Morphometry of the gallbladder during the fetal period

Yorumlar

Transkript

Morphometry of the gallbladder during the fetal period
Surg Radiol Anat
DOI 10.1007/s00276-009-0574-z
ORIGINAL ARTICLE
Morphometry of the gallbladder during the fetal period
Soner Albay • Mehmet Ali Malas • Esra Koyuncu
Emine Hilal Evcil
•
Received: 13 May 2009 / Accepted: 30 September 2009
Ó Springer-Verlag 2009
Abstract
Purpose In this study, our objective was to investigate the
development of the gallbladder, its morphological structure
and relationship with the adjacent organs during the fetal
period.
Materials and methods A total of 118 human fetuses (60
males, 58 females) between 9 and 40 weeks of gestation
without any external anomaly or pathology were included.
They were divided into four groups according the gestational age: I (9–12 weeks), II (13–25 weeks), III (26–
37 weeks) and IV (term, 38–40 weeks). The location of
gallbladder on the visceral surface of liver has been identified. The gallbladders have been classified into four different types. Width and length of the gallbladder were
measured and the relationship between fundus of gallbladder and inferior margin of the liver was noted.
Findings The gallbladder was located on the visceral surface of liver in all cases during the fetal period. There were no
differences between males and females by means of length
and width. There was a statistically significant relationship
between the size of gallbladder and the gestational age
(P \ 0.001). There was also a significant difference in the
distribution of gallbladder types among the groups during the
fetal period. The fundus of gallbladder was under the transverse plane passing from the part of inferior margin of the
liver near the gallbladder in 14% of the cases.
Presented in the 8th National Congress of Anatomy, 26–30 August
2004, Konya, Turkey.
S. Albay (&) M. A. Malas E. Koyuncu E. H. Evcil
Department of Anatomy, Faculty of Medicine,
Suleyman Demirel University, 32260 Isparta, Turkey
e-mail: [email protected]
Results We concluded that there could be different types of
gallbladders during the fetal period. We believe that the data
collected in our study may contribute to the evaluation of the
gallbladder development during the intrauterine period.
Keywords
Gallbladder Fetal period Development
Introduction
Liver, gallbladder and biliary ducts begin to differentiate
from the ventral side of the caudal part of foregut at the
beginning of the fourth week. Production of bile begins by
week 12 [18]. Having the knowledge of development of
gallbladder is considerably important; because abnormal
types of gallbladder may be associated with congenital
malformations or anomalies [6]. Anomalies and congenital
pathologies of gallbladder which can be diagnosed in
fetuses include floating, left sided, septated or bilobed
gallbladder, as well as agenesis of gallbladder [6]. It has
been reported that a detailed description of morphometric
structures related to localization and type of gallbladder
may be useful in diagnostic procedures such as ultrasonographic examination, and treatment [8]. Besides, having the
knowledge of normal development of gallbladder is
important in describing the conditions such as agenesis of
extrahepatic biliary ducts, variations of gallbladder and its
ducts [12].
In the previous studies, parameters related to normal
size of gallbladder have been measured such as width,
length, area, circumference, diameter, etc., and significant
correlation was found between these parameters and general parameters of fetuses [9, 12–14]. Fetal gallbladder can
be monitored in second and third trimesters by obstetric
ultrasonography (USG) [4, 9, 12, 14].
123
Surg Radiol Anat
Congenital absence of gallbladder [1, 21] and its relationship with some other congenital anomalies, and content
of gallbladder (sludge, stone, etc.) are important to examine in neonates [7, 16]. In the previous studies, the morphological data of gallbladder have been obtained via
obstetric USG, usually in fetuses within weeks 13–40.
Studies on formalin-fixed fetuses using anatomical dissection are rare [13].
The knowledge of pathologies and anomalies of gallbladder is of importance in diagnosis and treatment.
Detailed knowledge of gallbladder development is necessary in USG examination [12, 14]. Morphometric data of
fetal gallbladder are either limited or belong to some specific weeks of fetal period [4, 9, 12, 14]. The reported
reason of this is the difficulty to clearly visualize and
monitor the gallbladder. Anatomical dissection method
provides more clear and reliable findings compared to
radiological methods. In this study, our objective was to
investigate the development of gallbladder and its relationship between surrounding structures in a large spectrum
of fetal collection from 9 to 40 weeks.
Materials and methods
This study was carried out on 118 spontaneous aborted
human fetuses (60 males, 58 females) between 9 and
40 weeks of gestation. Fetuses without any external
pathology or anomaly were obtained from Isparta Maternity and Children’s Hospital between 1996 and 2003.
Written consent from the families and an approval from the
Ethics Board of Faculty of Medicine, Süleyman Demirel
University were obtained prior to the commencement of
the study. Gestational ages of the fetuses were determined
using crown-rump length (CRL) until 12th week, and
biparietal diameter, head circumference, femur length and
foot length between 13 and 40 weeks [8, 18]. Fetuses were
assigned to four groups according to the gestational age as
Group I (first trimester), Group III (second trimester),
Group III (third trimester) and Group IV (Term) comprised
of fetuses aged between 0–12, 13–25, 26–37 and 38–
40 weeks, respectively. A caliper, measuring tape, plastic
ruler or compasses were used for the measurements.
Macroscopic dissection was performed on 10% formaldehyde-fixed fetuses at the Department of Anatomy in
Faculty of Medicine, Suleyman Demirel University.
Abdomen was dissected and the liver and the structures
supporting the liver were exposed. The gallbladder was
located on the visceral surface of liver. Then, the liver was
dissected and removed from the abdomen with the gallbladder. In order to determine the relationship between the
liver and gallbladder, it is noted whether the fundus of
gallbladder was projecting from the inferior margin of the
123
liver. Additionally, the degree of protrusion of the gallbladder on the visceral surface of liver was identified.
After the localization of gallbladder was determined,
four different types were identified according the shape.
Type
Type
Type
Type
1:
2:
3:
4:
pear shaped with a long neck,
rectangular shaped,
fusiform shaped,
circular shaped with a short neck
Then, the width (distance between lateral margins at the
widest part of the body of gallbladder) and the length
(distance between inferior end of fundus of gallbladder and
the beginning of cystic duct) were measured.
SPSS 9.05 for windows statistics software (SPSS Inc,
Chicago, IL, USA) was used to calculate the mean values
of all parameters with respect to gestational age and
groups. A P value of less than 0.05 was taken as significant.
Measurements related to the weeks were expressed as
mean; related to groups were expressed as mean ± standard deviation. Non-parametric tests were used to compare
groups due to small sample size. Chi-square test was used
for comparisons of percent distributions among groups.
Analysis of variance was tested using Kruskall Wallis test
and two-by-two comparisons among significant groups
were performed with Mann–Whitney U test. Degrees of
significance were evaluated with Bonferroni correction.
Relationship between variables was tested using Pearson’s
correlation test.
Findings
Liver, abdominal organs and the structures holding down
the liver were dissected in all cases. The gallbladder was
located on visceral surface of liver, and the liver was
removed together with the gallbladder. Gallbladder was in
left hypochondrium in all cases. Then, the localization of
the gallbladder on the visceral surface and the relationship
between liver and gallbladder was evaluated. Macroscopically, neither gallbladders nor other abdominal organs
showed any anomalies.
Fetal gallbladder was observed to be embedded on the
visceral surface of liver (intrahepatic) in 25 of 118 cases
(age range 11–35 weeks). In the rest of the cases (96
cases), gallbladder had a sub-hepatic localization.
When the localization of fundus of the gallbladder was
evaluated according to inferior margin of the liver, it was
found that gallbladder was projecting from the inferior
border in 12% of cases (Table 1). Fundus of the gallbladder did not pass the inferior margin of the liver in all
first trimester cases. The incidence of the cases in which
fundus passed the inferior margin of the liver were 8% in
first trimester, 19% in second trimester and 20% in full
term.
Surg Radiol Anat
Table 1 Relationship between fundus of the gallbladder and inferior
margin of the liver according to trimesters (n, %)
Group (weeks)
Below
First trimester (9–12)
Above
0 (0)
Total
6 (100)
6
Second trimester (13–25)
5 (8)
61 (92)
Third trimester (26–37)
7 (19)
29 (81)
36
Full term (38–40)
2 (20)
8 (80)
10
14 (12)
104 (88)
118
Total (9–40)
66
Percentages are based on the sum of the lines
P \ 0.001, difference between groups (Chi-square: 26.303)
Table 2 Types of the gallbladder according to the trimesters (n, %)
Group (week)
First trimester (9–12)
Second trimester
(13–25)
Type I Type II Type III Type IV Total
4 (66)
1 (17)
6
19 (29) 10 (15) 29 (44)
1 (17)
0 (0)
8 (12)
66
Third trimester (26–37)
6 (17) 20 (55)
5 (14)
5 (14)
36
Full-term (38–40)
2 (20)
1 (10)
3 (30)
10
29 (24) 34 (29) 39 (33)
17 (14)
118
Total (9–40)
4 (40)
Percentages are based on the sum of the lines
P \ 0.001, difference between groups (Chi-square: 144.46)
Four different types of gallbladders were determined
(Table 2). In the first trimester type 3 was 66%, type 1 and
4 were 17%; type 2 was not observed during this gestational period. Type 3 (44%) was the most commonly
observed type together with the other three types in second
trimester (type 1 29%, type 2 15%, type 4 12%). All four
types were also observed in the third trimester (type 1 17%,
type 3 14%, type 4 14%) and full term (type 1 20%, type 3
10%, type 4 30%). Type 2 was the most common type
during these periods (55% in third trimester and 40% in
term) (Table 2).
The width and length of gallbladder were also measured.
Average values and standard deviations of fetal general
parameters and size parameters of gallbladder were demonstrated in Tables 3 and 4. There was a significant correlation between gestational age and these parameters
(P \ 0.001, r = 0.94 for the width, r = 0.95 for the
length).
Discussion
Obstetric USG was used in most of the previous studies on
fetal anatomy [13]. Although different results are obtained
for each organ, it has been reported that USG may not
provide reliable results [11]. In the literature, USG is the
leading method in studies on fetal gallbladder anatomy;
however, there is a limited number of studies in which
formalin-fixed fetuses were used [13].
Hertzberg et al. [14] examined the visualization of fetal
gallbladder in second and third trimester pregnancies. They
failed to monitor the fetal gallbladder in approximately
14% of normal pregnancies and also observed some minor
anomalies which were independent from biliary system in
the same cases. Blazer et al. [4] examined approximately
30,000 cases within gestational weeks 14–16; they reported
that they could not observe the gallbladder in 1/875 of
cases. If it is considered that the mean incidence of gallbladder agenesis is 0.016% [3], in case of gallbladder
visualization failure by USG, other anomalies that are not
related to biliary system should be kept in mind more than
gallbladder agenesis. Several malformations including
clubfoot, micropenis, facial dysmorphism and cardiac
anomalies [19]; and also abnormal karyotypes [4], cystic
fibrosis [5], trisomy 21 [14], trisomy X, tyroid aplasia and
various syndromes [19] may be associated with the failure
of gallbladder visualization.
In adults, the gallbladder is localized on the fossa for
gallbladder at the visceral surface of liver, in right
hypochondrium [2]. Haffajee [13] assessed the relationship between gallbladder and visceral surface of liver
during the fetal period; he stated that the gallbladder was
not on its own place from week 10 to late week 17, thus
it could not be monitorized on the visceral surface of
liver during this period. It is reported that fetal gallbladder was localized in an intrahepatic position as
covered by transverse and oblique fissures. Fissures on
visceral surface would be landmarks for determining the
localization of gallbladder in case of not visualising it. It
is also stated that the gallbladder could be partially
covered; as that the fundus and cystic canal might be
observed on visceral surface. Besides, fossa for gallbladder appears more prominent by the rising of the
hepatic tissue surrounding the gallbladder in two sides
after week 18. Finally, fetal gallbladder sits to the fossa
for gallbladder on the hepatic processes, and gets a
subhepatic location by late week 21.
In our study, an intrahepatic gallbladder was observed in
25 of 118 cases (between weeks 11 and 35) according to
Hafajee’s definition [13]. Twenty-one (18%) of these
intrahepatic cases were younger than week 22; there were 4
(3%) intrahepatic cases after the week 22.
Haffajee [13] reported that the fundus of gallbladder was
observed to be protrudes from the inferior margin of the
liver in only two cases (week 29). The reported cause of
this was the same amount of increase in the anteroposterior
distance of liver as the length of fetal gallbladder. In our
study, fundus was not protruding from the inferior margin
of the liver in 88% of the cases. However, fundus of the
gallbladder was passing the inferior margin of the liver by
123
Surg Radiol Anat
Table 3 Mean values of fetal
general parameters and
gallbladder parameters (mm)
Age (weeks)
N
General parameters
Head
circumference
Gallbladder parameters
Biparietal
diameter
Femur
length
Foot
length
Width
Length
9
1
63
16
14
9
1.0
4.5
10
2
66
18
19
11
1.0
5.0
11
3
76
23
21
14
1.3
6.0
12
3
78
22
13
16
1.3
7.0
13
4
90
22
16
16
1.5
6.8
14
12
99
26
17
22
2.3
8.0
15
16
3
3
112
124
30
34
20
23
22
24
3.0
3.0
9.2
10.0
17
6
138
37
26
28
3.2
10.7
18
5
150
40
30
30
3.6
12.2
19
4
162
43
33
35
3.5
13.0
20
5
172
48
35
40
4.0
13.4
21
3
187
50
38
42
5.0
15.0
22
8
199
53
41
43
5.3
16.0
23
5
208
57
43
44
5.2
17.0
24
3
219
60
48
52
6.0
18.7
25
2
233
63
50
52
7.0
20.5
26
3
244
65
52
54
6.0
22.3
27
3
254
67
54
56
7.3
21.3
28
4
264
71
58
60
7.8
22.5
29
3
273
73
60
66
8.7
23.3
30
31
2
5
282
288
76
78
62
65
70
71
8.5
8.4
24.5
23.8
32
4
296
80
67
74
9.0
24.8
33
2
303
82
69
75
8.0
25.5
34
2
310
84
70
77
8.5
26.0
35
3
317
87
72
78
8.3
23.7
36
3
324
89
75
79
8.7
25.3
37
2
334
91
76
80
9.0
26.0
38
2
341
92
78
80
10.0
26.0
39
2
347
95
80
81
9.5
27.5
40
6
352
97
82
82
9.5
26.3
Table 4 Mean values and standard deviations of fetal general parameters and gallbladder parameters according to the trimesters (mm)
Group (weeks)
General parameters
Head circumference
First trimester (9–12)
Second trimester (13-25)
Gallbladder parameters
Biparietal diameter
Femur length
Foot length
Width
Length
92 ± 9
25 ± 2
26 ± 30
13 ± 3
1.1 ± 0.4
6.3 ± 1.4
168 ± 46
48 ± 29
44 ± 14
32 ± 13
3.7 ± 2.2
12.8 ± 5.3
Third trimester (26–37)
299 ± 31
78 ± 10
80 ± 13
67 ± 10
8.0 ± 2.2
23.4 ± 5.8
Full-term (38–40)
359 ± 18
92 ± 5
94 ± 8
77 ± 4
9.5 ± 1.8
27.4 ± 6.6
Total (9–40)
222 ± 94
60 ± 29
54 ± 27
42 ± 23
5.3 ± 3.2
16.9 ± 8.2
second trimester in 12% of the cases (Table 1). Besides,
50% of these cases in which the fundus was protruding
from the inferior margin of the liver were in third trimester,
123
but 59% of the cases in which the fundus did not pass the
inferior margin of the liver were in the second trimester
(Table 1).
Surg Radiol Anat
investigated the length parameters of gallbladder in human
fetuses aged between 10 and 36 weeks by microdissection
and stated a linear increase. Mean length was 2.21 mm in
week 10 and 28.2 mm in week 32. In our study, there was
also a correlation between gestational age and size of the
gallbladder; a linear increase in gallbladder size was
accompanying the gestational age (Fig. 1). When it is
discussed with Fig. 1, a more prominent increase was
observed in the length of gallbladder than its width.
The results of Haffejee [13] about the length and width
of gallbladder are in consistent with our results; however,
some differences are present in lower age group (Table 5).
As known, gallbladder is a contractile organ [15]. Thus,
such differences in size may be observed between live and
postmortem studies. Our findings about the size of gallbladder are also comparable with the study of Hertzberg
et al. [14].
In other studies that evaluated the size of gallbladder,
there was not a sufficient number of cases in general nor in
gestational weeks. Our results are demonstrated in Table 5
together with the other postmortem [13] and ultrasonographic [17, 20] fetal studies. The similarities in the measurements can be seen in the table. However, the other
studies do not provide information covering all the fetal
period. As Hertzberg et al. [14] reported, the visualization
of the gallbladder between 24 and 32 weeks of gestation is
95%; however, it is less at the 16th week and ahead [17].
We argue that the difficulty in the visualization of gallbladder during the second trimester may account for the
difference between the visualization rates during these
periods. Moreover, it should be kept in mind that we
studied on formaldehyde-fixed fetuses, and this chemical
may have some effects on the organs. To our opinion,
having at least one case for every week and the high
number of cases in total are our advantages to get more
reliable results.
The knowledge of pathologies and anomalies of gallbladder is important in diagnosis and treatment. For this
reason, the normal anatomy of the fetal gallbladder should
be well known and understood. Anatomical dissection
method may provide more precise and reliable results than
Gallbladder width and length during the fetal period
40
width
length
30
mm
In a literature search, we found some studies and cases
about anomalies and variations of gallbladder. Anomalies
of gallbladder, such as ectopic gallbladder (transverse,
intrahepatic, left sided and retroperitoneal or retrohepatic
localization of gallbladder as a result of hypoplasia of right
lob of liver), duplication or triplication of gallbladder,
multiseptated gallbladder and gallbladder agenesis were
accompanied other congenital anomalies [2, 10]. Furthermore, fundus of the gallbladder might be elongated or
curved to back [2]. These data have been obtained from
children and adults, and they are not based on fetal
gallbladder.
Moreover, Hafajee [13] mentioned about the types of
fetal gallbladder in his study. He stated that fetal gallbladder was observed as a branch of hepatic duct (ductal
type) in week 10 and an elongated teardrop (tubular type)
in week 11. After week 11, two different parts (infundibulum and fundus) of gallbladder were distinguishable but it
did not have its normal shape as in adults (slender type). In
the same study, fundus, body and infundibulum of the
gallbladder were not distinguished in the first trimester but
each three parts could be distinguished after week 12 (pear
type).
In this study, we also determined and classified the
gallbladders and divided into four types according to the
shape of fundus and neck (Table 2): (Type 1 pear shaped
with a long neck, Type 2: rectangular shaped, Type 3:
fusiform, Type 4: circular with a short neck).
Type 2 was not observed in the first trimester. But all
four types of gallbladder were present in other trimesters.
Type 3 was the most common type in the first trimester and
had a declination towards full term. Type 2 have been
observed by second trimester and had a decreasing frequency from second trimester to full term (Table 2). In the
light of these data it can be stated that the type of the
gallbladder changes from fusiform to rectangular by gestational age. Additionally, type 4 of which has an
increasing incidence by the first trimester, was the second
common type in full term. Since the fetuses in our study
have been fixed with %10 formaldehyde, the shrinkage
effect of formaldehyde on tissues should be taken into
account.
In our study, the width and length of gallbladder were
also measured, and their relationships with fetal age and
other general parameters were determined. Goldstein et al.
[12] evaluated the size of gallbladder in 183 normal
pregnancies between 13 and 40 weeks of gestational age
by USG; and found a significant correlation between size
parameters and gestational age (P \ 0.001). The size of
gallbladder was compared to the parameters commonly
used in estimation of gestational age (femur length,
abdominal circumference and biparietal diameter), and a
significant correlation was also found. Haffajee [13]
20
10
0
0
10
20
30
40
Gestational age (week)
Fig. 1 The course of the width and length of the gallbladder during
the fetal period
123
Surg Radiol Anat
Table 5 Mean values of size parameters of gallbladder according to the fetal age (mm), and comparisons with the similar studies in literature
Age (weeks)
Width of gallbladder
Hafajee
[13]a
Saracoglu
[20]b
Length of gallbladder
Moon et al.
[17]b,c
9
Our
studya
Hafajee
[13]a
Saracoglu
[20]b
Moon et al.
[17]b,c
1.0
Our
studya
4.5
10
0.4
1.0
2.21
5.0
11
12
1
1.9
1.3
1.3
3.7
6.1
6.0
7.0
13
2.4
1.5
6.8
14
3.8
15
4.2
4
16
4.7
4
17
7.2
4
18
5.5
19
6.1
20
10
0.9
2.3
7
3.0
11
7
3.2
14
9
4
3.6
14
9
12.2
5
3.5
17
12
13.0
12
16
5
5.3
17
16
16.0
6
5.2
17
17.0
6
6
6
6
32
9.4
9.4
33
34
6
8
31
4.2
4.9
5.0
5.6
6.0
19
19
20
7.8
21
8.7
8.5
8.4
6.3
17
7.0
8
8
25
6.0
7.3
8
7
9.0
8.5
35
8
36
8
37
6
38
20
23
26
28
8.0
7
18.1
18.8
23.1
15.0
18.7
20.5
22.3
21.3
22.5
23.3
23
24.5
25
23.8
25
23
26.5
24.8
25.5
26.0
8.3
25
23.7
8.7
25
9.0
26
6
10.0
26
26.0
39
6
9.5
26
27.5
40
6
9.5
26
26.3
6.1
27.5
13.4
15.0
23
a
7.8
10.7
21
25
30
10.0
19
26
27
8.8
11.5
4.0
6.2
29
9.2
5.0
22
28
3.6
5
5
9.2
8.0
12
6.8
24
9.6
6.8
3.0
21
23
3.7
25.3
26.5
26.0
Study on formaldehyde-fixed fetuses
b
Ultrasonographic study
c
The data were given as mean values at specific weeks
radiological methods. In our study, morphometrical
parameters about fetal gallbladder were based on a wider
series, different from previous studies. Our findings—
especially those belonging to the first trimester that are
missing in the literature—may be considered as a pioneer
study for evaluating the gallbladder by USG during the
intrauterine period.
The failure in the visualization of gallbladder, its unusual shape or size should not be considered only as an
anatomical variation, but as a part of disorders that a
spectrum of clinical manifestations may accompany. In
123
conclusion, we think that our findings should contribute to
future studies, diagnosis and treatments in obstetrics, perinatology, forensic medicine and pathology to determine
anomalies, pathologies and variations of the gallbladder.
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