Morphometry of the gallbladder during the fetal period
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: soneralbay@yahoo.com 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. 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