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original papers
Dent. Med. Probl. 2010, 47, 1, 23–29
ISSN 1644-387X
© Copyright by Wroclaw Medical University
and Polish Dental Society
Marcin Kozakiewicz1, Anna Marciniak-Hoffman1, Marek Olszycki2
Comparative Analysis of Three Bone Substitute
Materials Based on Co-Occurrence Matrix
Analiza porównawcza trzech materiałów kościozastępczych
oparta na danych z macierzy zdarzeń
Department of Maxillofacial Surgery, Medical University of Lodz, Poland
Department of Radiology, Medical University of Lodz, Poland
1
2
Abstract
Background. Nowadays, bone substitute materials have become more popular.
Objectives. This article covers the comparison of tree bone-substitute materials – ChronOS®, Cerasorb® and
Straumann Bone Ceramic® (all pertain to β-tricalcium phosphates group), the quality of newly created bone was
compared.
Material and Methods. For the purposes of this paper, the analysis of X-ray photographs of 110 patients was conducted. Intraoral periapical radiographs were made on the day of a surgery and 3, 6, 9 and 12 months after the surgery such as extraction, resection and cyst removal. In the comparative analysis co-occurrence matrix was used.
Results. The above-mentioned materials belong to the same group of tricalcium phosphates, but have different shape, size, and surface structure of granule, as a result of which there are slight differences in the bone
regeneration activity observed during a few months post-operativelly. Moreover, Straumann Bone Ceramic
contains hydroxylapatite, which is visible in all radiographic images during 12 months.
Conclusions. During 12 months of tests, only the place where ChronOS is applied does not differ from reference
bone on radiographic images. Cerasorb and Straumann Bone Ceramic need longer period than 12 months in order
to create a full-value bone (Dent. Med. Probl. 2010, 47, 1, 23–29).
Key words: bone substitute materials, β-tricalcium phosphates.
Streszczenie
Wprowadzenie. Materiały kościozastępcze stają się obecnie coraz bardziej popularne.
Cel pracy. Porównanie 3 środków kościozastępczych – ChronOS®, Cerasorb® i Straumann Bone Ceramic® (wszystkie z grupy β-trójfosforanów wapniowych), pod względem jakości nowo powstałej kości.
Materiał i metody. W pracy dokonano analizy zdjęć RTG wykonanych u 110 pacjentów. Zdjęcia RTG zostały
wykonane w dniu zabiegu oraz po 3, 6, 9 i 12 miesiącach po zabiegach, takich jak: ekstrakcja, resekcja lub usunięcie
torbieli. W analizie porównawczej wykorzystano macierz zdarzeń.
Wyniki. Materiały te należą do jednej grupy β-trójwapniowych fosforanów, różnią się jednak między sobą kształtem, wielkością i strukturą powierzchni cząstek. Wpływa to na niewielkie zaobserwowane różnice w szybkości regeneracji kości w pierwszych miesiącach po zabiegu chirurgicznym. W składzie Straumann Bone Ceramic występuje
ponadto hydroksyapatyt, który jest widoczny na wszystkich zdjęciach RTG z 12 miesięcy.
Wnioski. W ciągu 12 miesięcy badań tylko miejsce aplikacji materiału ChronOS nie różni się na zdjęciu RTG od
kości referencyjnej. Cerasorb i Straumann Bone Ceramic potrzebują więcej czasu niż 12 miesięcy, aby uformowała
się na ich miejscu nowa, pełnowartościowa kość (Dent. Med. Probl. 2010, 47, 1, 23–29).
Słowa kluczowe: materiały kościozastępcze, β-fosforany trójwapniowe.
Nowadays, bone substitute materials have become more popular. Many doctors are aware of
their advantages, that is biocompatibility, angiogenesis stimulation, porosity, haemostatic activity,
full resorption [1]. The manufacturers are improving the content of bone substitite materials.
Recently, the most commonly used are
β-tricalcium phosphates (β-TPC). TCP is a syntet-
24
M. Kozakiewicz, A. Marciniak-Hoffman, M. Olszycki
ic. It is chemically and mineralogically similar to
osseous tissue and thanks to that it is bio-compatible and osteo-conductive. Moreover, it has good
tolerance, lack of innflamation reaction from host
tissues, and most importantly lack of any danger
connected with HIV, icterus, prions [2].
In the given article tree substitute bone materials are compared: Cerasorb®, ChronOS ®,
Straumann Bone Ceramic®. Cerasorb and ChronOS
are the materials where the chief component is
composition of elements is calcium phosphate [3,
4]. However Straumann Bone Ceramic is a mixture
of β-tricalcium phosphates and hydroxyapatite
[2]. In all these materials the element composition
indicates the presence of β-tricalcium phosphate,
amount of which is proportional to the bioresorption rate, which influences significantly the quality of newly built bone [5–8]. This feature enables
to shorten the period of vital and functional bone
creation in place of osseous defect.
Material and Methods
Three β-tricalcium phosphates granulated biomaterials were applied into 110 patients. Cerasorb®
(Curasan, Germany) of gradation 1–2 mm
particles was utilized in 58 cases, ChronOS®
(Synthes, USA) of gradation 0.7–1.4 mm particles was put into 32 cases and Straumann Bone
Ceramic® (Straumann, Switzerland) of gradiation
0.4–0.7 mm particles was put into 20 cases.
Materials were implanted into bone defects
after apicoectomies, impacted tooth removals and
cyst enucleations (i.e. periapical surgery and intraalveolar surgery).
Immediately after surgery was completed,
intra-oral radiological examination was taken. Digora Optime digital radiography device
(Soredex, Finland) and X-ray apparatus Focus
(Instrumentarium Dental, Finland) were used.
Technical parameters of exposure were the same
in all included cases: 7 mA, 70 mV and 0.06 s.
Radiographs were taken in a standardized way [9].
A modified RINN (Dentsply Rinn, USA) system
was applied. A bite index was prepared using a silicone material (occlusal bite duplicates the shape
of the film plate holder and also occlusal surfaces
of the teeth). The X-ray detector was placed in the
RINN positioner and the bite index with the connection bar and ring was replaced in the mouth of
the patient then fixed to the tube. Follow-up examinations were performed in the same condition
3, 6, 9 and 12 months post-operationally.
Regions of interest (ROI) were selected in radiographs. The ROI outlining limit was the line
running on the external border of the bone sub-
stitute materials image (and not bone defect).
Another region of normal bone with the least
diverse gray level was also selected in the radiographs as a reference.
Total registered number of gray levels was
decreased to 128, to reduce random noise in the
analyzed data. Then each ROI optical density was
normalized according to mean (mean ± 3 standard
deviation of optical density). Co-occurrence matrix was analysed in MaZda ver. 4.5. The secondorder histogram was defined as the co-occurrence
matrix hdθ(i,j) [10]. When divided by the total number of neighboring pixels R(d,θ) in ROI, this matrix becomes the estimate of the joint probability,
pdθ(i,j) , of two pixels, a distance of 5 pixels apart
along a given direction θ having particular (co-occurring) values i and j. Formally, given the image
f(x,y) with a set of 128 discrete levels of optical
density, the matrix hdθ(i,j) is defined such that its
(i,j)th entry is equal to the number of times that
f(x1y1) = and f(x2y2) = j, where (1)
(x2y2) = (x1y1) + (d cos β, d sin β) (2)
This yields a square matrix of dimension
equal to the number of intensity levels in the image, for selected distance of 5 pixels and orientation θ;. Angles θ; = 0°, 45°, 90 and 135° were investigated. Aritmethical mean of these four directions was calculated due to eliminate directional
dependence.
Sum of average of co-occurrence matrix was
extracted to describe bone structure variability. It
is defined by the equation that follow (3), where
µx denotes the mean of the row sums of the cooccurrence matrix (related to the marginal distributions px(i) and px(j)).
128
SumAverg = ∑ ip x+ y (i ), where
(3)
i =1
128
p x + y (k ) = ∑
i =1
128
∑ p(i, j )
j =1
k = 2, 3, ..., 256 [11, 12] (4)
i+j=k
The geometric adjustment was performed
with the use of ToothVis program on the radiographs of each patient, about 4–5 reference
points were selected. On the basis of these points
the program matched the radiographs with each
other. Then, using MaZda ver. 4.5 program, the
reports regarding parameter sum of average cooccurrence matrix for each patient’s radiographs
were calculated.
Statistical evaluation was performed in
Statgraphics Centurion XV.II version 15.2.06.
Multiple-sample comparison based on analysis
of variance was performed. Statistically signifi-
25
Three Bone Substitute Materials Based on Co-Occurrence Matrix
cant difference amongst the standard deviations
was not observed (p = 0.5953). Next, ANOVA was
applied to reveal the factor which influenced the
variability of texture.
Results
The ANOVA table (Tab. 1) decomposes the
variance of the data into two components: a between-group component and a within-group
component. The F-ratio, which in this case equals
2.62208, is a ratio of the between-group estimate
to the within-group estimate. Since the P-value of
the F-test is 0.0016, there is a statistically significant difference between the means of the 16 variables at the 95 confidence level.
Multiple Range Tests (Tabs. 2 and 3) determines which means are significantly different
from which others.
There is no statistically significant differences between radiological texture of implanted site
by Cerasorb and Straumann Bone Ceramic after
12 months.
Discussion
The difference in surface properties may then
have profound effects on the protein adhesion and
the following cellular attachment [13]. The blood
protein adsorption starts the process of new bone
creation [14, 15]. The next phase is an attachment
phase, in which physical and chemical interactions
between cells and material take place [16]. After that
step is adhesion phase, when osteoblast adhesion
appears [16]. The most important parameters in cell
interaction are surface topography – size [17], shape
[17, 18], surface texture [19] of the material and the
physical and chemical features [3, 4] of surface.
One of the bone substitute material feature is
the creation of scaffold (which can be observed
radiologically). The products from scaffold disintegration may become then the substrate for new
bone deposition. During bone substitute material
resorption, the calcium and phosphatic ions are
created in that place. These ions have the ability
to mineralize the newly created connective tissue
from which a new bone is created.
This study presents 3 bone-substitution materials that differ from one another as regards the
microscopic surface structure (Figs. 1–4).
Cerasorb® molecules are almost ball-shaped
with diameter 1–2 mm, pore with diameter 1–8 μm
and the whole molecule is created from micromolecules with diameter 4–8 μm [4]. ChronOS ®
molecules have different shapes with diameter
0.7–1.4 mm, pores with diameter 20–500 μm and
the whole molecule consists of 2–5 μm micro-molecules [3]. While Straumann Bone Ceramic molecules has 0.4–0.7 mm and pores 100–500 μm [2].
9 months after surgery the radio-texture of
implanted site by ChronOS became similar to
normal bone. It indicates a superiority of this bone
substitute material over two competitors.
Shape and structure of the surface may have an
influence on the new bone creation rapidity [13].
ChronOS® is characterized by the most favourable
proportion of pores and molecule diameter.
The textural alteration visible in radiographic
images of Straumann Bone Ceramic® is different
from the two other materials. It is caused by the
fact that this material contains slowly resorbing
hydroxylapatite [2], and therefore the newly created bone was incrusted with hydroxylapatite for
12 months of the test.
Table 1. ANOVA table
Tabela 1. Tabela ANOVA
Source (Suma
kwadratów)
Sum of squares
(Źródło
zmienności)
Df
(Stopnie
swobody)
Mean square
(Średnia
kwadratów)
F
(Współczynnik Fischera)
P
(Stopień istotności
statystycznej)
Between groups
(Międzygrupowe)
  34.4529
15
2.29686
2.62
0.0016
Within groups
(Wewnątrzgrupowe)
126.14
144
0.875969
Total (Razem)
160.592
159
Df – degrees of freedom.
F – Fisher coefficient.
p – level of significant statistics.
Df – stopnie swobody.
F – współczynnik Fishera.
p – stopień istotności statystycznej.
26
M. Kozakiewicz, A. Marciniak-Hoffman, M. Olszycki
Table 2. Multiple Range Tests. Fisher’s least significant
difference (LSD) procedure
Tabela 2. Wielokrotny test uszeregowujący. Procedura
Fishera najmniejszych różnic (LSD)
Groups
(Grupy)
Mean
(Średnia)
Homogeneous
groups*
(Homogenność
grup*)
Table 3. Details of observed between group differences
Tabela 3. Szczegóły obserwowanych różnic międzygrupowych
Contrast
(Kontrast)
Significant difference
(Różnica statystyczna)
REF - CER00M
–2.01025
REF - CER03M
–1.13767
REF
63.6652
X
REF - CER06M
–1.44412
CHR12M
64.2627
XX
REF - CER09M
–1.70122
CHR03M
64.4883
XXX
REF - CER12M
–1.36888
STR09M
64.6167
XXXX
REF - CHR00M
–1.10333
CHR09M
64.6233
XXXX
REF - CHR06M
–0.96192
CHR06M
64.6271
XXXX
REF - CHR09M
–0.958164
STR03M
64.7098
XXXX
REF - STR00M
–1.75362
CHR00M
64.7685
XXXX
REF - STR03M
–1.0446
CER03M
64.8028
XXXX
REF - STR06M
–1.30423
STR12M
64.9549
XXXXX
REF - STR09M
–0.95158
STR06M
64.9694
XXXXX
REF - STR12M
–1.28976
CER12M
65.034
XXXXX
CER00M - CER03M
  0.872579
CER06M
65.1093
XXXXX
CER00M - CHR00M
  0.906924
CER09M
65.3664
XXXXX
CER00M - CHR03M
  1.18708
STR00M
65.4188
XXXXX
CER00M - CHR06M
  1.04833
CER00M
65.6754
XXXXX
CER00M - CHR09M
  1.05209
CER00M - CHR12M
  1.41267
CER00M - STR03M
  0.965652
CER00M - STR09M
  1.05867
CER06M - CHR12M
  0.846544
CER09M - CHR03M
  0.878054
CER09M - CHR12M
  1.10364
CHR03M - STR00M
–0.930455
CHR12M - STR00M
–1.15604
* Homogeneous groups - a graphical illustration of which
means are significantly different from which others, based
on the contrasts displayed. Each column of X’s indicates
a group of means within which there are no statistically
significant differences.
REF – reference bone.
CHR...M – ChronOS ... months after surgery.
CER...M – Cerasorb ... months after surgery.
STR...M – Straumann Bone Ceramic ... months after surgery.
*Homogenność grup – graficzna ilustracja różnic między
średnimi na podstawie stwierdzonego kontrastu. Każda
kolumna X wskazuje grupę średnich, w obrębie których
nie ma różnic statystycznych.
REF – kość referencyjna.
CHR...M – ChronOS ... miesięcy po zabiegu.
CER...M – Cerasorb ... miesięcy po zabiegu.
STR...M – Straumann Bone Ceramic ... miesięcy po
zabiegu.
Radiographic image of Cerasorb® during
12 months also differs from the reference bone,
which is caused by the different structure of granules between Cerasorb® and ChronOS® – there
are discrepancies in the diameters of granules and
pores.
REF – reference bone.
CHR...M – ChronOS ... months after surgery.
CER...M – Cerasorb ... months after surgery.
STR...M – Straumann Bone Ceramic ... months after surgery.
REF – kość referencyjna.
CHR...M – ChronOS ... miesięcy po zabiegu.
CER...M – Cerasorb ... miesięcy po zabiegu.
STR...M – Straumann Bone Ceramic ... miesięcy po
zabiegu.
27
Three Bone Substitute Materials Based on Co-Occurrence Matrix
66
65
CER
CHR
STR
REF
64
63
00M
03M
06M
09M
12M
Fig. 1. Transformations of the texture (parameter on vertical axis: sum of square) of site implanted by different tricalcium phosphates: CER – Cerasorb, CHR – ChronOS, STR – Straumann Bone Ceramic, REF – reference bone,
M – months
Ryc. 1. Zmiany tekstury (cecha na osi pionowej: suma kwadratów gęstości optycznej) miejsca wszczepienia różnych
fosforanów trójwapniowych: CER – Cerasorb, CHR – ChronOS, STR – Straumann Bone Ceramic, REF – kość referencyjna, M – miesiące
Fig. 2. A) Cerasorb implantation site in patient after radicular cyst removal (red area), the radiological texture is different from reference bone (green area) till the RTG E, B) 3 months after the implantation, C) 6 months after the implantation, D) 9 months after the implantation, E) 12 months after the implantation
Ryc. 2. A) Implantacja materiału Cerasorb u pacjenta po usunięciu torbieli korzeniowej (obszar czerwony), struktura
radiologiczna jest odmienna od kości referencyjnej (obszar zielony) do ostatniego badania E, B) 3 miesiące po implantacji materiału, C) 6 miesięcy po implantacji materiału, D) 9 miesięcy po implantacji, E) 12 miesięcy po implantacji
28
M. Kozakiewicz, A. Marciniak-Hoffman, M. Olszycki
Fig. 3. A) ChronOS implantation site in patient after radicular cyst removal (red area), the radiological texture is different from reference bone till (green area) the image D, B) radiological examination 3 months post-operationally,
C) 6 months after the implantation, D) 9 months after the implantation, E) 12 months after the implantation
Ryc. 3. A) Implantacja materiału ChronOS u pacjenta po usunięciu torbieli korzeniowej (obszar czerwony), struktura
radiologiczna jest odmienna od referencyjnej kości (obszar zielony) do badania D, B) badanie radiologiczne 3 miesiące
po zabiegu chirurgicznym, C) 6 miesięcy po implantacji materiału, D) 9 miesięcy po implantacji materiału, E) 12 miesięcy po implantacji
Fig. 4. A) Straumann Bone Ceramic implantation site in patient after radicular cyst removal (red area), the radiological texture is different from reference bone till (green area) the RTG E, B) 3 months after the implantation,
C) 6 months after the implantation, D) 9 months after the implantation, E) 12 months after the implantation
Ryc. 4. A) Implantacja materiału Straumann Bone Ceramic u pacjenta po usunięciu torbieli korzeniowej (obszar
czerwony), struktura radiologiczna jest odmienna od referencyjnej kości (obszar zielony) do ostatniego badania E, B)
3 miesiące po implantacji materiału, C) 6 miesięcy po implantacji materiału, D) 9 miesięcy po implantacji, E) 12 miesięcy po implantacji
29
Three Bone Substitute Materials Based on Co-Occurrence Matrix
Straumann Bone Ceramic has the smallest particles among investigated series of materials and main part of its mass was rapidly
resorbed, but this phenomenon was balanced
by hydroxyapatite remnants from Straumann
Bone Ceramic®, which was much more stable
than residual mass of Cerasorb® and ChronOS®.
Finally, statistically, there is no significant difference in recovery of Cerasorb® and Straumann
Bone Ceramic® after 12 months from surgery.
Furthermore, the long-term observation of bone
substitute material after the implantation we
published previously [20].
Concluding, during 12 months after surgery
no total bone regeneration could be achieved in
case of all tricalcium phosphates. The creation of
a full-value bone may take much more time and
longer observation of patients.
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Address for correspondence:
Marcin Kozakiewicz
Cyberskiego 2 m. 14
92-447 Łódź
Poland
Tel./fax: +48 42 656 65 47
E-mail: [email protected]
Received: 1.02.2010
Revised: 15.03.2010
Accepted: 17.03.2010
Praca wpłynęła do Redakcji: 1.02.2010 r.
Po recenzji: 15.03.2010 r.
Zaakceptowano do druku: 17.03.2010 r.