K. Marcelis Sleeping vs.

loaded implants, long-term

M. Vercruyssen
E. Nicu
observations via a retrospective
I. Naert analysis
M. Quirynen

Authors’ affiliations: Key words: implants, loading, microbiology, overdentures, sleeping implants
K. Marcelis, M. Vercruyssen, E. Nicu, M. Quirynen,
Department of Periodontology, School of Dentistry,
Oral Pathology & Maxillo-Facial Surgery, Faculty of Abstract
Medicine, Catholic University Leuven, Objective: Several theories have been presented to explain initial and secondary marginal bone
Kapucijnenvoer 33, B-3000, Leuven, Belgium
loss around dental implants (e.g. microbial load, adverse loading, microbial leakage, compromised
I. Naert, Department of Prosthetic Dentistry,
School of Dentistry, Oral Pathology & Maxillo- healing/adaptation of host-implant interface).
Facial Surgery, Faculty of Medicine, Catholic Material and methods: This study compared the long-term outcome (up to 12 years) of sleeping
University Leuven, Kapucijnenvoer 33, B-3000,
with loaded implants in the mandible via a split-mouth concept. Fourteen patients with overden-
Leuven, Belgium
tures were enrolled (10 women, mean age at implant insertion: 56 years [range: 33–71]). They
Corresponding author: presented with 28 loaded (position 33/43) and 14 sleeping implants (mostly position 31/41). At
M. Quirynen
Department of Periodontology several follow-up visits, intra-oral radiographs (long-cone principle) were taken to observe marginal
School of Dentistry bone level changes.
Oral Pathology & Maxillo-Facial Surgery Results: At each observation, compared with abutment connection, the submerged non-loaded
Faculty of Medicine
Catholic University Leuven implants showed less bone loss (P-values: 1st year 0.007, 3 years 0.000, 5 years 0.002, 8 years 0.007,
Kapucijnenvoer 33 12 years 0.000) than their neighbouring functional implants. This difference was primarily due to a
B-3000 Leuven more significant bone loss during the first year of loading (0.8 vs. 0.1 mm respectively), since after-
Belgium
Tel.: +32 16 33 24 83 wards, the bone level changes remained quite similar for both implant types.
Fax: +32 16 33 24 07 Conclusions: Our data suggest that the first months of loading have a significant impact on the
e-mail: marc.quirynen@med.kuleuven.be
bone level (initial difference sleeping vs. loaded implants), followed by a more physiological bone
level change afterwards. This initial difference might be explained by the adaptation of the
surrounding bone to the loaded implant.

When Branemark et al. (1969) started treating
their patients with endosseous implants, their
first concern was the survival and osseointe-
gration of the implants. Later on, new criteria
for implant success were formulated (Al-
brektsson et al. 1986b; van Steenberghe 1997;
Karoussis et al. 2004). These criteria included,
among others, osseointegration, peri-implant
health, functionality of the implant and espe-
cially, the preservation of marginal bone and
soft tissues around the implant. According to
Albrektsson et al. (1986a, 1986b), a vertical
bone loss ranging from 0.9 to 1.6 mm during
the first year of function could be accepted;
afterwards, the annual bone loss should not
exceed 0.2 mm. More recently, with the
introduction of improved implant surfaces,
Date: the same group even proposed more stringent
Accepted 24 May 2011 criteria for implant success with no more
To cite this article: than 0.1 mm of bone loss after the first year
Marcelis K, Vercruyssen M, Nicu E, Naert I, Quirynen M.
Sleeping vs. loaded implants, long-term observations via a
of function (Albrektsson et al. 1994).
retrospective analysis. Several mechanisms have been suggested
Clin. Oral Impl. Res. 23, 2012, 1118–1122
doi: 10.1111/j.1600-0501.2011.02263.x
to explain the initial bone remodelling (dur-
ing the first 3–6 months after abutment
connection/loading) around implants includ-
ing surgical trauma at abutment connection,
establishment of a biological width apical
to the implant neck-abutment connection
(Berglundh & Lindhe 1996), and/or the micro-
gap leakage (Quirynen et al. 1994).
Secondary marginal bone loss around
endosseus implants (after the first 6 months of
loading) is classically explained by biomechan-
ical (Kim et al. 2005) and/or microbiological
factors (Quirynen et al. 2007). Peri-implantitis
is probably one of the most important factors
contributing to marginal bone remodelling
around dental implants. Several clinical (Sanz
et al. 1991; Schou et al. 1992; Teixeira et al.
1997) and animal (Lindhe et al. 1992; Mari-
nello et al. 1995; Persson et al. 1999) studies
have shown a correlation between inflamma-
tion of the peri-implant mucosa, in the pres-
ence of subgingival plaque and peri-implant
bone loss. The incidence of peri-implantitis
was estimated from 6% to 60% (Fransson

1118 © 2011 John Wiley & Sons A/S


et al. 2005; Roos-Jansaker et al. 2006a, 2006b).
In clinical reports and reviews, occlusal over-
load has also been suggested as a major factor
contributing to peri-implant bone loss and
even implant failure (Adell et al. 1981; Lind-
quist et al. 1988; Naert et al. 1992; Quirynen
et al. 1992; Kim et al. 2005). These data are
backed up by several animal studies that
provided evidence for marginal bone loss after
excessive and repetitive loading both in the
presence (Kozlovsky et al. 2007) and in the
absence (Isidor 1996, 1997; Miyata et al. 2000)
of peri-implant tissue inflammation. Con-
versely, other animal studies could not
confirm these findings (Barbier & Schepers
1997; Miyata et al. 1998; Gotfredsen et al.
2001a, 2001b, 2001c, 2002; Heitz-Mayfield
et al. 2004).
To date, there is still a lack of convincing
evidence in the literature regarding the
relative contribution of the different factors
leading to this marginal bone loss. Further-
more, one cannot fully explain the initial
remodelling after abutment connection.
Recently, another theory has been suggested
(Chvartszaid et al. 2008; Albrektsson et al.
2009) in which especially the peri-implant
bone loss was explained as function of a com-
promised healing/adaptation of host-implant
interface. This can be caused by genetic
disorders of the patient, poor bone quality,
adversely traumatic surgical techniques,
adverse loading (including underloading)
and lack of blood supply (Chvartszaid et al.
2008).
As sleeping implants are submerged and
thus not in contact with the microbiota of
the oral cavity, plaque-related inflammation
cannot occur along them. Moreover, as these
implants are not in function, they are not
subjected to the same loading forces as the
ones who retain a denture.
This short communication presents a unique
data set allowing to compare long-term (up
to 12 years) marginal bone levels around
sleeping submerged implants and their neigh-
bouring implants supporting a mandibular
overdenture, to verify the influence of both
the oral microbiota and the occlusal load.
Materials and methods
Patient selection and treatment strategy
Between January 1987 and June 2003, 18
patients (Table 1) were treated at the depart-
ment of Periodontology of the University
Hospital Leuven with implants (Brånemark
system) to retain a mandibular overdenture.
Each patient was provided with three
© 2011 John Wiley & Sons A/S
Marcelis et al
Sleeping vs. loaded implants
implants in the symphyseal area (Fig. 1). The Table 1. Characteristics of the study group
(values are means ± standard deviations or
two implants at the canine position (n = 36) number of subjects)
served as anchor for the overdenture. An Mean age (years) 56.6 ± 8.6
additional rescue implant (n = 18) was added, Gender: male/female 5/13
often at the midline. The latter mostly Ethnicity: Caucasian/other 17/1
Number of implants 54
remained submerged during the duration of
In function 36
this retrospective study (n = 14), although Sleeping 18
some showed a spontaneous soft tissue perfo- Non-submerged 4
ration (n = 4). All implants had a turned Submerged 14
Attachment system
surface. In all but three patients, a Dolder bar Bar 15
was used as attachment system. In the other Ball and o-ring 3
three patients, ball attachments were
installed. There were several reasons why time factor and implant type (sleeping/loaded)
these rescue implants were placed. In the as fixed factor. Thereafter, implant types were
early days when the prognosis of this kind of compared for each time interval and Sidak’s
treatment was not yet proven, an extra correction for simultaneous hypothesis testing
implant was installed as a precaution was applied.
measurement. In case of gradual treatment
failure, this implant could be incorporated to
Results
divide the occlusal forces among three
implants instead of two. Later on, sleeping
The characteristics of the cohort population
implants were still placed in patients with an
are summarized in Table 1. The mean age at
unfavourable medical history such as radio-
implant placement was 56.6 years (SD = 8.6).
therapy (Alsaadi et al. 2008), reduced bone
height, or in patients who previously lost an
(a)
implant. In our study, there was one patient
with a history of radiotherapy and three
patients with poor bone quality (type 4; Lek-
holm & Zarb 1985).
After placement of the implants, all
patients were incorporated in a recall system
and were seen every year by both a periodon-
tologist and a prosthodontist. When neces-
sary, the occlusion was corrected and/or oral
hygiene measures were reinforced. A relin-
ing/rebasing of the denture was performed (b)
when indicated.
Bone level estimation
Radiographs were taken in a standardized
manner at abutment connection and after 1,
3, 5, 8 and 12 years. These radiographs were
taken with the long-cone parallel technique,
keeping the film holder strictly perpendicular
to the implant axis. The marginal bone level
was evaluated, both mesially and distally of
each implant with the implant/abutment (c)
junction as reference level. If necessary, clear
markers were used: the end of the horizontal
part of the shoulder (0.8 mm more apically),
the 1st thread (1.8 mm more apically) and the
2nd, 3rd, 4th, etc. thread representing a dis-
tance of 0.6 mm more apically per thread (for
details, see Vercruyssen & Quirynen 2010).
Statistics
A linear mixed model was fitted to the mean
Fig. 1. Typical example of patient with two functional
bone loss after abutment insertion and another
and one sleeping (submerged) implant with radiographs
to the mean bone loss after 12 months. at abutment connection (a) and after 8 (b) and 12 years
Patients were taken as random factor, and the (c) respectively.
1119 | Clin. Oral Impl. Res. 23, 2012 / 1118–1122
Marcelis et al
Sleeping vs. loaded implants

A large majority were Caucasian (17/18),
women (13/18) and non-smoker (17/18). A
total of 54 implants were placed of which 18
were never loaded. Of these 18 implants, 14
remained submerged and four showed a spon-
taneous perforation. If perforation occurred, it
occurred within the first 12 months after
placement.
Initially, the cohort counted 18 patients,
but only 14 patients of whom the sleeping
implant remained submerged during the
entire follow-up were considered for analysis.
At the 3-, 8- and 12-year follow-up, this
number decreased to 12, 8 and 7 patients
respectively (the latter because four patients
had not yet reached that time window).
Table 2 shows the marginal bone level of
the functional and “sleeping & submerged”
implants at abutment connection, and the
bone loss over different time intervals (with
abutment connection as baseline). There was
always significantly more bone loss along
functional implants compared with sleeping
implants (P  0.002). During the first year of
loading, a loss of 0.8 and 0.1 mm for func-
tional for sleeping implants respectively was
close monitoring of the oral hygiene during
the 12 years of follow-up, the general health
of the subjects (only one smoker, one diabe-
tes patient and six patients with a history of
periodontitis), and/or surface characteristics
of the used implants (minimally rough). Also,
the fact that the patients were full edentu-
lous might explain their more favourable
conditions.
In this population, we could compare two
cohorts of identical implants, namely func-
tional and “sleeping & submerged” implants,
who shared the same host, but not the same
microbial and mechanical tread. The func-
tional implants showed an obvious bone
remodelling (±1.5 mm) during the first year
after abutment connection (Table 2) as has
been previously described by others (Al-
brektsson et al. 1986a; Albrektsson & Zarb
1993; Roos et al. 1997). After 12 years of
loading, the functional implants showed a
mean entire bone loss of 2.1 (±0.8) mm, thus
an annual loss of  0.1 mm.
During the first year of loading, functional
implants showed significantly more bone loss
than their sleeping and submerged neigh-
The significant difference in bone level
changes during the first year of loading
between sleeping and functional implants
can be explained in several ways: the absence
of a second flap elevation, in the knowledge
that every flap impairs the blood supply and
causes bone loss, and/or the absence of adap-
tation to functional and/or bacterial load in
contrast to functional implants (as suggested
by Chvartszaid et al. 2008). One can envisage
that both aspects played a role.
After the first year of bone remodelling, the
differences in bone level changes for func-
tional and sleeping implants became rather
small, indicating that the bone seems to be
adapted to its loading by implants, and that
the bacterial tread was small. Indeed, none of
the implants showed any signs of inflamma-
tion during the entire length of follow-up.
Possible explanations for this lower microbial
tread could be the surface characteristics of
the implants (Quirynen et al. 2007), and/or the
modified microbial environment in edentulous
patients (Danser et al. 1995, 1997; Quirynen

4
recorded. When the bone level changes were bours (0.8 vs. 0.1 mm respectively). After the
Sleeping
compared towards the bone level at the end first year, the bone level changes remained Functional

3
of the first year of loading (thus after the quite similar, although loaded implants regu-

Bone loss (mm)

period bone remodelling), however, signifi-
cant differences could no longer be observed
(P  0.39; Fig. 2), although functional
larly showed higher bone loss values. After
2
the 12-year follow-up, the mean entire bone
loss for sleeping implants was 0.7 vs. 2.1 mm
1

implants often showed more bone loss. for the loaded implants. This bone level
change along “sleeping & submerged”
Discussion
0

implants is also remarkably less than the

bone loss previously observed along loaded
b

Y1
None of the functional or non-submerged implants in the anterior mandibular region in
−A

−Y

−Y

−Y

2−
Y1

Y3

Y5

Y8

implants showed any clinical or radiological
signs of peri-implantitis as defined by the
Consensus report of the Sixth European
Workshop on Periodontology (Lindhe & Mey-
le 2008). This might be explained by the
full denture wearers (loss of 2.8 mm from 2
to 5 years; Sennerby et al. 1988). This bone
loss, being independent of the classic risk
factors for bone loss, can perhaps be consid-
ered a “physiologic” bone loss.
Y1
Fig. 2. Scatter plot with the bone loss (in mm, mesial
or distal observations) for functional and submerged and
sleeping implants over different time intervals (first
year of loading, year 1–3, year 1–5, year 1–8 and year
1–12). Some dots represent more observations.

Table 2. Distance between implant/abutment junction and marginal bone level (mean, standard deviation, median, n = number of implants) scored
mesially (M) and distally (D) per implant, at abutment connection and the change in this distance per time interval, for respectively functional and
sleeping implants. P-values for differences in bone loss between functional and sleeping were calculated via a linear mixed model with Sidak’s
correction
Functional implants
Corresponding submerged P-
Time interval 33 43 sleeping implants value
Abutment M 0.8 ± 0.8 (n = 14) median: 0.8 0.5 ± 0.7 (n = 14) median: 0.0 0.2 ± 0.4 (n = 14) median: 0.0
connection D 0.9 ± 1.1 (n = 14) median: 0.8 0.5 ± 0.8 (n = 14) median: 0.0 0.4 ± 0.6 (n = 14) median: 0.0
First year M 0.7 ± 0.8 (n = 14) median: 0.5 1.2 ± 1.1 (n = 14) median: 0.8 0.1 ± 0.3 (n = 14) median: 0.0 0.007
D 0.6 ± 0.7 (n = 14) median: 0.5 0.7 ± 0.9 (n = 14) median: 0.0 0.1 ± 0.3 (n = 14) median: 0.0
3 years M 0.9 ± 0.7 (n = 12) median: 0.7 1.4 ± 1.2 (n = 12) median: 0.9 0.1 ± 0.3 (n = 12) median: 0.0 0.000
D 0.9 ± 0.6 (n = 12) median: 0.9 0.9 ± 1.1 (n = 12) median: 0.7 0.2 ± 0.3 (n = 12) median: 0.0
5 years M 0.9 ± 0.7 (n = 12) median: 0.5 1.3 ± 1.1 (n = 12) median: 1.0 0.2 ± 0.3 (n = 12) median: 0.0 0.002
D 0.9 ± 0.6 (n = 12) median: 0.8 1.0 ± 0.9 (n = 12) median: 0.9 0.3 ± 0.4 (n = 12) median: 0.0
8 years M 1.3 ± 1.1 (n = 8) median: 0.8 1.6 ± 1.1 (n = 8) median: 1.3 0.5 ± 0.7 (n = 8) median: 0.0 0.007
D 1.4 ± 1.2 (n = 8) median: 1.0 1.3 ± 1.4 (n = 8) median: 0.8 0.5 ± 0.7 (n = 8) median: 0.0
12 years M 1.5 ± 1.0 (n = 7) median: 1.4 1.8 ± 1.1 (n = 7) median: 1.5 0.4 ± 0.4 (n = 7) median: 0.0 0.000
D 1.5 ± 1.3 (n = 7) median: 1.0 1.6 ± 1.5 (n = 7) median: 1.4 0.5 ± 0.4 (n = 7) median: 0.6

1120 | Clin. Oral Impl. Res. 23, 2012 / 1118–1122 © 2011 John Wiley & Sons A/S

et al. 2005) and/or the close monitoring of the
implants including oral hygiene instructions
and control of occlusion every year. There-
fore, one might conclude that the annual
bone loss around functional implants, after
initial bone remodelling, seems to be only lit-
tle aggravated by the occlusal load. The rea-
son why we could not find any significance
may be explained by the small sample size,
an insufficient succession period and/or more
importantly, a limited influence of occlusal
load on dental implants in patients with a
balanced occlusion.
Similar observations could be made within
the group of “non-submerged” sleeping
implants. These implants shared the same
bacterial load as the functional implants,
but lacked functional loading. At abutment
connection, the mean distance between the
implant/abutment junction and the marginal
bone for the four non-submerged sleeping
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