductions (p⬍0.0001) in terms
of bacteria vitality when compared to
NaCl (negative control). EmdogainA,
PGA and CHX were statistically highly
significantly different compared to
EMD (p⬍0.0001). Both EmdogainA
and PGA were found to be statistically
significantly different compared to
CHX (p⬍0.001) (positive control).
Discussion
The present study has shown that
EMD, EmdogainA, PGA, and CHX
possess a significantly higher anti-
microbial effect when compared to a
standard NaCl solution. EmdogainA,
PGA, and CHX were significantly more
effective in reducing plaque vitality
than EMD. Both EmdogainA and PGA
displayed a statistically significantly
higher reduction in the vitality of ex
vivo supragingival dental plaque than
the 0.2% CHX solution.
In the present experiment, a method
was chosen in which the in vivo grown
biofilm was carefully removed from the
tooth surfaces and then tested. The vi-
tal fluorescence technique employed in
this study offers the possibility to inves-
tigate the antibacterial effect of an anti-
microbial agent on an ex vivo biofilm
(Netuschil et al. 1989, Brecx et al.
1990). Generally, in dental plaque-re-
lated diseases enormous numbers of
densely-packed bacteria are present
(Listgarten 1994). Cells in the dental
plaque biofilm react differently from
those in suspension, because the biofilm
consists of a highly hydrated anionic
matrix and this may protect the inner-
most cells of the biofilm from anti-
microbial agents (Costerton et al.
1987). On the other hand, it cannot be
excluded that by removing the biofilm
from the tooth surface, its disruption
may have occurred. This in turn, may
have resulted in a greater vulnerability
of the plaque sample compared to the
intact, in situ, biofilm. Regarding this
issue, Millward & Wilson (1989) have
shown that this model is nearer to the
real situation than cell suspensions.
Thus, due to the fact that dental plaque
exists as a biofilm, it was suggested that
biofilm-based assays are of greater
value than cell suspensions when as-
sessing the effectiveness of chemical
agents for the treatment and/or preven-
tion of inflammatory periodontal dis-
ease (Millward & Wilson 1989).
In the present study, EMD also
showed an effect in reducing the vitality
of ex vivo supragingival dental plaque.
The mechanisms behind a possible anti-
bacterial effect of EMD are virtually
unknown. Furthermore, our results
have indicated that PGA itself may
have a comparable effect on the bac-
terial vitality than EmdogainA. These
findings together with the fact that
PGA has a low pH. (around 5.0) (Ges-
trelius et al. 1997a) suggest, that in the
present ex vivo model, the antimicrobial
effect was rather due to the PGA.
Moreover, the PGA showed an even
higher antimicrobial effect than 0.2%
CHX. A possible explanation for this
observation is the fact that, in the pres-
ent experiment, all tested solutions were
used in the same form as supplied by
the manufacturer and employed in the
routine periodontal therapy. Conse-
quently, it cannot be excluded that the
antimicrobial effect of PGA might have
been also influenced by its concen-
tration. On the other hand, it is unlikely
that a methodological error (i.e., an in-
terference of PGA with the penetration
and/or uptake of FDA) could have led
to this result. The vital fluorescence
technique was previously employed in
numerous studies investigating the anti-
microbial effects of different agents
such as chlorhexidine, MeridolA, Lis-
terineA, delmopinol and tee tree oil, but
an interference of any of the used sub-
stances with the uptake or penetration
of FDA was never observed (Brecx et
al. 1990, 1992, Netuschil et al. 1989,
Rundegren et al. 1992, Arweiler et al.
2000, 2001). Furthermore, after a reac-
tion time of 2 min, all tested substances
were sucked off and, therefore, only a
limited direct contact between PGA and
FDA might have occurred. This is also
illustrated by the obtained results,
which have indicated that after the ap-
plication of PGA the plaque vitality
was significantly reduced, but never
completely absent.
Another issue that still needs clarifi-
cation, is the possible effect of PGA on
the gingival, periodontal ligament
(PDL) and bone cells. However, in this
ex vivo study, only the antimicrobial ef-
fect on the supragingival dental plaque
was studied and, therefore, no con-
clusions regarding the effect of PGA on
gingival, PDL, or bone cells can be
drawn. It should, however, be noted
that results from in vitro studies have
indicated that once EMD was dissolved
in PGA, and the temperature increased
to 35æC, the pH of the formulation in-
creased significantly (Gestrelius et al.
1997a). Furthermore, in vivo studies in
rats have demonstrated that, when ap-
plied onto extracted and replanted first
molars in rats, PGA labelled with 111In-
dium colloid, left the site of application
within 24 h (Gestrelius et al. 1997a).
Thus, taken together, these data seem
to indicate that even if PGA might have
a direct effect on cell vitality, this effect
is limited to the first day(s) following its
application.
On the other hand, results from an in
vitro study have indicated that Emdo-
gainA, once precipitated onto a hard
surface, may have an influence on the
composition of the oral biofilm by pro-
moting the adherence of certain oral
bacteria (A. viscosus) while decreasing
the adherence of others (S. mutans, S.
gordonii) (Van der Pauw et al. 2000).
The authors suggested that this effect
was due to the hydrophobic property of
EmdogainA. Results from previous in
vitro studies have also indicated that
EmdogainA may inhibit the prolifer-
ation of epithelial cells, but the mechan-
ism(s) behind the different responses by
epithelial and mesenchymal cells are
still unknown (Gestrelius et al. 1997b).
Thus, all the mentioned findings, taken
together with the results from the pres-
ent study indicate that EmdogainA
might have a multiple influence on the
bacterial flora: immediately after appli-
cation, due to the low pH and, once
precipitated onto a hard surface, due to
its hydrophobic properties. Hence, it
cannot be excluded that the influence of
EmdogainAon the bacterial flora might
be one of the factors contributing to the
improved early healing of the operated
areas.
It is important to be kept in mind
that the present findings represent data
from an ex vivo dental plaque-model
and, therefore, further studies are
needed in order to definitively clarify
the effect of EmdogainA on an in situ
(not mechanically disrupted) dental
plaque biofilm.
Zusammenfassung
Effekt eines Schmelzmatrixproteinderivats
(EmdogainA) auf die ex vivo dentale Plaque-
vitalität
Hintergrund: Eine allgemeine klinische Beob-
achtung nach parodontalchirurgischer The-
rapie mit einem Schmelzmatrixderivat (Em-
dogainA) ist die verbesserte Heilung des
Weichgewebes und die begrenzte Entzündung
des operierten Gebietes: Diese klinischen Be-
obachtungen sind empirisch und schwierig

zu erklären. Ein Faktor, der die frühe Wund-
heilung beeinflusst, könnte ein potentieller
antimikrobieller Effekt von EmdogainA sein.
Ziel: Untersuchung des Effektes von Emdo-
gainA auf die Vitalität von ex vivo supragin-
givaler dentaler Plaque und Vergleich dieses
Effektes zu demjenigen einer Standard
0.2%igen Chlorhexidinlösung.
Material und Methoden: 24 Patienten, die an
einer Erwachsenen-Parodontitis litten, wur-
den in diese Studie aufgenommen. Zu Beginn
der Studie wurde bei allen Teilnehmern eine
professionelle Zahnreinigung durchgeführt.
An den folgenden 4 Tagen wurden keine ora-
len Hygienemaßnahmen erlaubt. Am Tag 5
wurde von jedem Teilnehmer eine voluminöse
Plaquebiofilmprobe mit einer sterilen Kürette
von der vestibulären Oberfläche des ersten
unteren Molaren genommen und in 5 gleiche
Teile aufgeteilt. Jeder Teil wurde mit 5 ml der
folgenden Lösungen gemischt: (1) NaCl, (2)
Schmelzmatrixderivat in Wasser gelöst
(EMD), (3) Schmelzmatrixderivat in einem
Vehikel gelöst (EmdogainA), (4) Vehikel (Pro-
pylenglycolalginat, PGA), (5) 0.2%iges
Chlorhexidindiglukonat (CHX). Nach einer
Reaktionszeit von 2 Minuten wurden die
Testlösungen aufgesaugt und folgend der
Biofilm mit Fluoreszenzfarbstoff gefärbt. Die
Vitalität der Plaqueflora nach den Behand-
lungen wurde unter dem Vitalfluoreszenz-
mikroskop (VF%) evaluiert.
Ergebnisse: Die Plaqueproben, die mit NaCl
behandelt wurden, zeigten eine mittlere Vita-
lität von 76.8∫8%. Das EMD, EmdogainA,
PGA und CHX zeigten VF Werte von
54.4∫9.2%, 21.4∫10.6%, 19.6∫11.6% und
32.3∫11.8%. EmdogainA, PGA und CHX
zeigten statistisch signifikant höhere Reduk-
tionen (p⬍0.0001) in Beziehung zur bakte-
riellen Vitalität, wenn zu Wasser (negative
Kontrolle) und EMD verglichen wurde. So-
wohl EmdogainA und PGA waren statistisch
signifikant unterschiedlich zu CHX
(p⬍0.0001) (positive Kontrolle).
Schlussfolgerung: Die Ergebnisse dieser Stu-
die zeigten, dass EmdogainA einen antibakte-
riellen Effekt auf die Vitalität von supragin-
givaler dentaler ex vivo Plaqueflora haben
könnte.
Résumé
Effet d’un dérivé de la matrice améllaire (Em-
dogainA) sur la vitalité de la plaque dentaire
ex vivo
Origine: Une observation clinique courante
durant un traitement parodontal chirurgical
à l’aide de protéines de la matrice améllaire
(EmdogainA) est une meilleure guérison des
tissus mous et une inflammation moindre.
Ces observations cliniques sont empiriques et
difficiles à expliquer. Un des facteurs in-
fluençant la guérison précoce peut être un ef-
fet antimicrobien de l’EMD.
But: Le but de cette étude a été d’évaluer l’ef-
fet de l’EmdogainA sur la vitalité de la plaque
dentaire sus-gingivale ex vivo et de comparer
cet effet avec une solution de chlorhexidine
2%.
Matériaux et Méthodes: 24 patients souffrant
de parodontite de l’adulte ont été inclus dans
cette étude. Au début de l’expérience, tous les
participants ont recu un nettoyage dentaire
professionnel. Pendant les 4 journées suivan-
tes, ils ont dû arrêté toute hygiène buccale.
Au jour 5, une quantité de plaque dentaire
volumineuse a été échantillonné des surfaces
vestibulaires des premières molaires inférieu-
res de chaque volontaire à l’aide d’une curet-
te stérile et divisée en 5 parts égales. Chaque
partie a été montée avec 5 ml des solutions
suivantes: (1) NaCl, (2) EMD: dérivé de la
matrice améllaire dissout dans l’eau (3) Em-
dogainA: dérivé de la matrice améllaire dis-
sout dans son véhicule, (4) PGA: le véhicule
propylène glycol alginate, (5) CHX:
chlorhexidine 0.2%. Après un temps de réac-
tion de 2 min, les solutions tests ont été aspi-
rées et le biofilm dentaire a été imprégné d’un
colorant de fluorescence. La vitalité de la
flore de la plaque dentaire après ces traite-
ments a été évaluée sous microscopie à fluo-
rescence (VF%).
Résultats: Les échantillons de plaque traités
avec NaCl possèdaient une vitalité moyenne
de 76.8∫8%. L’EMD, EmdogainA, PGA, et
CHX avaient des valeurs VF respectives de
54.4∫9.2%, 21.4∫10.6%, 19.6∫11.6% et
32.3∫11.8%. EmdogainA, PGA, et CHX ré-
duisaient la vitalité bactérienne de manière
très hautement significative (p⬍0.0001) lors-
que ces solutions étaient comparées aux
contrôle négatif NaCl et à EMD. Tant Emdo-
gainA que PGa étaient différents comparés
au contrôle positif CHX (p⬍0.001).
Conclusions: Les résultats de cette étude indi-
quent que EmdogainA pourrait avoir un effet
antibactérien sur la vitalité de la flore se trou-
vant dant la plaque dentaire sus-gingivale ex
vivo.
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Anton Sculean
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Department of Periodontology and Conserva-
the adherence of oral microbiota. Journal
tive Dentistry
of Dental Research 79 (special issue)
University of Saarland
(abstr. no. 111).
66421 Homburg
Yukna, R. A. & Mellonig, J. T. (2000) Histo-
Germany
logic evaluation of periodontal healing in
humans following regenerative therapy e-mail: anton.sculean/gmx.de