Received: 1 October 2019 Accepted: 26 November 2019

DOI: 10.1111/cid.12915

ORIGINAL ARTICLE

Comparison of histomorphometry and microradiography

of different implant designs to assess primary implant stability

Georgios Romanos DDS, PhD1,2 | Michael Damouras DDS2 |

Alexander A. Veis DDS, PhD3† | Pablo Hess DDS2 | Frank Schwarz DDS, PhD2 |
Silvia Brandt DDS, PhD4

1
Department of Periodontology, Stony Brook
School of Dental Medicine, Stony Brook, Abstract
New York Objectives: To contribute toward optimizing the long-term stability of dental
2
Department of Oral Surgery and Implant
implants. Our working hypothesis was that the degrees of immediate implant-bone
Dentistry, Center for Dentistry and Oral
Medicine, Johann Wolfgang Goethe contact, and hence of primary stability, would demonstrably differ between implant
University, Frankfurt am Main, Germany
systems due to their different external geometries and thread designs (macro-design).
3
Department of Dento-alveolar Surgery,
Implantology and Oral Radiology, School of This demonstration was provided in a bovine model (ex vivo) by employing and com-
Dentistry, Aristotle University of Thessaloniki, paring histomorphometry and microradiography as evaluation methods.
Thessaloniki, Greece
4
Materials and methods: A total of 120 implants, representing six different implant
Department of Prosthodontics, Center for
Dentistry and Oral Medicine, Johann thread designs, were inserted following the recommended surgical protocol in ribs of
Wolfgang Goethe University, Frankfurt am
freshly slaughtered cattle. Twenty specimens of implants with surrounding bone
Main, Germany
were prepared per system and were divided into two equally sized groups of 60 spec-
Correspondence
imens for analysis by either histomorphometry or micro-computed tomography. Data
Georgios Romanos, DDS, PhD, Department of
Periodontology, Stony Brook University, were analyzed by Mann-Whitney U test (P ≤ .05).
School of Dental Medicine, 106 Rockland Hall,
Results: One of the implant systems, featuring a slight tapered external geometry
Stony Brook, NY 11794.
Email: georgios.romanos@ and a progressive thread design, consistently revealed the most favorable bone-
stonybrookmedicine.edu
implant contacts in both histomorphometric and microradiographic evaluations.
Overall, consistently higher values of bone-implant contact were obtained with the
microradiographic than the histomorphometric approach, and this difference reached
statistical significance in three of the six implant systems tested.
Conclusions: Progressive threads offering a bone-condensing effect can significantly
help to maximize implant-bone contact percentages. Compared to his-
tomorphometry, microradiography is likewise a suitable method to evaluate bone-
implant contact, offering the additional benefits of being noninvasive and less time
consuming.

KEYWORDS

bone-implant contacts, dental implants, primary stability, x-ray microtomography

1 | INTRODUCTION

Dental implants are a well-established treatment modality to replace

†
Died November 21, 2016. missing teeth. Implants represent a treatment option in oral

Clin Implant Dent Relat Res. 2020;1–7. wileyonlinelibrary.com/journal/cid © 2020 Wiley Periodicals LLC 1
2 ROMANOS ET AL.
rehabilitation to secure different kinds of prostheses in partially or
fully edentulous patients or as a single tooth replacement in the
esthetic zone. The only way to ensure adequate retention of any fixed
or removable implant-supported restoration is by establishing reliable
anchorage with direct bone-implant contact. The term
osseointegration was introduced in reference to the functional direct
1,2
integration of load-bearing implants with living bone.
Osseointegration has been defined as successful whenever rigid
anchorage of an implant inside its endosseous bed is maintained, and
remains clinically asymptomatic, even under functional loading.3
Branemark first described the shapes and materials of dental implants.
Nowadays, the focus on the implant geometry shifted to the
osseoinductive potential of the implant surface.4
Achieving proper osseointegration is very much a function of pri-
5
mary implant stability whose level, and the related degree of bone-
implant contact, depends on a number of factors. Associations of pri-
mary stability have repeatedly been reported with implant macro-
geometry and with the surgical implant procedure.6-8 A major role has
9
also been ascribed to the surface characteristics of the implant, and
patient-specific factors, such as bone density and bone-condensation
methods are known to affect the bone-implant contact.10 In this latter
context, a classification system for bone quality (type I-IV) is available
11
to support decisions in the perioperative stages.
Once the implant has been inserted with primary stability, the fur-
ther course of osseointegration is characterized by the development
of secondary stability, which includes the formation of new tissue sur-
rounding the implant surface and depends on the degree of primary
stability achieved.12 The biomechanical process of secondary stability
is determined as the structural and functional connection between
newly formed bone and implant surface, namely osseointegration.13
Hence it is fair to state that primary stability is a fundamental prereq-
uisite for osseointegration and for the long-term stability of dental
implants. Various methods have been used to determine primary
implant stability, including the measurement of insertion or removal
torque6,8,14) or the Periotest device.15 This technique is, however,
highly user-dependent and therefore offers little sensitivity.
Much more objective and reproducible approaches to determin-
ing implant stability are available in the form of histological, notably
histomorphometric, and microradiographic techniques. The latter take
the form of micro-computed tomography (micro-CT) scans16,17 and
offer additional reliable insights into alveolar bone quantity and qual-
ity, which can pertinently be used to evaluate implant sites.18,19
Another benefit is their noninvasive nature, even though, as with any
radiological technique, radiation exposure is naturally a factor requir-
ing attention.
We designed the present study in an effort to contribute toward
optimizing the long-term stability of dental implants. Our working
hypothesis was that the degree of immediate implant-bone contact, and
hence of primary stability, would demonstrably differ between implant
systems due to the different external geometries and thread designs
involved. This demonstration was to be accomplished in a bovine ex vivo
model, including microradiographic and histomorphometric techniques
and also comparison between these two evaluation methods.
2 | M A T E R I A L S A N D M ET H O D S
2.1 | Implant systems and implant insertion
A total of 120 implants were included, representing six common implant
systems, which featured various shapes, thread designs, surface textures,
implant-abutment connections, and implant dimensions. Table 1 gives an
overview of these systems and these properties. In the following manu-
script, the systems investigated are divided into groups in alphabetic
order: group 1: Ankylos, group 2: Astra TiOblast, group 3: Frialit-2, group
4: Replace select tapered, group 5: Straumann, group 6: Xive.
Ten bovine rib bones (only the middle part of the ribs was selected in
order to have similar bone quality) from freshly slaughtered cattle were
obtained for implant insertion, which was performed in accordance with the
surgical protocol recommended by the manufacturer for each specific sys-
tem, using a standardized drilling unit (947/948 Intra K Boxes; KaVo,
Biberach, Germany) and an appropriate 1:5 contra-angled handpiece (W&H
Dentalwerk, Bürmoos, Austria). All implant beds were prepared with low
pressure, using irrigation with saline for cooling, at a speed of 800 rpm.
None of the implant systems required pretapping. All implants of each sys-
tem were inserted by six experienced oral surgeons having advanced train-
ing for the individual implant systems (each system placed by one clinician).
2.2 | Specimen preparation
Specimens from the implants and their surrounding bone were created
directly after the insertion procedure. Figure 1 illustrates how the bone
was cut into square pieces, resulting in a total of 20 specimens for each
implant system. Subsequently the specimens were divided into two
equally sized groups of 60 specimens each. One group of specimens was
evaluated histologically and histomorphometrically, while the other one
was analyzed by radiographic imaging in the form of micro-CT scans.
2.3 | Histological and histomorphometric
assessment
Following fixation in 10% formalin for 48 hours and subsequent dehy-
dration with alcohol, the specimens were embedded in methacrylate-
based resin (Technovit 7200; Heraeus Kulzer, Wehrheim, Germany)
and cut into thin sections (60-80 μm) using a high-speed microtome
(Accutom 2; Struers, Copenhagen, Denmark) and polishing machine
(DAP-V; Struers). Then the ground sections were stained with tolui-
dine blue 1% and pyronine G and analyzed using a light microscope
(Axiostar Plus; Zeiss, Göttingen, Germany) with an integrated color
video camera (DC88AP; Sony, Tokyo Japan) (Figure 2). For the subse-
quent histomorphometric investigation, a microscope (Zeiss;
Oberkochen, Germany) and a computer setup with appropriate soft-
ware (Videoplan; Kontron, Eching, Germany) were used. The BIC was
measured with a 2.5× objective lens. A 10× lens was used to calculate
the area of the peri-implant mineralized bone. For calculation, 10 pre-
viously defined fields of measurement were used.
ROMANOS ET AL. 3

TABLE 1 Overview of the six implant systems investigated in alphabetical order

I-A
System Manufacturer Surface pattern Shapes and thread designs connections Dimensions
Ankylos Dentsply Sirona Roughened by ablative processing Progressive thread depth and Conical Ø: 3.5 mm
(Group 1) (Mannheim, polished collar (2 mm) Length:
Germany) 11 mm
Astra Astra Tech OsseoSpeed (fluoride-modified Cylindrical Conical Ø: 3.5 mm
TiOblast (Gothenburg, roughened surface) Length:
(Group 2) Sweden) 11 mm
Frialit-2 Dentsply Sirona Trimodal morphology Stepped screw design Internal Ø: 3.5 mm
(Group 3) (Mannheim, hexagon Length:
Germany) 11 mm
Replace Nobel Biocare TiUnite (surface characterized by Tapered with non-self-tapping Internal Ø: 4.3 mm
select (Gothenburg, antioxidative modification) design tri-lobe Length:
tapered Sweden) 13 mm
(Group 4)
Straumann Straumann SLA (sandblasted, large-grit, Cylindrical in the middle and apical Internal Ø: 3.5 mm
(Group 5) (Waldenburg, acid-etched surface) and tapered in the cervical area octagon Length:
Switzerland) (tissue level) 12 mm
Xive Dentsply Sirona Sandblasted featuring a Advanced cylindrical design with a Internal Ø: 3.5 mm
(Group 6) (Mannheim, high-temperature-etched screw-type thread hexagon Length:
Germany) microstructure 11 mm

Note: I-A connection = implant-abutment connection.

Stanford, California) using the Wilcoxon-Mann-Whitney U test, a 95%

confidence interval, and P < .05 level of significance.

3 | RE SU LT S

3.1 | Histological findings

All implants had primary contacts with the bone surrounding them.
Some sites along the threads exhibited area-type bone contacts. Area-
type lingui-form bone contacts were typically seen along the coronal
and middle thirds of the implants. Different thread designs did not
involve differences in peri-implant bone quality.

3.2 | Histomorphometric findings

F I G U R E 1 Specimen preparation. Implants were inserted into
bone of uniformly high quality from freshly slaughtered cattle. Then,
the bone was cut into pieces incorporating one implant each
2.4 | Microradiographic assessment and statistical
analysis
The radiographic evaluations were performed using a cone-beam micro-
CT desktop unit (μCT 40; Scanco Medical, Bassersdorf, Switzerland) with
an x-ray tube featuring a focal point of 7 μm. Voxel size was 30 μm. For
each implant, 450 layers were scanned from coronal to apical, the scan
height being 13.5 mm, and the tube voltage 70 kV. A complementary
evaluation script allowed us to calculate the percentage values of contact
area between each implant and its surrounding bone (Figure 3). Descrip-
tive calculations were followed by analysis with statistical software
(SPSS; Statistical Product and Service Solutions, Stanford University,
Table 2 summarizes the percentages of bone-implant contact emerging from
the histomorphometric assessments based on both the total bone structures
and their cortical and cancellous compartments. A statistically significant dif-
ference was found between the six implant systems (Mann-Whitney U test/
t test: P < .05). The results for total bone-implant contact percentages were
significantly more favorable with group 1 than group 3, group 4 and group
6 implants, and they were significantly better with the group 6 than with the
group 4 implant system (all P < .001; also see Table 4).
3.3 | Microradiographic findings
Table 3 summarizes the bone-implant contact percentages as evaluated
by micro-CT scanning. Again, the most favorable results were obtained
4 ROMANOS ET AL.

F I G U R E 2 Micrograph of histological
ground sections, displaying inserted
implants and the surrounding bone

F I G U R E 3 Microradiographs (micro-CT views) of an inserted implant and its surrounding bone. Red lines indicate the presence of direct
implant-bone-contact; green lines indicate gaps along the interface

TABLE 2 Bone-implant contacts (%) as evaluated by histomorphometry

Total bone-implant contact (%) Cortical bone contact (%) Cancellous bone contact (%)

Implant system Mean ± SD Min Max Mean ± SD Min Max Mean ± SD Min Max
Group 1 64.80 ± 9.51 42 74 92.50 ± 12.86 58 100 37.1 ± 13.08 19 54
Group 2 52.15 ± 6.0 40.5 62 82.30 ± 8.70 64 92 22.00 ± 6.03 16 33
Group 3 56.05 ± 6.3 40 63 98.80 ± 7.19 79 100 18.90 ± 8.62 1 28
Group 4 49.15 ± 11.11 25 61 72.70 ± 20.19 31 91 25.60 ± 7.56 16 38
Group 5 51.15 ± 8.87 39 67 79.80 ± 16.91 55 100 22.50 ± 4.74 17 34
Group 6 58.25 ± 7.40 47.5 70.5 94.81 ± 9.65 70 100 28.60 ± 8.12 14 41

Note: Data are presented as mean values, SD, and ranges (minimum and maximum values).

with group 1, and good interlocking with the surrounding bone was also
seen with groups 4, 5, and 6 geometries. Less favorable results were
obtained for groups 2 and 3. Intergroup comparisons did reveal statisti-
cally significant (P < .001) differences between group 1 and group
3, group 1 and group 6 and group 1/6 and group 4, group 6 and group
4, group 6 and group 3, as well as between group 4 and group 3 (also
see Table 4).
3.4 | Histomorphometry vs microradiography
Table 3 also includes a method comparison. Overall, the microradio-
graphic evaluations yielded markedly higher values of bone-implant
contact than the histomorphometric evaluations. These differences
were not statistically significant for groups 4, 5, and 6 (Mann-Whitney
U test/t test: P = .08; also, see Table 4). The method-specific
ROMANOS ET AL. 5

TABLE 3 Bone-implant contacts (%) as evaluated by microradiography (micro-CT scanning) in comparison with histomorphometry

Microradiographic evaluation (%) Histomorphometric evaluation (%)

Implant system Mean ± SD Min Max Mean ± SD Min Max Method of comparison
Group 1 70.90 ± 3.68 64.95 73.83 64.80 ± 9.51 42 74 n.s.
Group 2 49.20 ± 6.53 38 55 52.15 ± 6.0 40.5 62 n.s.
Group 3 53.18 ± 10.46 43 70.28 56.05 ± 6.30 40 63 n.s.
Group 4 65.87 ± 8.30 55.67 74.39 49.15 ± 11.11 25 61 P = .08
Group 5 57.36 ± 3.15 55.15 63 51.15 ± 8.87 39 67 P = .08
Group-6 66.18 ± 2.33 62.29 68.01 58.25 ± 7.40 47.5 70.5 P = .08

Note: Data are presented as mean values, SD, and ranges (minimum and maximum values). In this table, the six implant systems are listed in the order of
mean values obtained by micro-CT. See Table 2 for the order emerging from the histomorphometric results (n.s. = not statistically significant).

TABLE 4 Overview of significant

Group 1 Group 2 Group 3 Group 4 Group 5 Group 6
differences in bone to implant contacts
between the implant systems evaluated Group 1 n.s. n.s. *,** *,** n.s. *,**
by either histomorphometry or Group 2 n.s. n.s. n.s. n.s. n.s. n.s.
microradiography and between the two Group 3 *,** n.s. n.s. ** n.s. **
evaluation methods (ie,
Group 4 *,** n.s. ** *** n.s. *,**
histomorphometry vs microradiography)
for any of the implant systems Group 5 n.s. n.s. n.s. n.s. *** n.s.
Group 6 *,** n.s. ** *,** n.s. ***

*P < .001 between any two implant systems for (total) bone-implant contact as evaluated by histomorphometry.
**P < .001 between any two implant systems for (total) bone-implant contact as evaluated by microradiography.
***P = .08 between histomorphometry vs microradiography for any implant system. (n.s. = not significant).

differences seen with groups 1, 2, and 3 showed lack of statistically
significant difference (Mann-Whitney U test/t test; P ≥ .05). Regard-
less of whether histomorphometry or microradiography was used, the
most favorable bone-implant contacts were consistently observed
with group 1 and group 6 (Figure 4).
4 | DISCUSSION
All bovine rib bones used as experimental implant beds in the present
study were of uniformly high quality, so that any influence of the
implant beds on the bone-implant contacts may be regarded as negli-
gible. Differences in bone quality between the median and the distal
end of the ribs were considered in the methodology of this experi-
mental protocol. Also, some differences in implant length between the
investigated systems was considered and therefore bone-implant con-
tact percentages were defined in relative terms and implant length
seems not to affect stress transmission to bone.20 Hence, it was rea-
sonable to attribute the different degrees of bone contact obtained
for the various implant systems exclusively to their different macro-
and microscopic design features.
Our histomorphometric evaluations yielded the highest values of
total bone contact for group 1 and group 6. Animal models have previ-
ously revealed that high degrees of bone-implant contact percentages,
and hence of primary (mechanical) implant stability, will set the stage
for uneventful bone healing and osseointegration by minimizing
micromovements inside the bone-implant-interface during the healing
period.21-23 As apparent from Table 2, we extended our
histomorphometric analysis of bone-implant contact from the total
bone structures to their cortical and cancellous compartments. Note
that an osteo-protective effect on cortical bone can be achieved via
increased tension in the cancellous areas and that group 1 revealed
the highest degrees of bone-implant contact even within the confines
of only this compartment, possibly as a result of its progressive and
non-self-tapping threads24 and load transmission being optimized by
the combination of these progressive threads with a rough surface.
Better primary stability can be achieved with tapered than with
cylindrical implants.25,26 Tapered implants have also been shown to
offer more favorable load transmission to the bone.20 A slightly
tapered macro-design might, on the other hand, even account for our
especially poor results of cortical bone contact with group 4 (see
Table 2). Further support for external implant geometry being a modi-
fier of bone contact is provided by the adverse combination of results
we obtained with the cylindrical group 3, which actually showed both
the highest cortical and the lowest cancellous bone contact of all six
implant systems investigated (see Table 2). Overall, the six implant
systems were invariably found to show considerably better cortical
than cancellous bone-to-implant contacts.
In our microradiographic evaluations, the highest values of bone-
implant contact percentages were recorded for groups 1, 4, and
6. Hence, this evaluation method supports the notion of external
macro-geometries like those of groups 1 and 4 being conducive to the
establishment of primary bone contacts. All three significant differ-
ences we found between both evaluation methods (ie, in conjunction
6 ROMANOS ET AL.
F I G U R E 4 Box-and-whisker diagram of total bone-implant
contacts (%) as evaluated by microradiography (R) and
histomorphometry (H)
with group 6, group 4, and group 5) reflected higher values of bone-
to-implant-contact generated by microradiography than by his-
tomorphometry (P = .08). Despite these differences, microradiography
remains a comparable and, above all, noninvasive alternative for
determining both existing and potential bone-implant contacts.27
What is more, micro-CT has emerged as a valid alternative for evalu-
ating bone-implant contacts and osseointegration even in direct com-
parison with histological assessment.28 For the purpose of in vitro
studies, histomorphometric methods do offer additional insights not
accessible by radiography.
In summary, the bone-to-implant contacts we observed in the
present study varied due to differences in the macro-design (macro-
geometry) and thread designs of different implant systems. Compared
to other thread geometries, progressive threads seem to offer a bone-
condensation effect to the surrounding bone during insertion and can
significantly help to ensure increased primary stability by maximizing
the bone-implant contacts. This can be evaluated noninvasively by
microradiographic (micro-CT) imaging. The present study concludes
also that the results obtained from histomorphometry are similar to
the less time-consuming microradiography.
ACKNOWLEDGMENTS
The authors would like to thank Drs Argyris Samiotis, and Frank
Spiegelberg for the implant placement of the individual systems
(Astra, Replace Select, respectively) as well as Mr Bruno Koller
und Mr Markus Burkhart (Scanco Inc.) for the professional
microradiographic analyses and the presentation of the photo-
graphic material. Also, special thanks to Mrs Nina Krymchanska
(Dental School, Frankfurt) for the statistical analysis of the
collected data.
AUTHOR CONTRIBU TIONS
Georgios Romanos developed the concept, obtained the funding,
placed implants, and edited the manuscript; Michael Damouras per-
formed the histomorphometric analysis and collected completely the
data; Alexander A. Veis and Frank Schwarz did the histological prepa-
rations, Pablo Hess placed implants and calibrated the other surgeons;
Silvia Brandt prepared the manuscript.
OR CID
Georgios Romanos https://orcid.org/0000-0002-5952-4752
Frank Schwarz https://orcid.org/0000-0002-5873-9903
Silvia Brandt https://orcid.org/0000-0001-5530-0412
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How to cite this article: Romanos G, Damouras M, Veis AA,
Hess P, Schwarz F, Brandt S. Comparison of
histomorphometry and microradiography of different implant
designs to assess primary implant stability. Clin Implant Dent
Relat Res. 2020;1–7. https://doi.org/10.1111/cid.12915