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The Effects of Subcrestal Implant Placement on

Crestal Bone Levels and Bone-to-Abutment Contact:


A Microcomputed Tomographic and
Histologic Study in Dogs
Michael Fetner, DMD, MS1/Alan Fetner, DMD2/Theofilos Koutouzis, DDS, MS3/
Emanuele Clozza, DDS4/Nick Tovar, PhD5/Alvin Sarendranath6/Paulo G. Coelho, DDS, PhD7/
Kathleen Neiva, DDS, PhD, MS8/Malvin N. Janal, PhD9/Rodrigo Neiva, DDS, MS10

Purpose: Implant design and the implant-abutment interface have been regarded as key influences on crestal
bone maintenance over time. The aim of the present study was to determine crestal bone changes around
implants placed at different depths in a dog model. Materials and Methods: Thirty-six two-piece dental
implants with a medialized implant-abutment interface and Morse taper connection (Ankylos, Dentsply) were
placed in edentulous areas bilaterally in six mongrel dogs. On each side of the mandible, three implants
were placed randomly at the bone crest, 1.5 mm subcrestally, or 3.0 mm subcrestally. After 3 months, the
final abutments were torqued into place. At 6 months, the animals were sacrificed and samples taken for
microcomputed tomographic (micro-CT) and histologic evaluations. Results: Micro-CT analysis revealed similar
crestal or marginal bone loss among groups. Both subcrestal implant groups lost significantly less crestal and
marginal bone than the equicrestal implants. Bone loss was greatest on the buccal of the implants, regardless
of implant placement depth. Histologically, implants placed subcrestally were found to have bone in contact
with the final abutment and on the implant platform. Conclusion: Implants with a centralized implant-abutment
interface and Morse taper connection can be placed subcrestally without significant loss of crestal or marginal
bone. Subcrestal placement of this implant system appears to be advantageous in maintaining bone height
coronal to the implant platform. Int J Oral Maxillofac Implants 2015;30:1068–1075. doi: 10.11607/jomi.4043

Key words: subcrestal, dental implant, bone levels, histology

 1
Clinical Instructor, Department of Periodontology, University
of Florida College of Dentistry, Gainesville, Florida; Private
Practice, Jacksonville, Florida.
 2Clinical Assistant Professor, Department of Periodontology,
D ental implants are a viable and popular form of
tooth replacement. Over the past 30 years, re-
search has validated the success of osseointegrated
University of Florida College of Dentistry, Gainesville, Florida;
Private Practice, Jacksonville, Florida. dental implants as an alternative to removable or
 3Assistant Professor, Department of Periodontology, University
tooth-supported prosthetic restorations.1 Modern
of Florida College of Dentistry, Gainesville, Florida.
 4Postgraduate Student, Department of Periodontology and engineering and research have developed even more
Implant Dentistry, New York University College of Dentistry, successful dental implants year after year, but ultimate
New York, New York. success is still dependent on the maintenance of the
 5Adjunct Professor, Department of Biomaterials, New York

University College of Dentistry, New York, New York. peri-implant tissues by the patient and dentist.2
 6Research Assistant, Department of Biomedical Engineering, Several factors may contribute to the success or fail-
The City College of New York, New York, New York. ure of a dental implant, including bone support and
 7
Associate Professor, Department of Biomaterials, New York
University College of Dentistry, New York, New York. the stability of the bone crest adjacent to the implant.
 8Clinical Assistant Professor, Department of Endodontics, A zone of epithelium and connective tissue integration
University of Florida College of Dentistry, Gainesville, Florida. forms a “biologic width” that surrounds and protects
 9Adjunct Associate Professor of Epidemiology and Health

Promotion, New York University College of Dentistry, New an abutment and implant from pathologic insults.3 It
York, New York. has been observed that if the biologic width is altered
10Clinical Associate Professor, Department of Periodontology,
in an apical direction, a corresponding marginal bone
University of Florida College of Dentistry, Gainesville, Florida.
loss will also occur. This area of bone loss usually starts
Correspondence to: Dr Michael Fetner, Fetner and Hartigan at the implant-abutment interface.3
Periodontics, 7043-B Southpoint Pkwy, Jacksonville, FL 32216. Early implant-abutment designs had an interface
Email: Mfetner@dental.ufl.edu
with an external connection and abutment walls that
©2015 by Quintessence Publishing Co Inc. were the same diameter as the implant. However,

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Fetner et al

manufacturing tolerance restrictions produce mat- implants to be placed closer to each other by limiting
ing parts that do not match perfectly, resulting in an the cumulative effect of their microgap.15,16 Implants
implant-abutment gap.4 The presence of this gap placed subcrestally may also retain more bone coronal
leads to bacterial contamination at the interface and to the implant-abutment interface, but may tend to
an associated inflammatory infiltrate. This zone of have a longer soft tissue attachment.17
inflammatory infiltrate can lead to bone loss at the Subcrestal implant placement can result in more
implant-abutment interface.4 crestal bone loss than equicrestal placement as a result
Several methods have been used to prevent bone of the microgap. Several studies have found that more
loss at the implant-abutment interface. One such inflammation at the microgap leads to greater bone
method is to centrally locate the margin of the abut- loss.4 To successfully place an implant subcrestally, the
ment on the platform of the implant, a technique inflammation from the microgap must be minimal to
known as “platform switching.”5 This method moves nonexistent, or more bone loss will occur.18 In vitro fi-
the zone of irritation of the interface further from the nite element analyses have shown that a depth of 0.5
bone and results in less bone loss than an interface to 2.5 mm subcrestal is ideal for stress distribution.19
that is flush between the implant and abutment.5,6 Precision Morse taper connections have been avail-
Another technique used in implant design to limit able for more than a decade20 and have been previ-
the irritation caused at the implant-abutment junction ously characterized as a configuration that produces
is to use an internal connection in conjunction with a a bacteria-resistant connection.21–23 Depending on its
centrally located abutment margin. Such a configura- design, the Morse taper allows the abutment to fit so
tion can result in a more mechanically stable connec- precisely to the implant that no microgap or micro-
tion that reduces contamination of the interface. These movement occurs under normal forces.24 The design
connections have been associated with less marginal features an aggressive platform switch that allows am-
bone loss than external, non–centrally located abut- ple space for connective tissue and bone homeostasis
ment connections.7 over the implant platform.18
Bacterial colonization of the peri-implant tissues These characteristics of the Morse taper connection
occurs within minutes of implant placement.8 These allow for subcrestal placement without corresponding
microorganisms may establish colonies at the implant- bone loss around the implant margin caused by the
abutment interface (the microgap).9 These microbial microgap that is present in most implant systems.11,25
colonies may lead to inflammation of the peri-implant A clinical study26 of Morse taper–connection implants
tissues and, eventually, bone loss around the im- placed at the bone crest or 1 or 2 mm subcrestally re-
plant.10 Prevention of the inflammatory effect of mi- sulted in no statistically significant difference in bone
crobial contamination at the microgap is important in loss between groups. This same study reported that
the design of two-piece implant systems.11 significantly more bone was observed on the plat-
Tissue-level implants with an implant-abutment in- form of the subcrestally placed implants versus those
terface located more than 1 mm from the bone crest implants placed at the bone crest (90% versus 35%).26
have been found to lose minimal to no bone at the However, it is not currently known whether there is an
interface.12 When two-piece implants are placed with ideal subcrestal depth of placement for this implant
the implant-abutment interface at the bone level, even system. The objective of the present study was to eval-
in a one-stage approach, bone is lost at the crest.2 Two- uate the effect of subcrestal implant placement depth
piece implants placed with the implant-abutment in- in a canine preclinical model.
terface 1 mm apical to the bone crest tend to lose even
more bone than those placed at the bone crest.4,13
These findings support the theory that the implant- MATERIALS AND METHODS
abutment interface influences the amount of bone
remodeling around implants over time. Experimental Subjects
Placement of the implant-abutment interface apical Six female hound-type dogs, approximately 25 to
to the bone crest—known as subcrestal implant place- 30 kg each and greater than 2 years of age, were se-
ment—has many proposed advantages. An implant lected for the experiment. The protocol was mod-
placed apical to the bone decreases the risk of expo- eled after a previous study27 and had a timeline of 9
sure of the metal top of the implant or the abutment months. Regular feeding, activities, and veterinary care
margin, thus preventing contamination of the surface were provided by the University of Florida Department
of the implant.14 It could allow sufficient vertical space of Animal Care Services. Tramadol and buprenorphine
to create an appropriate esthetic emergence profile, were used for postoperative pain management. The
even with a large platform switch. It has been speculat- dogs were fed a soft diet after the first surgery that
ed that subcrestal implant placement could also allow consisted of canned or moistened dog food.

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Fetner et al

Fig 1  Implants at placement. (Left to Fig 2   Implants at 3 months postplace- Fig 3  Flaps sutured at abutment
right) 3 mm, 0 mm, 1.5 mm subcrestal. ment, with abutments in place. placement.

First, all eight mandibular premolars were surgically were then sutured to obtain primary closure (Fig 3).
extracted from each dog under general anesthesia. The abutments were never removed from the implants
Antibiotics and anti-inflammatory medications were after they were placed.
given before and after all surgical procedures.
Sample Collection and Processing
Implant Placement The animals were sacrificed 6 months after implant
Following a healing period of 3 months, implants were placement and 3 months after abutment placement.
placed. Antibiotics and anti-inflammatory medications Samples were immediately preserved in 10% neutral
were given before and after surgical procedures. A buffered formalin for histologic examination. Prior to
crestal incision was made, and buccal and lingual flaps processing for histologic examination, all samples were
were elevated on the edentulous ridge. The ridge was scanned using microcomputed tomography (micro-CT).
flattened using a high-speed handpiece with a flat dia- Three-dimensional bone formation around the im-
mond bur under copious irrigation. Six 3.5- × 9.5-mm plant was examined using micro-CT (µCT40, Scanco
implants with a Morse taper connection were placed in Medical) with a slice resolution of 20 µm. Five hundred
each dog (total n = 36 implants; Ankylos, Dentsply). On micro-CT slices were imaged at an x-ray energy level
each side of the mandible, three implants were placed of 55 kVp and a current of 145 µA. Integration time
0 mm, 1.5 mm, or 3 mm subcrestally in a randomized was 200 ms, with a total scanning time of 45.4 minutes
order (Fig 1). Sulcus-forming abutments were placed (160 mA). All data were imported into Amira software
at the time of surgery in the two test implants at equal (FEI Visualization Sciences) for evaluation. The data
crestal heights. The equicrestal implant received the were cropped along the implant axis to where the cor-
cover screw provided with the implant packaging. The tical bone started to exclude unnecessary information
flaps were then sutured to provide primary closure. All above the cortical bone. Before segmentation, thresh-
implant procedures were completed according to the old levels for bone and implant were determined based
manufacturer’s guidelines. on the complete slices. This was done by determining
the upper and lower threshold levels for bone and im-
Abutment Placement plant. Threshold determination was repeated to evalu-
Three months after implant placement, implants were ate intraexaminer and interexaminer repeatability.
accessed by full-thickness flaps. Each implant received Measurements and analyses of the micro-CT data
a straight stock abutment with a height of 4.0 mm were completed with Amira software (FEI Visualization
from the margin. Implants placed at the crest received Sciences). Crestal bone height (CBH) was defined as the
an abutment with a margin 1.5 mm coronal to the im- most coronal extent of bone in relation to the implant
plant. Implants placed 1.5 mm subcrestally received platform. Marginal bone height (MBH) was defined as
an abutment with a margin 3.0 mm coronal to the im- the bone height coronal to the outside diameter of
plant. Implants placed 3.0 mm subcrestally received the implant on the mesial and distal of each implant
an abutment with a margin 4.5 mm from the implant. (Fig 4). Marginal bone level (MBL) was measured as the
These abutment heights ensured that the coronal bone height coronal to the diameter of the implant on
height of all abutments was the same (Fig 2). The sites the buccal and lingual of each implant (Fig 4).

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Fetner et al

Fig 4   Micro-CT images. (top) Crestally placed implant and abut-
ment; (bottom) implant and abutment placed subcrestally. CBH
was measured as the most coronal extent of bone in relation to Buccal
the implant platform. MBH was measured as the bone height Lingual
coronal to the outside diameter of the implant on the mesial Mesial Distal
and distal. MBL was measured as the bone height coronal to
the outside diameter of the implant on the buccal and lingual.

CBH
CBH
MBL MBH MBH Distal
Mesial
MBL
Buccal Lingual

Following micro-CT data acquisition, the blocks Statistical Analysis


were gradually dehydrated in a series of alcohol solu- Preliminary analysis of the data showed that one out-
tions (70% to 100% ethanol). Then the samples were lier greatly skewed the distribution of outcome data;
embedded in a methacrylate-based resin (Technovit, this one outlier was therefore ignored to maintain a
Heraeus Kulzer) according to the manufacturer’s in- symmetric distribution. Linear regression was used
structions. The blocks were then cut into slices (~300 µm to calculate correlation of subcrestal implant depth
thickness) at the center of the implant along its long (SID) and change in CBH (∆CBH), MBH, MBL, BIC, and
axis with a precision diamond saw (Isomet, Buehler); BAFO. A linear mixed-model analysis of variance with
glued to acrylic plates with an acrylate-based cement; fixed factors of depth and site was used to determine
and allowed to set for 24 hours prior to grinding and statistical differences between groups for ∆CBH, MBH,
polishing. The sections were then reduced to a final MBL, BIC, and BAFO. One-way analysis of variance and
thickness of ~30 µm by means of a series of silicon the Tukey multiple comparison test (P < .05) were used
carbide abrasive papers (400, 600, 800, 1,200, and to determine significance in regard to BIC and BAFO
2,400 grit) (Buehler) in a grinding/polishing machine in the histologic samples. The Kruskal-Wallis and Dunn
(Metaserv 3000, Buehler) under water irrigation.28 multiple-comparison tests (P < .05) were used to deter-
The sections were stained with Stevenel blue and van mine the significance of differences between individu-
Gieson fuchsin and examined under an optical micro- al groups regarding whether the bone approximated
scope for histomorphologic evaluation. For the 1-week the abutment surface.
histology samples, a second thin section was also pro-
duced and stained with Stevenel blue and van Gieson
fuchsin in an attempt to evaluate the interaction of RESULTS
osteogenic cells with the implant surface.
Bone-to-implant contact (BIC) was determined at A total of three implants failed, one in each group. One
×50 to ×200 magnification (Leica DM2500M, Leica of the failed implants had severe bone loss and was
Microsystems) by means of computer software (Leica excluded from statistical measurements as an outlier.
Application Suite, Leica Microsystems). All regions of Thus, the total number of implants used for analysis
bone-to-implant contact along the implant perimeter was 33, resulting in a survival rate of 91.7%.
were subtracted from the total implant perimeter, and
calculations were performed to determine the BIC. The Micro-CT Analysis of Bone Levels
bone area fraction occupied (BAFO) between threads Figure 5 illustrates the mean MBLs as a function of im-
in trabecular bone regions was determined at ×100 plantation depth and site. Thus, implants at the crest
magnification (Leica DM2500M) by means of computer of bone exhibited, on average, lower MBLs than the
software (Leica Application Suite). The areas occupied subcrestally placed implants, regardless of buccal/
by bone were subtracted from the total area between lingual site (P < .05). While MBLs were higher for im-
threads to determine the BAFO (reported in percent- plants placed 3 mm subcrestal than for those placed
age values).29 1.5 mm subcrestal, this difference failed to reach sta-
tistical significance (.05 < P < .10). Similarly, the buccal

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Fetner et al

Buccal Buccal Buccal


Lingual Lingual Lingual
1.5  3  1.5 
1.00 
2  1.0 
0.5 
MBL

CBH

MBH
0.00  1  0.5 
–0.5 
0  0.0 
–1.00 

–1.5  –1  –0.5 


0.0 1.5 3.0 0.0 1.5 3.0 0.0 1.5 3.0
Placement depth (mm) Placement depth (mm) Placement depth (mm)

Fig 5   Mean MBL as measured on micro- Fig 6   Mean CBH as measured on micro- Fig 7   Mean MBH as measured on micro-
CT scans on the buccal and lingual of im- CT scans on the buccal and lingual of im- CT scans on the mesial and distal of im-
plants placed per group. plants placed per group. plants placed per group.

Fig 8  Histologic images of implants


placed with evidence of bone-to-abutment
L B L B L B contact. (a) 0-mm group implant with no
0 mm 1.5 mm 3.0 mm
bone-to-abutment contact on the buccal
or lingual, (b) a 1.5-mm group implant with
bone-to-abutment contact on the lingual
but not the buccal, (c) a 3-mm group im-
plant with bone-to-abutment contact on
the buccal and the lingual.

a b c

sites showed lower MBLs than the lingual sites, regard- Figure 7 depicts MBH as a function of implanta-
less of implantation depth (P < .001). There was no in- tion depth and site. Analysis showed an interaction
dication of an interaction between depth and buccal/ between these factors (P = .03). Thus, while CBH was
lingual site (P = .74). Thus, as measured by MBL, im- lower at buccal than lingual sites for the 1.5- and 3-mm
plantation at the crest resulted in lower MBLs than im- implantation depths, there was no difference between
plantation at 1.5 or 3 mm subcrestal, and buccal sites sites for implants placed at the crest. In addition, there
showed lower MBLs than lingual sites. was a main effect of depth (P < .001), such that each
Figure 6 shows CBH as a function of implantation implantation depth resulted in significantly different
depth and buccal/lingual site. Analysis showed an in- CBH values.
teraction between these factors (P = .03). Thus, while
CBH was lower at buccal than lingual sites for the Histologic Analyses
1.5- and 3-mm implantation depths, there was no dif- Figure 8 shows histologic specimens from each group
ference between sites for implants placed at the crest. of implants placed. BIC and BAFO were very similar
In addition, there was a main effect of depth (P < .001), between all groups. The average percent perimeter of
such that each implantation depth resulted in signifi- bone in contact with the implant surface was around
cantly different levels of CBH. 60% for all groups (Fig 9). There was no significant

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Fig 9 (left)  Histologic mean percent of


implant perimeter, with BIC by group. No 100 
significant differences were seen between 80 
groups. 80 

Percent perimeter
60 

Percent area
60 
Fig 10 (right)  Histologic mean percent 40 
area with bone within the threads. 40 
20 20
0  0 
0.0 1.5 3.0 0.0 1.5 3.0
Placement depth (mm) Placement depth (mm)

Table 1  Histologic Data of Sites with Bone-to-Abutment Contact


Implant depth (mm) Buccal Lingual Percent of sites buccal Percent of sites lingual Percent of sites
0 0 0 0 0 0
1.5 1 5 8% 42% 25%
3.0 6 7 67% 78% 74%

difference between groups in BIC. BAFO also showed Table 2  Comparison of Groups Based on
no significant differences between groups in average Bone-to-Abutment Contact
percent area. Figure 10 shows an average percent area
for all groups of approximately 40%. The amount of Significant?
surfaces with bone-to-abutment contact in the differ- Depth of placement Buccal Lingual
ent groups is shown in Table 1. The 3-mm subcrestal 0 vs 1.5 mm No No
group showed the most sites with bone-to-abutment 0 vs 3 mm Yes Yes
contact. Lingual sites presented a higher percentage 1.5 vs 3 mm Yes No
of sites with bone-to-abutment sites than mesial sites.
Significance of differences between each of the groups
with regard to surfaces with bone-to-abutment con- marginal bone did not extensively remodel apical to
tact is shown in Table 2. A comparison of the 0-mm the implant-abutment interface, with some bone even
and 1.5-mm groups showed no significant differences remaining on the platform, in contrast to previous
regardless of site location; the 0-mm and 3-mm groups studies when implants were placed subcrestally.4,12
always showed a significant difference regardless of site This difference is probably a result of factors that allow
location; and the 1.5-mm and 3-mm groups showed a this implant to reduce the effects of the microgap. It
significant difference only on buccal sites. is speculated that the Morse taper connection reduces
the bacterial inflow into a microgap, which will cause
less inflammation in the area and thus limit bone loss.
DISCUSSION It is also speculated that the large platform switch re-
duces the effects felt from any irritation at the micro-
Subcrestal placement of most bone-level implants has gap by distancing it from the surrounding bone. These
been shown to lead to greater bone loss than crestal or factors probably allow the tested implant system to
supracrestal implant placement.3,29 The present study be placed subcrestally with minimal effect on the sur-
has shown that an implant with a connection that rounding bone.
minimizes the implant-abutment microgap and micro- Bone loss around implants occurs less than 3
movement, as well as presents with a large platform months after they are placed.4,10,12,30 The implants in
switch, can have the same amount of crestal bone loss this study also showed bone loss and remodeling dur-
when placed at the crest of the bone or up to 3 mm ing the 6 months after placement. The implants placed
subcrestally. The bone loss seen around the equicrestal at the crest of bone in this study had significantly
implant is consistent with similar studies in which two- greater loss of MBL, MBH, and CBH than implants
piece implants were placed at the bone crest.4 placed subcrestally. This bone loss may be seen as nor-
The implants placed subcrestally were able to main- mal physiologic bone loss following full-thickness flap
tain higher initial CBH and MBL at placement, even elevation.31 Because crestal implants are placed with
at 6 months after placement. This showed that the no bone coronal to the platform, this bone loss would

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then expose the rough surface of the implant to pos- occlusion with the opposing arch. Although the find-
sible microbial colonization. The bone loss present in ings of this study represent 6 months of healing, the
all groups could also be a result of the microgap and final abutment was in place for only 3 months. Clini-
the irritation caused by it, although this was less pro- cal studies are necessary to investigate the effects of
nounced than similar studies.4 subcrestally placed implants with a conical connection
A previous study has shown that there may be his- and a medialized implant-abutment interface.
tologically intimate contact between bone and abut-
ment.18 The present study shows intimate contact
histologically between bone and abutment in sev- ACKNOWLEDGMENTS
eral of the subcrestally placed implants. Moreover, the
implants placed further subcrestally have a greater The authors reported no conflicts of interest related to this study.
chance of bone approximating the abutment, espe-
cially on the buccal plate. The 3-mm group showed
significantly more bone-to-abutment contact on the REFERENCES
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the fact that the implants were not directly loaded in

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