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Implant-Abutment Connections and Their Effect on Implant

Survival Rates and Changes in Marginal Bone Levels (ΔMBL):


A Systematic Review and Meta-Analysis of 45,347 Oral Implants
Todd R. Schoenbaum, DDS, MS1/E. Dwayne Karateew, DDS2/Angela Schmidt, DDS3/Chaniun Jadsadakraisorn, DDS3/
Jörg Neugebauer, Dr Med Dent4/Clark M. Stanford, DDS, PhD, MHA5

Purpose: To quantify the cumulative oral implant survival rates and changes in radiographic bone levels based on the
configuration of the implant-abutment connection type over time. Materials and Methods: An electronic literature search
was conducted in four databases (PubMed/MEDLINE, Cochrane Library, Web of Science, and Embase), and records were
refereed by two independent reviewers based on the inclusion criteria. Data from included articles were grouped by
implant-abutment connection type into four categories ([1] external hex; [2] bone level, internal, narrow cone < 45 degrees;
[3] bone level, internal wide cone ≥ 45 degrees or flat; and [4] tissue level) and duration of follow-up (short-term 1 to 2 years,
mid-term 2 to 5 years, and long-term > 5 years). Meta-analyses were performed for cumulative survival rate (CSR) and
changes in marginal bone level (ΔMBL) from baseline (loading) to last reported follow-up. Studies were split or merged
as appropriate based on the implants and follow-up duration in the study and trial design. The study was compiled under
PRISMA 2020 guidelines and registered in the PROSPERO database. Results: A total of 3,082 articles were screened. Full-
text review of 465 articles resulted in a total of 270 articles (representing 16,448 subjects with 45,347 implants) included
for quantitative synthesis and analysis. Mean ΔMBL (95% CI) was as follows: short-term external hex = 0.68 mm (0.57, 0.79);
short-term bone level, internal, narrow cone < 45 degrees = 0.34 mm (0.25, 0.43); short-term bone level, internal wide
cone ≥ 45 degrees = 0.63 mm (0.52, 0.74); short-term tissue level = 0.42 mm (0.27, 0.56); mid-term external hex = 1.03 mm
(0.72, 1.34); mid-term bone level, internal, narrow cone < 45 degrees = 0.45 mm (0.34, 0.56); mid-term bone level, internal
wide cone ≥ 45 degrees = 0.73 mm (0.58, 0.88); mid-term tissue level = 0.4 mm (0.21, 0.61); long-term external hex = 0.98 mm,
0.70, 1.25); long-term bone level, internal, narrow cone < 45 degrees = 0.44 mm (0.31, 0.57); long-term bone level, internal
wide cone ≥ 45 degrees = 0.95 mm (0.68, 1.22); and long-term tissue level = 0.43 mm (0.24, 0.61). CSRs (95% CI) were:
short-term external hex = 97% (96%, 98%); short-term bone level, internal, narrow cone < 45 degrees = 99% (99%, 99%);
short-term bone level, internal wide cone ≥ 45 degrees = 98% (98%, 99%); short-term tissue level = 99% (98%, 100%);
mid-term external hex = 97% (96%, 98%); mid-term bone level, internal, narrow cone < 45 degrees = 98% (98%, 99%); mid-
term bone level, internal wide cone ≥ 45 degrees = 99% (98%, 99%); mid-term tissue level = 98% (97%, 99%); long-term
external hex = 96% (95%, 98%); long-term bone level, internal, narrow cone < 45 degrees = 98% (98%, 99%); long-term
bone level, internal wide cone ≥ 45 degrees = 99% (98%, 100%); and long-term tissue level = 99% (98%, 100%). Conclusion:
The configuration of the implant-abutment interface has a measurable effect on the ΔMBL over time. These changes can
be observed over a period of at least 3 to 5 years. At all measured time intervals, similar ΔMBL was noted for external hex
and internal wide cone ≥ 45-degree connections, as were internal, narrow cone < 45-degree and tissue-level connections.
Int J Oral Maxillofac Implants 2023;38(suppl):37–45. doi: 10.11607/jomi.10411

Keywords: abutment, bone level, bone loss, connection, failure, implant, review, survival

C
1Department of Restorative Sciences, Dental College of Georgia, ontemporary implant-supported dental restora-
Augusta University, Augusta, Georgia, USA.
2Department of Periodontics, University of Illinois Chicago, College tions are considered to be a favorable method of
of Dentistry, Chicago, Ilinois, USA. replacement for missing or hopeless dentition due to
3Department of Prosthodontics, University of Illinois Chicago, their reported high rates of survival and predictabil-
College of Dentistry, Chicago, Illinois, USA.
4Steinbeis University, Berlin, Germany.
ity, as reported in numerous clinical studies.1–5 The
5University of Iowa, College of Dentistry, Iowa City, Iowa, USA. current trend in thought regarding implant longevity
is no longer focused on equating success to short or
Presented before the Academy of Osseointegration Summit, Chicago,
Illinois, August 2022. medium temporal survival, but rather equating suc-
cess to peri-implant hard and soft tissue stability and
Correspondence to: Dr Todd R. Schoenbaum, The Dental College
of Georgia at Augusta University, 1120 15th Street, GC-4220, metrics associated with marginal bone change. 3,5,6,7
Augusta, GA 30912, USA. Email: tschoenbaum@augusta.edu Marginal bone stability is a long-term goal, as loss of
peri-implant bone and its overlying soft tissues, com-
Submitted December 19, 2022; accepted January 4, 2023.
 2023 by Quintessence Publishing Co Inc.
© prising connective tissue and epithelium, could lead

The International Journal of Oral & Maxillofacial Implants 37

© 2023 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Schoenbaum et al

to esthetic and functional compromises.6 Early obser- 1 to 2 years; mid-term, 2 to 5 years; and long-term,
vations with machined, external-hex, and platform- ≥ 5 years).
matched implants anticipated marginal bone loss
of < 1.5 mm during the first year of function, and in
consecutive years, a loss of < 0.2 mm annually. 2 Re- MATERIALS AND METHODS
modeling may be considered to be physiologically
acceptable and anticipated. This postplacement mar- This systematic review followed the PRISMA 2020
ginal bone loss has been discussed by many authors, (Preferred Reporting Items for Systematic Reviews)47
and the amount of marginal bone loss may be con- guidelines using Population, Intervention, Control,
sidered as one of the variables defining the success and Outcome (PICO) format, to analyze clinical stud-
criteria. 2,8–11 ies of patients treated with two-piece titanium den-
Multiple factors have been suggested as potential tal implants (P) with fixed prostheses (I), with various
causative agents for biologic remodeling of the coronal implant-abutment configurations (C), and their ef-
bone profile. Postulated factors for early and long-term fects on changes in peri-implant bone levels and sur-
bony remodeling include, but are not limited to, trauma vival over time (O). This protocol was registered with
to the bone from surgical manipulation, occlusal over- PROSPERO #42022313835.
load transferred through the restoration/abutment
to the implant-bone interface, temporal sequence of Focused Question
implant placement, whether or not bone grafting has The focused question was as follows: Does implant-
been completed in the immediate area, horizontal and abutment connection design influence changes in
vertical violation of the peri-implant biologic width (su- marginal bone levels (ΔMBL) and survival in two-piece
pracrestal tissue attachment), influence of the implant titanium implants with fixed restorations?
collar design, neck design, implant surface macroto-
pography and microtopography, shape and configura- Search Strategy
tion of the implant-abutment connection,12 prosthetic An electronic search was conducted in PubMed/
design,13 soft tissue thickness,14 oral hygiene,15 history MEDLINE, Cochrane Library, Web of Science, and Em-
of periodontitis,16 smoking,17 and the position of the base to identify English language publications from
implant-abutment microgap.12,13,15,17–29 peer-reviewed journals (Fig 1). The search was con-
Revisions of engineered implant characteristics ducted using the Medical Subject Headings (MeSH)
have been a scientific and industry focus to reduce the keywords: “(dental implants [MESH] OR dental implant
negative factors unrelated to patient history or con- OR dental implants) AND (connection OR platform)
founding biologic circumstances. Smooth machined AND (survival rate [MESH] OR dental restoration failure
implant surfaces compared to rough surfaces30,31 and [MESH] OR dental prosthesis failures OR implant fail-
implants with and without cervical threads have been ure OR survival rates OR implant survival OR complica-
examined32 to determine their influence(s) on mar- tion OR marginal bone loss OR marginal bone level OR
ginal bone loss. Other designs modeled and in use for peri-implant bone loss OR peri-implant bone level OR
many years are evidence for clinical acceptance. These crestal bone level).”
include “platform-matched” and “platform-switched”
implant-abutment interfaces, external and internal Study Selection
connections, narrow and wide cone interfaces at the Abstracts and selected full texts were screened, and the
implant-abutment junction (IAJ), and designs at sub- following inclusion and exclusion criteria were applied.
crestal, equicrestal, supercrestal, or soft tissue level Inclusion criteria were as follows:
positions.33–43 Current trends suggest that platform-
switched implants enjoy not only greater favor among • ≥ 1 year follow-up postloading
clinicians (vs platform-matched implants) but that • Patients > 18 years of age
they may be superior with respect to maintenance of • Human studies (no limitations on patients’ systemic
healthy bone levels around the most coronal aspect of status)
the implants.41,44–46 • Titanium-based, two-piece implants
The aim of this meta-analysis and systematic • Must measure MBL or implant survival
review was to quantify the effect of four implant- • MBL only measured with 2D radiographs (no CBCT,
abutment configurations (external hex connections, panographic, or histology)
internal connections < 45 degrees, internal connec- • Fixed prostheses only (single- or multi-unit or
tions ≥ 45 degrees, and tissue-level implant designs full-arch)
on marginal bone changes and implant survival), • Minimum of 20 implants/study
grouped into three follow-up intervals (short-term, • English language publication

38 Volume 38, Supplement, 2023

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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Schoenbaum et al

Exclusion criteria were as follows:


Records identified from:

Identification
Records removed before
•Medline (n = 539)
• Animal or benchtop studies •Cochrane Trials (n = 431)
screening:
• One-piece zirconia implant or < 2.9- •Duplicate records removed
•Web of Science (n = 956) (n = 1,124)
mm–diameter implants •Embase (n = 1,156)
• Scalloped implant or intermobile
element IAJs

Screening
• Solid zirconia or alumina abutments Records screened (n = 1,958) Records excluded (n = 1,482)
directly interfacing the implant (ie,
those with no titanium component
Reports sought for retrieval
interface) Reports not retrieved (n = 11)
(n = 476)

Eligibility
• Implants splinted to teeth
• Abutments cemented onto implants
Reports assessed for eligibility Reports excluded:
• Extensive active periodontitis patients (n = 465) •Excluded implant type (n = 4)
or active peri-implantitis patients •Excluded abutment or prostheses

Included
• Implants used as orthodontic Studies included in review (n = 43)
anchorage (n = 270) •Data incomplete or unextractable
(n = 70)
• Partial extraction therapy techniques •Insufficient reporting follow-up or
• Studies in which the data could not sample size (n = 5)
match (due to a lack of disclosure) the •Incorrect/excluded measurement
reported (n = 49)
standard rubrics for the extraction •Insufficient information regarding
format materials and methods (n = 24)

Full texts of all selected articles were re- Fig 1   PRISMA 2020 diagram.
trieved and screened independently by two
independent reviewers (A.S. and C.J.) ap-
plying the inclusion and exclusion criteria. design at three follow-up intervals using a random-effects model
Both evaluation stages were performed in in OpenMeta v. 12.11.14 (Brown University). Forest plots were used
Rayyan software (Rayyan.ai, Qatar Founda- to synthesize pooled means and 95% CIs for ΔMBL and survival for
tion).48 In case of disagreement, the two each connection group at each follow-up time interval. Heteroge-
reviewers discussed the study or a third ref- neity was assessed using the I2 test.
eree (T.S.) reconciled with a final vote.

Data Extraction RESULTS


Data extraction was performed manually by
one author (T.S.) using a customized data Study Selection
instrument (Excel v16.61, Microsoft) with Initial database searches resulted in 3,082 total records meeting
the following headings: authors, publica- the inclusion criteria (1,156 from Embase, 431 from Cochrane tri-
tion year, follow-up time, connection type, als, 956 from Web of Science, 539 from PubMed); 1,124 duplicated
number of patients, number of implants, records deleted; 1,958 abstracts screened; 1,482 records excluded
number of surviving or failed implants, MBL for failure to meet inclusion; and 476 records sought for retrieval.
(mean and SD), depth of implant place- Eleven full-text records could not be located. The 465 remaining
ment, platform switch design, and implant full-text records were screened for inclusion and synthesis. A total
manufacturer. Studies containing implants of 270 studies were included in the quantitative analyses.
with more than one connection design or
more than one-follow up time interval were Peri-implant Bone Loss Meta-analyses
split, and data were extracted separately. The 270 included studies represent 16,448 patients and 45,347 im-
Studies that did not report MBL or survival plants. Implant counts for each group were: external hex = 14,598;
or did not separate reporting for included bone level, internal, narrow cone < 45 degrees = 22,613; bone level,
and excluded implants or prosthesis de- internal wide cone ≥ 45 degrees or flat = 4,729; and tissue level
signs were excluded from the study. = 3,310 (Fig 2).
Changes in marginal bone levels were summarized at three time
Meta-analysis intervals with the mean ΔMBL (95% CI) as follows: short-term ex-
Single-arm weighted meta-analyses were ternal hex = 0.68 mm (0.57, 0.79); short-term bone level, internal,
performed for each implant connection narrow cone < 45 degrees = 0.34 mm (0.25, 0.43); short-term bone

The International Journal of Oral & Maxillofacial Implants 39

© 2023 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Schoenbaum et al

Fig 2   Diagrammatic representa-


n = 14,598 n = 22,613 n = 4,729 n = 3,310 tion of the four classes of implant
connections included in this
IAJ analy­sis, including number of im-
Abutment/prosthesis IAJ IAJ IAJ
IAJ plants per group.

Implant

External hex Bone level, internal con- Bone level, internal con- Tissue level
(ie, Brånemark, 3i ext) nection < 45 degrees nection ≥ 45 degrees (ie, Straumann TL)
(ie, Astra, Nobel CC, (ie, Nobel TriLobe,
Straumann BL, Bicon, 3i Certain, BioHorizons,
Ankylos, Conelog) Zimmer, Camlog)

level, internal wide cone ≥ 45 degrees = 0.63 mm (0.52, connection on change in mean MBL between a baseline
0.74); short-term tissue level = 0.42 mm (0.27, 0.56); and follow-up defined as changes in mesial and/or distal
mid-term external hex = 1.03 mm (0.72, 1.34); mid-term radiographic measured osseous vertical bone height or
bone level, internal, narrow cone < 45 degrees = 0.45 “ΔMBL” (change in marginal bone level) and survival over
mm (0.34, 0.56); mid-term bone level, internal wide time. Since the early studies by Albrektsson and Zarb2
cone ≥ 45 degrees = 0.73 mm (0.58, 0.88); mid-term and others, changes in marginal bone levels and other
tissue level = 0.4 mm (0.21, 0.61); long-term external clinical criteria have been noted as a direct indicator of
hex = 0.98 mm, 0.70, 1.25); long-term bone level, inter- success or a harbinger of future biologic and mechanical
nal, narrow cone < 45 degrees = 0.44 mm (0.31, 0.57); problems. Preservation of marginal bone level has been
long-term bone level, internal wide cone ≥ 45 degrees the goal of implant therapy from implant placement,
= 0.95 mm (0.68, 1.22); long-term tissue level = 0.43 mm definitive prosthetic abutment connection, and through
(0.24, 0.61). Cumulative survival rates (CSRs; 95% CI) the functional life of the implant/prosthetic unit. Loss of
were: short-term external hex = 97% (96%, 98%); short- bone from the coronal aspect of the implant body has
term bone level, internal, narrow cone < 45 degrees been radiographically measured and recorded as ΔMBL,
= 99% (99%, 99%); short-term bone level, internal wide a metric of crestal stability. Notably, this measure usu-
cone ≥ 45 degrees = 98% (98%, 99%); short-term tissue ally does not include the midfacial aspect of the implant
level = 99% (98%, 100%); mid-term external hex = 97% body, which can be esthetically the most important
(96%, 98%); mid-term bone level, internal, narrow cone aspect.
< 45 degrees = 98% (98%, 99%); mid-term bone level, The quantified results from this systematic review
internal wide cone ≥ 45 degrees = 99% (98%, 99%); are notable. Over the 10-year interval of time cov-
mid-term tissue level = 98% (97%, 99%); long-term ered by this systematic review, two implant groups,
external hex = 96% (95%, 98%); long-term bone level, (1) internal connection, bone level, < 45-degree con-
internal, narrow cone < 45 degrees = 98% (98%, 99%); nection and (2) tissue-level implants, performed bet-
long-term bone level, internal wide cone ≥ 45 degrees ter than their counterparts of either (3) external-hex
= 99% (98%, 100%); long-term tissue level = 99% (98%, connections and (4) internal connection, bone level,
100%). Heterogeneity was high in all groups (Table 1; > 45-degree connection. However, one may question
Figs 3 to 6 can be found at the end of the article, and all whether these results are clinically significant. Certainly,
24 forest plots can be seen in the online version of this at the 10-year completion of this analysis, the difference
article at www.quintpub.com/journals). in ΔMBL is both statistically and clinically significant be-
tween the above groups 1 and 2 and groups 3 and 4, as
there is a demonstrable difference of 0.5 mm. However,
DISCUSSION when earlier temporal points are noted, the difference
in ΔMBL is not as distinct. It appears from the data that
This systematic review and meta-analysis was conducted the internal-connection, bone-level, < 45-degree con-
to focus on a unique PICO question: to analyze clinical nection, and tissue-level implants show an early ΔMBL
studies of patients treated with two-piece titanium den- of approximately 0.4 mm and lose less mesial/distal
tal implants with fixed prostheses, with various implant- bone over the 10-year observation period. Conversely,
abutment configurations, and the effect on changes in the group of external-hex and internal-connection,
peri-implant bone levels and survival over time. Essen- bone-level, > 45-degree connection have a ΔMBL rep-
tially, this systematic review and meta-analysis sought resenting approximately 1 mm at > 5 years. Note that
to determine the effect of the implant-abutment tables present results to the hundredth of a millimeter,

40 Volume 38, Supplement, 2023

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Schoenbaum et al

Table 1 Data Summarized from Individual Meta-analyses of Each Implant Connection Group at Each
Follow-up Interval for DMBL and Survival
Survival rate (%) DMBL (mm)
Connection
category <2y 2–5 y >5y <2y 2–5 y >5y
External hex
Mean (95% CI) 96.8 (95.8, 97.7) 97 (96, 98) 96.4% (95.2, 97.6) 0.68 (0.57, 0.79) 1.03 (0.72, 1.34) 0.98 (0.70, 1.25)
Patients, n 1,039 1,860 1,818 1,039 1,860 1,818
Implants, n 3,034 5,184 6,380 3,034 5,184 6,380
Internal, bone level <
45-degree cone
Mean (95% CI) 99.2 (99.1, 99.4) 98.4 (97.9, 98.8) 98.1 (97.6, 98.6) 0.34 (0.25, 0.43) 0.45 (0.34, 0.56) 0.44 (0.31, 0.57)
Patients, n 2,738 2,800 2,808 2,738 2,800 2,808
Implants, n 7,769 7,758 7,086 7,769 7,758 7,086
Internal, bone level ≥
45-degree cone
Mean (95% CI) 98.3 (97.7, 98.8) 98.6 (97.9, 99.2) 98.5 (97.5, 99.5) 0.63 (0.52, 0.74) 0.73 (0.58, 0.88) 0.95 (0.68, 1.22)
Patients, n 977 385 801 977 385 801
Implants, n 1,991 1,225 1,513 1,991 1,225 1,513
Tissue level
Mean (95% CI) 98.9 (98.1, 99.6) 98.0 (96.8, 99.1) 99.0 (98.0, 99.9) 0.42 (0.27, 0.56) 0.41 (0.21, 0.61) 0.43 (0.24, 0.61)
Patients, n 352 221 491 352 221 491
Implants, n 826 1,393 975 826 1,393 975

but caution should be exercised in interpretation at this unlikely to disproportionately affect one implant con-
level due to the inability of the individual interpreting nection design group more than another. On the other
the dental radiograph to measure and accquire data to hand, from a provider perspective, the heterogeneity
this level. adds to the validity of the effectiveness of specific im-
The tissue-level implant-abutment connection in- plant configurations in daily practice. The typical stan-
terface is positioned to minimize the influence of the dard clinical trial design is to homogenize the inclusion
implant-abutment microgap on peri-implant bone and exclusion criteria so much that the outcomes of the
levels. The data suggest that the most stable long- study are very limited (a measure of efficacy). The value
term bone-level connection is the internal, bone-level, of the heterogeneity described with the “guardrails”
< 45-degree connection, which may minimize the mi- on inclusion and exclusion criteria in this study allows
crogap and increase long-term stability at the implant- for a comprehensive understanding of the influence
abutment interface, thereby minimizing microleakage. of implant/abutment designs on a specific but narrow
This microgap movement and associated microleak- outcome assessment (a common one that the literature
age has been suspected to be a causative agent of allows). As such, a measure of common everyday out-
ΔMBL, resulting in significant complications in the comes in practice (ie, effectiveness) is suggested.
peri-implant tissues, specifically peri-implant mucocitis, As with any systematic review and data synthesis
peri-implantitis, and implant loss.49 from multiple investigations (in this case, 465), it is im-
Due to the nature of a systematic review involving plausible to control for all confounding variables. Also,
hundreds of investigators, implant designs, surfaces, while a confounding variable (ie, patients with higher
patient populations, etc, there are several factors that HbA1c levels) may reduce CSRs or ΔMBL in one study
may have an influential role that cannot be accounted and not another, there is no compelling reason for any
for. Patient population variability, including age, ge- one of the connection classification groups to have a
netics, epigenetic influences, and oral hygiene norms higher prevalence of that variable than another con-
cannot be accounted/adjusted for. This is also true for nection class.
variations in implant macrodesign and microdesign, Confounding variables unaccounted for in this analy­
surface preparation and collar finishing, and for varia- sis but unlikely to disproportionately affect any one
tions in abutment design, including macrofeatures and group, though not exhaustive, include: publication and
microfeatures as well as composition of the abutment observer bias (efficacy, not effectiveness); reliability in
(CP Ti vs TiN treated). Lastly, there is likely heterogene- skill, training, and experience of surgeons, prosthodon-
ity in depth of the placement of the shoulder of the tists, restorative clinicians, and technicians; variations
implant and arch location. All these factors may influ- in prosthesis designs, materials, and configuration;
ence the results in the individual studies reviewed and variation in follow-up and maintenance practices; in-
thus have biased the final results here, though most are consistencies in radiographic measurements between

The International Journal of Oral & Maxillofacial Implants 41

© 2023 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
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Schoenbaum et al

studies; inconsistencies in radiograph capture within a CONCLUSIONS


study; variations in amount of native/grafted bone, soft
tissue thickness, width of keratinized peri-implant tis- The results of this systematic review and meta-analysis
sue, flap vs flapless surgical approaches, and occlusion; suggest that there are significant differences in ΔMBL
and variations in surgical techniques, tooth arch posi- between various implant-abutment configuration de-
tion, immediate vs early vs delayed placement, original signs at short-term, mid-term, and long-term periods
equipment manufacturer (OEM) vs non-OEM prosthetic of observation (up through 10 years). The data present-
components, “one-abutment, one-time” vs abutment ed suggest that at each of the temporal observations,
removal, and cement- vs screw-retained restorations. the external-hex and internal wide cone ≥ 45-degree
This study used the measurement ΔMBL, which was configurations behaved similarly with respect to
not always consistently used in the included reports. ΔMBL, as did the tissue-level and internal narrow cone
Some investigators simply measured the total distance < 45-degree configurations. The respective CSRs for
from the IAJ to the bone attachment on the implant all implant-abutment configurations at all times were
without accounting for the bone position at T0 (load- ≥ 96%.
ing). Failure to account for initial bone position follow- The results of this systematic review and meta-
ing integration confounds the changes in bone levels analysis should be interpreted with caution due to the
based on initial placement depth. The use of ΔMBL miti- presence of uncontrolled confounding factors in the
gates this concern. Included data were adjusted to take included studies. However, it is interesting to note the
this into account and standardize the measurements. implant-abutment geometries that performed similarly
The use of ΔMBL gives a better understanding of bone at each juncture.
changes over time compared to the use of simply mar-
ginal bone loss or level.
The secondary outcome variable of implant survival ACKNOWLEDGMENTS
was selected over implant “success” due to inherent
difficulties in synthesizing the latter across multiple in- No authors have any conflicts of interest relevant to this investiga-
vestigations. Survival is a binary outcome measure with tion. The authors would like to thank the Academy of Osseointegra-
no ambiguity. Implant “success” is certainly more useful tion for the opportunity to contribute on this topic.
clinically, but there exist a myriad of definitions of what
is or is not “success,” and reporting is inconsistent. What
merits a successful outcome for one group of investiga- REFERENCES
tors would be deemed a failure by others. 1. Moraschini V, Poubel LA, Ferreira VF, Barboza Edos S. Evaluation of
The results of this report indicate that the general survival and success rates of dental implants reported in longitudinal
design classification of dental implant connections studies with a follow-up period of at least 10 years: A systematic
review. Int J Oral Maxillofac Surg 2015;44:377–388.
does result in differential bone loss over time. The pres- 2. Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-term
ent systematic review and meta-analysis found that efficacy of currently used dental implants: A review and proposed
bone-level connections with a narrow cone fit at the IAJ criteria of success. Int J Oral Maxillofac Implants 1986;1:11–25.
3. Geraets W, Zhang L, Liu Y, Wismeijer D. Annual bone loss and success
and tissue-level implants maintained more bone over rates of dental implants based on radiographic measurements.
time compared to the alternatives. However, individual Dentomaxillofac Radiol 2014;43:20140007.
clinicians must consider dozens of individual factors 4. Hadzik J, Botzenhart U, Krawiec M, et al. Comparative evaluation
of the effectiveness of the implantation in the lateral part of the
when selecting an implant, and the ΔMBL difference mandible between short tissue level (TE) and bone level (BL) implant
between groups is just one of these factors. Differences systems. Ann Anat 2017;213:78–82.
in survival between groups were not clear, except that 5. Albrektsson T, Zarb GA. Current interpretations of the osseointegrat-
ed response: Clinical significance. Int J Prosthodont 1993;6:95–105.
external-hex implants averaged a few percent lower 6. Sanz M, Ivanoff CJ, Weingart D, et al. Clinical and radiologic out-
long-term. Caution should be exercised in interpret- comes after submerged and transmucosal implant placement with
ing this difference, however, as the investigations on two-piece implants in the anterior maxilla and mandible: 3-year
results of a randomized controlled clinical trial. Clin Implant Dent
external-connection implants were on average older, Relat Res 2015;17:234-246
this difference may be due to improvements in implant 7. Hermann F, Lerner H, Palti A. Factors in influencing the preservation
surfaces, prosthetic designs/materials, and surgical of the periimplant marginal bone. Implant Dent 2007;16:165–175.
8. Albrektsson T, Isidor F, Consensus Report of Session IV. In: Lang NP, Kar-
protocols/techniques. Most investigations reported ring T (eds). Proceedings of the First European Workshop on Periodon-
CSRs and not proper survival modeling, which would tology, London: Quintessence, 1994: 365–369.
account for subject attrition. It is also worth noting that 9. Buser D, Mericske-Stern R, Pierre Bernard JP, et al. Long-term evalua-
tion of non-submerged ITI implants. Part 1: 8-year life table analysis
there are likely strong observer and publication biases of a prospective multi-center study with 2359 implants. Clin Oral
at play. As such, it should be well noted that the data Implants Res 1997;8:161–172.
reported here are likely optimistic.

42 Volume 38, Supplement, 2023

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Schoenbaum et al

10. Roos J, Sennerby L, Lekholm UL, Jemt T, Gröndahl K, Albrektsson T. A 30. Bassetti R, Kaufmann R, Ebinger A, et al. Is a grooved collar implant
qualitative and quantitative method for evaluating implant success: design superior to a machined design regarding bone level altera-
A 5-year retrospective analysis of the Brånemark implant. Int J Oral tion? An observational pilot study. Quintessence Int 2014;45:
Maxillofac Implants 1997;12:504–514. 221–229.
11. Zarb GA, Albrektsson T. Consensus report: Towards optimized 31. den Hartog L, Meijer HJA, Vissink A, Raghoebar GM. Anterior single
treatment outcomes for dental implants. J Prosthet Dent implants with different neck designs: 5 year results of a randomized
1998;80:641. clinical trial. Clin Implant Dent Relat Res 2017;19:717–724.
12. Lemos CAA, Verri FR, Bonfante EA, Santiago Júnior JF, Pellizzer EP. 32. Hudieb MI, Wakabayashi N, Kasugai S. Magnitude and direction of
Comparison of external and internal implant-abutment connections mechanical stress at the osseointegrated interface of the micro-
for implant supported prostheses. A systematic review and meta- thread implant. J Periodontol 2011;82:1061–1070.
analysis. J Dent 2018;70:14–22. 33. Bratu EA, Tandlich M, Shapira L. A rough surface implant neck with
13. Derks J, Schaller D, Håkansson J, Wennström JL, Tomasi C, Berglundh microthreads reduces the amount of marginal bone loss: A prospec-
T. Effectiveness of implant therapy analyzed in a Swedish population: tive clinical study. Clin Oral Implants Res 2009;20:827–832.
prevalence of peri-implantitis. J Dent Res 2016;95:43–49. 34. Nickenig HJ, Wichmann M, Happe A, Zöller JE, Eitner S. A 5-year pro-
14. Suárez-López del Amo F, Lin GH, Monje A, Galindo-Moreno P, Wang spective radiographic evaluation of marginal bone levels adjacent to
HL. Influence of soft tissue thickness on peri-implant marginal parallel-screw cylinder machined-neck implants and rough-surfaced
bone loss: A systematic review and meta-analysis. J Periodontol microthreaded implants using digitized panoramic radiographs. J
2016;87:690–699. Craniomaxillofac Surg 2013;41:564–568.
15. Ramanauskaite A, Tervonen T. The efficacy of supportive peri- 35. Koodaryan R, Hafezeqoran A. Evaluation of implant collar surfaces
implant therapies in preventing peri-implantitis and implant loss: a for marginal bone loss: a systematic review and meta-analysis.
systematic review of the literature. J Oral Maxillofac Res 2016;7:e12. Biomed Res Int 2016;2016:4987526
16. Roccuzzo M, Bonino F, Aglietta M, Dalmasso P. Ten-year results of a 36. Shin YK, Han CH, Heo SJ, Kim S, Chun HJ. Radiographic evaluation
three arms prospective cohort study on implants in periodontally of marginal bone level around implants with different neck designs
compromised patients. Part 2: clinical results. Clin Oral Implants Res after 1 year. Int J Oral Maxillofac Implants 2006;21:789–794.
2012;23:389–395. 37. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material
17. Chrcanovic BR, Albrektsson T, Wennerberg A. Smoking and characteristics and/or surface topography on biofilm development.
dental implants: A systematic review and meta-analysis. J Dent Clin Oral Implants Res 2006;17(suppl 2):68–81.
2015;43:487–498. 38. Buser D, Mericske-Stern R, Dula K, Lang NP. Clinical experience
18. Quirynen M, Naert I, van Steenberghe D. Fixture design and overload with one-stage, non-submerged dental implants. Adv Dent Res
influence marginal bone loss and fixture success in the Brånemark 1999;13:153–161.
system. Clin Oral Implants Res 1992;3:104–111. 39. Sánchez-Siles M, Muñoz-Cámara D, Salazar-Sanchez N, Ballester-Fer-
19. Oh TJ, Yoon J, Misch CE, Wang HL. The causes of early implant bone randis JF, Camacho-Alonso F. Incidence of peri-implantitis and oral
loss: Myth or science? J Periodontol 2002;73:322–333. quality of life in patients rehabilitated with implants with different
20. Kinaia BM, Shah M, Neely AL, Goodis HE. Crestal bone level changes neck designs: a 10-year retrospective study. J Craniomaxillofac Surg
around immediately placed implants: A systematic review and meta- 2015;43:2168–2174 .
analyses with at least 12 months’ follow-up after functional loading. J 40. Cochran DL, Bosshardt DD, Grize L, et al. Bone response to loaded im-
Periodontol 2014;85:1537–1548. plants with non-matching implant-abutment diameters in the canine
21. Yang J, Cheng Z, Shi B. Augmentation of the alveolar ridge compared mandible. J Periodontol 2009;80:609–617.
with shorter implants in atrophic jaws: A meta-analysis based on 41. Guerra F, Wagner W, Wiltfang J, et al. Platform switch versus platform
randomised controlled trials. Br J Oral Maxillofac Surg 2016;54:68–73. match in the posterior mandible—1-year results of a multicentre
22. Canullo L, Tallarico M, Radovanovic S, Delibasic B, Covani U, randomized clinical trial. J Clin Periodontol 2014;41:521–529.
Rakic M. Distinguishing predictive profiles for patient-based risk 42. Degidi M, Perrotti V, Shibli JA, Novaes AB, Piattelli A, Iezzi G.
assessment and diagnostics of plaque induced, surgically and Equicrestal and subcrestal dental implants: A histologic and
prosthetically triggered peri-implantitis. Clin Oral Implants Res histomorphometric evaluation of nine retrieved human implants. J
2016;27:1243–1250. Periodontol 2011;82:708–715.
23. Vandeweghe S, Cosyn J, Thevissen E, Teerlinck J, De Bruyn H. The in- 43. Lago L, da Silva L, Martinez-Silva I, Rilo B. Crestal bone level
fluence of implant design on bone remodeling around surface-mod- around tissue-level implants restored with platform matching
ified Southern Implants. Clin Implant Dent Rel Res 2012;14:655–662. and bone- level implants restored with platform switching: A
24. Peñarrocha-Diago M, Flichy-Fernandez AJ, Alonso-Gonzalez R, 5-year randomized controlled trial. Int J Oral Maxillofac Implants
Peñarrocha-Oltra D, Balaguer-Martinez J, Penarrocha-Diago M. Influ- 2018;33:448–456.
ence of implant neck design and implant–abutment connection type 44. Trammell K, Geurs NC, O’Neal SJ, et al. A prospective, randomized,
on peri-implant health. Radiological study. Clin Oral Implants Res controlled comparison of platform-switched and matched-abutment
2013;24:1192–1200. implants in short-span partial denture situations. Int J Periodontics
25. De Bruyn H, Christiaens V, Doornewaard R, et al. Implant surface Restorative Dent 2009;29:599–605.
roughness and patient factors on long-term peri-implant bone loss. 45. Enkling N, Jöhren P, Klimberg V, Bayer S, Mericske-Stern R, Jepsen S.
Periodontol 2000 2017;73:218–227. Effect of platform switching on peri-implant bone levels: A random-
26. Sgolastra F, Petrucci A, Severino M, Gatto R, Monaco A. Periodontitis, ized clinical trial. Clin Oral Implants Res 2011;22:1185–1192.
implant loss and peri-implantitis. A meta-analysis. Clin Oral Implants 46. Pan YH, Lin HK, Lin JC, et al. Evaluation of the peri-implant bone
Res 2015;26:e8–e16. level around platform-switched dental implants: A retrospec-
27. Scarano A, Assenza B, Piattelli M, et al. Interimplant distance and tive 3-year radiographic study. Int J Environ Res Public Health
crestal bone resorption: A histologic study in the canine mandible. 2019;16:2570.
Clin Implant Dent Relat Res 2004;6:150–156. 47. Page MJ, McKenzie JE, Bossuyt PM, et al.. The PRISMA 2020 state-
28. Sasada, Y., Cochran DL. Implant-abutment connections: A review of ment: An updated guideline for reporting systematic reviews. Br
biologic consequences and peri-implantitis implications. Int J Oral Med J 2021;372:n71.
Maxillofac Implants 2017;32:1296–1307. 48. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan—A
29. van Eekeren PJ, Tahmaseb A, Wismeijer D. Crestal bone changes web and mobile app for systematic reviews. Syst Rev 2016;5:210.
around implants with implant-abutment connections at epicrestal 49. Alves DC, Carvalho PS, Martinez EF. In vitro microbiological analysis
level or above: Systematic review and meta-analysis. Int J Oral Maxil- of bacterial seal at the implant-abutment interface using two Morse
lofac Implants 2016;31:119–124. taper implant models. Braz Dent J 2014;25:48–53.

The International Journal of Oral & Maxillofacial Implants 43

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Schoenbaum et al

APPENDIX FOREST PLOTS

Fig 3   Forest plot summary of long-term (> 5-year follow-up) ΔMBL for external-hex implants (group 1).

Fig 4   Forest plot summary of long-term (> 5-year follow-up) ΔMBL for bone-level, internal-connection < 45-degree implants (group 2).

44 Volume 38, Supplement, 2023

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Fig 5   Forest plot summary of long-term (> 5-year follow-up) ΔMBL for bone-level, internal-connection ≥ 45-degree implants (group 3).

Fig 6   Forest plot summary of long-term (> 5-year follow-up) ΔMBL for tissue-level implants (group 4).

The International Journal of Oral & Maxillofacial Implants 45

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Schoenbaum et al

ONLINE-ONLY APPENDIX FOREST PLOTS

Appendix Fig 1   Forest plot summary of short-term (1 to 2 years) ΔMBL for external-hex implants (group 1).

45a Volume 38, Supplement, 2023

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Appendix Fig 2   Forest plot summary of short-term (1 to 2 years) ΔMBL for bone-level, internal-connection < 45-degree implants (group 2).

The International Journal of Oral & Maxillofacial Implants 45b

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Appendix Fig 3   Forest plot summary of short-term (1 to 2 years) ΔMBL for bone-level, internal-connection ≥ 45-degree implants (group 3).

45c Volume 38, Supplement, 2023

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Appendix Fig 4   Forest plot summary of short-term (1 to 2 years) ΔMBL for tissue-level implants (group 4).

Appendix Fig 5   Forest plot summary of mid-term (2 to 5 years) ΔMBL for external-hex implants (group 1).

The International Journal of Oral & Maxillofacial Implants 45d

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Appendix Fig 6   Forest plot summary of mid-term (2 to 5 years) ΔMBL for bone-level, internal-connection < 45-degree implants (group 2).

45e Volume 38, Supplement, 2023

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Appendix Fig 7   Forest plot summary of mid-term (2 to 5 years) ΔMBL for bone-level, internal-connection ≥ 45-degree implants (group 3).

Appendix Fig 8   Forest plot summary of mid-term (2 to 5 years) ΔMBL for tissue-level implants (group 4).

The International Journal of Oral & Maxillofacial Implants 45f

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Appendix Fig 9   Forest plot summary of short-term (1 to 2 years) cumulative survival rate for external-hex implants (group 1).

45g Volume 38, Supplement, 2023

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Appendix Fig 10   Forest plot summary of short-term (1 to 2 years) cumulative survival rate for bone-level, internal-connection < 45-degree
implants (group 2).

The International Journal of Oral & Maxillofacial Implants 45h

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Appendix Fig 11   Forest plot summary of short-term (1 to 2 years) cumulative survival rate for bone-level, internal-connection ≥ 45-degree
implants (group 3).

45i Volume 38, Supplement, 2023

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Appendix Fig 12   Forest plot summary of short-term (1 to 2 years) cumulative survival rate for tissue-level implants (group 4).

Appendix Fig 13   Forest plot summary of mid-term (2 to 5 years) cumulative survival rate for external-hex implants (group 1).

The International Journal of Oral & Maxillofacial Implants 45j

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Appendix Fig 14   Forest plot summary of mid-term (2 to 5 years) cumulative survival rate for bone-level, internal-connection < 45-degree
implants (group 2).

45k Volume 38, Supplement, 2023

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Appendix Fig 15   Forest plot summary of mid-term (2 to 5 years) cumulative survival rate for bone-level, internal-connection ≥ 45-degree
implants (group 3).

Appendix Fig 16   Forest plot summary of mid-term (2 to 5 years) cumulative survival rate for tissue-level implants (group 4).

The International Journal of Oral & Maxillofacial Implants 45l

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Appendix Fig 17   Forest plot summary of long-term (> 5 year) cumulative survival rate for external-hex implants (group 1).

45m Volume 38, Supplement, 2023

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Appendix Fig 18   Forest plot summary of long-term (> 5 year) cumulative survival rate for bone-level, internal-connection < 45-degree im-
plants (group 2).

The International Journal of Oral & Maxillofacial Implants 45n

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Schoenbaum et al

Appendix Fig 19   Forest plot summary of long-term (> 5 year) cumulative survival rate for bone-level, internal-connection ≥ 45-degree im-
plants (group 3).

Appendix Fig 20   Forest plot summary of long-term (> 5 year) cumulative survival rate for tissue-level implants (group 4).

45o Volume 38, Supplement, 2023

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