Wim Teughels Effect of material characteristics and/or

Nele Van Assche

Isabelle Sliepen
surface topography on biofilm
Marc Quirynen development

Authors’ affiliations:
Wim Teughels, Nele Van Assche, Isabelle Sliepen,
Marc Quirynen, Department of Periodontology,
Faculty of Medicine, Research Group for Microbial
Adhesion, School of Dentistry, Oral Pathology &
Maxillo-facial Surgery, Catholic University of
Leuven, Leuven, Belgium
Correspondence to:
Marc Quirynen
Department of Periodontology,
Kapucijnenvoer 33
3000 Leuven
Belgium
e-mail: marc.quirynen@med.kuleuven.be
Key words: biofilm, implants, peri-implantitis, periodontal disease, plaque growth, surface
characteristics, surface free energy, surface roughness
Abstract
Background: From an ecological viewpoint, the oral cavity, in fact the oro-pharynx, is an ‘open
growth system’. It undergoes an uninterrupted introduction and removal of both
microorganisms and nutrients. In order to survive within the oro-pharyngeal area, bacteria
need to adhere either to the soft or hard tissues in order to resist shear forces. The fast turn-
over of the oral lining epithelia (shedding 3
/day) is an efficient defence mechanism as it
prevents the accumulation of large masses of microorganisms. Teeth, dentures, or endosseous
implants, however, providing non-shedding surfaces, allow the formation of thick biofilms. In
general, the established biofilm maintains an equilibrium with the host. An uncontrolled
accumulation and/or metabolism of bacteria on the hard surfaces forms, however, the primary
cause of dental caries, gingivitis, periodontitis, peri-implantitis, and stomatitis.
Objectives: This systematic review aimed to evaluate critically the impact of surface
characteristics (free energy, roughness, chemistry) on the de novo biofilm formation, especially
in the supragingival and to a lesser extent in the subgingival areas.
Methods: An electronic Medline search (from 1966 until July 2005) was conducted applying
the following search items: ‘biofilm formation and dental/oral implants/surface characteristics’,
‘surface characteristics and implants’, ‘biofilm formation and oral’, ‘plaque/biofilm and
roughness’, ‘plaque/biofilm and surface free energy’, and ‘plaque formation and implants’.
Only clinical studies within the oro-pharyngeal area were included.
Results: From a series of split-mouth studies, it could be concluded that both an increase in
surface roughness above the Ra threshold of 0.2 mm and/or of the surface-free energy facilitates
biofilm formation on restorative materials. When both surface characteristics interact with
each other, surface roughness was found to be predominant. The biofilm formation is also
influenced by the type (chemical composition) of biomaterial or the type of coating. Direct
comparisons in biofilm formation on different transmucosal implant surfaces are scars.
Conclusions: Extrapolation of data from studies on different restorative materials seems to
indicate that transmucosal implant surfaces with a higher surface roughness/surface free
energy facilitate biofilm formation.

To cite this article:

Teughels W, Van Assche N, Sliepen I, Quirynen M.
Effect of material characteristics and/or surface
topography on biofilm development.
Clin. Oral Imp. Res. 17 (Suppl. 2), 2006; 68–81
r 2006 The Authors
Journal compilation r Blackwell Munksgaard 2006
Complexity of bacterial adhesion within
the oro-pharynx
In the oro-pharyngeal areas, a dynamic
equilibrium exists between the adhesion
capacity of microorganisms and a variety
of removal forces such as: swallowing,
frictional removal by diet, tongue and oral
hygiene, and the washing out by the sali-
vary and crevicular flow. Most pathogenic
organisms can only survive in the

68

oro-pharynx when they firmly adhere to a
non-shedding surface. The latter is clearly
illustrated by the spontaneous disappear-
ance of most pathogens after a full-mouth
tooth extraction (Danser et al. 1994) and/or
by the microbiological differences in peri-
implant flora between partially and fully
edentulous patients. In the latter, teeth and
their periodontal pocket serve as a reservoir
for pathogens (for a review, see Quirynen et
al. 2002).
The initial bacterial adhesion to non-
shedding surfaces, the first step in the
formation of a biofilm after the formation
of a conditioning film has been studied
extensively over the past decades in many
diverse areas, such as on solid surfaces in
the oral cavity, on biomaterials implanted
into the human body, on catheter surfaces,
in water pipes, on ship hulls, and in the
food industry. The adhesion process can be
regarded either from a biochemical or from
a physicochemical point of view.
The biochemical approach highlights the
specific interaction between complemen-
tary surface components (the specific li-
gand–receptor interactions, Dalton &
March 1998). Within the realm of cell–
cell interaction, recent advances suggest
that flagella, fimbriae, and other protein
receptors are essential for bacterial attach-
ment to surfaces. Gene expression changes
and intra- and interspecies cell–cell com-
munication further complicate the under-
standing of the process of adhesion and/or
biofilm formation.
Other researchers emphasized the non-
specific physicochemical mechanisms of
bacterial adhesion (Bakker et al. 2004).
They involve either a thermodynamic
model (based on the interfacial free energies
of liquids and interacting surfaces), or the
Derjaguin, Landau, Verwey, Overbeek
(DLVO) theory in which adhesion is re-
garded as the total sum of Lifshitz–Van der
Waals, acid–base, and electrostatic interac-
tions (the long-range forces). From a review
by Bos et al. (1999), it became obvious that
bacterial adhesion is unlikely ever to be
captured in one generally valid mechanism.
The complexity of the oral flora with
more than 500 species, together with the
presence of a pellicle, a dynamic variety in
availability of nutrients, temperature, and
humidity, and the large variety of shear
forces, renders a simple explanation of the
adhesion processes nearly impossible. Ad-
Teughels et al . Effect of material characteristics and/or surface topography
vanced technologies recently provided novel
insights into how dental plaque functions as
a biofilm (Marsh 2004). Confocal micro-
scopy confirmed that plaque has an open
architecture with channels and voids.
Within the biofilm, oral bacteria do not exist
as independent entities but function as a
coordinated, spatially organized, and fully
metabolically integrated microbial commu-
nity, whose properties are greater than the
sum of the component species.
Owing to the tremendous complexity of
the adhesion process and the fact that
many aspects are still under investigation,
this paper primarily aims to review the
impact of surface characteristics on biofilm
formation, especially from a clinical point
of view.
Biofilm as a community
Bacteria within dental plaque do not exist as
independent entities but rather function as a
coordinated, metabolically integrated micro-
bial community (Marsh & Bradshaw 1999;
Marsh & Bowden 2000). This community
life-style within dental plaque provides en-
ormous potential benefits to the participat-
ing organisms (Caldwell et al. 1997; Shapiro
1998; Marsh & Bowden 2000; Marsh 2005)
including: (i) a broader habitat range for
growth (the metabolism of early colonizers
alters the local environment, making condi-
tions suitable for attachment and growth of
later more fastidious species), (ii) an in-
creased metabolic diversity and efficiency
(molecules that are normally recalcitrant to
catabolism by individual organisms can be
broken down by the microbial consortia),
and (iii) an enhanced resistance to environ-
mental stress, antimicrobial agents, and the
host defences.
Recent studies suggest that the environ-
mental heterogeneity generated within bio-
films promotes accelerated genotypic and
phenotypic diversity that provides a form of
‘biological insurance’ that can safeguard
the ‘microbial community’ (Boles et al.
2004). This diversity can affect several
key properties of cells, including motility,
nutritional requirements, secretion of pro-
ducts, detachment, and biofilm formation.
The pellicle coating
When microorganisms and substratum sur-
faces are in an aqueous environment, in
which organic material is present (e.g. sea
water, milk, tear fluid, urine, blood or
69 |
saliva), they immediately (within seconds)
become covered with a layer of adsorbed,
organic molecules. This is commonly
called ‘conditioning film’, simply because
transport and adsorption of molecules to a
substratum proceed relatively fast com-
pared with that of microorganisms. This
conditioning film in the oral cavity,
called pellicle, consists of numerous com-
ponents including glycoproteins (mucins),
proline-rich proteins, phosphoproteins (e.g.
statherin), histidine-rich proteins, enzymes
(e.g. a-amylase), and other molecules that
can function as adhesion sites for bacteria
(receptors). The bacterial adhesion thus
occurs between a with pellicle-coated bac-
terium and a with pellicle-coated surface.
The mechanisms involved in pellicle
formation include electrostatic, van der
Waals, and hydrophobic forces. Studies of
early (2 h) pellicle on tooth enamel revealed
that for example its amino acid composi-
tion differs from that of saliva. This clearly
indicates that the pellicle is formed by a
selective adsorption of environmental
macromolecules. The physicochemical
surface properties of a pellicle, including
its composition, packing, density, and/or
configuration, are largely dependent on the
physical and chemical nature of the under-
lying hard surface (Lee et al. 1974; Baier &
Glantz 1978; de Jong et al. 1984; Fine et al.
1984; Ruan et al. 1986; Pratt-Terpstra et al.
1989, 1991; Rykke & Sonju 1991; Sipahi
et al. 2001). Thus, the characteristics of the
underlying hard surface are transferred
through the pellicle layers, and as such
will still have its influence on the initial
bacterial adhesion. Absolom et al. (1987)
even observed a clear relationship between
the type of proteins adsorbed in the pellicle
and the substratum surface free energy
(SFE) of the underlying surface. For exam-
ple, on polyethylene hydrophobicity gradi-
ents exposed to blood serum, less proteins
were absorbed at the hydrophobic end with
relatively more fibrinogen, while on the
hydrophilic end more albumin was present
(Rakhorst et al. 1999). Busscher et al (1995)
also observed that the detachment of ad-
hering bacteria could occur through a
cohesive failure within the pellicle.
Specific biochemical mechanisms of
bacterial adhesion
The bonding between bacteria and pellicle
is mostly mediated by specific extracellular
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
Teughels et al . Effect of material characteristics and/or surface topography
proteinaceous components (adhesins) of
the organism and complementary receptors
(i.e. proteins, glycoproteins, or polysac-
charides) on the surface (e.g. the pellicle),
and is species specific. These specific inter-
actions are in fact non-specific forces acting
on highly localized regions of the interact-
ing surfaces over distances smaller than
5 nm. Most bacteria possess several speci-
fic mechanisms for adherence (Whittaker
et al. 1996). Porphyromonas gingivalis
strains possess the armament to coaggre-
gate, to bind to saliva-coated hydroxyapa-
tite, to haemagglutinate, and to adhere to
and/or to invade epithelial cells. This bac-
terium also binds to several matrix mole-
cules, like fibronectin, fibrinogen, and
collagen, and produces proteases that may
promote adherence. Streptococcus gordonii
PK488 adheres to saliva-coated hydroxya-
patite and coaggregates with Actinomyces
naeslundii PK606, other streptococci, and
fusobacteria by different mechanisms.
Mutants of strain PK488 that fail to
coaggregate with PK606 retain the
lactose-inhibitable coaggregations with
streptococci and the lactose-noninhibitable
coaggregations with fusobacteria, and
bind to saliva-coated hydroxyapatite. Mul-
tiple adhesins on a given cell are likely to
mediate distinct interactions with different
surfaces, which can be animate or inani-
mate.
Streptococcal and actinomyces strain,
the early colonizers, bind specific salivary
molecules (Fachon-Kalweit et al. 1985;
Fives-Taylor & Thompson 1985; Mergen-
hagen et al. 1987). Streptococci (especially
Streptococcus sanguis), the principal early
colonizers, bind to acidic proline-rich pro-
teins and to other receptors in the pellicle
like a-amylase and sialic acid (Hsu et al.
1994; Scannapieco et al. 1995). Actino-
myces viscosus possesses fimbriae that
contains adhesins that specifically
bind to proline-rich proteins of the dental
pellicle (Mergenhagen et al. 1987; Gibbons
et al. 1988). Some molecules from the
pellicle (e.g. proline-rich proteins) evi-
dently undergo a conformational change
when they adsorb to the tooth surface,
so that new receptors become exposed.
Indeed, for example A. viscosus recognizes
cryptic segments of the proline-rich
proteins that are only available in
adsorbed molecules (Gibbons & Hay
1988; Gibbons et al. 1988). This provides
70 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
a microorganism with a mechanism for Non-specific physicochemical mechanisms
of bacterial adhesion
efficiently attaching to teeth and also offers
So far, no completely satisfactory picture
a molecular explanation for their sharp
has been proposed for the physicochemical
tropisms.
mechanisms involved in bacterial adhesion
After the formation of a monolayer on
to non-shedding surfaces (Morra & Cassi-
the surface, biofilm formation can start,
nelli 1997; Bos et al. 1999). The following
either by multiplication of adhering species
concept can help to understand most as-
and/or the adhesion of new species. From
pects of this adhesion process. In the for-
this stage on, new mechanisms are in-
mation of a biofilm to a non-shedding
volved, because each newly accreted cell
surface in an aqueous environment, such
itself becomes a nascent surface and there-
as the oral cavity, four well-defined stages
fore may act as a coaggregation bridge to
(Fig. 1) have been described (Busscher &
the next potentially accreting cell type that
Weerkamp 1987; Busscher et al. 1990; Van
passes by. At least 18 genera from the oral
Loosdrecht & Zehnder 1990; Van Loos-
cavity have shown some form of coaggrega-
drecht et al. 1990a, 1990b; Scheie 1994;
tion (Kolenbrander et al. 1993). Essentially
Bos et al. 1999). The same steps apply to
all oral bacteria possess surface molecules
the marine environment, pipe lines, cardi-
that foster some sort of cell-to-cell interac-
ovascular prostheses, air planes wings, etc.
tion (Kolenbrander & London 1993). This
process occurs primarily through the highly
Phase 1: transport to the surface
specific stereo-chemical interaction of pro-
The initial transport of a bacterium to the
tein and carbohydrate molecules located on
surface may occur through Brownian mo-
the bacterial cell surfaces in addition to the
tion (average displacement of 40 mm/h),
less specific interactions resulting from
through sedimentation of the bacterium
hydrophobic, electrostatic, and Van der
in the solution, through liquid flow
Waals forces (Kolenbrander 1989; Kolen-
(several orders of magnitude faster than
brander & London 1993). Fusobacteria
diffusion), or through active bacterial
coaggregate with all other human oral bac-
movement (chemotactic activity). Alterna-
teria, while veillonellae, capnocytophagae,
tively, microorganisms in suspension may
and prevotellae species preferably bind to
also be transported towards each other from
streptococci and/or actinomyces (Kolen-
microbial (co)aggregates.
brander & London 1993; Kolenbrander et
al. 1995; Whittaker et al. 1996). Most
Phase 2: initial adhesion
coaggregations among strains of different
This stage results in a weak and reversible
genera are mediated by lectin-like adhesins
adhesion of the bacterium via its interac-
and can be inhibited by lactose and
tion with the surface at a certain distance
other galactosides. The significance on
(50 nm) through long- and short-range
biofilm formation of coaggregation in
forces. The organisms will be attracted or
oral colonization has been documented in
repelled by the surface, depending on the
in vitro studies as well as in animal studies
resultant of the different non-specific inter-
(Bradshaw et al. 1998). Secondary
action forces. Two physicochemical ap-
colonizers (e.g. Prevotella intermedia, Pre-
proaches, initially considered distinctly
votella loescheii, Capnocytophaga spp.,
different, are available to describe microbial
Fusobacterium nucleatum, and P. gingiva-
adhesive interactions: the thermodynamic
lis) do not initially colonize clean tooth
and the DLVO approach.
surfaces but adhere to bacteria already in
the plaque mass (Kolenbrander & London a. The thermodynamic approach is based
1993). on the SFE of the interacting surfaces
In the saliva, each strain of early coloni- and does not include an explicit role for
zers becomes quickly coated with distinct electrostatic interactions. Before a bac-
molecules. Identical cells therefore can terium can come in direct contact with
agglutinate, which will lead to a microcon- a surface, the water film between the
centration and juxta-positioning of a parti- interacting surfaces has to be removed.
cular strain. Alternatively, growth of a The interaction energy for this process
particular accreted strain can lead to a can be calculated from the assumption
microcolony, coated with specific salivary that the interfaces between bacterium/
molecules. liquid (bl) and surface/liquid (sl) are
 Teughels et al . Effect of material characteristics and/or surface topography

terfacial free energy of adhesion for

bacteria (DGadh) is correlated with the
surface–bacterium interfacial free en-
ergy (gsb), the surface–liquid interfacial
free energy (gsl), and the bacterium–
liquid interfacial free energy (gbl). If
DGadh is negative (nature tends to
minimize free energy), adhesion is
thermodynamically favoured and will
proceed spontaneously.
b. The classical DLVO approach de-
scribes the interaction energies be-
tween surface and bacterium. When a
bacterium approaches a surface, it will
interact with that surface by means of
two forces: the Lifshitz–van der Waals
attractive forces (GA: the first force
becoming active at distances even
above 50 nm), and the electrostatic
repulsive forces (GF: available at a
closer distance). The latter force occurs
due to the formation, in water, of a
counter-charged layer, diffusely dis-
tributed around the particle, to neutra-
lize the negative charge of the
bacterium and of the surface (the elec-
trical double layer or Stern layer, Figs
1a and b). When this double layer
overlaps the double layer of the surface
(the pellicle coating confers a negative
charge to all surfaces), an electrostatic
interaction will take place. As both
surfaces have the same charge, this
electrostatic interaction is repulsive in
nature. The distance at which this
interaction appears depends on the
thickness of the double layers, which
themselves depend on the ionic charge
of the surface and the ionic concentra-
tion of the suspension medium.

DLVO have postulated that, above a

Fig. 1. (a) Schematic representation of the dynamic plaque formation process as a four-stage sequence: (I)
separation distance of 1 nm, the summa-
random transport of bacterium to the surface, (II) initial adhesion at secondary minimum (which often does not tion of the above-mentioned two forces
reach large negative values so that the adhesion is reversible), or directly at the primary minimum (with an describes the total long-range interaction
irreversible binding) depending on the resultant of the van der Waals attractive force (GA) and the electrostatic between bacterium and surface (Rutter &
repulsive force (GE), (III) attachment of bacterium to the surface by specific interactions after bridging the
Vincent 1984). Figure 1b shows the total
separation gap or after passing the energy barrier, (IV) colonization of the surface and biofilm formation
(primarily by cell dividing and by bacterial intra- and/or intergeneric coaggregation). (b) Long-range interaction
interaction energy (also called the total
between a negatively charged bacterium and a negatively charged surface according to the Derjaguin, Landau, Gibbs energy (GTOT ), as the result of this
Verwey, Overbeek (DLVO) theory (Rutter & Vincent 1984). The Gibbs energy of interaction (GTOT ) is summation of the above-mentioned forces
calculated, in relation to the separation gap (D), as the summation of the van der Waals force (GA) and the (GTOT ¼ GA þ GE), and in function of the
electrostatic interaction (GE). Electrostatic interactions start when the electrical double layers overlap each
distance between bacterium and surface.
other (see the upper part of the figure with T: solid surface (e.g. tooth) and C: bacterial cell). Adapted from
Busscher et al. (1990), Quirynen & Bollen (1995), Van Loosdrecht et al. (1990b).
For most bacteria, GTOT consists of a sec-
ondary minimum (where a reversible bind-
replaced by a surface/bacterium (sb) described by the formula (Absolom et ing takes place: 5–20 nm from the surface),
interface. The change in the interfacial al. 1983; Bellon-Fontaine et al. 1990): a positive maximum (an energy barrier B to
excess Gibbs energy upon adhesion is DGadh ¼ gsb  gsl  gbl in which the in- adhesion), and a steep primary minimum

71 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81

Teughels et al . Effect of material characteristics and/or surface topography
(located o2 nm away from the surface)
where an irreversible adhesion is estab-
lished. For bacteria in the mouth, the
secondary minimum does not frequently
reach large negative values (Van Loosdrecht
& Zehnder 1990), which means a ‘weak’
reversible adhesion (defined as a deposition
to a surface in which the bacterium con-
tinues to exhibit Brownian motion and can
readily be removed from the surface by
mild shear or by the bacterium’s own
mobility).
Both approaches have proven merits for
microbial adhesion, when certain collec-
tions of strains and species are considered.
They have, however, failed so far to yield a
generalized description of all aspects of
microbial adhesion valid for each and every
strain (Van Loosdrecht & Zehnder 1990;
Van Loosdrecht et al. 1990b). Van Oss et al.
(1986) therefore introduced a so-called ex-
tended DLVO theory. This theory consid-
ers four fundamental, non-covalent
interactions: Lifshitz–van der Waals, elec-
trostatic, Lewis acid–base and Brownian
motion forces. The acid–base interactions
are based on electron-donating and elec-
tron-accepting interactions between polar
moieties in aqueous solutions. The polar or
acid–base interfacial free energy balance
DGABadh is incorporated into the extended
DLVO approach by attributing a decay
function to this balance. The influence of
the acid–base interactions is enormous
when compared with electrostatic and Lif-
shitz–van der Waals interactions. However,
the acid–base interactions are also rela-
tively short ranged, and a close approach
between the interacting surfaces (less than
5 nm) is required before these forces can
become operative. This new concept has
been very useful for the prediction of bac-
terial adhesion in several in vitro experi-
ments (Liu & Zhao 2005).
Phase 3: attachment
After contact is established between bac-
terium and surface, either directly or via
bridging of the gap (fimbriae), a firm an-
chorage between bacteria and surface can
be established by specific interactions
(covalent, ionic, or hydrogen bonding).
After adhesion, most organisms also start
to secrete slime and embed themselves in a
slime layer, the glycocalix, which forms an
important virulence factor as it provides
72 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
protection against humoral and cellular
immune components.
Phase 4: colonization/plaque maturation
When the firmly attached microorganisms
start growing and newly formed cells re-
main attached, biofilms can develop. The
growth rate of sessile microorganisms has
been found to be partially depending on the
biomaterial involved (Barton et al. 1996a,
1996b). At this stage, other processes, in-
cluding quorum-sensing, start to play an
additional role.
On a rough surface, bacteria are better
protected against shear forces so that a
change from reversible-to-irreversible
bonding occurs more easily and more fre-
quently. The substratum SFE becomes im-
portant when the water film between the
interacting surfaces has to be removed
before short-range forces (direct contact or
bridging) can be involved.
Material and methods
Search strategy
A Medline search was conducted, and
work from 1966 until July 2005 was in-
cluded in the systematic review. The fol-
lowing search items were explored:
‘biofilm formation and dental/oral im-
plants’, ‘biofilm formation and surface
characteristics’, ‘surface characteristics
and implants’, ‘biofilm formation and
oral’, ‘plaque or biofilm and roughness’,
‘plaque or biofilm and surface-free energy’,
and ‘plaque formation and implants’. Only
clinical studies within the oro-pharyngeal
area have been considered. Studies were
only included if they were controlled
(either via a split-mouth design or a parallel
group concept). Thirty-six studies from an
initial yield of 374 studies were selected.
No further validity analysis had been per-
formed.
The heterogeneity of the studies and
outcome variables rendered a meta-analysis
impossible.
Results and discussion
Surface roughness and biofilm formation
Table 1 summarizes the data of 24 papers
dealing with the effect of surface roughness
on supra/subgingival plaque formation in
vivo. Nearly all papers had a randomized,
split-mouth, controlled design and were
prospective. The following general conclu-
sions can be drawn:
 rougher surfaces (crowns, implant abut-
ments, and denture bases) accumulate
and retain more plaque (applying para-
meters such as thickness, area, and
colony-forming units),
 after several days of undisturbed plaque
formation, rough surfaces harbour a
more mature plaque characterized by
an increased proportion of rods, motile
organisms, and spirochetes,and
 as a consequence of the former, tooth
surfaces with rough surfaces are more
frequently surrounded by an inflamed
periodontium, characterized by a
higher bleeding index, an increased cre-
vicular fluid production, and/or an
increased inflammatory infiltrate.
The clinical impact of surface roughness
is, for example, illustrated in Fig. 2. It
shows the clinical picture of two
strips that were divided into two halves: a
rough (Ra ¼ 2 mm) and a smooth region
(Ra ¼ 0.1 mm). Whereas the smooth regions
were only for 1/4 covered with plaque, the
rough parts were completely colonized
within 3 days of undisturbed plaque forma-
tion. The impact of surface roughness be-
comes especially important when larger
shear forces are active (Hannig 1999).
The impact of surface roughness of oral
implants was explored in a series of studies.
A pilot study (parallel groups) reported a
faster supragingival plaque formation on
titanium abutments when compared with
teeth (Quirynen 1986). In a second study,
plaque formation on standard and rough-
ened abutments (Ra of 0.3 and 0.8 mm,
respectively) was evaluated after 3 months
of habitual oral hygiene (Quirynen et al.
1993). Supragingivally, rough abutments
harboured significantly fewer cocci (64%
vs. 81%), which is indicative of a more
mature plaque. Subgingivally, rough sur-
faces harboured 25
more bacteria (espe-
cially when all plaque was scraped away
from the abutment instead of using paper-
spoints), with a slightly lower density of
cocci. Two later studies examined the ef-
fect of smoothening the abutment surface.
A smoothening below an Ra ¼ 0.2 mm
showed no further significant changes,
either in the total amount of or in the
pathogenicity of adhering bacteria (Bollen
 Table 1. Clinical studies in humans on the influence of surface roughness on biofilm formation and periodontal health, sorted by year of publication, for restorative materials and oral
implants separately
Authors Study design Sup/sub Surface Time OH nP Roughness Biofilm parameters Crev
range
Area CFU Flora Gi Fluid Infection

Restorative materials
Larato (1972) Pros CCT spl b Class V composite restoration with supra or 2m H 59 NR
subgingival margin
Subgingival " "
Trivedi & Talim (1973) Pros CCT Supr Class V restoration # materials, different protocols, 2m H 54 NR
tooth extracted þ biopsy
Rougher "
Mörmann et al. (1974) Pros CCT spl b Proximal inlays in contra-lateral teeth polished vs. 3m H 8
roughened
Roughened " S ¼
Weitman & Eames (1975) Pros CCT b Class V composite restoration vs. contra-lateral tooth 3d + NR
Restored "
Gildenhuys & Stallard (1975) Pros CCT spl Supr Gold crowns adjoining teeth: polished vs. sand-blasted 30 h + ? NR
interproximal surface
Sand-blasted " S
Blank et al. (1979) Pros CCT spl b Class V composite restoration vs. contra-lateral tooth 1 y þþþ 20 NR
Restored " NS " NS
Keenan et al. (1980) Pros CCT spl Supr Retainer þ cast gold sets þ 6 # surface finishes 72 h + 10 NR
4 Rough " S
De Wet & Ferreira (1980) Pros CCT spl Supr Partially glazed class IV composite restorations 10 d + 100 Ra: 0.2–2.5
Rough part " S
Smales (1981) Pros CCT spl Supr Artificial class V restorations in dentures, # materials 3wþ H 10 Ra: 0.1–2.7
n
2d + 4 Rough  "
Shafagh (1986) Pros CCT spl Supr Two adjacent cast gold crowns # finishing  72 h + 10 NR
Rougher " S
Budtz-Jorgensen et al. (1986) Pros CCT spl – Denture fitting surface-glazed vs. non-glazed half 1w ? 21 NR
Non-glazed " S " S " s yeast
Van Dijken et al. (1987a) Pros Parallel groups b Class III composite, # materials: 1 vs. 4y H 42 NR
3–4 years old/vs. tooth

73 |
Composites " S " S " S
Van Dijken et al. (1987b) Pros Parallel groups b Class III composites 3 # materials per 7d + 18 NR
neighbouring site vs. tooth
Composites " " S
Scheutzel (1989) Pros CCT spl – Denture base surface-glazed vs. coated 6m ? 150 NR
surface ( ¼ rougher)
Coated " S
Nakazato et al. (1989) Pros CCT spl Supr Stent with 6 disks of # material, SFE ¼ ,  48 h + 2 Ra: 0.1–0.9
but different Ra Rough 4 h " NS w ¼
Rough 48 h ¼ ¼
Quirynen et al. (1990) Pros CCT spl Supr De novo plaque growth on strips 6d + 12 Ra: 0.1–2.1
(# SFE & Ra 0.1–2.3 mm ) glued to teeth
4 Rough z S " 4 Rods
Siegrist et al. (1991) Pros Cross-over Supr Test facings (# materials) from pontics of bridges  24 h + 3 NR
4 Rough " S ¼ y
Gatewood et al. (1993) Pros CCT spl b In pockets  6 mm, pieces of # material  10 d + 10 NR
glued (cementum vs. ps Ti vs. HA) ¼ Rough z ¼ z
Rimondini et al. (1997) Pros CCT spl – Stent with Ti disks with 3 # polishing techniques 24 h + 8 Ra: 0.1–2.1
Rougher disk " S 4 Rods

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81

Teughels et al . Effect of material characteristics and/or surface topography
Teughels et al . Effect of material characteristics and/or surface topography

no plaque control; H, habitual oral hygiene; þ þ þ , optimal plaque control; nP, number of patients; roughness, surface roughness either NR, not reported; Ra values, rougher sites; biofilm parameters with area,
full prosthesis; FPP, fixed partial prosthesis; Ti, titanium; ps, plasma sprayed; HA, hydroxyapatite); time, duration study in h, hours; d, days; w, weeks; m, months; y, years; OH, oral hygiene performance with +,
Pros, prospective; retro, retrospective; CCT, controlled clinical trial; spl, split-mouth; sup/sub, supra or subgingival area examined or b:both; surface, test surfaces and summary of experimental set-up (FFP, fixed

plaque index or extension parameters; CFU, colony-forming units; flora, data on composition of plaque; Gi, gingivitis index; Crev fluid, crevicular fluid measurements; infection, parameters on inflammation
et al. 1996; Quirynen et al. 1996). An Ra

Infection
value of 0.2 mm was therefore suggested as

" S
a threshold surface roughness, below
which bacterial adhesion cannot be reduced
Fluid

further (Bollen et al. 1997). These studies

failed to demonstrate significant differ-
" S
Crev

Gi

s " mutans ences in the proportion or the detection

frequency of potentially pathogenic species
between the different abutment surfaces.
o cocci

ococci
¼ nn
Flora

Key pathogens like P. gingivalis, P. inter-

¼
25
" k
media and F. nucleatum were always
found in comparable proportions on all
Biofilm parameters

" Ns
" S

surfaces. The inter-patient variation, how-

CFU

ever, was of a greater magnitude.

" NS ww These observations were further con-
" S

" S
Area

firmed by an in vivo study of Rimondini

et al. (1997), who examined initial supra-
Ra: 0.05–0.51

Ra: 0.05–0.21
Treated site

Rough supr

Rough supr
4 Rough z

Rough sub

Rough sub
Roughness

Ra: 0.4–0.8

gingival plaque formation on titanium spe-

Sa: 0.3–1.8

Rough

cimens (first 24 h) by scanning electron

range

19 NR

microscopy (SEM, Ra ranging from 0.1 to

2.4 mm). Whereas smooth surfaces hosted
9

6
nP

comparable amounts of bacteria, the rough

surface harboured significantly higher
OH

numbers. Two papers reported contradic-

Besides roughness, other parameters also seem to play a role (e.g. antibacterial activity of material), only 2 patients.
3m

3m

tory observations on the impact of surface

Time

24 h

4w
6y

roughness. Gatewood et al. (1993) glued

small pieces (6.5
2 mm) of teeth (with a
Replacement 5 Ti abutments: FFP prosthesis by new
FPP supported by 4 Ti abutments with # roughness

smooth enamel part and a fairly rough part

Unilaterally direct composite additions treated vs.

of cementum) and implants (with a smooth

Four disks of # material # SFE & Ra glued on

collar and a plasma-sprayed endosseous

surface) in  6 mm deep pockets (21
(data with S, statistically significant; NS, not statistically significant; ¼ , means no difference).
prosthesis by new smooth/rough one
Replacement 2 Ti abutments: FFP/FPP

Is especially patient-dependent, partially edentulous patients have more pathogenic flora.

days post-scaling) in such a way that the

smooth part remained supragingivally. The
test pieces were removed after several days
and SEM pictures were made to analyse
buccal surface teeth

smooth/rough ones

subgingival plaque maturation. No signifi-

cant differences could be detected between
intact surface

the cementum and the rough implant sur-

Sup/sub Surface

faces. The latter could, however, have been

zSurface roughness overrules the effect of surface free energy.

expected because the test pieces were in-

serted into pockets with an established
yQuantitative and not necessarily qualitative differences.
Supr

Supr

Supr

microbiota and all test surfaces were fairly

b

rough. Wennerberg et al. (2003) followed

the plaque growth and development of
gingivitis in patients with  5 titanium
Retro CCT spl

CCT spl

CCT spl

CCT spl

CCT spl
Study design

zAll three surfaces had similar features.

abutments with varying degrees of rough-

ness. They could not find significant dif-
Pros

Pros

Pros

Pros

ferences in plaque and bleeding indices.

kTotal amount on abutment.

The latter might be explained by the ap-

plied parameters (present/absent), by the
wwVery rough parameter.
Wennerberg et al. (2003)

oral hygiene of subjects (low plaque scores

Quirynen et al. (1993)

Quirynen et al. (1996)

wOnly two patients.

Peumans et al. (1998)
Table 1. Continued

Tanner et al. (2005)

in general), and by the patient selection

(fully edentulous patients). However, when
Oral implants

the turned implants in the latter study

Authors

were compared with the roughest samples,

the incidence of bleeding or plaque was
nn
n

found to be 2.5
higher.

74 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81


Fig. 2. Photographs showing the clinical impact of surface roughness and surface-free energy (SFE) on de novo
plaque formation. Two small strips were glued to the central upper incisors of a patient who refrained from oral
hygiene for 3 days. Each strip was divided into two halves: a rough region (Ra 2 mm) located mesially, and a
smooth region (Ra 0.1 mm) located distally. The left strip was cellulose acetate (medium SFE: 58 erg/cm2) and
the right strip was Teflon (low SFE: 20 erg/cm2). Plaque was disclosed with 0.5% neutral red solution. The
smooth regions show a decrease in biofilm formation due to the low SFE; the rough regions demonstrate the
predominance of surface roughness, i.e. more plaque and no difference between the two materials. Sample from
the clinical study of Quirynen et al. (1990).
The impact of surface roughness on the
biofilm formation can be explained by
several factors:
 the initial adhesion of bacteria prefer-
ably starts at locations where they are
sheltered against shear forces so that
they find the time to change from
reversible to irreversible attachment,
 roughening of the surface increases the
area available for adhesion by a factor
2–3, and
 rough surfaces are difficult to clean,
resulting in a rapid re-growth of the
biofilm by multiplication of remaining
species, rather than by recolonization
(for a review, see Quirynen & Bollen
1995).
Only one RCT study (parallel groups)
compared the subgingival plaque formation
along different implant systems over a
period of 6 months (Mombelli et al.
1995). Both the collar of ITI and abutment
Brånemark implant surfaces showed a si-
milar distribution pattern of periodonto-
pathogens. Several papers compared the
microbiota of teeth and implants within
partially edentulous patients (Lekholm et
al. 1986; Apse et al. 1989; Quirynen &
Listgarten 1990; Koka et al. 1993; Leon-
hardt et al. 1993; Kohavi et al. 1994;
Mombelli et al. 1995; Mengel et al. 1996;
Papaioannou et al. 1996; Gouvoussis et al.
1997; Sbordone et al. 1999; Hultin et al.
2000, 2002) and consistently reported a
striking similarity between both abutment
types. Two recent studies (De Boever & De
Boever 2006; Quirynen et al. 2006) ex-
Teughels et al . Effect of material characteristics and/or surface topography
plored the ‘early’ colonization of the pris-
tine peri-implant pocket (after placement
of one-stage implant or connection of abut-
ment to a two-stage implant) in partially
edentulous patients. Both studies indicated
a rapid colonization; within 2 weeks, the
subgingival area around implants was colo-
nized by similar numbers of bacteria (in-
cluding significant proportions of
periopathogens) as observed along the
neighbouring teeth. Again, a striking in-
tra-subject similarity in the composition of
the subgingival flora from teeth and im-
plants was observed. The quick coloniza-
tion of the peri-implant pocket is in
agreement with previous observations by
Mombelli et al. (1988), who followed the
initial colonization of implants in fully
edentulous patients and also reported a
nearly complete maturation 1 week after
insertion.
SFE and biofilm formation
Table 2, summarizing eight prospective in
vivo RCT studies, illustrates the signifi-
cant correlation between the substratum
SFE (also called wettability) and its pla-
que-retaining capacity. It is obvious that
surfaces with a higher SFE are more prone
to bacterial adherence. Glantz (1969) was
the first to recognize this in vivo. When he
followed undisturbed supragingival biofilm
formation on test surfaces of different free
energies – mounted on a partial fixed bridge
– he detected a ‘positive’ correlation be-
tween substratum SFE and the weight of
accumulated plaque (measured at days 1, 3,
and 7). Rölla et al. (1991) demonstrated
75 |
that the application of a silicone oil to
teeth, which lowered their SFE, resulted
in a significant reduction in plaque forma-
tion. Quirynen and co-workers studied the
influence of SFE on undisturbed plaque
growth in humans over a 9-day period
and reported that hydrophobic surfaces
(e.g. teflon) harboured 10
less plaque
than hydrophilic ones (enamel) (Quirynen
et al. 1989, 1990). The latter was well
confirmed in animal studies (Van Dijk
et al. 1987).
The effect of substratum SFE on supra
and subgingival plaque maturation around
implants was investigated by comparing 3-
month-old plaque from abutments with
either a high (titanium) or a low (teflon
coating) SFE (Quirynen et al. 1993). Low-
SFE substrata harboured a significantly less
mature plaque supra – as well as subgingiv-
ally, characterized by a higher proportion of
cocci and a lower proportion of motile
organisms and spirochetes.
These qualitative and quantitative differ-
ences clearly illustrate that the impact of
the substratum SFE remains after the pel-
licle formation, even though the latter
had a homogenizing effect in terms of the
remaining SFE (convergence to 50 mJ m  2,
a moderate hydrophobic character (Van Pelt
et al. 1983; de Jong et al. 1984; Van Dijk et
al. 1987; Sipahi et al. 2001). Thus, the SFE
properties are transferred through the ab-
sorbed protein layer (Sipahi et al. 2001).
The surface SFE also had an impact on
the SFE of the colonizing bacteria. Surfaces
with a low SFE were preferably colonized
by bacteria with a low afe, whereas the
opposite was observed for surfaces like e.g.
titanium or enamel with a higher SFE
(Weerkamp et al. 1988; Mabboux et al.
2004). Moreover, colonies from a specific
strain, collected form surfaces with a low
SFE, even had a lower SFE than colonies of
the similar strain, collected from a surface
with a higher SFE (Weerkamp et al. 1989).
The latter suggests a bacterial selection by,
or adaptation to, the surfaces, up to and
even within the species level.
In some clinical and in vitro trials, it had
been observed that the reduced biofilm
formation on surfaces with a low SFE could
partially be explained by a low binding
strength between bacteria and substratum,
probably because of a cohesive failure
within the conditioning layer (Christersson
et al. 1989; Busscher et al. 1995). The
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
76 |
Table 2. Clinical studies in humans on the influence of surface free energy on biofilm formation and periodontal health, sorted by year of publication, for restorative materials and oral
implants separately
Authors Study design Sup/sub Surface Time OH nP SFE Biofilm parameters

Area CFU Flora

Restorative materials
Glantz (1969) Pros CCT spl Supr De novo plaque formation on test 7d + 4 SFE supr S "
surfaces with # SFE

Quirynen et al. (1989) Pros CCT spl Supr De novo plaque formation on strips 9d + 6 23–88 erg/cm2
(# SFE) glued to teeth
4 SFE supr S "
Weerkamp et al. (1989) Pros CCT spl Supr De novo plaque growth on strips 3d 4 Rough S " S " rods
(# SFE  Ra 0.1–2.3 mm ) glued to teeth
4 SFE S " (
5) S " SFE
Quirynen et al. (1990) Pros CCT spl Supr De novo plaque growth on strips 6d + 12 23–58 erg/cm2

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81

(# SFE & Ra 0.1–2.3 mm ) glued to teeth 4 SFE S " ¼
Rölla et al. (1991) Pros Supr SFE reduction of teeth via application of oil 4 SFE supr S "
Olsson et al. (1992) Pros CCT spl Supr Ceramic crowns (untreated vs. hydro-) 7d + 1
Phobized vs. polyethylene oxide film 4 SFE supr " " Actinomyces mutans
Everaert et al. (1999) Pros CCT spl l Partially surface-modified voice prosthesis 8w 15 . . . erg/cm2
4 SFE S " S " CFU S " yeast
Oral implants
Quirynen et al. (1993) Pros CCT spl b Replacement 2 abutments: FFP/FPP ti vs. 3m H 9 23–80 erg/cm2
Teughels et al . Effect of material characteristics and/or surface topography

teflon surface Ra: Ti 0.8, tefl 5.3 mm

4 SFE supr S " rods, s " spir
4 SFE sub NS " (x5) " [path]

Pros, prospective; CCT, controlled clinical trial; spl, split-mouth; sup/sub, supra or subgingival area examined; b, both; surface, test surfaces and summary of experimental set-up (FFP, fixed full prosthesis; FPP,
fixed partial prosthesis; Ti, titanium; tefl, teflon); time, duration study in d, days; m, months; OH, oral hygiene performance with +, no plaque control; H, habitual oral hygiene; nP, number of patients; SFE,
surface free energy (NR, not reported); biofilm parameters with area, plaque index or extension parameters; CFU, colony-forming units; flora, data on composition of plaque. Gingivitis indices and data on
crevicular fluid or degree of inflammation were not available; S, statistically significant; NS, not statistically significant; ¼ , means no difference.










1984).
and SFE
1984),
1985),
1986),
& Reid 1990),
previous phenomena.

teria (Harkes et al. 1992),

has a universal value such as for:

to solid substrata (Crisp et al. 1985),

aircraft wings (Siochi et al. 1987), and

ium to soil particles (Stenstrom 1989).

SFE, glued to a tooth surface. Each strip

angle; and for surfaces with initial contact
reflect the SFE has been studied exten-
the adhesion of catheter-associated bac-
latter will increase the detachment of ad-

polymer strips with low and medium

the adhesion of uropathogens to poly-

vivo by Quirynen et al. (1990). They fol-

angles between 601 and 861, surface rough-
is below 601 (e.g. enamel), surface rough-
smooth surface: if the initial contact angle
sively. Changes in solid surface Ra below
resulting contact angles of droplets that
the adhesion of Salmonella typhimur-
The influence of the substratum SFE, for
terial retention, being the resultant of the
and detachment, but prefer the term bac-

lowed undisturbed plaque formation on

meters (SFE and roughness) on supragingi-
val plaque formation has been examined in
The ‘relative’ importance of both para-
ening has no influence (Busscher et al.
roughening will further increase this
initial contact angle is above 861, surface
ening will further decrease this angle; if the
above 0.1 mm the effect depends on the
0.1 mm, have no effect on contact angle;
the attachment of insect residues to
the binding strength of green algae to
to solid surfaces (Fletcher & Pringle
mer materials of catheters (Hawthorn

the attachment of freshwater bacteria

wall reconstruction (Schmitt et al.
the colonization of vascular prostheses
binding strength and facility of adhesion,
no longer speak about bacterial adhesion
hering bacteria. Therefore, several authors

The effect of surface roughening on the

Interaction between surface roughness
several surfaces (Fletcher & Baier
the adhesion of mussels and barnacles
or prosthetic materials for abdominal

initial contact angle as measured on a

 Teughels et al . Effect of material characteristics and/or surface topography

with +: no plaque control; H, habitual oral hygiene; nP, number of patients; biofilm parameters with area, plaque index or extension parameters; CFU, colony-forming units; flora, data on composition of
hydroxyapatite; Y-TZP, tetragonal zirconia polycrystals stabilized with yttrium; TiN, titanium nitride; ZrN, zirconium nitride); time, duration of study in h: hours, d: days, y: years; OH, oral hygiene performance
had a smooth (Ra 0.1 mm) and a rough

Metabolic activity
part (Ra42 mm). After 3 days of undis-

ZrN ¼ TiNoTi
turbed plaque formation, significant inter-

Pros, prospective; CCT, controlled clinical trial; spl, split-mouth; sup/sub, supra or subgingival area examined or b: both; surface, test surfaces and summary of experimental set-up (Ti, titanium; HA,
Ti S4rods
substrata differences were observed on

Flora
the smooth regions, while the rough

¼
regions of the strips were nearly all

plaque. Gingivitis indices and data on crevicular fluid or degree of inflammation were not available. S, statistically significant; NS, not statistically significant; ¼ , means no difference.
completely covered with plaque (Fig. 2).

s ZrNoTiNoTi
Table 3. Clinical studies in humans on the influence of different implant materials with similar surface roughness on biofilm formation and periodontal health

AmalgamoTi
Surface roughening resulted for both mate-
rials in a fourfold increase in plaque forma-
tion (plaque extension as well as thickness)
CFU
Biofilm parameters

¼ for both polymers. Surface roughness

seems prominent towards SFE where
Y-TZPoTi

S TiNoTi
bacterial adhesion is concerned. Similar

ZroTi
Area

observations were made by Tanner et al.

¼

(2005).
nP

10

10
6

Chemical composition of the surface

Table 3 summarizes the data of seven
OH

+
clinical RCT studies on the impact of
H

different potential implant surfaces on in

 72 h

 14 d

vivo biofilm formation. Even though the

1 y
Time

24 h

24 h

60 h

24 h

surfaces had similar roughness characteris-

tics, these RCT studies clearly highlighted
significant differences both in the amount
Stent with pieces of Ti, HA, or amalgam Ra: 0.20–0.35

13
4 mm implant mounted on splint per quadrant:

OD patient: 2# abutments Ti – ceramic (Prozyr) Ra:

as well as in the composition of the flora on

Stent with disks of Ti or CerAdapt Ra: 0.6 and 0.7

different implant/abutment surfaces. This

Stent with disks of Ti or Zirconium oxide per

can be explained by the antibacterial prop-

(as-fired or rectified), Ra: 0.2, 0.2 and 0.04

Coated glass sheets mounted on splint

erties of some materials. Titanium for ex-

ample has a bacteriostatic effect on oral
bacteria (Bundy et al. 1980; Leonhardt &
Stent with disks of Ti or Y-TZP

quadrant: Ra: 0.73 and 0.76

Ti vs. TiN, Ra: 0.76 and 0.79

Dahlen 1995), although some others failed

0.2–0.06 mm, respectively

to prove such an effect (Joshi & Eley 1988;

TiN vs. ZrN vs. pure Ti

Elagli et al. 1992).

Recently, several modifications have
been suggested in order to increase the
Surface

antimicrobial capacity of titanium. These

include the following:

 the photocatalytic bactericidal effect of

Sup/sub

anastase titanium dioxide (TiO2) under

Supr

Supr

Supr

Supr

Supr

Supr

Supr

ultraviolet A illumination, added onto

commercially pure titanium surfaces
via plasma source ion implantation
CCT spl

CCT spl

CCT spl

CCT spl

CCT spl

CCT spl

CCT spl

(Suketa et al. 2005); a photocatalyst

Study design

can decompose various organic com-

pounds by generating active-oxygen
Pros

Pros

Pros

Pros

Pros

Pros

Pros

species such as OH, HO 2 , HO2, and

H2O2,
 the dry ion implantation of F þ on
Groessner-Schreiber et al. (2004)

titanium (Yoshinari et al. 2001),

 anodized titanium being discharged in
Leonhardt et al. (1995)

Rimondini et al. (2002)

Quirynen et al. (1996)

Rasperini et al. (1998)

NaCl resulting in Ti–Cl, which exhibit

Scarano et al. (2003)

Scarano et al. (2004)

high antibacterial activity, and

 antibiotics incorporated into the tita-
nium surface (Parvizi et al. 2004).
Authors

In vitro these modification look very

promising, but their efficiency in clinic

77 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81

Teughels et al . Effect of material characteristics and/or surface topography
still has to be proven. When antibiotics
are concerned, other side-effects such
as microbial resistance have to be
considered.
The implant–abutment fit
The interstitia between implant compo-
nents, especially those located subgingiv-
ally, offer an ideal environment for de novo
plaque formation and/or for plaque reten-
tion during cleaning. The size of the gap
between implant and abutment of nine
different systems, including those with
conical interfaces, was found to range be-
tween 1 and 10 mm (Jansen et al. 1997) and
49 mm (Binon et al. 1992) depending on
whether or not the rounded edges of the
abutment margin were included. Although
the discrepancies of these prefabricated
References
Absolom, D.R., Lamberti, F.V., Policova, Z., Zingg,
W., van Oss, C.J. & Neumann, A.W. (1983)
Surface thermodynamics of bacterial adhesion.
Applied and Environmental Microbiology 46:
90–97.
Absolom, D.R., Zingg, W. & Neumann, A.W.
(1987) Protein adsorption to polymer particles:
role of surface properties. Journal of Biomedical
Materials Research 21: 161–171.
Apse, P., Ellen, R., Overall, C. & Zarb, G. (1989)
Microbiota and crevicular fluid collagenase activ-
ity in the osseointegrated dental implant sulcus: a
comparison of sites in edentulous and partially
edentulous patients. Journal of Periodontal
Research 24: 96–105.
Baier, R.E. & Glantz, P.O. (1978) Characterization
of oral in vivo films formed on different types of
solid surfaces. Acta odontologica Scandinavica
36: 289–301.
Bakker, D.P., Postmus, B.R., Busscher, H.J. &
van der Mei, H.C. (2004) Bacterial strains
isolated from different niches can exhibit different
patterns of adhesion to substrata. Applied
and Environmental Microbiology 70: 3758–
3760.
Barton, A.J., Sagers, R.D. & Pitt, W.G. (1996a)
Bacterial adhesion to orthopedic implant poly-
mers. Journal of Biomedical Materials Research
30: 403–410.
Barton, A.J., Sagers, R.D. & Pitt, W.G. (1996b)
Measurement of bacterial growth rates on poly-
mers. Journal of Biomedical Materials Research
32: 271–278.
Bellon-Fontaine, M.N., Mozes, N., van der Mei,
H.C., Sjollema, J., Cerf, O., Rouxhet, P.G. &
Busscher, H.J. (1990) A comparison of thermo-
dynamic approaches to predict the adhesion of
dairy microorganisms to solid substrata. Cell
Biophysics 17: 93–106.
Binon, P.P., Weir, D.J. & Marshall, S.J. (1992) Sur-
face analysis of an original Branemark implant
78 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
parts are significantly smaller compared
with those of dental restorations (ranging
from 50 to 150 mm), it still allows micro-
bial leakage (Wahl et al. 1992; Quirynen &
van Steenberghe 1993; Quirynen et al.
1994; Jansen et al. 1997). This microleak-
age is comparable for different implant
systems and decreases significantly when
the closing torque is increased (Gross et al.
1999). As observed by Ericsson et al. (1995)
in the Labrador dog model, bacterial leak-
age results in an inflammatory cell infil-
trate (called abutment ICT) in the peri-
implant mucosa at the borderline between
abutment and implant, irrespective of the
oral hygiene. The connection between the
abutment and the prosthetic supra-struc-
ture (sometimes located subgingivally in
order to improve aesthetics) shows even
and three related clones. International Journal of
Oral & Maxillofacial Implants 7: 168–175.
Blank, L.W., Caffesse, R.G. & Charbeneau, G.T.
(1979) The gingival response to well-finished
composite resin restorations. Journal of Prosthetic
Dentistry 42: 626–632.
Boles, B.R., Thoendel, M. & Singh, P.K. (2004) Self-
generated diversity produces ‘‘insurance effects’’
in biofilm communities. Proceedings of the Na-
tional Academy of Sciences of the USA 101:
16630–16635.
Bollen, C.M., Lambrechts, P. & Quirynen, M.
(1997) Comparison of surface roughness
of oral hard materials to the threshold
surface roughness for bacterial plaque retention:
a review of the literature. Dental Materials 13:
258–269.
Bollen, C.M., Papaioanno, W., Van Eldere, J., Sche-
pers, E., Quirynen, M. & van Steenberghe, D.
(1996) The influence of abutment surface rough-
ness on plaque accumulation and peri-implant
mucositis. Clinical Oral Implants Research 7:
201–211.
Bos, R., van der Mei, H.C. & Busscher, H.J. (1999)
Physico-chemistry of initial microbial adhesive
interactions – its mechanisms and methods.
FEMS Microbiology Reviews 23: 179–230.
Bradshaw, D.J., Marsh, P.D., Watson, G.K. & Alli-
son, C. (1998) Role of Fusobacterium nucleatum
and coaggregation in anaerobe survival in plank-
tonic and biofilm oral microbial communities
during aeration. Infection and Immunity 66:
4729–4732.
Budtz-Jorgensen, E. & Kaaber, S. (1986) Clinical
effects of glazing denture acrylic resin bases using
an ultraviolet curing method. Scandinavian Jour-
nal of Dental Research 94: 569–574.
Bundy, K.J., Butler, M.F. & Hochman, R.F. (1980)
An investigation of the bacteriostatic properties of
pure metals. Journal of Biomedical Materials
Research 14: 653–663.
larger discrepancies (Binon et al. 1992),
especially for cemented restorations (Keith
et al. 1999).
Conclusion
Surface roughness and to a lesser extent
SFE have a significant impact on the bio-
film formation. The composition of bio-
materials per se also influences the
biofilm. As these surface features also
depict the quality of the soft tissue sealing,
they have to be handled with caution in
order to prevent infections. This applies
especially to the oral environment, where
the dental plaque forms a constant threat
for periodontitis and peri-implantitis, in
susceptible individuals.
Busscher, H.J., Bos, R. & van der Mei, H.C. (1995)
Initial microbial adhesion is a determinant for the
strength of biofilm adhesion. FEMS Microbiology
Letters 128: 229–234.
Busscher, H.J., Sjollema, J. & van der Mei, H.C.
(1990) Relative importance of surface free energy
as a measure of hydrophobicity in bacterial adhe-
sion to solid surfaces. In: Doyle, R.J. & Rosen-
berg, M., eds. Microbial Cell Surface
Hydrophobicity, 335–359. Washington, DC:
American Society for Microbiology.
Busscher, H.J., Vanpelt, A.W.J., Deboer, P., Dejong,
H.P. & Arends, J. (1984) The effect of surface
roughening of polymers on measured contact
angles of liquids. Colloids and Surfaces 9:
319–331.
Busscher, H.J. & Weerkamp, A.H. (1987) Specific
and nonspecific interactions in bacterial adhesion
to solid substrata. FEMS Microbiology Reviews
46: 165–173.
Caldwell, D.E., Wolfaardt, G.M., Korber, D.R. &
Lawrence, J.R. (1997) Do bacterial communities
transcend Darwinism? In: Jones, J.G., ed. Ad-
vances in Microbial Ecology, 105–191. New
York: Plenum Press.
Christersson, C.E., Dunford, R.G., Glantz, P.O. &
Baier, R.E. (1989) Effect of critical surface tension
on retention of oral microorganisms. Scandina-
vian Journal of Dental Research 97: 247–256.
Crisp, D.J., Walker, G., Young, G.A. & Yule, A.B.
(1985) Adhesion and substrate choice in mussels
and barnacles. Journal of Colloid and Interface
Science 104: 40–50.
Dalton, H.M. & March, P.E. (1998) Molecular
genetics of bacterial attachment and biofouling.
Current Opinion in Biotechnology 9: 252–255.
Danser, M.M., van Winkelhoff, A.J., de Graaff, J.,
Loos, B.G. & van, d.V. (1994) Short-term effect of
full-mouth extraction on periodontal pathogens
colonizing the oral mucous membranes. Journal
of Clinical Periodontology 21: 484–489.

De Boever, A.L. & DeBoever, J.A. (2006) Erly
colonization of non-submerged dental implants
in patients with a history of advanced aggressive
periodontitis. Clinical Oral Implants Research
17: 8–17.
de Jong, H.P., de Boer, P., van Pelt, A.W., Busscher,
H.J. & Arends, J. (1984) Effect of topically applied
fluoride solutions on the surface free energy of
pellicle-covered human enamel. Caries Research
18: 505–508.
de Wet, F.A. & Ferreira, M.R. (1980) The durability
of dental glazes. Journal of Prosthetic Dentistry
44: 300–306.
Elagli, K., Neut, C., Romond, C. & Hildebrand,
H.F. (1992) In vitro effects of titanium powder on
oral bacteria. Biomaterials 13: 25–27.
Ericsson, I., Persson, L.G., Berglundh, T., Mari-
nello, C.P., Lindhe, J. & Klinge, B. (1995) Differ-
ent types of inflammatory reactions in peri-
implant soft tissues. Journal of Clinical Perio-
dontology 22: 255–261.
Everaert, E.P., Mahieu, H.F., Belt-Gritter, B., Pe-
eters, A.J., Verkerke, G.J., van der Mei, H.C. &
Busscher, H.J. (1999) Biofilm formation in vivo on
perfluoro-alkylsiloxane-modified voice pros-
theses. Archives of Otolaryngology – Head and
Neck Surgery 125: 1329–1332.
Fachon-Kalweit, S., Elder, B.L. & Fives-Taylor, P.
(1985) Antibodies that bind to fimbriae block
adhesion of Streptococcus sanguis to saliva-coated
hydroxyapatite. Infection and Immunity 48:
617–624.
Fine, D.H., Wilton, J.M. & Caravana, C. (1984) In
vitro sorption of albumin, immunoglobulin G,
and lysozyme to enamel and cementum from
human teeth. Infection and Immunity 44:
332–338.
Fives-Taylor, P.M. & Thompson, D.W. (1985) Sur-
face properties of Streptococcus sanguis
FW213 mutants nonadherent to saliva-coated
hydroxyapatite. Infection and Immunity 47:
752–759.
Fletcher, M. & Pringle, J.H. (1985) The effect of
surface free-energy and medium surface-tension
on bacterial attachment to solid-surfaces. Journal
of Colloid and Interface Science 104: 5–14.
Fletcher, R.L. & Baier, R.E. (1984) Influence of
surface-energy on the development of the green-
alga Enteromorpha. Marine Biology Letters 5:
251–254.
Gatewood, R.R., Cobb, C.M. & Killoy, W.J. (1993)
Microbial colonization on natural tooth structure
compared with smooth and plasma-sprayed dental
implant surfaces. Clinical Oral Implants
Research 4: 53–64.
Gibbons, R.J. & Hay, D.I. (1988) Human salivary
acidic proline-rich proteins and statherin promote
the attachment of Actinomyces viscosus LY7 to
apatitic surfaces. Infection and Immunity 56:
439–445.
Gibbons, R.J., Hay, D.I., Cisar, J.O. & Clark, W.B.
(1988) Adsorbed salivary proline-rich protein 1
and statherin: receptors for type 1 fimbriae of
Actinomyces viscosus T14V-J1 on apatitic sur-
faces. Infection and Immunity 56: 2990–2993.
Gildenhuys, R.R. & Stallard, R.E. (1975) Compar-
ison of plaque accumulation on metal restorative
surfaces. Dental Survey 51: 56–59.
Teughels et al . Effect of material characteristics and/or surface topography
Glantz, P.O. (1969) On wettability and adhesive-
ness. Odontologisk Revy 20: 1–132.
Gouvoussis, J., Sindhusake, D. & Yeung, S. (1997)
Cross-infection from periodontitis sites to failing
implant sites in the same mouth. International
Journal of Oral & Maxillofacial Implants 12:
666–673.
Groessner-Schreiber, B., Hannig, M., Duck, A.,
Griepentrog, M. & Wenderoth, D.F. (2004) Do
different implant surfaces exposed in the oral
cavity of humans show different biofilm composi-
tions and activities? European Journal of Oral
Sciences 112: 516–522.
Gross, M., Abramovich, I. & Weiss, E.I. (1999)
Microleakage at the abutment-implant interface
of osseointegrated implants: a comparative study.
International Journal of Oral & Maxillofacial
Implants 14: 94–100.
Hannig, M. (1999) Transmission electron micro-
scopy of early plaque formation on dental materi-
als in vivo. European Journal of Oral Sciences
107: 55–64.
Harkes, G., Dankert, J. & Feijen, J. (1992) Growth
of uropathogenic Escherichia coli strains at solid
surfaces. Journal of Biomaterials Science Polymer
edition 3: 403–418.
Hawthorn, L. & Reid, G. (1990) The effect of
protein and urine on uropathogen adhesion to
polymer substrata. Journal of Biomedical Materi-
als Research 24: 1325–1332.
Hsu, S.D., Cisar, J.O., Sandberg, A.L. & Kilian, M.
(1994) Adhesive properties of viridans streptococ-
cal species. Microbial Ecology in Health and
Disease 125–137.
Hultin, M., Gustafsson, A., Hallstrom, H., Johans-
son, L.A., Ekfeldt, A. & Klinge, B. (2002) Micro-
biological findings and host response in patients
with peri-implantitis. Clinical Oral Implants Re-
search 13: 349–358.
Hultin, M., Gustafsson, A. & Klinge, B. (2000)
Long-term evaluation of osseointegrated dental
implants in the treatment of partly edentulous
patients. Journal of Clinical Periodontology 27:
128–133.
Jansen, V.K., Conrads, G. & Richter, E.J. (1997)
Microbial leakage and marginal fit of the implant-
abutment interface. International Journal of Oral
& Maxillofacial Implants 12: 527–540.
Joshi, R.I. & Eley, A. (1988) The in-vitro effect of a
titanium implant on oral microflora: comparison
with other metallic compounds. Journal of Med-
ical Microbiology 27: 105–107.
Keenan, M.P., Shillingburg, H.T. Jr, Duncanson,
M.G. Jr & Wade, C.K. (1980) Effects of cast gold
surface finishing on plaque retention. Journal of
Prosthetic Dentistry 43: 168–173.
Keith, S.E., Miller, B.H., Woody, R.D. & Higgin-
bottom, F.L. (1999) Marginal discrepancy of
screw-retained and cemented metal-ceramic
crowns on implant abutments. International Jour-
nal of Oral & Maxillofacial Implants 14: 369–
378.
Kohavi, D., Greenberg, R., Raviv, E. & Sela, M.N.
(1994) Subgingival and supragingival microbial
flora around healthy osseointegrated implants in
partially edentulous patients. International Jour-
nal of Oral and Maxillofacial Implants 9:
673–678.
79 |
Koka, S., Razzoog, M.E., Bloem, T.J. & Syed, S.
(1993) Microbial colonization of dental implants
in partially edentulous subjects. Journal Prosthe-
tic Dentistry 70: 141–144.
Kolenbrander, P.E. (1989) Surface recognition
among oral bacteria: multigeneric coaggregations
and their mediators. Critical Reviews in Micro-
biology 17: 137–159.
Kolenbrander, P.E., Ganeshkumar, N., Cassels, F.J.
& Hughes, C.V. (1993) Coaggregation: specific
adherence among human oral plaque bacteria.
Federation of American Societies for Experimen-
tal Biology 7: 406–413.
Kolenbrander, P.E. & London, J. (1993) Adhere
today, here tomorrow: oral bacterial adherence.
Journal of Bacteriology 175: 3247–3252.
Kolenbrander, P.E., Parrish, K.D., Andersen, R.N.
& Greenberg, E.P. (1995) Intergeneric coaggrega-
tion of oral Treponema spp. with Fusobacterium
spp. and intrageneric coaggregation among Fuso-
bacterium spp. Infection and Immunity 63:
4584–4588.
Larato, D.C. (1972) Influence of a composite resin
restoration on the gingiva. Journal of Prosthetic
Dentistry 28: 402–404.
Lee, R.G., Adamson, C. & Kim, S.W. (1974)
Competitive adsorption of plasma proteins
onto polymer surfaces. Thrombosis Research 4:
485–490.
Lekholm, U., Ericsson, I., Adell, R. & Slots, J.
(1986) The condition of the soft tissues at tooth
and fixture abutments supporting fixed bridges. A
microbiological and histological study. Journal of
Clinical Periodontology 13: 558–562.
Leonhardt, A., Adolfsson, B., Lekholm, U., Wik-
ström, M. & Dahlén, G. (1993) A longitudinal
microbiological study on osseointegrated titanium
implants in partially edentulous patients. Clinical
Oral Implants Research 4: 113–120.
Leonhardt, A. & Dahlen, G. (1995) Effect of tita-
nium on selected oral bacterial species in
vitro. European Journal of Oral Sciences 103:
382–387.
Liu, Y. & Zhao, Q. (2005) Influence of surface
energy of modified surfaces on bacterial adhesion.
Biophysical Chemistry 117: 39–45.
Mabboux, F., Ponsonnet, L., Morrier, J.J., Jaffrezic,
N. & Barsotti, O. (2004) Surface free energy and
bacterial retention to saliva-coated dental implant
materials – an in vitro study. Colloids and
Surfaces B, Biointerfaces 39: 199–205.
Marsh, P.D. (2004) Dental plaque as a microbial
biofilm. Caries Research 38: 204–211.
Marsh, P.D. (2005) Dental plaque: biological signif-
icance of a biofilm and community life-style.
Journal of Clinical Periodontology 32 (Suppl. 6):
7–15.
Marsh, P.D. & Bowden, G.H.W. (2000) Microbial
community interactions in biofilms. In: Allison,
D.G., Gilbert, P., Lappin-Scott, H.M. & Wilson,
M., eds. Community Structure and Co-operation
in Biofilms. Society for Gneral Microbiology
Symposium no. 59, 167–198. Cambridge: Cam-
bridge University Press.
Marsh, P.D. & Bradshaw, D.J. (1999) Microbial
community aspects of dental plaque. In: New-
man, H.N. & Wilson, M., eds. Dental Plaque
Revisited, 237–253. Cardiff: Bioline.
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
Teughels et al . Effect of material characteristics and/or surface topography
Mengel, R., Stelzel, M., Hasse, C. & Flores-de-
Jacoby, L. (1996) Osseointegrated implants in
patients treated for generalized severe adult perio-
dontitis. A interim report. Journal of Perio-
dontology 67: 782–787.
Mergenhagen, S.E., Sandberg, A.L., Chassy, B.M.,
Brennan, M.J., Yeung, M.K., Donkersloot, J.A. &
Cisar, J.O. (1987) Molecular basis of bacterial
adhesion in the oral cavity. Reviews of Infectious
Diseases 9 (Suppl. 5): S467–S474.
Mombelli, A., Buser, D. & Lang, N.P. (1988)
Colonization of osseointegrated titanium im-
plants in edentulous patients. Early results. Jour-
nal of Oral Microbiology and Immunology 3:
113–120.
Mombelli, A., Marxer, M., Gaberthüel, T., Grun-
der, U. & Lang, N.P. (1995) The microbiota of
osseointegrated implants in patients with a history
of periodontal disease. Journal of Clinical Perio-
dontology 22: 124–130.
Mormann, W., Regolati, B. & Renggli, H.H. (1974)
Gingival reaction to well-fitted subgingival prox-
imal gold inlays. Journal of Clinical Perio-
dontology 1: 120–125.
Morra, M. & Cassinelli, C. (1997) Bacterial adhe-
sion to polymer surfaces: a critical review of sur-
face thermodynamic approaches. Journal of
Biomaterials Science Polymer Edition 9: 55–74.
Nakazato, G., Tsuchiya, H., Sato, M. & Yamauchi,
M. (1989) In vivo plaque formation on implant
materials. International Journal of Oral & Max-
illofacial Implants 4: 321–326.
Olsson, J., van der, H.Y. & Holmberg, K. (1992)
Plaque formation in vivo and bacterial attachment
in vitro on permanently hydrophobic and
hydrophilic surfaces. Caries Research 26:
428–433.
Papaioannou, W., Quirynen, M. & van Steenberghe,
D. (1996) The influence of periodontitis on the
subgingival flora around implants in partially
edentulous patients. Clinical Oral Implants
Research 7: 405–409.
Parvizi, J., Wickstrom, E., Zeiger, A.R., Adams,
C.S., Shapiro, I.M., Purtill, J.J., Sharkey, P.F.,
Hozack, W.J., Rothman, R.H. & Hickok, N.J.
(2004) Titanium surface with biologic activity
against infection. Clinical Orthopaedics and Re-
lated Research 429: 33–38.
Peumans, M., Van Meerbeek, B., Lambrechts, P.,
Vanherle, G. & Quirynen, M. (1998) The influ-
ence of direct composite additions for the correc-
tion of tooth form and/or position on periodontal
health. A retrospective study. Journal of Perio-
dontology 69: 422–427.
Pratt-Terpstra, I.H., Mulder, J., Weerkamp, A.H.,
Feijen, J. & Busscher, H.J. (1991) Secretory IgA
adsorption and oral streptococcal adhesion to hu-
man enamel and artificial solid substrata with
various surface free energies. Journal of Biomater-
ials Science Polymer Edition 2: 239–253.
Pratt-Terpstra, I.H., Weerkamp, A.H. & Busscher,
H.J. (1989) The effects of pellicle formation on
streptococcal adhesion to human enamel and
artificial substrata with various surface free-ener-
gies. Journal of Dental Research 68: 463–467.
Quirynen, M. (1986) Anatomical and inflammatory
factors influence bacterial plaque growth and
retention in man. Thesis, Leuven.
80 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81
Quirynen, M. & Bollen, C.M. (1995) The influence
of surface roughness and surface-free energy on
supra- and subgingival plaque formation in man.
A review of the literature. Journal of Clinical
Periodontology 22: 1–14.
Quirynen, M., Bollen, C.M., Eyssen, H. & van
Steenberghe, D. (1994) Microbial penetration
along the implant components of the Branemark
system. An in vitro study. Clinical Oral Implants
Research 5: 239–244.
Quirynen, M., Bollen, C.M., Papaioannou, W., Van
Eldere, J. & van Steenberghe, D. (1996) The
influence of titanium abutment surface roughness
on plaque accumulation and gingivitis: short-term
observations. International Journal of Oral &
Maxillofacial Implants 11: 169–178.
Quirynen, M., De Soete, M. & van Steenberghe, D.
(2002) Infectious risks for oral implants: a review
of the literature. Clinical Oral Implants Research
13: 1–19.
Quirynen, M. & Listgarten, M.A. (1990) The dis-
tribution of bacterial morpho types around natural
teeth and titanium implants ad modum
Brånemark. Clinical Oral Implants Research 4:
8–12.
Quirynen, M., Marechal, M., Busscher, H.J., Weer-
kamp, A.H., Arends, J., Darius, P.L. & van
Steenberghe, D. (1989) The influence of surface
free-energy on planimetric plaque growth in man.
Journal of Dental Research 68: 796–799.
Quirynen, M., Marechal, M., Busscher, H.J., Weer-
kamp, A.H., Darius, P.L. & van Steenberghe, D.
(1990) The influence of surface free energy and
surface roughness on early plaque formation. An
in vivo study in man. Journal of Clinical Perio-
dontology 17: 138–144.
Quirynen, M., van der Mei, H.C., Bollen, C.M.,
Schotte, A., Marechal, M., Doornbusch, G.I.,
Naert, I., Busscher, H.J. & van Steenberghe, D.
(1993) An in vivo study of the influence of the
surface roughness of implants on the microbiology
of supra- and subgingival plaque. Journal of
Dental Research 72: 1304–1309.
Quirynen, M. & van Steenberghe, D. (1993) Bacter-
ial colonization of the internal part of two-stage
implants. An in vivo study. Clinical Oral Im-
plants Research 4: 158–161.
Quirynen, M., Vogels, R., Peeters, W., van Steen-
berghe, D., Naert, I. & Haffajee, A. (2006) Dy-
namics of initial subgingival colonization of
‘pristine’ peri-implant pockets. Clinical Oral Im-
plants Research 17: 25–37.
Rakhorst, G., van der Mei, H.C., Van Oeveren, W.,
Spijker, H.T. & Busscher, H.J. (1999)
Time-related contact angle measurements with
human plasma on biomaterial surfaces.
International Journal of Artificial Organs 22:
35–39.
Rasperini, G., Maglione, M., Cocconcelli, P. &
Simion, M. (1998) In vivo early plaque formation
on pure titanium and ceramic abutments: a com-
parative microbiological and SEM analysis. Clin-
ical Oral Implants Research 9: 357–364.
Rimondini, L., Cerroni, L., Carrassi, A. & Torri-
celli, P. (2002) Bacterial colonization of zirconia
ceramic surfaces: an in vitro and in vivo study.
International Journal of Oral & Maxillofacial
Implants 17: 793–798.
Rimondini, L., Fare, S., Brambilla, E., Felloni, A.,
Consonni, C., Brossa, F. & Carrassi, A. (1997)
The effect of surface roughness on early in vivo
plaque colonization on titanium. Journal of Perio-
dontology 68: 556–562.
Rolla, G., Ellingsen, J.E. & Herlofson, B. (1991)
Enhancement and inhibition of dental plaque
formation-some old and new concepts. Biofouling
3: 175–181.
Ruan, M.S., Di Paola, C. & Mandel, I.D. (1986)
Quantitative immunochemistry of salivary pro-
teins adsorbed in vitro to enamel and cementum
from caries-resistant and caries-susceptible
human adults. Archives of Oral Biology 31:
597–601.
Rutter, P.R. & Vincent, B. (1984) Physicochemical
interactions of the substratum, microorganisms
and the fluid phase. In: Marshall, K.C., eds.
Microbial Adhesion and Aggregation, 21–38.
Berlin: Springer Verlag.
Rykke, M. & Sonju, T. (1991) Amino acid
composition of acquired enamel pellicle collected
in vivo after 2 hours and after 24 hours.
Scandinavian Journal of Dental Research 99:
463–469.
Sbordone, L., Barone, A., Ciaglia, R.N., Ramaglia,
L. & Iacono, V.J. (1999) Longitudinal study of
dental implants in a periodontally compromised
population. Journal of Periodontology 11: 1322–
1329.
Scannapieco, F.A., Torres, G.I. & Levine, M.J.
(1995) Salivary amylase promotes adhesion of
oral streptococci to hydroxyapatite. Journal of
Dental Research 74: 1360–1366.
Scarano, A., Piattelli, M., Caputi, S., Favero, G.A.
& Piattelli, A. (2004) Bacterial adhesion on com-
mercially pure titanium and zirconium oxide
disks: an in vivo human study. Journal of Perio-
dontology 75: 292–296.
Scarano, A., Piattelli, M., Vrespa, G., Caputi, S. &
Piattelli, A. (2003) Bacterial adhesion on titanium
nitride-coated and uncoated implants: an in vivo
human study. Journal of Oral Implantology 29:
80–85.
Scheie, A.A. (1994) Mechanisms of dental plaque
formation. Advances in Dental Research 8: 246–
253.
Scheutzel, P. (1989) [Effect of light cured sealants for
occlusal surfaces on discoloration and plaque ac-
cumulation on removable partial dentures]. ZWR
98: 857–8, 860–1.
Schmitt, D.D., Bandyk, D.F., Pequet, A.J. &
Towne, J.B. (1986) Bacterial adherence to vascular
prostheses. A determinant of graft infectivity.
Journal of Vascular Surgery 3: 732–740.
Shafagh, I. (1986) Plaque accumulation on cast gold
complete crowns polished by a conventional and
an experimental method. Journal of Prosthetic
Dentistry 55: 339–342.
Shapiro, J.A. (1998) Thinking about bacterial popu-
lations as multicellular organisms. Annual
Review of Microbiology 52: 81–104.
Siegrist, B.E., Brecx, M.C., Gusberti, F.A., Joss, A.
& Lang, N.P. (1991) In vivo early human dental
plaque formation on different supporting sub-
stances. A scanning electron microscopic and
bacteriological study. Clinical Oral Implants
Research 2: 38–46.

Siochi, E.J., Eiss, N.S., Gilliam, D.R. & Wightman,
J.P. (1987) A fundamental-study of the sticking of
insect residues to aircraft wings. Journal of
Colloid and Interface Science 115: 346–356.
Sipahi, C., Anil, N. & Bayramli, E. (2001) The effect
of acquired salivary pellicle on the surface free
energy and wettability of different denture base
materials. Journal of Dentistry 29: 197–204.
Smales, R.J. (1981) Plaque growth on dental
restorative materials. Journal of Dentistry 9:
133–140.
Stenstrom, T.A. (1989) Bacterial hydrophobicity, an
overall parameter for the measurement of adhe-
sion potential to soil particles. Applied and
Environmental Microbiology 55: 142–147.
Suketa, N., Sawase, T., Kitaura, H., Naito, M.,
Baba, K., Nakayama, K., Wennerberg, A. & At-
suta, M. (2005) An antibacterial surface on dental
implants, based on the photocatalytic bactericidal
effect. Clinical Implant Dentistry and Related
Research 7: 105–111.
Tanner, J., Robinson, C., Soderling, E. & Vallittu, P.
(2005) Early plaque formation on fibre-reinforced
composites in vivo. Clinical Oral Investigations
9: 154–160.
Trivedi, S.C. & Talim, S.T. (1973) The response of
human gingiva to restorative materials. Journal of
Prosthetic Dentistry 29: 73–80.
Van Dijk, J., Herkstroter, F., Busscher, H., Weer-
kamp, A., Jansen, H. & Arends, J. (1987) Surface-
free energy and bacterial adhesion. An in vivo
Teughels et al . Effect of material characteristics and/or surface topography
study in beagle dogs. Journal of Clinical Perio-
dontology 14: 300–304.
Van Dijken, J.W., Sjostrom, S. & Wing, K. (1987a)
The effect of different types of composite resin
fillings on marginal gingiva. Journal of Clinical
Periodontology 14: 185–189.
Van Dijken, J.W., Sjostrom, S. & Wing, K. (1987b)
Development of gingivitis around different types
of composite resin. Journal of Clinical Perio-
dontology 14: 257–260.
Van Loosdrecht, M.C., Lyklema, J., Norde, W. &
Zehnder, A.J. (1990a) Influence of interfaces on
microbial activity. Microbiology Reviews 54:
75–87.
Van Loosdrecht, M.C., Norde, W. & Zehnder, A.J.
(1990b) Physical chemical description of bacterial
adhesion. Journal of Biomaterials Applications 5:
91–106.
Van Loosdrecht, M.C. & Zehnder, A.J. (1990) En-
ergetics of bacterial adhesion. Experientia 46:
817–822.
Van Oss, C.J., Good, R.J. & Chaudhury, M.K.
(1986) Nature of the antigen-antibody interaction.
Primary and secondary bonds: optimal conditions
for association and dissociation. Journal of Chro-
matography 376: 111–119.
Van Pelt, A.W., de Jong, H.P., Busscher,
H.J. & Arends, J. (1983) Dispersion and
polar surface free energies of human enamel.
Journal of Biomedical Materials Research 17:
637–641.
81 |
Wahl, G., Muller, F. & Schaal, K.P. (1992) The
microbial colonization of implant elements made
of plastics and titanium. Schweiz Monatsschr
Zahnmed 102: 1321–1326.
Weerkamp, A., Quirynen, M., Marechal, M., van
der Mei, H.C., van Steenberghe, D. & Busscher,
H. (1989) The role of surface free energy in the
early in vivo formation of dental plaque on human
enamel and polymeric substrata. Microbial Ecol-
ogy in Health and Disease 2: 11–18.
Weerkamp, A.H., Uyen, H.M. & Busscher, H.J.
(1988) Effect of zeta potential and surface energy
on bacterial adhesion to uncoated and saliva-
coated human enamel and dentin. Journal of
Dental Research 67: 1483–1487.
Weitman, R.T. & Eames, W.B. (1975) Plaque accu-
mulation on composite surfaces after various fi-
nising procedures. Journal of the American
Dental Association 91: 101–106.
Wennerberg, A., Sennerby, L., Kultje, C. & Le-
kholm, U. (2003) Some soft tissue characteristics
at implant abutments with different surface topo-
graphy. A study in humans. Journal of Clinical
Periodontology 30: 88–94.
Whittaker, C.J., Klier, C.M. & Kolenbrander, P.E.
(1996) Mechanisms of adhesion by oral bacteria.
Annual Review of Microbiology 50: 513–552.
Yoshinari, M., Oda, Y., Kato, T. & Okuda, K. (2001)
Influence of surface modifications to titanium on
antibacterial activity in vitro. Biomaterials 22:
2043–2048.
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 68–81