We are pleased to present to your attention a rare article on the histology of ligamentum capitis femoris (LCF). The authors focused on analyzing changes in the LCF of congenital hip dysplasia and assessing the proteinases involved in the breakdown of extracellular matrix proteins. We are sincerely grateful to our colleagues for the right to publish their work on another resource for its popularization.
Histological Structure and Immunohistochemical
Properties of the Ligamentum Teres in Patients With Developmental Dysplasia of
the Hip
Baran Sarıkaya, Mehmet
Ali Dolap, Ahmet Yiğit Kaptan, Celal Bozkurt, Nihat Yumuşak, Akin Yigin, Serkan
Sipahioğlu, Baki Volkan Çetin, Mehmet Akif Altay
Published: May 06, 2024
Abstract
Introduction
This study aims to evaluate the histology of the ligamentum
teres and its relationship with matrix metalloproteinases (MMPs) and a
disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS), which
are involved in the destruction of extracellular matrix proteins in patients
with developmental dysplasia of the hip (DDH).
Methodology
The patients who underwent open reduction and pelvic
osteotomy due to DDH were included in the study. Patient groups were formed
according to Tönnis stages, positive family history, consanguineous marriage,
age, and bilateral involvement. The histology and immunohistochemical
properties (MMP-2, MMP-9, and ADAMTS-7) of ligamentum teres tissue obtained
from the patients were evaluated according to these groups.
Results
Thirty-five patients (female 30, 85.7%; male 5, 14.3%) with
DDH between the ages of 14 and 99 months were included in the study.
Preoperative and postoperative Tönnis stages, positive family history,
consanguineous marriage, age, and bilaterality did not cause a significant
difference between histological parameters. A significant correlation was found
between MMP-2, MMP-9, and ADAMTS-7 and all histological parameters.
Conclusions
The histological structure of ligamentum teres in patients with DDH shows moderate inflammation, fibrosis, neovascularization, hyalinization, and fatty infiltration regardless of age and radiological stage. ADAMTS-7, MMP-2, and MMP-9 correlate positively with the histological parameters of the ligamentum teres in patients with DDH.
Introduction
The
ligamentum teres has been defined as a broad-based, triangular, and slightly
flattened ligament with an overlying layer of investing synovium, and it was
demonstrated that the part of the ligament between the femoral head and the
acetabular margin had the appearance and the consistency of cartilage [1-3].
However, in developmental dysplasia of the hip (DDH), due to the change in the
hip anatomy, the ligamentum teres becomes elongated and hypertrophied in
accordance with the capsule [1]. Therefore, it is considered one of
the potential obstacles to reduction in DDH.
There are
many studies in the literature regarding the anatomy and biomechanics of the
ligamentum teres [1-10]. With the demonstration of the effect of the
ligament teres on hip stabilization, some authors suggested preserving the
ligamentum teres during open reduction in patients with DDH [3,4,10].
However, the histological structure of the ligament was not investigated in these
studies, and there are a limited number of studies regarding the histology of
the ligamentum teres in patients with DDH [1].
Matrix
metalloproteinases (MMPs) and a disintegrin and metalloproteinase with
thrombospondin motifs (ADAMTS) enzymes are proteases that are involved in the
destruction of extracellular matrix (ECM) proteins [11,12]. ADAMTS-7 gene
from the ADAMTS family is expressed in muscle, bone, ligament, meniscus,
skeletal muscle, fat tissue, and cartilage tissues containing cartilage
oligometric matrix protein (COMP) [13]. COMP is one of the ECM
proteins and is a well-known substrate of active ADAMTS-7. Current studies emphasize the role of ADAMTS-7
in the regulation of collagen, which forms the ligament structure [13]. In
addition, MMP-2 (gelatinase A) and MMP-9 (gelatinase B), which are members of
the MMP family, have been reported to have crucial roles in collagen
degradation and tendon physiology [14].
This study aims to analyze the histological structure of the
ligamentum teres in patients with DDH and put forth its relationship with ECM
proteases, which have critical functions in protecting the ligament structure.
We also aimed to examine the relationship between the demographic and
radiological features of DDH with the histological and immunohistochemical
structure of the ligamentum teres.
Materials & Methods
This research was approved by the IRB of the authors’
affiliated institutions (HRU/20.02.25). The study was conducted at Harran
University Faculty of Medicine Hospital. Informed consent was obtained from
each patient’s parents. The patients who underwent open reduction and pelvic
osteotomy due to DDH between May and December 2020 were included in the study.
The ligamentum teres excised during surgery was evaluated histologically, and
Tönnis staging was used for the radiological classification of all patients both
before surgery and after cast termination. Patients with neuromuscular and
genetic disorders associated with teratological hip dislocation were excluded
from the study. A total of 35 patients (female 30, 85.7%; male 5, 14.3%) with
DDH aged between 14 and 99 months were included in the study. Demographics of
the patients are given in Table 1.
Table 1: Demographics of the patients.
Demographic variables |
Count, n |
% |
|
Gender |
Female |
30 |
85.7 |
Male |
5 |
14.3 |
|
Age
(month) |
<24 |
17 |
48.6 |
>24 |
18 |
51.4 |
|
Preop
Tönnis grade |
1-2 |
7 |
20.0 |
3-4 |
28 |
80.0 |
|
Post-op
Tönnis grade |
1.00 |
30 |
85.7 |
2.00 |
2 |
5.7 |
|
3.00 |
3 |
8.6 |
|
Bilateral |
Yes |
21 |
60.0 |
No |
14 |
40.0 |
|
Family
history |
Yes |
6 |
17.1 |
No |
29 |
82.9 |
|
Consanguineous
marriage |
Yes |
19 |
54.3 |
No |
16 |
45.7 |
Immunohistochemistry
For immunohistochemical studies, 4-µm-thick sections were
obtained from the paraffin-embedded tissue blocks on poly-L-lysine-coated glass
slides. They were stained with the streptavidin-biotin-peroxidase complex (ABC)
technique after routine deparaffinization and rehydration procedures (Zymed,
Histostain Plus Kit, CA). Antigen retrieval was performed in a microwave oven
with citrate buffer (pH 6.0; 700 W, 20 minutes). Endogenous peroxidase
activation in the tissues was blocked for 15 minutes with 0.3% hydrogen
peroxide in 0.01 M phosphate-buffered saline (PBS) in methanol at room
temperature. Before applying the primary antibody, the tissues were incubated
for 20 minutes with 5% normal goat serum for protein blocking. Then sections
were incubated with MMP-2 (1:100, Invitrogen, CA-4001), MMP-9 (1:50,
Invitrogen, PA5-13199), and ADAMTS-7 (1:100, Abcam, ab28557) primer antibodies
for one hour at room temperature. Sections were then reacted with a
biotinylated secondary antibody for 30 minutes after removing the unbound
primary antibody. Then, the sections were reacted with horseradish peroxidase
(HRP)-streptavidin for 30 minutes. The diaminobenzidine (DAB, Dako, Glostrup,
Denmark) for MMP-9 and AEC (3-Amino 9-Ethyl Carbasole, Dako) for ADAMTS-7 and
MMP-2 was used as the chromogen. Finally, the background of the tissue sections
was stained with hematoxylin. All staining steps were carried out at 37 °C and
in humidity cabinets. PBS solution was used as a wash-away solution during all
the staining steps. To assess the immunohistochemistry, 10 fields were randomly
chosen and the cytoplasmic staining intensity in the cells was globally scored:
negative, 0 (<1% positive); weak, 1 (1%-25% positive); intermediate, 2
(>25% to 75% positive); and strong, 3 (>75% positive).
Histopathological studies
To remove the fixed tissue samples from formalin, they were
washed in running water overnight. Afterward, it was subjected to routine
pathological tissue follow-up and passed through graded alcohol (50%, 75%, 96%,
and 100%) and xylol series and blocked in paraffin. Five-micrometer-thick
sections were separated from the prepared blocks and the first three sections,
and every tenth section was taken on slides with Leica RM 2125 RT. The
prepared preparations were passed through alcohol and xylol series and stained
with hematoxylin and eosin (H&E). All samples were examined under a
high-resolution light microscope (Olympus DP-73 camera, Olympus BX53-DIC
microscope, Tokyo, Japan). All the changes detected in tissue structures were
noted and graded according to the presence and severity of any particular
finding as 0, none; 1, mild (<25%); 2, moderate (25%-50%); and 3, severe
(>50%).
Statistical analyses
The normality of the distribution of continuous variables
was tested by the Shapiro-Wilk test. Kruskal-Wallis and Dunn multiple
comparison tests were used to compare non-normal numerical data among groups.
Spearman rank correlation coefficients were calculated for correlations between
non-normal numerical variables. Mean ± standard deviations (mean ± SD) and
median and interquartile ranges were given as descriptive statistics.
Statistical analysis was performed with IBM SPSS Statistics for Windows,
Version 24.0 (IBM Corp., Armonk, NY), and a P-value < 0.05 was accepted
as statistically significant.
Results
Four open reduction and 31 open reduction + pelvic
osteotomies were performed as surgical procedures. The mean age of the patients
was 27.71 ± 16.6 months, and the follow-up duration was 7.89 ± 3.8 months. Additional histological data are
given in Table 2.
Table 2:
Treatment results and histological data of the patients.
Variables |
Median (min-max) |
Preop
Tönnis grade |
3
(1-4) |
Postop
Tönnis grade |
1
(1-3) |
IMMP-2 |
2
(0-2) |
IMMP-9 |
2
(0-3) |
IADAMTS-7 |
2
(0-3) |
Inf |
2
(0-2) |
Fib |
2
(0-3) |
Neo |
2
(0-3) |
Sinf |
2
(0-3) |
Hyl |
2
(0-3) |
Shyp |
2
(1-3) |
Cclu |
2
(1-3) |
Fatinf |
2
(0-3) |
Significant at 0.05 level. Mann-Whitney U test.
Inf,
inflammation; Fib, fibroblast; Neo, neovascularization; Sinf, synovial
inflammation; Hyl, hyalinization; Shyp, synovial lining cell hyperplasia; Cclu,
condrocyte clustering; Fatinf, fat infiltration; IMMP-2,
immunohistochemical analysis of MMP-2; IMMP-9, immunohistochemical
analysis of MMP-9; IADAMTS-7, immunhistochemical analysis of ADAMTS-7
Preoperative
and postoperative Tönnis stages had no significant effects on histological
parameters (Table 3). The presence of DDH in the family history,
consanguineous marriage, and bilaterality did not cause a significant
difference between histological parameters (Table 4). In addition, when
the patients were divided into two groups younger than 24 months old and older,
no significant difference was found between the histological parameters between
the two groups (Table 4).
Table 3:
Comparison of histological data according to pre-op Tönnis staging and post-op
Tönnis staging.
Pre-op Tönnis 1-2 (n =
7), Median (25%-75%) |
Pre-op Tönnis 3-4 (n =
28), Median (25%-75%) |
P-value* |
Post-op Tönnis 1 (n =
30), Median (25%-75%) |
Post-op Tönnis 2 (n =
2), Median (25%-75%) |
Post-op Tönnis 3 (n =
3), Median (25%-75%) |
P-value** |
|
Inf |
1
(0-2) |
2
(1-2) |
0.146 |
2
(1-2) |
1
(0-2) |
1
(0-2) |
0.686 |
Fib |
1
(1-3) |
2
(1.5-2) |
0.643 |
2 (1-2) |
2
(2-2) |
2
(1-2) |
0.898 |
Neo |
2
(2-3) |
2
(1.5-2.5) |
0.672 |
2
(2-3) |
2
(2-2) |
2
(0-2) |
0.505 |
Sinf |
0
(0-2) |
2
(0-2) |
0.146 |
2
(0-2) |
1
(0-2) |
0
(0-2) |
0.521 |
Hyl |
2
(2-2) |
2
(1.5-2) |
0.920 |
2
(2-2) |
2
(2-2) |
2
(0-2) |
0.622 |
Shyp |
2
(2-3) |
2
(1.5-3) |
0.762 |
2
(2-3) |
2.5 (2-3) |
2
(1-3) |
0.674 |
Cclu |
2
(2-3) |
2
(1.5-3) |
0.856 |
2
(2-3) |
2.5
(2-3) |
2
(1-2) |
0.444 |
Fatinf |
2
(2-3) |
2
(1-2.5) |
0.558 |
2
(1-3) |
2
(2-2) |
2
(0-3) |
0.982 |
IMMP2 |
2
(0-2) |
2
(1-2) |
0.672 |
2
(1-2) |
2
(2-2) |
2
(0-2) |
0.561 |
IMMP9 |
2
(1-2) |
2
(2-3) |
0.340 |
2
(2-3) |
2.5
(2-3) |
2 (1-2) |
0.459 |
IADAMTS7 |
2
(1-3) |
2
(2-3) |
0.479 |
2
(2-3) |
2.5
(2-3) |
2
(1-2) |
0.425 |
*Significant
at 0.05 level. Mann-Whitney U test.
**Significant at 0.05 level. Kruskal-Wallis test.
Inf,
inflammation; Fib, fibroblast; Neo, neovascularization; Sinf, synovial
inflammation; Hyl, hyalinization; Shyp, synovial lining cell hyperplasia; Cclu,
condrocyte clustering; Fatinf, fat infiltration; IMMP-2,
immunohistochemical analysis of MMP-2; IMMP-9, immunohistochemical
analysis of MMP-9; IADAMTS-7, immunhistochemical analysis of ADAMTS-7
Table 4:
Comparison of histological data according to family history, consanguineous
marriage, age of patients, and bilateral hip involvement.
Histological variables |
Family history + (n = 6), median (25%-75%) |
Family history – (n = 29), median (25%-75%) |
P-value* |
Consanguineous marriage + (n = 19), median (25%-75%) |
Consanguineous marriage – (n = 16), median (25%-75%) |
P-value* |
Age < 24 months (n = 17), median (25%-75%) |
Age > 24 months (n = 18), median (25%-75%) |
P-value* |
Bilateral + (n = 21), median (25%-75%) |
Bilateral – (n = 14), median (25%-75%) |
P-value* |
Inf |
1.5
(0-2) |
2
(1-2) |
0.681 |
1
(0-2) |
2
(1-2) |
0.103 |
1
(0-2) |
2
(1-2) |
0.130 |
2
(1-2) |
1.5
(0-2) |
0.402 |
Fib |
1.5
(1-2) |
2
(1-2) |
0.492 |
2
(1-2) |
2
(1.5-2.5) |
0.298 |
2
(1-2) |
2
(2-2) |
0.158 |
2
(2-2) |
2
(1-2) |
0.130 |
Neo |
2
(1-3) |
2
(2-2) |
0.962 |
2
(1-2) |
2
(2-3) |
0.427 |
2
(1-2) |
2
(2-3) |
0.272 |
2
(2-3) |
2
(1-2) |
0.270 |
Sinf |
2
(1-2) |
2
(0-2) |
0.541 |
1
(0-2) |
2
(0.5-2) |
0.171 |
2
(0-2) |
2
(0-2) |
0.883 |
2
(0-2) |
2
(0-2) |
0.865 |
Hyl |
2
(1-2) |
2
(2-2) |
0.709 |
2
(1-2) |
2
(2-2.5) |
0.337 |
2
(1-2) |
2
(2-2) |
0.302 |
2
(2-2) |
2 (1-2) |
0.515 |
Shyp |
2
(1-3) |
2
(2-3) |
0.849 |
2
(1-3) |
2
(2-3) |
0.615 |
2
(1-3) |
2
(2-3) |
0.668 |
2
(2-3) |
2
(1-2) |
0.391 |
Cclu |
2
(1-2) |
2
(2-3) |
0.358 |
2
(1-2) |
2
(2-3) |
0.219 |
2
(1-2) |
2
(2-3) |
0.110 |
2
(2-3) |
2
(1-2) |
0.301 |
Fatinf |
2
(1-3) |
2
(2-2) |
0.944 |
2
(1-3) |
2
(2-2.5) |
0.383 |
2
(2-2) |
2
(1-3) |
0.958 |
2
(1-3) |
2
(2-2) |
0.677 |
IMMP2 |
1.5
(1-2) |
2
(1-2) |
0.819 |
1
(1-2) |
2
(2-2) |
0.067 |
2
(1-2) |
2
(1-2) |
0.514 |
2
(1-2) |
2
(1-2) |
0.969 |
IMMP9 |
2
(1-3) |
2
(2-3) |
0.814 |
2
(1-2) |
2
(2-3) |
0.122 |
2
(2-3) |
2
(2-3) |
0.845 |
2
(2-2) |
2
(2-3) |
0.437 |
IADAMTS7 |
2
(1-3) |
2
(2-3) |
0.606 |
2
(1-3) |
2.5
(2-3) |
0.271 |
2
(2-3) |
2
(2-3) |
0.646 |
2
(2-3) |
2
(2-3) |
0.928 |
*Significant at 0.05 level. Mann-Whitney U test.
Inf, inflammation; Fib, fibroblast; Neo, neovascularization;
Sinf, synovial inflammation; Hyl, hyalinization; Shyp, synovial lining cell
hyperplasia; Cclu, condrocyte clustering; Fatinf, fat
infiltration; IMMP-2, immunohistochemical analysis of MMP-2; IMMP-9,
immunohistochemical analysis of MMP-9; IADAMTS-7, immunhistochemical
analysis of ADAMTS-7
The correlation between the immunohistochemical analysis of
MMP-2 (IMMP-2), immunohistochemical analysis of MMP-9 (IMMP-9),
immunohistochemical analysis of ADAMTS-7 (IADAMTS-7), and histological data was
evaluated. A significant correlation was found between IMMP-2, IMMP-9, and
IADAMTS-7 and all histological parameters. A moderate correlation was found for the R-value between 0.4 and 0.6, a
strong correlation for 0.6 and 0.8, and a very strong correlation for a value
of 0.8 and above (Table 5).
Table 5:
Comparison of histological data according to IMMP-2, IMMP-9, and IADAMTS-7.
Histological variables |
IMMP-2 |
IMMP-9 |
IADAMTS-7 |
|
Inf |
r |
0.515* |
0.592* |
0.580* |
P |
0.002 |
0.001 |
0.001 |
|
Fib |
r |
0.757* |
0.720* |
0.775* |
P |
0.001 |
0.001 |
0.001 |
|
Neo |
r |
0.730* |
0.772* |
0.813* |
P |
0.001 |
0.001 |
0.001 |
|
Sinf |
r |
0.465* |
0.709* |
0.682* |
P |
0.005 |
0.001 |
0.001 |
|
Hyl |
r |
0.720* |
0.757* |
0.755* |
P |
0.001 |
0.001 |
0.001 |
|
Shyp |
r |
0.736* |
0.803* |
0.776* |
P |
0.001 |
0.001 |
0.001 |
|
Cclu |
r |
0.745* |
0.717* |
0.741* |
P |
0.001 |
0.001 |
0.001 |
|
Fatinf |
r |
0.625* |
0.661* |
0.591* |
P |
0.001 |
0.001 |
0.001 |
*Significant
at 0.01 level.
r, Spearman rank correlation coefficient; Inf, inflammation; Fib, fibroblast; Neo, neovascularization; Sinf, synovial inflammation; Hyl, hyalinization; Shyp, synovial lining cell hyperplasia; Cclu, condrocyte clustering; Fatinf, fat infiltration; IMMP-2, immunohistochemical analysis of MMP-2; IMMP-9, immunohistochemical analysis of MMP-9; IADAMTS-7, immunhistochemical analysis of ADAMTS-7
Histological results
Histomorphological examination of the tissues revealed
varying severity of damage. Inflammation
(Figures 1a-1b) and clustering of chondrocytic cells (Figure 1c) were
observed focally in some areas. It was also observed that fibrosis
was formed around the inflammation and hyalinization. Fat infiltrates spreading as focal areas in the
ligamentum teres and synovial membrane (Figure 1d) were noted, along with
an increase in neovascular structures (Figure 1a). Similar damage and
inflammation also occurred in the synovial membrane, and cellular hyperplasia
was also noted (Figures 1e-1f).
Immunohistochemical
results
It was
determined that there were positive reactions with varying intensities in the
studies performed in terms of MMP-2, MMP-9, and ADAMTS-7 antibodies
immunohistochemically (Figure 2). In examinations conducted for
MMP-2, intense positive reactions were observed in both chondrocytes and the
synovial membrane. However, the presence of negative cells was noted in some
areas. On the other hand, the results of the study conducted with MMP-9 and
ADAMTS-7 antibodies revealed a widespread positive reaction in both the
ligamentum teres and the synovia.
Discussion
This study shows that the histological structure of the
ligamentum teres and IMMP-2, IMMP-9, and IADAMTS-7 in patients with DDH is not affected
by age, stage of dysplasia, family history, bilateral dysplasia, and
consanguineous marriage. IMMP-2, IMMP-9, and IADAMTS-7 showed a positive
correlation with ligamentum teres histological features.
It was
shown that degenerative and inflammatory processes in tissues increase as a
result of ECM degradation when ADAMTS-7, MMP-2, and MMP-9 were
overexpressed [13,15]. The increase of these proteases in an injured
tendon can be an indicator of tissue remodeling, repair, and healing [12-17].
As it is seen, these metalloproteinases can be involved in the
pathogenesis of degenerative and inflammatory diseases, as well as in the
repair and remodeling processes of healing tissues. ADAMTS-7 gene, together with MMP-2 and MMP-9
enzymes, play an important role in ECM regulation in tendon physiology [12-14].
Karousou et al. [14] compared
MMP activity in ruptured and healthy parts of the Achilles tendon and showed
that MMP-2 and MMP-9 activity was increased in the ruptured tendon region. Mead
et al. [17] showed
the effect of ADAMTS-7 on tendon organization in their study on mice. Accordingly,
in our study, we found that deterioration in histological parameters correlated
positively with IMMP-2, IMMP-9, and IADAMTS-7. This result shows that the
ADAMTS-7 gene has an effect on ligament healing together with MMP-2 and MMP-9
enzymes per the literature.
In DDH disease, the histological structure of the ligamentum
teres differentiates as it elongates and becomes hypertrophied. Ipplito et
al. [1] studied the
histological structure of the ligamentum teres in patients with DDH and
reported that ligamentum teres had fibrocartilaginous metaplasia close to
the femoral insertion. In addition, they added that the arteriolar walls
were thicker in patients with DDH and that the thickness increased with age.
Similar to Ippliton et al.'s findings, we also found moderate fibrosis,
hyalinization, and chondrocyte clustering in the ligamentum teres of patients
with DDH. Differently, we found moderate neovascularization and fatty
infiltration in this study. In addition, there were nine patients in the study
of Ipplito et al., while there were 35 patients in our study. According to the
results of the present study, pediatric orthopedics who prefer tenodesis by
shortening and suturing this ligament during DDH open reduction surgery should
also take into consideration the altered structure of the ligament.
Some recent studies suggested shortening and reattaching the
ligamentum teres into the acetabulum instead of excision in DDH surgery. Wenger et al. showed the
biomechanical effect of the ligamentum teres with an in vitro porcine
model [3] and later reported early positive results with the
ligamentum teres reattachment technique in patients with DDH [10]. Bache
et al. [4] also
described the ligamentum teres tenodesis technique with medial open reduction
and reported good results in patients up to two years of age in their study. Contrary
to these studies, Ertürk et al. [18] reported that there are unmyelinated free nerve endings in the
ligamentum teres structure, and since these receptors play a role in pain
sensation, ligamentum teres excision does not cause a significant loss of
sensory function. Although the methods and necessity of ligamentum teres
tenodesis are not the subjects of this study, the present study reveals that
the age and radiological stage of DDH do not have a significant effect on
ligamentum teres structure.
The findings of this study have to be seen in light of some
limitations. First, there was a limited number of patients included in the
study. Second, histological comparison could not be made with healthy
ligamentum teres tissue because only patients with DDH were included in the
study. In addition, genetic analysis of ADAMTS-7, MMP-2, and MMP-9 was not
evaluated.
Conclusions
The histopathological studies on the ligamentum teres are
quite insufficient in the literature. The limited number of studies includes
mostly adults in the adult age group. We could not find a recent study
examining the histological or histopathological features of the ligamentum
teres in children with DDH. Therefore, the findings we obtained in this study
may contribute to future histopathological studies.
In conclusion, the histological structure of the ligamentum teres in patients with DDH shows moderate inflammation, fibrosis, neovascularization, hyalinization, and fatty infiltration regardless of age and radiological stage. ADAMTS-7, MMP-2, and MMP-9 correlate positively with the histological parameters of the ligamentum teres in patients with DDH.
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Original Article
Authors & Affiliations
Baran Sarıkaya
Department of Orthopaedics and Traumatology,
University of Health Sciences, Ankara Bilkent City Hospital, Ankara, TUR
Mehmet Ali Dolap (Corresponding Author, mali_dolap@hotmail.com)
Department of
Orthopaedics and Traumatology, Faculty of Medicine, Harran University,
Sanliurfa, TUR
Ahmet Yiğit Kaptan
Department of Orthopaedics and Traumatology, Faculty
of Medicine, Harran University, Sanliurfa, TUR
Celal Bozkurt
Department of
Orthopaedics and Traumatology, Gaziosmanpaşa Taksim Training and Research
Hospital, University of Health Sciences, Istanbul, TUR
Nihat Yumuşak
Department of
Pathology, Faculty of Veterinary, Harran University, Sanliurfa, TUR
Akin Yigin
Department of
Genetics, Faculty of Veterinary, Harran University, Sanliurfa, TUR
Serkan Sipahioğlu
Department of
Orthopaedics and Traumatology, Faculty of Medicine, Ordu University, Ordu, TUR
Baki Volkan Çetin
Department of
Orthopaedics and Traumatology, Faculty of Medicine, Harran University,
Sanliurfa, TUR
Mehmet Akif Altay
Department of
Orthopaedics and Traumatology, Faculty of Medicine, Harran University, Sanliurfa,
TUR
Copyright
©Copyright 2024; Sarıkaya
et al. This is an open access article distributed under the terms of the
Creative Commons Attribution License CC-BY 4.0., which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author
and source are credited.
Keywords
ligamentum capitis femoris, ligamentum teres, ligament
of head of femur, hip dysplasia, pathological anatomy,
histology
NB! Fair practice / use: copied for the purposes of criticism, review, comment, research and private study in accordance with Copyright Laws of the US: 17 U.S.C. §107; Copyright Law of the EU: Dir. 2001/29/EC, art.5/3a,d; Copyright Law of the RU: ГК РФ ст.1274/1.1-2,7
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