Received: 27 September 2016 | Revised: 12 July 2018 | Accepted: 9 August 2018

DOI: 10.1111/clr.13367

ORIGINAL RESEARCH

Histological and micro‐CT analysis of peri‐implant soft

and hard tissue healing on implants with different healing
abutments configurations

André Barbisan Souza1 | AbdulMonem Alshihri1,2 | Peer W. Kämmerer3 | Maurício

4 1
G. Araújo | German O. Gallucci

1
Division of Regenerative and
Implant Sciences, Department of Abstract
Restorative Dentistry and Biomaterials Objective: The aim of this study was to assess the effect of different abutment con‐
Sciences, Harvard School of Dental
Medicine, Boston, Massachusetts figurations on peri‐implant soft and hard tissue healing.
2
Department of Prosthodontics and Materials and Methods: Two‐piece dental implants, 3.5 mm in diameter and 8 mm in
Biomaterial Sciences, King Saud University,
length, were placed in four beagle dogs. Two different transmucosal healing abut‐
Riyadh, Saudi Arabia
3 ment configurations were randomly selected: one with a wide emergence profile
Department of Oral, Maxillofacial and
Plastic Surgery, University Medical Centre (WE) (45° angulation with implant long axis) and the other with a narrow emergence
Rostock, Germany
profile (NE) (15° angulation with implant long axis). After four months of healing, the
4
Department of Dentistry, State University
of Maringá, Paraná, Brazil animals were sacrificed. Micro‐CT scans were taken for mesio‐distal analysis; subse‐
quently, the biopsies were prepared for bucco–lingual histometric analyses. Several
Correspondence
German O. Gallucci, Department of measurements were taken using the following reference points: marginal mucosal
Restorative Dentistry and Biomaterials level (MML), apical barrier epithelium (aBE), implant shoulder (IS), marginal bone crest
Sciences, Harvard School of Dental
Medicine, Boston, MA. (BC), and first bone‐to‐implant contact (fBIC).
Email: german_gallucci@hsdm.harvard.edu Results: In the micro‐CT analysis, the distance from IS‐fBIC was 1.11 ± 0.66 mm for

Funding information WE and 0.12 ± 0.21 mm for NE (p = 0.004). The IS‐BC of WE was −0.54 ± 0.80 mm,
DENTSPLY Implants; Department of whereas NE presented 0.76 ± 0.48 mm (p = 0.002). The histometric analysis showed
Restorative Dentistry and Biomaterials
Sciences ‐ Harvard School of Dental that both groups presented comparable dimensions of peri‐implant biologic width
Medicine (p > 0.05). However, in the distance from IS to BC, the WE showed a mean distance
of −0.66 ± 0.78 mm while NE was 0.06 ± 0.42 mm (p = 0.039); the IS to fBIC was
0.89 ± 0.68 mm for WE while NE was 0.30 ± 0.30 mm (p = 0.041).
Conclusion: The design of the transmucosal component can influence the establish‐
ment of the peri‐implant biologic width. The flat and wide emergence profile induced
an apical displacement of the peri‐implant biologic width and more bone loss.

KEYWORDS
abutment design, bone remodeling, peri‐implant healing

1 | I NTRO D U C TI O N survival rate is conditioned by the integrity and stability of the

osseointegration phenomenon. In addition, specific criteria such
Dental implant treatment outcomes are influenced by associ‐ as peri‐implant soft and hard tissue stability and patient‐cen‐
ated long‐term survival and success rates (Albrektsson, Zarb, tered outcomes are also considered when assessing implant suc‐
Worthington, & Eriksson, 1986; Buser, Weber, & Lang, 1990). The cess (Papaspyridakos, Chen, Singh, Weber, & Gallucci, 2012). The

Clin Oral Impl Res. 2018;1–9. wileyonlinelibrary.com/journal/clr © 2018 John Wiley & Sons A/S. | 1
Published by John Wiley & Sons Ltd
2 | SOUZA et al.

amount of peri‐implant bone loss following implant placement and Maringá, Brazil, approved the research protocol (N° 062/2010).
abutment connection is a major factor for implant long‐term suc‐ This approval was revised and deemed acceptable according to
cess. Several factors including implant design, surface treatment, the Harvard Medical Area Standing Committee on Animals and
and type of implant connection appear to influence the peri‐implant the Office for Research Subject Protection of the Harvard Medical
hard tissue stability (Albrektsson et al., 2014; Alharbi et al., 2015; School. This study also states compliance with ARRIVE Guidelines
Galindo‐Moreno et al., 2015; Hermann, Buser, Schenk, Schoolfield, for animal research (Kilkenny, Browne, Cuthill, Emerson, & Altman,
& Cochran, 2001). 2010).
Peri‐implant bone remodeling after implant placement is con‐
sidered a physiological process that occurs as a part of the estab‐
2.1 | Animals
lishment of peri‐implant biologic width (Berglundh et al., 1991;
Cochran et al., 2009). This process occurs irrespective of whether a Four beagle dogs aged between 12 and 15 months weighing
one‐stage (i.e., transmucosal healing) or a two‐stage surgical proto‐ 10–12 kg were used in this study. Appropriate housing was provided
col (i.e., a second stage procedure) is required to expose the implant for the experimental animals. This housing was maintained and
(Berglundh & Lindhe, 1996, Hermann, Buser, et al., 2001). Several cleansed every day. The animals had adequate structures for resting
protocols attempting to minimize the amount of peri‐implant bone and sleeping under controlled temperature and had unrestricted ac‐
remodeling were reported in the dental literature. A well‐docu‐ cess to water and a nutritionally balanced diet.
mented approach is the use of a smaller diameter abutment on top
of a wider implant platform resulting in a platform switching (Lazzara
2.2 | Surgical interventions and experimental model
& Porter, 2006; Linkevicius & Apse, 2008). This method was intro‐
duced as a way of minimizing the amount of bone remodeling by For the surgical procedures, the dogs were anesthetized with intra‐
using a narrower abutment connection on top of a wider implant venously administered xylazine (Rompun 0.1 ml/kg, Bayer do Brazil
platform in a two‐piece dental implant. S/A, São Paulo, Brazil) and ketamine 10% (8 mg/kg; Agener União,
Several clinical trials have reported less peri‐implant bone São Paulo, Brazil). In the first surgical procedure, the mandibular
loss when implants with horizontal offset have been employed as premolars (P1–P4) and the first molar (M1) were extracted. For the
opposed to the standard platform connection (Canullo, Fedele, extraction, the roots were first hemi‐sected with a diamond bur, only
Iannello, & Jepsen, 2010; Canullo, Rosa, Pinto, Francischone, & intra‐sulcular incisions were performed, and the roots were carefully
Gotz, 2012; Crespi, Capparè, & Gherlone, 2009). It was stated that removed with the use of elevators. Interrupted sutures were placed.
the increased horizontal offset between the implant shoulder to The sutures were removed 10 days after extraction. Once every
the implant/abutment connection would lead to superior results. second day, the animals were exposed to mechanical tooth clean‐
However, the amount of horizontal offset does not affect the peri‐ ing using a toothbrush embedded in chlorhexidine gluconate 0.12%.
implant bone loss when more than 0.3 mm horizontal distance is Following a three‐month healing period, the animals were anes‐
established between implant shoulder to abutment connection thetized using the same protocol previously described for the im‐
(Finelle et al., 2015; Galindo‐Moreno et al., 2016). Controversially, plant surgery. Implants were installed on both sides of the mandible
other studies have shown that the mismatch between the implant/ with a minimal distance of 4 mm between them and 1 mm subcre‐
abutment connection to implant shoulder may play a minimal role in stally. For both groups, two‐piece pure titanium (grade IV) dental
the bone remodeling (Becker et al., 2007, 2009 ); other systemic and implants with an acid‐etched surface (Dentsply Implants, Waltham,
local factors may also influence the amount of peri‐implant bone loss MA, USA) were used. The implants had a platform shifting design
(Galindo‐Moreno et al., 2016). with 0.3 mm of horizontal offset and conical internal connection. In
Furthermore, it is possible that the geometry of the implant abut‐ this study, all implants had the same dimensions: 3.5 mm in diameter
ment associated with a horizontal offset implant design could also and 8 mm in length. Two implants in each dog were placed, for a total
influence the peri‐implant bone remodeling (Becker et al., 2007). of eight implants in each experimental group. A total of 16 implants
However, the evidence on the effect of different abutment config‐ were included in the analysis of this study. The transmucosal healing
urations on peri‐implant soft and hard tissue healing is scarce. The abutment was an internal conical tapered implant‐abutment connec‐
objective of this preclinical study was to assess in vivo the effect of tion, inserted at the time of implant placement (Figure 1).
different transmucosal abutment configurations on the peri‐implant Two different investigational groups, with differing transmu‐
soft and hard tissue healing. cosal abutment designs, were assessed in this study: one with a
wide emergence profile and an angulation of 45° with implant long
axis (WE), and the other with a narrow emergence profile and an
2 | M ATE R I A L A N D M E TH O DS angulation of 15° with implant long axis (NE; Figure 2). Both heal‐
ing abutments were made of pure titanium. The type of abutment
The study was performed at the University of Maringá in Parana, was randomly allocated on each side of the mandible using a per‐
Brazil, and the Harvard School of Dental Medicine in Boston, mutated‐block randomization protocol, with a block size of six.
Massachusetts. The ethical committee of the State University of Post‐surgical standardized radiographs were obtained of all implants
SOUZA et al. | 3

(a) (b)

(c) (d)

F I G U R E 1 Clinical photographs
illustrating the following procedures
performed: (a) full‐thickness flap
elevation, (b) implant placement, (c)
interrupted sutures at immediate
postoperative, and (d) healed sites with
4 months of follow‐up

high‐resolution micro‐CT analysis (Xradia MicroXCT‐200 system,

Pleasanton, CA). The parameters, system settings, and images
acquirement followed the study of Finelle et al. (2015). The fol‐
lowing landmarks were identified: implant shoulder (IS), marginal
bone crest (BC), first bone‐to‐implant contact (fBIC), and horizon‐
tal bone apposition (HBA) at the horizontal axis of the implant
platform (Figure 3). Using these landmarks, the following distances
were measured at mesial and distal aspects of the implants: (a) BC‐
IS, defined by the vertical distance from BC to IS; this distance was
represented with positive (+) and negative (−) results, according to
the presence of the location of marginal bone coronally (+) or api‐
F I G U R E 2 Illustration representing the two studied groups: (a) a
cally to the implant shoulder (−); (b) IS‐fBIC, defined as the vertical
wide emergence profile with 45° angulation (WE) and (b) a narrow
emergence profile with 15° angulation (NE) distance from IS to fBIC; and (c) HBA, defined by the horizontal
distance of implant platform to the greatest inward extent of bone
ingrowth on the IS.
immediately after implant placement, according to a previously de‐
scribed technique (Hermann, Schoolfield, Schenk, Buser, & Cochran,
2.4 | Histological preparation
2001). During the healing period, a mechanical plaque control reg‐
imen using a toothbrush and topical application of a custom‐made All the samples containing the implants and surrounding soft and
chlorhexidine gel (0.12%) was provided every second day until the hard tissue were carefully resected and fixed in a 4% neutral‐buff‐
end of the experiment. ered formalin solution. Each implant with surrounding tissue was
After 4 months of healing, the dogs were euthanized with an cut by a hand saw into different sections. Subsequently, immersion
overdose of ketamine and perfused, through the carotid arteries, fixation and preparation for histological examination as described
with a fixative containing a mixture of 5% glutaraldehyde and 4% by Donath and Breuner (1982) were performed. Each implant sam‐
formaldehyde (Karnovsky, 1965). The mandibles were sectioned, ple with the surrounding bone was cut into slices of 5 mm with a
and tissue samples, comprising the implant and the surrounding soft water‐cooled saw (Exakt, Hamburg, Germany). The direction of the
and hard peri‐implant tissues, were removed using a diamond saw slices was perpendicular to the implants’ axis. After embedding of
(Exact®, Norderstedt, Hamburg, Germany). the slides with PMMA (Technovit 7200, Heraeus Kulzer, Hanau,
Germany), samples were ground to a thickness of 30–40 μm. Two
samples per implant were obtained, one was stained with hematoxy‐
2.3 | Micro‐CT analysis
lin and eosin (HE) and for the other sample, van Gieson staining was
The biopsies comprising all implants included in this study were used. All slides were examined with a Leica DM8000 M microscope
examined first with a radiographic computed microtomogra‐ (Leica microsystems, Heidelberg, Germany), and the images were
phy (micro‐CT) system. Micro‐CT images were subjected to a digitalized for further evaluation.
4 | SOUZA et al.

(a) (b) (a) (b)

F I G U R E 3 Micro‐CT image at the mesio‐distal aspect of (a) WE F I G U R E 4 Microphotograph representing the buccal–lingual
group and (b) NE group. The following landmarks were used for section of (a) WE group and (b) NE group. The following landmarks
the radiographic analysis: IS, implant shoulder; fBIC, first bone‐to‐ were used for the histometric analysis: IS, implant shoulder; fBIC,
implant contact; BC, marginal bone crest; and HBA, horizontal bone first bone‐to‐implant contact; BC, marginal bone crest; MML,
apposition marginal mucosal level; and aBE, apical barrier epithelium. Note the
apical displacement of the peri‐implant bone crest of WE compared
to the NE 4 months after implant placement. Original magnification
×2.5. Hematoxylin–eosin (HE) staining
2.5 | Histometric analysis
The images were transferred to a computer pixel counting software Four months after implant placement, the peri‐implant soft tissue
(Image J, U.S. National Institutes of Health) where the measurements presented as clinically healed and attached to the healing abutment.
were performed. The following landmarks were identified: MML:
marginal mucosal level; fBIC: first bone‐to‐implant contact; IS: implant
3.1 | Gross histological description
shoulder; BC: Marginal Bone Crest and aBE: apical Barrier Epithelium
(Figure 4). In all specimens, the following histometric variables were After 4 months of healing, the peri‐implant soft tissue configuration
measured at buccal and lingual aspects: (a) height of MML to fBIC followed the dimensions and format of the healing abutment inter‐
(heMML‐fBIC); (b) length of MML to fBIC (leMML‐fBIC); (c) MML‐IS; face. Both groups presented a keratinized oral epithelium continu‐
(d) MML‐BC; (e) MML‐aBE; (f) aBE‐fBIC; (g) IS‐BC, in sites with BC ously with the barrier epithelium. Apically the specimens exhibited
above the IS a positive (+) value was given, whereas those with BC a dense connective tissue compartment on the healing abutment
below IS a negative (−) value was used; and (h) IS‐fBIC. The area of extending to the implant platform. The connective tissue was found
connective tissue compartment at implant‐abutment interface was in the volumetric space delineated by the implant shoulder and the
also measured (mm2) at mesial and distal aspects for both groups. healing abutment design. In a histological observation, the WE group
presented less area of connective tissue compartment at the im‐
plant‐abutment interface (mean: 0.74 mm2) compared to the
2.6 | Statistical analysis 2
NE (mean: 0.24 mm ).
Descriptive analysis with mean values, median, and standard devia‐
tion was conducted for all variables. The implant was used as the unit
3.2 | Micro‐CT analyses
of analysis. Comparisons between the two experimental groups were
taken for the mesial and distal aspects of Micro‐CT analysis and buc‐
3.2.1 | Marginal bone crest to implant shoulder
cal and lingual for the histological evaluation. The mean values were
obtained for each implant site and each type of analysis (e.g., mesial NE group presented a mean value of +0.76 ± 0.48 mm, whereas WE
and distal for Micro‐CT/buccal and lingual for histometric). Shapiro– group was −0.54 ± 0.80 mm. The corresponding median values were
Wilk normality test was applied, and comparison between the two ex‐ +0.71 mm and −0.51 mm for NE and WE groups, respectively. The
perimental groups was conducted using independent t test. A p‐value statistical analysis demonstrated a statistically significant difference
<0.05 was used to determine statistically significant differences. between the two groups (p = 0.002). For details, see Table 1.

3.2.2 | Implant shoulder to first bone‐implant‐

3 | R E S U LT S
contact
All experimental sites included in this study healed uneventfully. In the analysis of the implant shoulder to first bone‐implant‐
Implant osseointegration was assessed clinically and radiographically. contact (IS–fBIC), the mean values and standard deviation were
SOUZA et al. | 5

TA B L E 1 Mean, standard deviation

Group differences
(SD), median values (mm), and group
WE NE t test
differences in micro‐CT analysis of WE
and NE groups Mean SD Median Mean SD Median p‐value

IS—BC −0.54 0.80 −0.51 0.76 0.48 0.71 0.002*

IS—fBIC 1.11 0.66 1.13 0.12 0.21 0.00 0.004*
HBA 0.00 – 0.00 0.23 0.22 0.16 0.010*

Note. BC: bone crest; fBIC: first bone‐to‐implant contact; HBA: horizontal bone apposition; IS: im‐
plant shoulder; NE: narrow emergency group; WE: wide emergency group.
Significance testing was confirmed by independent t test.
*
Statistically significant difference.

TA B L E 2 Mean, standard deviation (SD), median values (mm), and group differences in histometric analysis of WE and NE groups

Group differences
WE NE t test

Mean SD Median Mean SD Median p‐value

heMML—fBIC 2.03 0.34 1.93 2.35 0.32 2.46 0.130

leMML—fBIC 3.10 0.79 3.13 2.77 0.41 2.80 0.194
MML—IS 2.23 0.51 2.23 2.55 0.68 2.11 0.200
MML—BC 2.71 0.70 2.80 2.61 2.80 2.54 0.380
MML—aBE 1.82 0.36 1.80 1.67 0.33 1.59 0.238
aBE—fBIC 1.28 0.43 1.34 1.10 0.04 1.15 0.249
IS—BC −0.66 0.78 −0.70 0.06 0.42 0.04 0.039*
IS—fBIC 0.89 0.68 0.69 0.30 0.30 0.11 0.041*

Note. aBE: apical barrier epithelium; BC: bone crest; fBIC: first bone‐to‐implant contact; heMML: height of marginal mucosal level; IS: implant shoulder;
leMML: length of marginal mucosal level; MML: marginal mucosal level; NE: narrow emergency group; WE: wide emergency group.
Significance testing was confirmed by independent t test.
*
Statistically significant difference.

0.12 ± 0.21 mm for NE sites and 1.11 ± 0.66 mm for WE (Table 1). and NE was 2.77 ± 0.41 mm. The difference in length was not statis‐
Statistically significant differences between groups were observed tically significant (p = 0.194), showing an apical displacement of the
(p = 0.004). marginal peri‐implant soft tissue in those sites with WE.
The length of junctional barrier epithelium (MML–aBE) was
1.82 ± 0.36 mm for WE; the corresponding value for NE was
3.2.3 | Horizontal bone apposition
1.67 ± 0.33. The slight numeric difference between groups was not
The Horizontal bone apposition (HBA) was described by mean val‐ statistically significant (p = 0.238). The length of the peri‐implant
ues and standard deviation; additionally, the percentage of sites with connective tissue attachment (aBE–fBIC) was 1.28 ± 0.43 mm for
HBA was evaluated. In the NE sites, 62.5% presented HBA with a WE and 1.10 ± 0.04 mm for NE sites. In sum, there was no significant
mean value was 0.22 ± 0.18 mm, whereas in the WE, none of the difference in the dimensions of connective tissue attachment in the
implants (0%) presented HBA and the corresponding mean value two types of healing abutment (p = 0.249).
was 0.00 ± 0.00 mm. A statistically significant difference between
groups was found (p = 0.010).
3.3.2 | Dimensions peri‐implant hard tissue
The dimensions of the peri‐implant bone level were described by
3.3 | Histometric measurements
the distances between implant shoulder (IS) to the marginal bone
crest (BC) and first bone‐to‐implant contact (fBIC). The distance be‐
3.3.1 | Dimensions of peri‐implant soft tissue
tween IS–BC was −0.66 ± 0.78 mm for WE and 0.06 ± 0.42 mm for
The results of the histometric analysis are described in NE (Figure 5). The difference of this variable between groups was
Table 2. The height of peri‐implant soft tissue (heMML‐fBIC) of WE on average 0.60 mm, and there was a statistically significant differ‐
was 2.03 ± 1.93 mm, whereas NE was 2.35 ± 0.32 mm. The length ence between them (p = 0.039). The distance between IS‐fBIC was
of peri‐implant soft tissue (leMML‐fBIC) of WE was 3.10 ± 0.79 mm, 0.89 ± 0.68 mm for WE, and the corresponding value for NE was
6 | SOUZA et al.

0.30 ± 0.30 mm (Figure 6). There was also a statistically significant compared to a narrower and straight healing abutment (NE). It
difference between groups (p = 0.041) with a mean difference of is worth noting that regardless of the use of different abutment
0.59 mm between WE and NE (Table 2). designs, the length of peri‐implant soft tissue resulted with sim‐
ilar dimensions in both groups. This outcome revealed that the
peri‐implant biologic width followed the shape of the abutment
4 | D I S CU S S I O N design, but with similar dimensions. Other studies demonstrated
that irrespective of the implant design (Abrahamsson, Berglundh,
This study investigated the effect of different transmucosal abut‐ Wensström, & Lindhe, 1996) or after type of resective surgery
ment configurations on peri‐implant hard and soft tissue stability (Sukekava et al., 2016), the epithelial and connective tissue com‐
after placement of a two‐piece dental implant. The findings dem‐ ponents will arrange with similar dimensions. In contrast, other
onstrated that both groups (WE and NE) presented comparable di‐ studies reported that the vertical position of the implant shoulder
mensions of peri‐implant biologic width. However, the micro‐CT and according to the bone crest (Farronato et al., 2012) and the im‐
histological analysis verified a larger amount of peri‐implant bone plant macrodesign (Becker et al., 2007) could influence the length
remodeling at WE sites compared to NE. of the epithelium attachment. However, all of them reported
The dimensions of peri‐implant epithelial and connective tissue stable and similar dimensions of connective tissue attachment.
dimensions are a representative evaluation of the peri‐implant bio‐ Berglundh, Abrahamsson, Welander, Lang, and Lindhe (2007)
logic width (Cochran et al., 2013; Sukekava, Pannuti, Lima, Tormena, clearly demonstrated the chronological formation of peri‐implant
& Araujo, 2016). Previous studies demonstrated that the establish‐ mucosal attachment with transmucosal healing. The study showed
ment of peri‐implant biologic width on a dental implant with a hori‐ that, in 2 weeks, mostly fibroblasts were present at implant inter‐
zontal offset configuration led to different outcomes at the implant face, and at 6–8 weeks, a mature epithelium barrier was found.
shoulder/abutment interface (Canullo et al., 2010; Canullo et al., The apical part of the connective matrix was comprised mostly
2011; Canullo et al., 2012, Rocha et al., 2016, Strietzel, Neumann, of fibroblasts and collagen fibers both parallel and perpendicular
& Hertel, 2015). Special, interest is in studying how the horizontal oriented to the implant long axis. After a 6‐week healing period,
offset of implant‐abutment connection displaces the bacterial colo‐ the histometric analysis showed the barrier epithelium had an av‐
nization and inflammatory cells far from the bone crest (Broggini et erage measurement of 2 mm, whereas the connective tissue was
al., 2006; Cochran et al., 2013; Hermann, Schoolfield, et al., 2001). 1.5 mm (Berglundh et al., 2007). Furthermore, another recently
Moreover, less biomechanical stress at the marginal bone crest has published preclinical study demonstrated comparable histometric
also been suggested as the reason for improved clinical outcomes results with a two‐piece dental implant. The authors reported that
(Maeda, Miura, Taki, & Sogo, 2007; Rodríguez‐Ciurana et al., 2009). the dimension of peri‐implant barrier epithelium was 1.7 ± 0.2 mm
Other studies discussed other factors including implant macrodesign and the connective tissue attachment was 1.5 ± 0.5 mm (Sukekava
(Chappuis, Bornstein, Belser, & Buser, 2016; Shin, Han, Heo, Kim, & et al., 2016). The present study presented similar results regard‐
Chun, 2006) and the quantity of abutment dis‐ and re‐connection ing the dimensions of peri‐implant soft tissue. The dimensions
during restorative phase (Abrahamsson, Berglundh, & Lindhe, 1997) of barrier epithelium (MML‐aBE) were 1.82 ± 0.36 mm for WE
as important factors for peri‐implant soft and hard tissue stability. and 1.67 ± 0.33 mm NE, whereas the measurements for the
The present study showed that despite the implant macrode‐ connective tissue (aBE‐fBIC) were 1.28 ± 0.43 mm for WE and
sign, the transmucosal component also influenced the establish‐ 1.10 ± 0.04 mm for NE.
ment of peri‐implant biologic width. The use of a flat and wide
abutment (WE) decreased the height of peri‐implant soft tissue

F I G U R E 6 Graph illustrating the histometric measurements of

F I G U R E 5 Graph illustrating the histometric measurements of the distance between the implant shoulder (IS) to the first bone‐to‐
the distance between the implant shoulder (IS) to the bone crest implant contact (fBIC) with mean values and standard deviation of
(BC) with mean values and standard deviation of NE and WE groups NE and WE groups
SOUZA et al. | 7

The findings of the present study demonstrated that wider abut‐

ment designs induced an apical displacement of the peri‐implant bi‐
ologic width. This results in more bone loss compared to the narrow
and straight abutment (Figures 3 and 4). An understanding of the
peri‐implant soft tissue barrier formation and collagen fibers ori‐
entation into the different types of abutment designs is important
to elucidate those findings. Previous studies of a two‐piece dental
implant with mismatching abutment connection showed the peri‐im‐
plant connective tissue attaches to the implant‐abutment interface
(Cochran et al., 2013) with organized and parallel‐oriented collagen
fibers (Becker et al., 2007). In the study of Rodríguez, Vela, Calvo‐
Guirado, Nart, and Stappert (2012), the effect of mismatching im‐
plant‐abutment connection and the orientation of the collagen fibers
were evaluated. The authors reported that collagen fibers formation
adjacent to the bone crest presented a circular‐directed fashion
with a mechanical retention formed by this orientation, which might
prevent the apical down‐growth of barrier epithelium and bone re‐
sorption (Rodríguez et al., 2012). In this study, it was observed that,
when implants with a horizontal offset are placed subcrestally, a bi‐
ological compartment is established and confined by the following F I G U R E 7 Microphotograph representing the buccal–lingual
structures: the alveolar bone, the implant platform or shoulder, and section of the lingual aspect of an implant from NE group showing
the implant abutment (Figure 7). When a wider and more divergent the establishment of the biological compartment by the following
abutment configuration is used, the inner wall of the compartment structures: (a) the alveolar bone; (b) implant platform or implant
shoulder; (c) and the implant abutment. Original magnification ×8.
is located closer to the marginal alveolar bone limiting the space for
Van Gieson staining
the establishment of peri‐implant biologic width. Thus, the alveo‐
lar bone remodels to accommodate the newly formed attachment.
Interestingly, the vertical component combined with the horizontal fabricate implant‐abutment and frameworks with proper marginal
mismatching creates a biologic compartment between the implant‐ adaptation and a low risk of biological and technical complica‐
abutment connection to the implant shoulder, which appears to be tions (Cooper, Stanford, Feine, & McGuire, 2016; Kapos, Ashy,
critical for organization and direction of the collagen fibers and the Gallucci, Weber, & Wismeijer, 2009; Sailer, Pjetursson, Zwahlen,
establishment of peri‐implant biological width. However, the appli‐ & Hammerle, 2007). Thus, the concept of slim abutments could
cability of these results is limited by the small number of animals be used for the designing and customization of the implant trans‐
used. Similar results may need to be studied in humans. mucosal component with digital technology. In such a way, the
A few clinical studies have focused on the effect of abutment de‐ desirable volumetric dimensions for the establishment of collagen
sign and peri‐implant bone remodeling. Galindo‐Moreno et al. (2016) fibers could be controlled to favor to the establishment of peri‐im‐
evaluated the influence of abutment height on platform‐switching plant biologic width minimizing bone remodeling. A custom heal‐
implants in a radiographic analysis. The study reported that abut‐ ing abutment and later, the final abutment with a narrow and more
ment height of ≥2 mm leads to less marginal bone loss compared to straight contour designed with CAD‐CAM technology may bring
abutments with <2 mm. In another randomized clinical trial study, clinical benefits in the long‐term.
Schepke, Meijer, Kerdijk, Raghoebar, and Cune (2017) reported that
implant‐supported customized zirconia abutment did not differ clin‐
ically and radiographically from the prefabricated abutment in pre‐ 5 | CO N C LU S I O N S
molar sites. Another study evaluated the influence of two different
implant neck designs on facial bone crest in a tomographic analysis Within the limitations of this preclinical histological and radiographic
(Chappuis et al., 2016). These studies reported superior bone sta‐ study, it can be summarized that the implant‐abutment design may
bility on the facial aspect of platform‐switching bone‐level implant influence the establishment of the peri‐implant biologic width. A
design compared to the soft tissue level with machined tapered neck wide and more divergent from the main implant axis abutment de‐
design. sign induced an apical displacement of the peri‐implant biologic
Based on the results of the present study, the implant‐abut‐ width and resulted in more bone remodeling.
ment design and, in particular, the portion of the abutment that Further translational studies including larger sample sizes and
forms the inner wall of the compartment appears to be an im‐ more variations of abutment configurations may be needed to fully
portant factor for the maintenance of peri‐implant marginal bone. understand the influence of implant abutment on peri‐implant hard
Moreover, CAD‐CAM technology seems to be a reliable way to and soft tissue healing.
8 | SOUZA et al.

AC K N OW L E D G E M E N T S teeth. Clinical Oral Implants Research, 2, 81–90. https://doi.

org/10.1034/j.1600-0501.1991.020206.x
This study was supported by a research grant from DENTSPLY Broggini, N., McManus, L. M., Hermann, J. S., Medina, R., Shenk, R. K.,
Implants. The entire rights, title, interest in and to all investigators, Buser, D., & Cochran, D. L. (2006). Peri‐implant inflammation defined
by the implant‐abutment interface. Journal of Dental Research, 85,
and results are owned by Harvard University.
473–478. https://doi.org/10.1177/154405910608500515
Buser, D., Weber, H. P., & Lang, N. P. (1990). Tissue integration of non‐
submerged implants. 1‐year results of a prospective study with 100
C O N FL I C T O F I N T E R E S T
ITI hollow‐cylinder and hollow‐screw implants. Clinical Oral Implants
The authors have stated explicitly that there are no conflict of inter‐ Research, 1, 33–40.
Canullo, L., Fedele, G. R., Iannello, G., & Jepsen, S. (2010). Platform
ests in connection with this article.
switching and marginal bone level alterations: The results of a ran‐
domized‐controlled trial. Clinical Oral Implants Research, 21, 115–121.
https://doi.org/10.1111/j.1600-0501.2009.01867.x
ORCID Canullo, L., Pellegrini, G., Allievi, C., Trombelli, L., Annibali, S., & Dellavia,
C. (2011). Soft tissues around long‐term platform switching im‐
André Barbisan Souza http://orcid.org/0000-0002-3835-7262
plant restorations: A histological human evaluation. Preliminary
Peer W. Kämmerer http://orcid.org/0000-0002-1671-3764 results. Journal of Clinical Periodontology, 38, 86–94. https://doi.
org/10.1111/j.1600-051X.2010.01641.x
German O. Gallucci http://orcid.org/0000-0001-6386-594X
Canullo, L., Rosa, J. C., Pinto, V. S., Francischone, C. E., & Gotz, W. (2012).
Inward‐inclined implant platform for the amplified platform‐switch‐
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