JCM 11 07189 v4

Journal of
Clinical Medicine
Article
Exploring the Importance of Corticalization Occurring in
Alveolar Bone Surrounding a Dental Implant
Marcin Kozakiewicz * and Tomasz Wach
Department of Maxillofacial Surgery, Medical University of Lodz, 113 Żeromskiego Str., 90-549 Lodz, Poland
* Correspondence: [email protected]; Tel.: +48-42-6393422
Abstract: Several measures describing the transformation of trabecular bone to cortical bone on
the basis of analysis of intraoral radiographs are known (including bone index or corticalization
index, CI). At the same time, it has been noted that after functional loading of dental implants such
transformations occur in the bone directly adjacent to the fixture. Intuitively, it seems that this
is a process conducive to the long-term maintenance of dental implants and certainly necessary
when immediate loading is applied. The authors examined the relationship of implant design
features to marginal bone loss (MBL) and the intensity of corticalization over a 10-year period of
functional loading. This study is a general description of the phenomenon of peri-implant bone
corticalization and an attempt to interpret this phenomenon to achieve success of implant treatment
in the long term. Corticalization significantly increased over the first 5-year functional loading (CI
from 200 ± 146 initially to 282 ± 182, p < 0.001) and maintained a high level (CI = 261 ± 168) in the
10-year study relative to the reference bone (149 ± 178). MBL significantly increased throughout
the follow-up period—5 years: 0.83 ± 1.26 mm (p < 0.001), 10 years: 1.48 ± 2.01 mm (p < 0.001).
MBL and radiographic bone structure (CI) were evaluated in relation to intraosseous implant design
features and prosthetic work performed. In the scope of the study, it can be concluded that the
Citation: Kozakiewicz, M.; Wach, T. phenomenon of peri-implant jawbone corticalization seems an unfavorable condition for the future
Exploring the Importance of fate of bone-anchored implants, but it requires further research to fully explain the significance of
Corticalization Occurring in Alveolar this phenomenon.
Bone Surrounding a Dental Implant.
J. Clin. Med. 2022, 11, 7189. https:// Keywords: dental implants; long-term results; long-term success; marginal bone loss; functional
doi.org/10.3390/jcm11237189 loading; intra-oral radiographs; radiomics; texture analysis; corticalization; bone remodeling
Academic Editors: Michał Strzelecki,
Rafał Obuchowicz, Andrzej Urbanik
and Adam Piorkowski
1. Introduction
Received: 22 October 2022
The use of dental implants is the primary method of replacing missing teeth. Nowa-
Accepted: 30 November 2022
Published: 2 December 2022
days, it is very widely modified [1–3] and applied from simple oral surgery [4] to very
advanced craniomaxillofacial procedures [5–8]. This implant treatment has good long-term
Publisher’s Note: MDPI stays neutral results, but still some implants are lost.
with regard to jurisdictional claims in It has long been noted that bone apposition and remodeling processes occur around
published maps and institutional affil-
dental implants. Direct evidence of these phenomena is provided by dental implants
iations.
removed after many years of their functional load [9]. Retrieval and histological analysis of
dental implants for fracture or other reasons (such as orthodontic, psychological, esthetic,
and hygienic reasons) [10] is able to explain the corticalization phenomenon induced by
Copyright: © 2022 by the authors.
implants. Most of the present histological studies on human specimens find compact,
Licensee MDPI, Basel, Switzerland.
lamellar bone with many Haversian systems and osteons near the implant surface with
This article is an open access article
increased bone-implant contact (BIC) up to 60–90% in 7–8 years mean duration of functional
distributed under the terms and loading [11–31]. It is also worth summarizing two well-known truths on the basis of these
conditions of the Creative Commons studies. First, loaded implants presented an average of 10% higher BIC when compared
Attribution (CC BY) license (https:// with unloaded ones. Second, approx. 10–12% higher BIC is reported for immediately
creativecommons.org/licenses/by/ loaded dental implants [32–35]. In loaded implants, transverse collagen fibers of the bone
4.0/). are more abundant, while in unloaded implants, these collagen fibers in bone tended to
J. Clin. Med. 2022, 11, 7189. https://doi.org/10.3390/jcm11237189 https://www.mdpi.com/journal/jcm

J. Clin. Med. 2022, 11, 7189 2 of 20
run in a more longitudinal way. Peri-implant bone is particularly thickened around the top
of the threads [36]. Rougher surfaces have approx. a 10% higher area of bone apposition
than machined surfaces. However, the Scandinavians, having introduced implants with
a machined surface in the 1970s, still believe that these implants have superiority over
implants with a moderately rough surface [37]. Multiple remodeled regions representing
many remodeling cycles over the years are found in peri-implant bone. Ongoing apposition
and resorption phenomena were present inside the threads. The osteocyte number is higher
near loaded versus unloaded implants [10].
Moreover, it was already reported [38] that loading was able to stimulate bone re-
modeling at the interface, that a higher percentage of lamellar bone was found in loaded
implants and more osteoblasts and osteoclasts were found in those loaded implants. The
implant loading seemed to determine differences in the distribution of the bone collagen
fibers too [14,39,40]. The transverse collagen fibers were mainly located at the lower flank
of the threads, where compressive loads exerted their effects. Transverse collagen fibers
have been described as the fibers most able to resist compressive loads, and this fact can
explain their higher quantity in loaded than unloaded implants. A lower mineral density
was present in the peri-implant bone around unloaded implants [41]. The loading forces
direction could have determined a higher mineralization of the osseous tissue located in
the coronal side of the threads when compared to that in an apical location [42].
The above-mentioned observations are probably so pronounced in the jaws because
the bone appositional index here is one of the highest in the human body [43]. It is higher
than in the iliac bone, femur or vertebrae. This process leads to the osseointegration of
the dental implants firstly but later probably is responsible for the corticalization. The
remodeling and the superimposition of new osteons on the older ones is found too [44].
Knowing that crestal bone is the basis for dental implants to function as intended [45,46],
it seems that other factors such as gingival pocket, biotype, width of keratinized gingival
zone, color and translucency of soft tissues [47–49] are secondary. In recent years, there
seems to be a growing interest in the phenomenon of corticalization [50–52]. It has been
hypothesized that almost no bone loss can be expected after bone remodeling over the
implant neck [53]. It will be interesting to see whether the corticalization phenomenon
affects the height of the bone supporting the implant. The question arises as to how this
process is related to vertical bone loss and how it relates to the long-term success of implant
treatment. For this, analysis of the microstructure of the bone surrounding the implant is
needed [54], and the key place is the bone adjacent to the implant neck [55,56].
Fine bone morphology can be registered using microcomputed tomography as well as
even using 3-tesla magnetic-resonance imaging (MRI) [57]. Magnetic resonance tomogra-
phy instruments that trigger a field of 7 tesla have also been available for several years and
are being used to analyze bone microstructure [58]. However, a series of limitations of these
advanced technologies should be highlighted. In daily clinical practice, it is standard prac-
tice to use intraoral radiographs [59–64] or pantomographic radiographs [65–68] to analyze
the condition of the peri-implant jawbone. Cone-beam tomographs [69] are used much less
frequently. The cost of a 7-tesla scanner is not inconsiderable. There is little availability
of this newly developed technology. There are no developed sequences for peri-implant
jawbone imaging. Metal components such dental implants and parts of prosthetic work
can create artifacts in MRI images and interfere with the diagnostic process, not to mention
advanced studies of the bone structure at the implant wall [70], and most importantly, MRI
is used to study the cancellous bone, not the structure of the cortical bone [71–75]. This is
still a matter of the future [76], and for now, one can rely on imaging studies with the use
of intraoral, periapical radiographs [77,78] for the reasons cited above.
The suspected long-term disadvantage of corticalization [79] is based on bone index
(BI) analysis. There are some doubts about the specificity of this measure in detecting
corticalization [80]. It seems that this measure does not discriminate very strongly between
homogeneous dark areas (crestal bone loss) and homogeneous bright areas (corticalization
of trabecular bone). Another inconvenience is the need to use the inverse of the bone index,
J. Clin. Med. 2022, 11, 7189 3 of 20
i.e., 1/BI. Next, it is known that 1/BI is highest in bone loss regions, significantly lower in
cortical bone and lowest significantly at the site of trabecular bone [80].
The aim of this study was to determine whether corticalization (basing on the corticaliza-
tion index) in long-term follow-up is a negative phenomenon for the fate of dental implants.
2. Materials and Methods

The collected material is the result of prospective acquisition of radiological data
during the clinical course of oral implantological treatment of patients with missing teeth
in the maxillary and mandibular region. Inclusion criteria: at least 18 years of age, bleeding
on gingival probing < 20%, probing depth ≤ 3 mm, good oral hygiene, regular follow-ups,
following doctor’s orders. Exclusion criteria: uncontrolled internal co-morbidity (diabetes
mellitus, thyroid dishormonoses, rheumatoid disease and other immunodeficiencies),
a history of oral radiation therapy, past or current use of cytostatic drugs, soft tissue
augmentation, low quality or lack of follow-up radiographs. General health was confirmed
via anamnesis and evaluation of body mass index (BMI) using a serum test of thyrotropin,
calcium and triglycerides (the way to describe their general condition, i.e., emanation of the
health status on entry to the study). Finally, clinical and radiological data of 911 persons
were included in this study.
The dental implants were inserted by one dentist (M.K.) according to the protocols
recommended by the manufacturers. A total of 22 types of dental implant were used in
this study: AB Dental Devices I5 (www.ab-dent.com (accessed on 21 July 2022), Ashdod,
Israel) 102 pieces, ADIN Dental Implants Touareg (www.adin-implants.com (accessed on
21 July 2022), Afula, Israel) 89 pieces, Alpha Bio ARRP (www.alpha-bio.net (accessed on
21 July 2022), Petah-Tikva, Israel) 14 pieces, Alpha Bio ATI (www.alpha-bio.net (accessed on
21 July 2022), Petah-Tikva, Israel) 139 pieces, Alpha Bio DFI (www.alpha-bio.netv (accessed
on 21 July 2022), Petah-Tikva, Israel) 43 pieces, Alpha Bio OCI (www.alpha-bio.net (accessed
on 21 July 2022), Petah-Tikva, Israel) 28 pieces, Alpha Bio SFB (www.alpha-bio.net (accessed
on 21 July 2022), Petah-Tikva, Israel) 62 pieces, Alpha Bio SPI (www.alpha-bio.net (accessed
on 21 July 2022), Petah-Tikva, Israel) 448 pieces, Argon K3pro Rapid (www.argon-dental.de
(accessed on 21 July 2022), Bingen am Rhein, Germany) 182 pieces, Bego Semados RI
(www.bego-implantology.com (accessed on 21 July 2022), Bremen, Germany) 12 pieces, Den-
tium Super Line (www.dentium.com (accessed on 21 July 2022), Gyeonggi-do, South Korea)
38 pieces, Friadent Ankylos C/X (www.dentsplysirona.com (accessed on 21 July 2022),
Warszawa, Poland) 14 pieces, Implant Direct InterActive (www.implantdirect.com (ac-
cessed on 21 July 2022), Thousand Oaks, United States of America) 139 pieces, Implant
Direct Legacy 3 (www.implantdirect.com (accessed on 21 July 2022), Thousand Oaks,
United States of America) 48 pieces, MIS BioCom M4 (www.mis-implants.com (accessed
on 21 July 2022), Bar-Lev Industrial Park, Israel) 8 pieces, MIS C1 (www.mis-implants.com
(accessed on 21 July 2022), Bar-Lev Industrial Park, Israel) 307 pieces, MIS Seven (www.
mis-implants.com (accessed on 21 July 2022), Bar-Lev Industrial Park, Israel) 921 pieces,
MIS UNO One Piece (www.mis-implants.com (accessed on 21 July 2022), Bar-Lev Industrial
Park, Israel) 40 pieces, Osstem Implant Company GS III (www.en.osstem.com (accessed
on 21 July 2022), Seoul, South Korea) 15 pieces, SGS Dental P7N (www.sgs-dental.com
(accessed on 21 July 2022), Schaan, Liechtenstein) 12 pieces, TBR Implanté (www.tbr.dental
(accessed on 21 July 2022), Toulouse, France) 6 pieces, and Wolf Dental Conical Screw-Type
(www.wolf-dental.com (accessed on 21 July 2022), Osnabrück, Germany) 31 pieces. The
total number of introduced dental implants was 2700 pieces. The appearance of the tested
implants is shown in Figure 1.
All implants were loaded late, i.e., min. 3 months after the implants were placed in the
bone. Standardized intraoral radiographs [81] were taken immediately before prosthetic
restoration (initial radiograph), 5 and 10 years later. Focus X-ray apparatus (Instrumental
Dental, Tuusula, Finland) was set to the constant technical parameters: exposure time
0.1 s, voltage in the lamp 70 kV and current 7 mA. An intraoral parallel technique was
used. To ensure an identical relative position of the implant, an X-ray tube and radiation
J. Clin. Med. 2022, 11, 7189 4 of 20
detector and a set of RINN XCP rings and holders were utilized (Dentsply International
Inc., Cheung Sha Wan, Hong Kong, China) with a silicone bite index. The video part of
the system was a recording plate with a photosensitive storage surface (Digora Optime
digital radiography system—Soredex, Tuusula, Finland [61]). Immediately after the X-ray
exposure, the storage phosphor plate was placed in a scanner that reads radiographic
information (the image size was 476 × 620 pixels; the pixel size was 70 µm × 70 µm). A
computer coupled with the scanner processed, presented and archived acquired images.
Patients included in the study were followed by a single dentist during the entire period.
The average marginal bone loss (MBL) of the alveolar crest after osseointegration (initial) at
5 and 10 years of functional loading was measured. In addition, the bone texture 4features
J. Clin. Med. 2022, 11, x FOR PEER REVIEW of 21
at these time periods were calculated. The influence of factors related to implant design
(Table 1) was evaluated.
(a) (b) (c) (d) (e) (f)
(g) (h) (i) (j) (k) (l)
(m) (n) (o) (p) (q) (r)
(s) (t) (u) (v)

Figure 1.
Figure 1. The
The appearance
appearance of
of the
the dental
dental implants
implants compared
compared in
in this
thisstudy,
study,ininalphabetical
alphabeticalorder:
order:(a)
(a)AB
AB Dental Devices I5; (b) ADIN Dental Implants Touareg; (c) Alpha Bio ARRP; (d) Alpha Bio ATI;
Dental Devices I5; (b) ADIN Dental Implants Touareg; (c) Alpha Bio ARRP; (d) Alpha Bio ATI; (e) Alpha
(e) Alpha Bio DFI; (f) Alpha Bio OCI; (g) Alpha Bio SFB; (h) Alpha Bio SPI; (i) Argon Medical Pro-
ductions K3pro Rapid; (j) Bego Semados RI; (k) Dentium Super Line; (l) Friadent Ankylos C/X; (m)
Implant Direct InterActive; (n) Implant Direct Legacy 3; (o) MIS BioCom M4; (p) MIS C1; (q) MIS
Seven; (r) MIS UNO One Piece; (s) Osstem Implant Company GS III; (t) SGS Dental P7N; (u) TBR
Implanté; (v) Wolf Dental Conical Screw-Type.
All implants were loaded late, i.e., min. 3 months after the implants were placed in
J. Clin. Med. 2022, 11, 7189 5 of 20
Bio DFI; (f) Alpha Bio OCI; (g) Alpha Bio SFB; (h) Alpha Bio SPI; (i) Argon Medical Productions
K3pro Rapid; (j) Bego Semados RI; (k) Dentium Super Line; (l) Friadent Ankylos C/X; (m) Implant
Direct InterActive; (n) Implant Direct Legacy 3; (o) MIS BioCom M4; (p) MIS C1; (q) MIS Seven;
(r) MIS UNO One Piece; (s) Osstem Implant Company GS III; (t) SGS Dental P7N; (u) TBR Implanté;
(v) Wolf Dental Conical Screw-Type.
Table 1. Design features of dental implant used in this study (www.spotimplant.com/en/ (access on
21 July 2022)). Alphabetical order of the implant names.
Titanium Connection Connection Neck Apex Apex Apex

Manufacturer Level
Neck Micro- Body Body
Implant Type Alloy Type Shape Shape Shape Threads Shape Hole Groove
threads
AB Dental Bone No
Devices Grade 5 Level Internal Hexagon Straight No Tapered Square Flat Hole Yes
I5
ADIN Dental Bone No
Implants Grade 5 Level Internal Hexagon Straight Yes Tapered Square Flat Hole Yes
Touareg
Alpha Bio Tissue Custom One Piece No Reverse Cone No No
ARRP Grade 5 Level Abutment Straight Tapered Buttress Hole
Alpha Bio Bone Hexagon Yes Square No Yes
ATI Grade 5 Level Internal Straight Straight Flat Hole
DFI Grade 5 Level Internal Straight Tapered Flat Hole
Alpha Bio Bone Hexagon No No Dome No
OCI Grade 5 Level Internal Straight Straight Threads Round
Alpha Bio Bone Hexagon No V No Yes

SFB Grade 5 Level Internal Straight Tapered Shaped Flat Hole
SPI Grade 5 Level Internal Straight Tapered Flat Hole
Argon
Yes V Dome No Yes
Medical Prod. Grade 4 Subcrestal Internal Conical Straight Tapered Shaped Hole
K3pro Rapid
Bego Semados Bone Hexagon Yes Reverse Cone No Yes
RI Grade 4 Level Internal Straight Tapered Buttress Hole
Dentium Bone No Buttress Dome No Yes
Super Line Grade 5 Level Internal Conical Straight Tapered Hole
Friadent No V Dome No Yes
Ankylos C/X Grade 4 Subcrestal Internal Conical Straight Tapered Shaped Hole
Implant Direct Bone Yes Reverse Dome No Yes
InterActive Grade 5 Level Internal Conical Straight Tapered Buttress Hole
Implant Direct Bone Hexagon Yes
Reverse
Dome
No
Yes
Grade 5 Level Internal Straight Tapered Buttress Hole
Legacy 3
MIS Bone Hexagon No V No
Yes
BioCom M4 Grade 5 Level Internal Straight Straight Shaped Flat Hole
MIS Bone Yes Reverse Dome No Yes
C1 Grade 5 Level Internal Conical Straight Tapered Buttress Hole
MIS Bone Reverse No
Seven Grade 5 Level Internal Hexagon Straight Yes Tapered Buttress Dome Hole Yes
MIS Tissue One Piece

UNO One Custom No Square Dome No Yes
Grade 5 Level Abutment Straight Tapered Hole
Piece
Osstem
Implant Bone Yes V Dome No
Company Grade 5 Level Internal Conical Straight Tapered Shaped Hole Yes
GS III
SGS Dental Bone V No
Grade 5 Level Internal Hexagon Straight Yes Tapered Shaped Flat Hole Yes
P7N
TBR Bone Octagon No No Yes
Implanté Grade 5 Level Internal Straight Straight Threads Flat Round
Wolf Dental Bone V No

Conical Grade 4 Level Internal Hexagon Straight No Tapered Shaped Cone Hole Yes
Screw-Type
J. Clin. Med. 2022, 11, x FOR PEER REVIEW 6 of 21
J. Clin. Med. 2022, 11, 7189 6 of 20

Wolf Dental Bone
Grade 4 Internal Hexagon Straight No Tapered V Shaped Cone No Hole Yes
Conical Screw-Type Level
In
Inthe
theradiographs
radiographs obtained in this
obtained in this way,
way, aaregion
regionof
ofinterest
interest(ROI)
(ROI)was
wasestablished
establishedinin
the area of bone near the implant neck (Figure 2, green). The second ROI was
the area of bone near the implant neck (Figure 2, green). The second ROI was established established
in
inan
animage
image ofof intact
intact bone distant from
bone distant from the
thedental
dentalimplant
implant(it(itwas
wasreferent
referentbone,
bone, yellow).
yellow).
The surface area of each ROI was 1500 pixels squared.
The surface area of each ROI was 1500 pixels squared.
Figure 2. Image data acquisition method for texture analysis in intraoral radiographs. ROIs high-
lighted2.inImage
Figure data
yellow areacquisition
sites in themethod forcrest
alveolar texture analysis
distant frominthe
intraoral
dentalradiographs. ROIs highlighted
implants (reference). ROIs
inmarked
yellowin are sitesare
green in the
sitesalveolar crest
examined distant
along thefrom
neck the dental
portion of implants (reference).
the implants ROIs marked
and represent, respec-in
tively:
green radiographs
are taken
sites examined immediately
along prior to of
the neck portion prosthetic work—initial
the implants ROI; radiographs
and represent, respectively:taken after
radiographs
five years
taken of functional
immediately prior toloading—5
prostheticyears ROI; radiographs
work—initial taken after
ROI; radiographs tenafter
taken years of years
five functional load-
of functional
ing—10 years
loading—5 ROI.
years ROI;The data extracted
radiographs takenfrom
afterthese ROIsof
ten years were later analyzed
functional in freeware
loading—10 MaZda
years ROI. The 4.6
data
[79,80,82] and used to calculate the corticalization index.
extracted from these ROIs were later analyzed in freeware MaZda 4.6 [79,80,82] and used to calculate
the corticalization index.
Radiologically recorded peri-implant bone structure was studied via digital texture
analysis using the corticalization
Radiologically index previously
recorded peri-implant proposed
bone structure was[80]studied
as versionvia 1digital
(CI). Ittexture
con-
sists of the product of a measure that evaluates the number of long series of pixels
analysis using the corticalization index previously proposed [80] as version 1 (CI). It consists of sim-
ilar
of theoptical density
product with the that
of a measure meanevaluates
optical density of theof
the number studied site (in
long series of the numerator)
pixels of similar
and the magnitude of the chaotic arrangement of the texture pattern, i.e.,
optical density with the mean optical density of the studied site (in the numerator) and differential en-
the
tropy (in the denominator).
magnitude of the chaotic arrangement of the texture pattern, i.e., differential entropy (in
The texture of X-ray images was analyzed in MaZda 4.6 freeware invented by the
the denominator).
University of Technology
The texture in Lodzwas
of X-ray images [82] analyzed
to test measures
in MaZda of corticalization in the per-im-
4.6 freeware invented by the
plant environment of trabecular bone (representing original bone before implant-depend-
University of Technology in Lodz [82] to test measures of corticalization in the per-implant
ent alterations) and soft tissue (representing product of marginal bone loss). MaZda pro-
environment of trabecular bone (representing original bone before implant-dependent
vides both first-order (mean optical density) and second-order (differential entropy:
alterations) and soft tissue (representing product of marginal bone loss). MaZda provides
DifEntr, long-run emphasis moment: LngREmph) data. Due to the fact that the second-
both first-order (mean optical density) and second-order (differential entropy: DifEntr,
order data are given for four directions in the image and in the present study the authors
long-run emphasis moment: LngREmph) data. Due to the fact that the second-order data
do not wish to search for directional features, the arithmetic mean of these four primary
are given for four directions in the image and in the present study the authors do not
data was included for further analysis. The regions of interest (ROIs) were normalized (μ
wish to search for directional features, the arithmetic mean of these four primary data was
± 3σ) to share the same mean (μ) and standard deviation (σ) of optical density within the
included for further analysis. The regions of interest (ROIs) were normalized (µ ± 3σ)
ROI. To eliminate noise [83] further, worked on data were reduced to 6 bits. For analysis
to share the same mean (µ) and standard deviation (σ) of optical density within the ROI.
in a co-occurrences matrix, a spacing of 5 pixels was chosen. In the formulas that follow,
To eliminate noise [83] further, worked on data were reduced to 6 bits. For analysis in a
p(i) is a normalized histogram vector (i.e., histogram whose entries are divided by the total
co-occurrences matrix, a spacing of 5 pixels was chosen. In the formulas that follow, p(i) is a
number of pixels in ROI), i = 1,2,…, Ng, and Ng denotes the number of optical density lev-
normalized histogram vector (i.e., histogram whose entries are divided by the total number
els. The mean optical density feature (only a first order feature) was calculated as below:
of pixels in ROI), i = 1,2, . . . , Ng , and Ng denotes the number of optical density levels. The
mean optical density feature (only a first order feature) was calculated as below:
J. Clin. Med. 2022, 11, 7189 7 of 20
N
Mean Optical Density = ∑i=g1 ip(i) (1)
Second order features:
Ng
DifEntr = − ∑i=1 p x−y (i )log p x−y (i )

(2)
where Σ is the sum, Ng is the number of levels of optical density in the radiograph, i and j
are the optical density of pixels 5 pixels distant one from another, p is the probability and log
is the common logarithm [54]. The differential entropy calculated in this way is a measure
of the overall scatter of bone structure elements in a radiograph. Its high values are typical
for cancellous bone [64,84–86]. Next, the last primary texture feature was calculated:
Ng
∑i=1 ∑kNr 2
=1 k p (i, k )
LngREmph = Ng
(3)
∑i=1 ∑kNr
=1 p (i, k )
where Σ is the sum, Nr is the number of series of pixels with density level i and length
k, Ng is the number of levels for image optical density, Nr is the number of pixel in the
series and p is the probability [87,88]. This texture feature describes thick, uniformly dense,
radio-opaque bone structures in intra-oral radiograph images [84,86].
The equations for mean optical density, DifEntr and LngREmph were subsequently
used for the corticalization index (CI) construction [80]:
Ng
∑i=1 ∑kNr 2
=1 k p (i, k )
LngREmph = Ng
(4)
∑i=1 ∑kNr
=1 p (i, k )
Statistical analysis includes feature distribution evaluation, mean (t-test) or median

(W-test) comparison, analysis of regression and one-way analysis of variance or the Kruskal-
Wallis test as no-normal distribution or between-group variance indicated significant
differences in investigated groups. Detected differences or relationships were assumed to
be statistically significant when p < 0.05. Statgraphics Centurion version 18.1.12 (StatPoint
Technologies, Warrenton, VA, USA) was used for statistical analyses.
3. Results
In the implantological material collected, it was found at baseline (initial) that 86.7% of
the implants were not affected by marginal bone loss at all and 13.3% of the implants had
some degree of bone loss (in this subgroup the MBL was 1.93 ± 1.85 mm). After 5 years,
bone loss was not present in 54.4% of the implants, and bone loss was noted in 43.6% of the
implants (in this subgroup the MBL was 1.91 ± 1.26 mm). At the final point of the study,
i.e., after 10 years of functional loading, there was zero bone loss in 44.4% of implants,
while 55.6% were affected to some degree by marginal bone loss (in this subgroup the MBL
was 2.67 ± 2.04 mm).
A sequential, significant increase in the CI in peri-implant bone was observed from
the initial study (i.e., just after functional loading) to five years (p < 0.001). Subsequently, a
slight decrease in the CI was noted at the ten-year study (p < 0.05), but the CI is significantly
higher than on the day functional loading began. When analyzing MBL, it was found to
progress statistically significantly throughout the study with high significance (p < 0.001).
When examining the relationship between CI and MBL, it was noticed that the two variables
were associated with each other from five years after the functional loading of the dental
implants, i.e., at the fifth year: CC = 0.11, R2 = 1.2%, p < 0.001, and at the tenth year:
CC = 0.12, R2 = 1.4%, p < 0.01. MBL was directly proportionally related with an increase in
the CI (Table 2 and Figure 3).
J. Clin. Med. 2022, 11, 7189 8 of 20
Table 2. The progressive increase in the difference in bone structure of implant-loaded versus ref-
Table 2.
erence The progressive
cancellous bone andincrease in therelationship
the observed difference with
in bone structure
marginal boneofloss.
implant-loaded versus
reference cancellous bone and the observed relationship with marginal bone loss.
Region of Interest/Period Corticalization Index Marginal Bone Loss [mm] Simple Regression
Region of Interest/Period
Reference Cancellous Bone Corticalization
149 ± 178Index Marginal
0.00Bone Loss [mm]
± 0.00 Simplen.a.Regression
Initial Peri-Implant
Reference Observation
Cancellous Bone 200±± 178
149 146 0.25
0.00±±0.94
0.00 n.s.
n.a.
5Initial
YearsPeri-Implant
Peri-Implant Observation
Observation 282±± 146
200 182 0.25±±1.26
0.83 0.94 CC = 0.11; R2 =n.s.
1.2%; p < 0.001
2 = 1.2%; p < 0.001
105 Years
YearsPeri-Implant
Peri-ImplantObservation
Observation 261±± 182
282 168 0.83±±2.01
1.48 1.26 CC = 0.11; R
CC = 0.12; R 2 = 1,4%; p < 0.01
2
10 Years Peri-Implant Observation 261 ± 168 1.48 ± 2.01 CC = 0.12; R = 1,4%; p < 0.01
Abbreviations: n.a.—not applicable; n.s.—no statistical significance; CC—correlation coefficient:
R2 —coefficientn.a.—not
Abbreviations: applicable; n.s.—no statistical significance; CC—correlation coefficient: R2 —coefficient
of determination.
of determination.
Figure 3. The results of peri-implant bone corticalization assessment (corticalization index, blue line,
Figure 3. The results of peri-implant bone corticalization assessment (corticalization index, blue line,
data without
data without aa unit)
unit) and
and marginal
marginal bone
bone loss
loss (red
(red line,
line, data
data in
in millimeters).
millimeters). There
There was
was aa statistically
statistically
significant increase in the values of both variables at each stage of the study. Moreover, it was itnoted
significant increase in the values of both variables at each stage of the study. Moreover, was
notedthere
that that was
thereawas a directly
directly proportional
proportional relationship
relationship of marginal
of marginal bonebone
lossloss
withwith
the the progression
progression of
corticalization at 5at
of corticalization years and 10
5 years andyears of functional
10 years loadingloading
of functional of the implants. Abbreviations:
of the implants. n.r.—no
Abbreviations:
relationship.
n.r.—no relationship.
corticalization in
It is important to evaluate corticalization in relation
relation to
to basic
basic epidemiological
epidemiological data.
data.
Hence, the relationship with gender,gender, smoking,
smoking, location,
location, etc.
etc. is shown
shown below
below.(Table
(Table3).
3)
Sex, pre-prosthetic surgical augmentation procedures and surgical technique for aug-
mentation
Table are not a differentiating
3. Presentation factor for
of included population. the studyofpopulation
Assessment the impact at any stage
of baseline of the survey.
epidemiological
data on the corticalization
In contrast, the opposite index observed
is true in peri-implant
of localization. Forbone.
smokers with implants put in the
mandible or posterior part of the dental arch, corticalization is higher than in the smoker
Corticalization Index
Clinical Feature group (excluding
Option/Value of5-year observation) with implants in the maxilla or posterior dental arch,
the Feature
Initial 5 Years 10 Years
throughout the study period. The association of increasing weight, height and BMI (as
well as serum Female 205 ± 169
calcium levels) in patients with a decreasing279 ± corticalization
176 263 ± 151
index can be
Sex
Male 194 ± 114 285 ± 190
seen. On the other hand, increasing age (but no relation found in 10-year investigation) 260 ± 190 and
thyrotropinNon-Smoker 200 ±are
levels in the patients studied 152accompanied
L 283by± an
185increasing257 ± 166 L
corticalization
Tobacco Smoking
index (Figure Smoker
4). 203 ± 91 H 272 ±155 301 ± 184 H
The results obtained for the different
Maxilla 175 ± types
108 L of implants239 that
± 151 remained
L under
223 ±long-term
148 L
Jaw follow-up Mandible
are shown below (Figure190 5).± 179
They H are arranged in all four graphs fromH the
336 ± 203 H 302 ± 179
implant type with the lowest peri-implant
Anterior 166 ± bone
92 L corticalization to the
247 ± 163 L highest226
corticalization
± 162 L
Localization in Dental Arch (for both CI and MBL). It is noticeable that MBL does not correspond directly to CI values
Posterior 212 ± 174 H 295 ± 188 H 273 ± 169 H
for individual implants. Therefore, further analyses were performed in groups organized
Augmented 220 ± 210 267 ± 164 263 ± 142
Jawbone Status differently, i.e., according to the features of the implant designs (Table 4) and the prosthetic
Intact
restoration used (Table 5). 193 ± 116 286 ± 188 261 ± 176
Implant Neck Bone Chips 236 ± 269 292 ± 187 271 ± 133
Augmentation Technique Implant Neck Bone Substitute 183 ± 107 210 ± 138 280 ± 211
Bone Substitute Sinus Lift 210 ± 143 248 ± 138 252 ± 135
Age 47 ± 13 years Direct Relation * Direct Relation * No Relation
Patient Height 1.70 ± 0.09 m No Relation No Relation Inverse Relation *
J. Clin. Med. 2022, 11, 7189 9 of 20
Table 3. Presentation of included population. Assessment of the impact of baseline epidemiological

data on the corticalization index observed in peri-implant bone.
Corticalization Index
Clinical Feature Option/Value of the Feature
Initial 5 Years 10 Years
Patient Weight 75 ± 19 Kg No Relation Inverse Relation * Inverse Relation *
Body Mass Index
Sex
Female
26 ± 4 No±Relation
205 169 279 ±
Inverse 176
Relation * Inverse 263 ± 151 *
Relation
Male 194 ± 114 285 ± 190 260 ± 190
Serum Thyrotropin 1.73 ± 1.07 mU/l Direct Relation * Direct Relation * Direct Relation *
Non-Smoker 200 ± 152 L 283 ±Relation
185 ± 166 L *
257Relation
Total Serum
Tobacco Calcium
Smoking 2.39 ± 0.61 mmol/dl Inverse Relation * Inverse * Inverse
Smoker 203 ± 91 H 272 ±155 ± 184 H
Serum Triglycerides 1.24 ± 0.57 mmol/l Direct Relation * No Relation No301
Relation
Maxilla 175 L
± 108options ± 151 L period (p <223 ± 148 L
H value higher than in other implant design within239
observation 0.05); L value
Jaw H H H
Mandible
lower than 190 ± 179
in other implant design options within observation ± 203(p < 0.05); * means
336period 302 ± 179
significant
relationship (p < 0.05) between corticalizationLindex and the clinical quantitative (i.e., numerical)
Anterior 166 ± 92 247 ± 163 L 226 ± 162 L
Localization in Dental Arch feature. H H
Posterior 212 ± 174 295 ± 188 273 ± 169 H
Augmented
Sex, 220 ± 210
pre-prosthetic surgical augmentation procedures 267and± 164
surgical technique 263 ±for
142aug-
Jawbone Status
mentation Intact
are not a differentiating193 ± 116
factor 286 ± 188 at any stage
for the study population of±the
261 176sur-
vey. In contrast,
Implant Neck Bone the opposite is true
Chips 236of± localization.
269 For292
smokers
± 187 with implants 271put in the
± 133
Augmentation Technique Implant Neckor
mandible Bone Substitute
posterior part of the 183 ± 107
dental 210 ± is
arch, corticalization 138
higher than in280 the±smoker
211
Bone
group Substitute
(excluding Sinus Lift observation)
5-year 210 ± with
143 implants in 248the± 138
maxilla or posterior 252 ± dental
135
Age arch, 47
throughout
± 13 years the study period. The association
Direct Relation * of increasing
Direct Relation *weight, height and
No Relation BMI
(as well as serum calcium levels) in patients with a decreasing corticalization index can be
Patient Height 1.70 ± 0.09 m No Relation No Relation Inverse Relation *
seen. On the other hand, increasing age (but no relation found in 10-year investigation)
Patient Weight 75 ± 19 Kglevels in the patients
and thyrotropin No Relation Inverse Relation
studied are accompanied by an* increasing
Inverse corticali-
Relation *
Body Mass Index 26 ±(Figure
zation index 4 4). No Relation Inverse Relation * Inverse Relation *
Serum Thyrotropin The results
1.73 ± 1.07 mU/L obtained for the different types
Direct Relation * of implants that
Direct Relation * remained under
Direct long-*
Relation
term follow-up are shown below (Figure 5). They are arranged in all four graphs from the
Total Serum Calcium 2.39 ± 0.61 mmol/dL Inverse Relation * Inverse Relation * Inverse Relation *
implant type with the lowest peri-implant bone corticalization to the highest corticaliza-
Serum Triglycerides 1.24
tion ± 0.57
(for bothmmol/L
CI and MBL). ItDirect Relationthat
is noticeable * MBL No does Relation No Relation
not correspond directly to CI
H values for individual
value higher implants.
than in other Therefore,
implant design further
options within analyses
observation were performed
period (p < 0.05); in groups
L value or-than
lower
inganized differently,
other implant i.e., according
design options to the features
within observation period (pof<the implant
0.05); * meansdesigns
significant(Table 4) and(pthe
relationship < 0.05)
between corticalization
prosthetic index
restoration and (Table
used the clinical
5). quantitative (i.e., numerical) feature.
Figure 4. An example of the relationship found between patients’ general condition (TSH: thyrotro-
Figure 4. An example of the relationship found between patients’ general condition (TSH: thyrotropin
pin serum level in mU/l) and the corticalization index. Both relationships are statistically significant
serum level in mU/L) and the corticalization index. Both relationships are statistically significant
(p < 0.05).
(p < 0.05).
J. Clin. Med. 2022, 11, 7189 10 of 20
Figure 5. The results obtained for the types of dental implants studied. The charts on the left show
Figure 5. The
the results of results obtained forevaluation
the corticalization the types of dental
(five andimplants studied.
ten years). The charts
The results on arranged
here are the left show
fromthe
results
lowestofmean
the corticalization evaluation
(top) to highest (five and
mean (bottom). Onten
theyears). Thethe
right are results here
results ofare arranged
marginal from
bone losslowest
ar-
ranged
mean in the
(top) same order
to highest meanas(bottom).
for corticalization—it can the
On the right are be seen that
results of bone loss bone
marginal does not
lossabsolutely
arranged in
correspond
the same order to corticalization.
as for corticalization—it can be seen that bone loss does not absolutely correspond
to corticalization.
Table 4. Peri-implant bone feature observed among examined implant designs groups.
Table 4. Peri-implant
Design Parameterbone feature observed among
Option examined
Feature implant designs
Initial 5 Yearsgroups.
10 Years
MBL 0.00 L 0.00 L 0.00
Design Parameter Grade 4
Option Feature Initial 5 Years 10 Years
Titanium Alloy CI 184 H 179 L 189
MBL L L
n = 2196 Grade 4 5 MBL 0.00
0.00 H
H
0.000.00
H
L
0.910.00
Titanium Alloy Grade CI 184 179 189
CI 163 L 225 H 209
n = 2196 MBL H H
Grade 5 MBL 0.00
0.00 L 0.000.00
L 0.00 0.91
L
Subcrestal CI 163 L 225 H 209
CI 198 H 181 201 L
Immersion Level MBL

MBL 0.00 L
0.00 0.00 L
0.00 0.970.00
H
L
Subcrestal
Bone Level CI H L
n = 2196 CI 163198
L 224181 201
205 L
Immersion Level MBL
MBL 0.000.00
H 1.24 0.00
H 0.97 H
0.00
n = 2196 Tissue
Bone Level
Level CI L L
CI 163
154 222224 439205
H
MBL
MBL 0.00
0.00L H L H
0.001.24 0.910.00
Internal
Tissue Level CI 154 H
Connection Type CI 167 221222 205439
L
n = 2196 MBL
MBL 0.00
0.00H L H L
1.240.00 0.000.91
Custom
Internal CI 167 L
Connection Type CI 154 222221 439205
H
n = 2196 Shape
Connection MBL
MBL 0.00 H
0.00 1.24 H
0.00 0.000.00
Conical
Custom H
n = 2196 CI
CI 202154
H 225222 200439
L
J. Clin. Med. 2022, 11, 7189 11 of 20
Table 4. Cont.
Design Parameter Option Feature Initial 5 Years 10 Years

MBL 0.00 0.00 0.00
Conical CI 202 H 225 200 L
MBL 0.00 0.00 0.97
Internal Hexagon
Connection Shape CI 151 L 220 205 L
n = 2196 MBL 0.00 0.67 2.91
Internal Octagon CI 205 168 268
MBL 0.00 1.24 0.00
One Piece Abutm CI 154 222 439 H
MBL 0.00 0.00 L 0.73 L
Head Yes CI 170 H 221 201
Microthreads
n = 2196 MBL 0.00 0.61 H 1.15 H
No CI 158 L 222 227
MBL 0.00 0.00 L 0.85
Tapered
Body Shape CI 167 226 H 206
n = 2196 MBL 0.00 1.33 H 1.15
Straight
CI 172 147 L 206
MBL 0.00 2.15 H n.a.
Butteress CI 190 383 H n.a
MBL 0.00 L 0.00 L 0.79 L
Reverse Butteress CI 171 H 239 H 213
Body Threads MBL 0.00 L 0.00 L 0.00 L
n = 1760 V Shape
CI 174 H 197 L 184
MBL 0.00 L 0.00 L 0.91 L
Square
CI 150 L 201 L 211
MBL 0.30 H 1.54 H 2.57 H
No Threads CI 190 164 L 232
MBL 0.00 0.00 0.00
Cone CI 122 L 199 193
Apex Shape MBL 0.00 0.00 0.79
n = 2196 Dome CI 174 H 230 H 213
MBL 0.00 0.45 H 1.21
Flat CI 148 103 L 201
MBL 0.00 L 1.54 H 2.57 H
Round CI 190 164 L 232
Apex Hole
n = 1447 MBL 0.30 H 0.00 L 0.79 L
No or other CI 167 221 H 206
MBL 0.00 L 0.00 L 0.79 L
Yes CI 167 220 105
Apex Groove
n = 2196 MBL 0.00 H 1.66 H 2.00 H
No CI 154 297 258
H value higher than in other implant design options within observation period (p < 0.05); L value lower than
in other implant design options within observation period (p < 0.05); n—number of evaluated dental implants;
MBL—marginal bone loss is given as median due to non-normal distribution in mm; CI—corticalization index is
given as median due to non-normal distribution.
In the group of implants made of grade 5 titanium alloy, lower corticalization was
noted in the initial period, which increased significantly at 5 years. A higher MBL occurred
in the later observation periods. Throughout the observation period, implants inserted
subcrestally have the lowest MBL. However, surprisingly, during the initial period, the
J. Clin. Med. 2022, 11, 7189 12 of 20
lowest bone loss is accompanied by the highest level of corticalization. These differences
disappear at the five-year follow-up period, and then at the ten-year follow-up period
the relationships reverse—the lowest corticalization is with subcrestally inserted implants
as also the MBL is the lowest. One-piece implants (i.e., of the “Custom” connection type
contrary to internal connection) were characterized by higher MBL up to and including the
fifth year of observation. This is not followed by the CI value. Evaluating the connection
shape, it could be seen that corticalization is greatest with one-piece implants (i.e., without
a socket for the abutment), but this does not go hand in hand with the MBL value at five
and ten years. When the implants do not have a haed microthread, higher MBL values are
recorded with them. CI values are also elevated, but statistically insignificant. The shape of
the implant body has no effect on corticalization and marginal loss at either the initial or
the 10-year follow-up period. It was only noted that in the fifth year of functional loading
there was less corticalization and more bone loss with tapered implants. The lowest MBL
and highest CI were noted in implants with a V shape and reverse butteress thread. The
lowest bone loss supported by an increased CI occurred with flat apex implants. Only
increasing bone loss over time was observed in implants with apex groove. This was not
followed by increasing CI values.
Table 5. The prosthetic works examined in this study.
Prosthetic n Feature Initial 5 Years 10 Years

MBL 0.00 H 0.00 0.91
Single Crown 734
CI 153 L 196 L 186 L
MBL 0.00 0.00 1.20 H
Splinted Crowns 794
CI 198 224 227 H
MBL 0.00 L 0.00 L 0.00 L
Bridge 576
CI 172 H 251 H 215
MBL 0.00 0.49 H 0.00 L
Overdenture 160
CI 185 H 392 H 239 H
MBL 0.00 0.00 1.06
Platform Switching 509
CI 155 L 197 L 200
H value higher than in other prosthetic solutions (p < 0.05); L value lower than in other prosthetic solutions
(p < 0.05); n—number of evaluated dental implants; MBL—marginal bone loss is given as median due to non-
normal distribution in mm; CI—corticalization index is given as median due to non-normal distribution.
Platform switching induces less corticalization of peri-implant bone, as do single-

crown restorations. Such restorations have low MBLs, but the lowest MBLs are found
in cases of bridges. Implant-supported bridges initially have a high CI, but at 10-year
follow-up, corticalization is already lower than in splinted crowns and overdentures.
4. Discussion
The healing process and osseointegration in dental implants is a dynamic phenomenon.
When an implant is installed, the next surgical procedure causes some marginal bone
loss [89]. Within the initial healing phase, the recruitment and migration of osteoprogenitor
cells to the surface of the implant occurs. During the secondary healing phase, new bone is
apposited. Next, the peri-implant bone is reabsorbed and replaced with a new viable bone,
i.e., remodeling is featured [32–35,44,89]. In cases of successful treatment, this reaction
reaches a balance with the patient’s body, and only in disequilibrium does the MBL increase,
thereby damaging peri-implant bone [90]. Pinpointing what underlies this dysfunction is
crucial for current dental implantology.
In a long-term study [91], assessment of corticalization in peri-implant bone was
performed only visually (Figure 2 in Buser’s study) and described in the 10-year data as
“well-corticalized”. In the current state of development of image analysis methods, a much
more precise description can be obtained [82,92]. However, this is a high-quality study,
and the authors collected results depicting the corticalization phenomenon. This can be
J. Clin. Med. 2022, 11, 7189 13 of 20
seen in the radiological figures, e.g., Figure 9 in Ref. [91], where MBL is preceded in the
bone by a pronounced disappearance of trabeculation and an increase in bone density.
However, the authors did not point out the corticalization. Similarly, this is seen in Figure 5
in Albrektsson’s publication [93]. Today, the phenomenon of bone density increase can be
analyzed qualitatively and, of course, in relation to the MBL [44,45]. Similar interesting
illustrative material can be found in another 10-year follow-up study [37] where there are
clear features of severe peri-implant bone corticalization in their Figure 1b. Unfortunately,
the corticalization term is not used at all by the authors. This is probably due to the purpose
of the paper and the lack of publications analyzing bone texture at dental implants in detail.
One can also find a publication based on radiographic material, which does not include
a single X-ray in the text [94]. In this case, it is impossible to determine what the authors
faced in their study. The second issue is the use of simple quantitative measures (they do
not describe the internal state of the bone), e.g., the percentage of implant surface remaining
in contact with the jawbone (bone-to-implant contact, BIC) or the amount of marginal bone
loss from the alveolar crest (MBL). Intuitively, it seems that bone quality (structure testing)
is important in the long-term maintenance of dental implants [95].
Corticalization (and associated marginal bone loss) related with the type of implant
used is not easy to interpret but is definitely the result of the aforementioned balance and
bone remodeling. It probably depends on the type of implant, but implant selection is
not random. It depends on the bone conditions and the possibility of using prosthetic
solutions in a given implantological system, which correspond to a given dento-gnathic
status. Finally, certainly, it depends on the dentist’s preferences for using a particular
implant system. The results presented here are derived from these many influencing
factors, but this is a typical situation in everyday clinical work and hence worth considering
and trying to understand.
It is now known from everyday clinical work that implant treatment is very long
term or even over a lifetime [96]. It seems that the changes in peri-implant bone structure
observed at this time are not a simple projection of the occlusal load in the bone [40],
but a complex modulation of osteoimmunological activity [97–99]. Recently, it has been
noticed that mechanotransduction may promote the alteration of bone marrow monocyte
activation. Thus, occlusal force may modulate the osteoimmunity in peri-implant bone [100].
In addition, there is a synergy between mechanical loading and the signaling pathway
for macrophage function, which is related to the αM integrin controlling the activity
of the mechanosensitive ion channel Piezo1 [101] and the genetically determined bone
reaction [102]. Further confirmation of an osteoimmodulatory mechanism, rather than a
simple loading reaction, in peri-implant bone remodeling is the positive role of topically
applied bisphosphonates in reducing MBL [103–105]. In the near future, a biological
analysis approach combining genomic with clinical data including bone structure will be
able to explain the mechanism of corticalization [102].
The arrangement of implant types from causing the least peri-implant bone cortical-
ization at 5 and 10 years to the implant causing the most corticalization does not reflect
the same arrangement of implant types relative to marginal bone loss (Figure 5). Thus, the
relationship is not a simple one of the type given implant = defined bone loss, and yet,
this would be supported by the corticalization index value. However, when considering
all 2700 implants, the association of corticalization with marginal bone loss is statistically
highly significant (p < 0.001). Therefore, the study material here was divided differently
(see Table 4). The names of the implants were discarded, and the design features were
taken, and thus, the implants were combined into groups with common design features.
It is interesting to note that one-piece implants are not associated with the smallest
MBLs, despite not having a micro-gap or the possibility of bacterial contamination in the
gingival sulcus and junctional epithelium [106]. Perhaps this is due to the fact that these
implants are narrower than two-part implants and can be used in a narrower alveolar crest.
Probably, the smaller volume of the bone base is prone to atrophy due to limited bone
vascularization and mechanical reasons even though there is no contamination from the
J. Clin. Med. 2022, 11, 7189 14 of 20
microgap. On the other hand, it is not surprising that implants inserted subcrestally have
low MBL and low corticalization values [107]. Considering the 10-year follow-up period,
these 2 characteristics indicate a good prognosis for subcrestal implants. Prosthetic work
placed on such implants leaves adequate biological space for good marginal periodontal
function [108], and there is certainly more bone around them from the start than if one-
piece implants are used. This ensures permanent maintenance of the peri-implant bone
level [109]. When considering the significance of the micro-thread implant neck, it should
be noted that the MBL observed in this study is slightly lower than in studies known from
the literature [110,111]. At the same time, these studies here confirmed the effectiveness of
micro-thread use in minimizing MBL over a 10-year period of functional loading. However,
there was no significant change in the peri-implant jawbone cortication of micro-thread
implants. The interaction of thread parameters has a significant influence on the peak
compressive and tensile strains at the cancellous as well cortical bone. Body-related
parameters are more effective on the peak compressive strain at the cortical interface
only [112]. The results of this work here seem to confirm these results from the numerical
analysis. CI and MBL proceed independently of the implant body, or in other words,
alternative further features determine corticalization and marginal bone loss (general
health, osteopenia, sarcopenia, dietary supplements taken, drug or behavioral weight loss,
details of prosthetic work, occlusion, parafunctions, history of prosthetic repairs, additional
dental treatment, saliva composition and active protein content, overactive tongue, etc.).
The high MBL (and disparate CI results) observed with rounded apex hole implants seems
to be more related to the fact that they are cylindrical implants without threads and with
no modifications in the neck area rather than to the effect of the apex hole on the condition
of the neck peri-implant bone.
Single crowns do not cause bone structure changes around the implants on which
they are set. At the same time, they characterize low marginal bone loss. In cases loaded
with bridges, lower measures of corticalization and lower MBL were noted at 5 years
than in overdentures and compared to splinted crowns at 10 years. In the case of works
using switching platforms, it was noted that corticalization values are always lower than
in works without prosthetic platform switching. No differences were noted in terms of
MBL. Among the multitude of implant design features and series of prosthetic solutions
considered, it should be noted that the lowest long-term bone loss was observed in cases
of implant loading with bridges. In contrast, the highest MBL was recorded in cases of
splinted crowns. These changes were accompanied by corresponding CI values (higher
in high MBL and lower in low MBL). Surprisingly, platform switching was not noted to
affect MBL, but there was a significantly lower CI with such implants. However, MBL in
the platform-switched prosthetic was lower than total MBL at the 10-year follow-up.
Marginal bone loss has been postulated to have a multi-factorial etiology [113] and can
be considered to occur early or late in the lifetime of an implant. It is certain that within the
first year after placement, MBL observed is a consequence of bone remodeling subsequent
to surgical and prosthetic work [56] as well early loading challenges undertaken by an
implant and its associated prosthesis [113,114]. It has been known for a long time that
smoking as well as previous history of periodontitis are associated with peri-implantitis
and may represent risk factors for this disease [115]. Given the role of adaptive bone
remodeling, corticalization may be influenced by infection as a barrier for oral microflora
invasion. Over the longer term, the cumulative effect of chronic etiological factors that
are immunological, environmental, patient-related factors such as motivation, smoking,
para- or disfunctions, infection and inflammation, as well the influence of the surgeon
or prosthodontist can affect the increase of corticalization and bone loss in long-term
observation [113,114,116,117]. Due to the poorly studied phenomenon of corticalization
in dental implantology, the authors speculate that the phenomenon of increased bone
structure density itself may be heterogeneous. They would not be surprised if it turns out
that some specific form of corticalization or the degree of its severity may be prognostically
favorable, while another form may be unfavorable, as appears to be the case after this study.
J. Clin. Med. 2022, 11, 7189 15 of 20
Corticalization index increasing with age (although observed in 5-year follow-up),

rising TSH levels and decreasing serum calcium levels seem to support the negative sig-
nificance of the peri-implant bone corticalization phenomenon. These selected markers
similarly behave with the progression of the aging process [118,119]. In this regard, the
matter of interpreting the observed phenomenon in bone is not clear. Only a narrow frag-
ment of possible systemic effects on bone has been examined. However, it is a contribution
to further interesting research.
The conclusions of this work cannot be radical. The suspicion of corticalization as
an unfavorable predictor for the development of marginal bone loss is based on several
hundred implants observed over a 10-year period. This, unfortunately, confirms previous
suspicions [79]. Undoubtedly, to establish more certain relationships [120–122], studies
should be conducted on a larger number of implants. This kind of research is prompted by
the relationship noted here between low MBL and surprisingly high CI with V shape and
reverse butteress threaded implants. Multicenter studies are also needed. Different surgical
and prosthetic protocols are worth testing. Both authors of this study believe that other
(easier and widely available) techniques for assessing the corticalization phenomenon in
peri-implant bone should also be tried.
5. Conclusions
In the scope of the study, it can be concluded that the phenomenon of peri-implant
jawbone corticalization clearly seems to be a condition that is unfavorable for the future
fate of bone-anchored implants.
Author Contributions: Conceptualization, M.K.; data curation, T.W.; formal analysis, T.W.; funding
acquisition, M.K.; investigation, T.W.; methodology, T.W.; resources, T.W.; software, T.W.; supervision,
M.K.; validation, T.W.; visualization, M.K. and T.W.; writing—original draft, M.K.; writing—review
and editing, T.W. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the Medical University of Lodz (grant numbers 503/5-061-
02/503-51-001-18, 503/5-061-02/503-51-001-17, and 503/5-061-02/503-51-002-18).
Institutional Review Board Statement: The study was conducted according to the guidelines of the
Declaration of Helsinki and approved by the Institutional Ethics Committee of the Medical University
of Lodz, PL (protocol no. RNN 485/11/KB and date of approval: 14 June 2011).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: The data on which this study is based will be made available upon
request at https://www.researchgate.net/profile/Marcin-Kozakiewicz (accessed on 22 October 2022).
Conflicts of Interest: The authors declare no conflict of interest.
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J. Clin. Med. 2022, 11, 7189. https://doi.org/10.3390/jcm11237189 https://www.mdpi.com/journal/jcm

2. Materials and Methods

(a) (b) (c) (d) (e) (f)

(g) (h) (i) (j) (k) (l)

(m) (n) (o) (p) (q) (r)

(s) (t) (u) (v)

Titanium Connection Connection Neck Apex Apex Apex

Alpha Bio Bone Hexagon No V No Yes

MIS Tissue One Piece

Wolf Dental Bone V No

J. Clin. Med. 2022, 11, 7189 6 of 20

Statistical analysis includes feature distribution evaluation, mean (t-test) or median

Table 3. Presentation of included population. Assessment of the impact of baseline epidemiological

Immersion Level MBL

Design Parameter Option Feature Initial 5 Years 10 Years

Table 5. The prosthetic works examined in this study.

Prosthetic n Feature Initial 5 Years 10 Years

Platform switching induces less corticalization of peri-implant bone, as do single-

Corticalization index increasing with age (although observed in 5-year follow-up),

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