(2010 Weng) Influence of Microgap Location and Configuration On Peri-Implant Bone Morphology in Nonsubmerged Implants - An Experimental Study in Dogs

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Influence of Microgap Location and Configuration

on Peri-implant Bone Morphology in


Nonsubmerged Implants:
An Experimental Study in Dogs
Dietmar Weng, DDS, Dr Med Dent1/Maria José Hitomi Nagata, DDS, MSc, PhD2/
Matthias Bell, DDS, Dr Med Dent3/Luiz Gustavo Nascimento de Melo, DDS, MSc, PhD4/
Alvaro Francisco Bosco, DDS, MSc, PhD2

Purpose: It is unknown whether different microgap configurations can cause different peri-implant bone
reactions. Therefore, this study sought to compare the peri-implant bone morphologies of two implant
systems with different implant-abutment connections. Materials and Methods: Three months after
mandibular tooth extractions in six mongrel dogs, two oxidized screw implants with an external-hex con-
nection were inserted (hexed group) on one side, whereas on the contralateral side two grit-blasted
screw implants with an internal Morse-taper connection (Morse group) were placed. On each side, one
implant was inserted level with the bone (equicrestal) and the second implant was inserted 1.5 mm
below the bony crest (subcrestal). Healing abutments were inserted immediately after implant place-
ment. Three months later, the peri-implant bone levels, the first bone-to-implant contact points, and the
width and steepness of the peri-implant bone defects were evaluated histometrically. Results: All 24
implants osseointegrated clinically and histologically. No statistically significant differences between the
hexed group and Morse group were detected for either the vertical position for peri-implant bone levels
(Morse equicrestal –0.16 mm, hexed equicrestal –0.22 mm, Morse subcrestal 1.50 mm, hexed subcre-
stal 0.94 mm) or for the first bone-to-implant contact points (Morse equicrestal –2.08 mm, hexed
equicrestal –0.98 mm, Morse subcrestal –1.26 mm, hexed subcrestal –0.76 mm). For the parameters
width (Morse equicrestal –0.15 mm, hexed equicrestal –0.59 mm, Morse subcrestal 0.28 mm, hexed
subcrestal –0.70 mm) and steepness (Morse equicrestal 25.27 degree, hexed equicrestal 57.21 degree,
Morse subcrestal 15.35 degree, hexed subcrestal 37.97 degree) of the peri-implant defect, highly sig-
nificant differences were noted between the Morse group and the hexed group. Conclusion: Within the
limits of this experiment, it can be concluded that different microgap configurations influence the size
and shape of the peri-implant bone defect in nonsubmerged implants placed both at the crest and sub-
crestally. INT J ORAL MAXILLOFAC IMPLANTS 2010;25:540–547

Key words: bone morphology, equicrestal placement, histometric study, microgap, subcrestal placement

mplant therapy has become a very predictable and more attention has been paid to factors that may
I highly successful treatment option to restore eden-
tulous sites.1 The more successful it has become, the
alter or improve the implant-host interaction.2–5 Cur-
rently the connection between implant and abut-
ment is a focus of research.6 There seems to be a shift
from external to internal connection types in most
1Visiting Scholar, Department of Prosthodontics, Propaedeutics, implant systems, based on the knowledge that differ-
and Dental Materials, School of Dentistry, Christian-Albrechts-Uni- ent connection types influence microbial leakage7
versity at Kiel, Germany; Private Practice, Starnberg, Germany.
2Associate Professor, Division of Periodontics, Department of and mechanical stability,8 factors that, if left uncon-
Surgery and Integrated Clinic, Dental School of Araçatuba, trolled, can cause a series of peri-implant hard and
UNESP–Universidade Estadual Paulista, Araçatuba, Brazil. soft tissue reactions.
3Private practice, Gießen, Germany.
The microgap is the connection line between an
4Private practice, Goiania, Brazil.
implant and an abutment. This gap has been a matter
Correspondence to: Dr Dietmar Weng, Private Practice Böhm &
of intense investigation during the last 10 years. Sev-
Weng, Maximilianstraße 17, 82319 Starnberg, Germany. eral radiographic and histologic animal studies of sub-
Fax: +49-8151-652511. Email: dw@max-17.de merged and nonsubmerged implants with butt-joint

540 Volume 25, Number 3, 2010

© 2009 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF THIS ARTICLE
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Weng et al

Fig 1 (Left) Equicrestal insertion of an


implant of the hexed group. The implant
shoulder is level with the surrounding bone.

Fig 2 (Right) A Morse group implant


inserted 1.5 mm subcrestally.

connections came to the conclusions that (1) the first MATERIALS AND METHODS
bone-to-implant contact settles at a vertical radiologic
distance of 2 mm from the microgap, irrespective of The protocol of this animal study was approved by the
the location of the microgap relative to the surround- Ethical Committee for Animal Investigations of the
ing bone level at implant insertion9; (2) the bone-to- Dental School of Araçatuba, UNESP–Universidade
implant contact histologically keeps a distance of 1.3 Estadual Paulista, Araçatuba, Brazil. All surgical proce-
to 2.6 mm from the microgap depending on the loca- dures were performed under general anesthesia using
tion of the microgap relative to the surrounding bone atropine sulfate, xylazine, tiletamine/zolazepam, and
level at implant insertion10,11; and (3) the actual size of lidocaine with epinephrine. Perioperatively, antibiotics
the microgap itself does not influence the amount of (espiramizine/metronidazol) and non-steroidal anti-
peri-implant bone resorption, as long as micromove- inflammatory drugs (flunixine/meglumine) were applied.
ment does not become an additional factor.11,12 These During early wound healing, chlorhexidine diglu-
radiographic and histologic findings have been conate rinses were administered three times per week.
observed on radiographs for more than 20 years as Sample size calculations were based on the pre-
“dish-shaped” defects around the implant shoulder sumption that a mean difference of 0.5 mm with a
and termed “peri-implant bone remodeling (down to standard deviation of 0.5 should be detected at a sig-
the first thread).” They were taken into account for the nificance level of .05, warranting a statistical power of
definition of the implant success criteria from 198613 80%.
and reinforced in 199814 by eliminating from consid-
eration the amount of peri-implant bone loss in the Surgery
vertical dimension prior to the first year of loading as Six mongrel dogs were utilized in this investigation. At
a relevant factor to an implant’s success. the beginning of the study, all mandibular premolars
If seen from the perspective of implant function, the (P1 to P4) and the first mandibular molar (M1) were
amount of peri-implant bone loss during the healing extracted bilaterally. After extraction, the sockets were
and early loading phases might not be a key factor in left untreated for 3 months. Full mucoperiosteal flaps
the overall success or survival rate of a given implant. were then raised, and the ridges were flattened with
Seen from the esthetic viewpoint, however, any loss of surgical burs to obtain a buccolingual width of 6 to
peri-implant hard tissue might signal the beginning of 7 mm. Thereafter, osteotomies for two implants were
peri-implant soft tissue collapse, since bony support of drilled on each side of the mandible according to the
soft tissues is still considered the most important implant manufacturers’ protocols. On one side, two
determinant in peri-implant soft tissue stability. screw-type implants with an oxidized surface and an
It was the objective of this histometric experiment external-hex connection were placed (TiUnite Bråne-
in dogs to study the influence of different vertical mark Mk III, Nobel Biocare; diameter 3.75 mm, length
microgap locations on the peri-implant bone reac- 8.5 mm, smooth collar height 0.75 mm; hexed group)
tions in two different implant-abutment connection in such a manner that the shoulder of one implant was
types after nonsubmerged healing. located at the same level as the surrounding bone
(equicrestal position) (Fig 1), whereas the shoulder of

The International Journal of Oral & Maxillofacial Implants 541

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Weng et al

Fig 3 (Left) An implant of the hexed group


presenting with healthy peri-implant soft
tissue conditions after 3 months of non-
submerged healing.

Fig 4 (Right) An implant of the Morse group


showing uninflamed peri-implant soft tissue
structures after 3 months of nonsubmerged
healing.

Fig 5 Example of parameter assessment. MG (white line) =


microgap level; PBL = peri-implant bone levels; BICP = first bone-
HBD to-implant contact point; HBD = width of the peri-implant bone
defect; SLO = steepness of the peri-implant bone defect.
PBL
MG

SLO BICP

the second implant was placed 1.5 mm below the level Histology
of the surrounding bone (subcrestal position). The After 3 months of healing (Figs 3 and 4) the animals
same procedure was carried out on the contralateral were sacrificed by exsanguination. Two to three
side of the mandible, but two implants with a smooth mesiodistally cut ground sections were produced
collar, a grit-blasted body, and an internal Morse-taper from each implant and subsequently stained with
connection were inserted (Ankylos A8, Dentsply Fri- toluidine blue solution.15 The following parameters
adent; diameter 3.5 mm, length 8 mm, smooth collar were evaluated histometrically (Fig 5):
height 1.5 mm; Morse group) (Fig 2). In the six animals,
left and right sides were alternated between implant 1. Peri-implant bone level (PBL): vertical distance
systems as well as the anterior and posterior positions between the most coronal point of the peri-
of the subcrestal and equicrestal groups. On each side, implant bone and the implant shoulder; expressed
however, only one implant system was used, and the as a positive value if the peri-implant bone was
vertical positions of the implant shoulders were the located coronal to the implant shoulder
same on each side of the mandible. Finally, healing 2. Bone-to-implant contact point (BICP): vertical dis-
abutments were attached manually to the implants tance between the most coronal bone-to-implant
according to the manufacturers’ guidelines. The heal- contact point and the implant shoulder; expressed
ing abutments of the subcrestally inserted implants as a negative value if the bone-to-implant contact
were chosen to be 1.5 to 2 mm higher than those for point was located apical to the implant shoulder
the equicrestal implants so as to keep the tops of the 3. Horizontal bone distance (HBD): horizontal dis-
healing abutments at a similar height above the tance between the most coronal point of the peri-
mucosa. The flaps were then adapted around the heal- implant bone and a vertical line along the outer
ing abutments and sutured. The implants were left in implant surface; expressed as a negative value
this nonsubmerged healing mode for 3 months. unless bone had grown onto the implant shoulder
Sutures were removed after 1 week. Swabbing and 4. Peri-implant bone slope (SLO): angle between a
rinsing with chlorhexidine digluconate was carried out line extending along the peri-implant bone defect
three times per week. and a vertical line along the outer implant surface

542 Volume 25, Number 3, 2010

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Weng et al

Fig 6 (Left) Implant of the equicrestal


Morse group. Note the overall maintenance
of PBL and the tight cuff (small SLO value) of
the peri-implant bone around the microgap
area. Red dots indicate microgap. Yellow line
shows bone level at implant placement.

Fig 7 (Right) Implant of the equicrestal


hexed group. Note the typical “dish-shaped”
character of the bone defect extending to the
first implant thread. Red dots = microgap;
yellow line = bone level at implant placement.

1 mm

1 mm

Statistics insertion depth of the implants, the histologic sec-


Each parameter was measured on both the mesial tions presented well-osseointegrated implants in
and distal sides of a histologic section and summa- mature bone structures (Figs 6 to 9). When the
rized to result in a mean value per section. These implants were inserted subcrestally, the PBLs were
means of the two to three sections available per located coronal to the implant shoulder (Figs 8 and 9).
implant were then summarized to obtain a mean per With equicrestal placement, PBL usually was found at
implant. Therefore the statistical unit was the implant or slightly below the implant shoulder (Figs 6 and 7).
(equal to the animal). Comparisons of the two In most of the sections, BICP was located apical to the
implant systems within the same vertical groups and implant shoulder. Only around implants from the sub-
of the same vertical positions within the same crestally placed Morse group was bone tissue found
implant system were made by using paired t tests. overgrowing the implant shoulder and establishing
the first bone-to-implant contact on the crestal face of
the implant shoulder (Fig 8). The horizontal extent of
RESULTS the peri-implant bone defect and its “dish-shaped”
character were more pronounced in the hexed group,
Clinical Results especially when placed subcrestally (Fig 9). The “fun-
The 3-month healing period was uneventful. All nel” of bone around the implants was narrower in the
implants osseointegrated clinically and did not show Morse groups, with regular bone growth over the
any signs of mobility at the time of sacrifice. Loosen- implant shoulder when the Morse implants were
ing of the healing abutments was not noted. The clin- inserted subcrestally (Fig 8).
ical peri-implant tissue condition was characterized
by healthy or occasional slightly inflamed mucosal Histometric Measurements
margins. Means, standard deviations, and P values of the four
histometric parameters are summarized in Table 1. A
Histologic Findings graphic depiction of those results can be found in
Regardless of the implant system and the vertical Figs 10 and 11. Between the Morse group and the

The International Journal of Oral & Maxillofacial Implants 543

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Weng et al

Fig 8 (Left) Implant of the subcrestal


Morse group. Note the narrow “funnel”
establishing close proximity between the
peri-implant bone, the healing abutment,
and the microgap area. Bone tissue has
grown onto the implant shoulder. Red dots
= microgap; yellow line = bone level at
implant placement.

Fig 9 (Right) Implant of the subcrestal


hexed group. Note the establishment of a
classical “dish-shaped” defect around the
microgap-abutment complex. The peri-
implant bone tissue seems to avoid direct
contact with the microgap. Red dots =
microgap; yellow line = bone level at
implant placement.

1 mm

1 mm

Table 1 Histometric Measurements (Means ± Standard Deviations)


Group (n = 6 each) PBL (mm) BICP (mm) HBD (mm) SLO (deg)

Equicrestal Morse group


Mean –0.16 ± 0.83 –2.08 ± 1.20 –0.15 ± 0.16* 25.27 ± 25.20**
Range –0.61 to 1.38 –0.86 to 4.31 –0.42 to 0.05 8.33 to 76.01
Equicrestal hexed group
Mean –0.22 ± 0.80 –0.98 ± 0.41 –0.59 ± 0.16 57.21 ± 29.84
Range –1.44 to 0.76 –1.52 to –0.52 –0.39 to –0.75 33.76 to 113.94
Subcrestal Morse group
Mean 1.50 ± 0.66 –1.26 ± 1.48 0.25 ± 0.22** 15.35 ± 11.70*
Range 0.61 to 2.38 –4.09 to 0.25 –0.07 to 0.47 9.07 to 39.06
Subcrestal hexed group
Mean 0.94 ± 0.44 –0.76 ± 0.41 –0.70 ± 0.28 37.91 ± 18.57
Range 0.35 to 1.44 –1.53 to –0.32 –1.13 to –0.32 22.76 to 72.35
PBL = peri-implant bone level; BICP = bone-to-implant contact point; HBD = horizontal bone distance of the peri-implant defect;
SLO = peri-implant bone slope of the peri-implant defect.
*P < .005 versus hexed group placed at same level; **P < .001 versus hexed group placed at same level; all other values P > .05
between groups placed at same level.

hexed group, statistically significant differences were the Morse implants and no differences for the hexed
detected for the parameters HBD and SLO in the implants. A comparison of PBL was not carried out
equicrestal and subcrestal groups. Comparisons of because differences in the height of the peri-implant
the two vertical positions within the same implant bone can be expected whenever the implants are
system group (with regard to BICP, HBD, and SLO) placed in different vertical positions.
showed a significant difference for HBD (P < .05) in

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Weng et al

Fig 10 (Left) Illustration of the average


bone morphology for the Morse group (left
side) and the hexed group (right side) in
equicrestally placed implants. Drawing is
based on the mean values of the parame-
ters PBL, BICP, and HBD. The horizontal line
separating the orange from the red area
delineates the bone level at the time of
implant placement.

Fig 11 (Right) Illustration of the average


bone morphology for the Morse group (left
side) and the hexed group (right side) in
subcrestally placed implants. Drawing is
based on the mean values of the parame-
ters PBL, BICP, and HBD. The horizontal line
separating the orange from the red area
delineates the bone level at the time of
implant placement.

1 mm 1 mm

DISCUSSION Also, Piattelli et al16 observed the BICP at –2.11 mm in


equicrestal, nonsubmerged, titanium plasma–sprayed
Regardless of the implant system used or the vertical implants. However, when they inserted the implants 1
position of the microgap, it was generally observed to 1.5 mm subcrestally, Piattelli et al16 found a BICP of
that the level of the peri-implant bone was main- –3.65 mm. A possible explanation might be that their
tained quite well. The PBL was kept close to 0 mm in implants underwent early and immediate loading.
the equicrestal group and close to 1.5 mm in the sub- Considerably better BICP values were found by Abra-
crestal group. Although the subcrestal hexed group hamsson et al 17; their equicrestal, nonsubmerged
presented a difference of more than 0.5 mm in PBL implants exhibited a BICP of –0.68 mm after a healing
compared to the Morse group, the difference was not time of 6 months. A reason for their finding might be
significant. Despite these stable results for PBL, it may the fact that they used implants with a rough surface
be noteworthy that the BICP established itself consid- that extended to the implant shoulder, without a
erably below the microgap in both the equicrestal smooth collar. This may be a hint that microroughen-
group (hexed group –0.98 mm, Morse group –2.08 ing of implants to the level of the microgap might
mm) as well as in the subcrestal group (hexed group help to decrease the distance between the implant
–0.76 mm, Morse group –1.26 mm). The equicrestal shoulder and the BICP in equicrestally placed
BICP difference of 1.10 mm was not significant implants. The fact that in the present study BICP val-
because of the higher standard deviation in the Morse ues were better (although insignificantly so) for both
group, which was caused by an outlier. Without this equicrestally and subcrestally placed implants in the
outlier, the BICP value for the equicrestal Morse group hexed groups (0.75-mm smooth collar height) than in
would have amounted to a mean of 1.63 mm with a the Morse groups (1.5 mm smooth collar height)
standard deviation of 0.55 mm. Nevertheless, it seems lends support to this idea.
that BICP in equicrestally inserted, nonsubmerged Pronounced differences were noticed when the
implants with a smooth collar can be found around 1 horizontal parameters HBD and SLO were compared.
to 1.5 mm below the microgap. This finding is con- These parameters measure how close the peri-
firmed by Hermann et al,10 who demonstrated a BICP implant bone is to the microgap area in a horizontal
of –1.68 mm in equicrestal nonsubmerged implants. direction. The most coronal point of the peri-implant

The International Journal of Oral & Maxillofacial Implants 545

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Weng et al

bone was chosen as the reference point for HBD. In group. Of course the question arises whether the hori-
histologic sections with an asymptotic shape (eg, Fig zontal offset between implant and healing abutment
5, right side), this might overestimate HBD. As an alter- is the only factor accounting for this difference. As
native, the bone tangents as described by Gomez- shown by Zipprich et al,8,20 mechanical micromove-
Roman et al18 could have been used. However, the ment is extremely low in Morse taper–connected
use of the most coronal point accounts for the fact implant systems, which may allow for reduced micro-
that the original bone level was a flattened ridge. In bial contamination of the microgap and subsequently
both the equicrestal group and the subcrestal group, lower concentrations of bacterially produced bone-
the bone was four times closer to the implant-abut- resorbing agents. Furthermore, Hansson21,22 was able
ment connection in Morse implants versus hexed to show that crestal bone receives less stress upon
implants. This difference in HBD was statistically axial loading if the implant-abutment connection has
highly significant. Earlier studies did not evaluate the a Morse-taper design. The overall impression in the
horizontal effects of the implant-abutment connec- subcrestal as well as in the equicrestal Morse group
tion. Only Tarnow et al19 assessed HBD radiographi- was that of a considerably narrower “dish-shaped”
cally in 36 patients 1 to 3 years after stage-two defect compared to the hexed groups.
surgery in implants with a microgap configuration Because in the present study the healing abut-
similar to that used in the present external-hex ments were not repeatedly loosened and retightened
implants. Tarnow et al observed considerably higher to simulate prosthetic procedures (impression, try-in,
HBD values (–1.34 mm and –1.40 mm) than in the crown insertion), one may ask whether such proce-
present study, but the earlier study described a clini- dures would have a worsening effect on the appear-
cal situation several years after loading. As a conse- ance and shape of the “bone funnel” around the
quence of the low HBD values in the Morse groups, implant. In the studies of Hermann et al,9,10 the non-
SLO, ie, the angulation of the peri-implant bone submerged, equicrestally placed implant type C
defect, was only half as big in the Morse group as in (butt-joint connection without horizontal offset) was
the hexed group, again at a high significance level. subjected to a triple loosening and retightening pro-
Obviously, the implant connection type of the hexed cedure of the healing abutment, and histologic exam-
group (non–Morse taper butt joint with no horizontal ination after 6 months showed a typical dish-shaped
offset) seemed to exert a more horizontally pro- defect. This defect and the corresponding loss of peri-
nounced influence on the peri-implant bone tissue implant bone contact (ie, BICP value), however, were
than the connection type of the Morse group (Morse- already detectable in the very first radiograph 4
taper connection with horizontal offset). For both the weeks after implant placement, ie, 3 months before
Morse and hexed groups, SLO was 10 to 20 degrees the first loosening and retightening procedure was
smaller when a subcrestal insertion mode was cho- performed. Furthermore, the triple unscrewing and
sen compared to an equicrestal placement. However, screwing procedures, done 4, 5, and 5.5 months after
this difference was not statistically significant. implant placement, did not seem to produce addi-
Another significant difference was found when tional detrimental effects on the peri-implant bone.
subcrestal insertion was compared to equicrestal Therefore, it may be concluded that the bone-resorb-
insertion in the Morse group with regard to HBD (0.25 ing effect of a micromechanically and microbiologi-
mm versus –0.15 mm). The low standard deviation of cally challenged implant-abutment connection
0.22 mm in the subcrestal group showed that, in balances out the possibly detrimental effects of
almost all the sections of the Morse group, bone had repeated abutment changes.
grown onto the crestal face of the implant shoulder
when they were inserted apical to the bone level. It
seemed that the peri-implant bone accepted the CONCLUSIONS
space offered by the horizontal offset and
approached the implant-abutment interface by Within the limits of this animal experiment it can be
actively growing into this void. Interestingly enough, concluded that, 3 months after insertion of nonsub-
the remaining horizontal distance between the bone merged implants: (1) the resorption of the original
and the healing abutment was always smaller in the peri-implant bone height can be kept within 0.5 mm,
subcrestally placed Morse group than in the subcre- (2) the first bone-to-implant contact establishes itself
stally inserted hexed group; with a manufactured hor- 1 to 1.5 mm apical to the implant shoulder regardless
izontal offset of 0.5 mm and a mean HBD of 0.25 mm, of the vertical position of the microgap, and (3) the
the mean distance between bone and healing abut- “dish-shaped” defect configuration is more pro-
ment amounted to only 0.25 mm, compared to the nounced in a non–Morse taper, butt-joint connection
mean HBD of –0.70 mm seen in the subcrestal hexed without horizontal offset. The clinical consequences of

546 Volume 25, Number 3, 2010

© 2009 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF THIS ARTICLE
MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Weng et al

these observations might be that the amount and 10. Hermann JS, Buser D, Schenk RK, Cochran DL. Crestal bone
shape of a peri-implant “dish-shaped” bone defect changes around titanium implants. A histometric evaluation
of unloaded non-submerged and submerged implants in the
depend on the implant-abutment connection (espe-
canine mandible. J Periodontol 2000;71:1412–1424.
cially if the implant is placed subcrestally), and that 11. Hermann JS, Schoolfield JD, Schenk RK, Buser D, Cochran DL.
narrowing the “bone funnel” of such defects might be Influence of the size of the microgap on crestal bone changes
beneficial for the peri-implant soft tissue support. around titanium implants. A histometric evaluation of
unloaded non-submerged implants in the canine mandible.
J Periodontol 2001;72:1372–1383.
12. King GN, Hermann JS, Schoolfield JD, Buser D, Cochran DL.
ACKNOWLEDGMENTS Influence of the size of the microgap on crestal bone levels in
non-submerged dental implants: A radiographic study in the
The authors wish to express their gratitude to Mrs Waltraut Schnei- canine mandible. J Periodontol 2002;73:1111–1117.
der for the preparation of the histologic sections in this study. This 13. Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-
study was supported by a grant from Dentsply Friadent. term efficacy of currently used dental implants: A review and
proposed criteria of success. Int J Oral Maxillofac Implants
1986;1:11–25.
14. Zarb GA, Albrektsson T. Consensus report: Towards optimized
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