MRI analysis of gallbladder changes with gestational weeks between fetuses with type I congenital choledochal cyst and healthy fetuses

doi:10.21203/rs.3.rs-2588593/v1

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MRI analysis of gallbladder changes with gestational weeks between fetuses with type I congenital choledochal cyst and healthy fetuses

https://doi.org/10.21203/rs.3.rs-2588593/v1

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Purpose

To retrospectively analyze the prenatal MRI image characteristics of fetuses with type I congenital choledochal cyst and healthy fetuses, and to clarify the changes of gallbladder with gestational weeks.

Methods

We retrospectively reviewed prenatal MRI features of healthy fetuses and fetuses with type I choledochal cysts confirmed by operation after birth from January 2018 to March 2022. Clinical data and image findings (the maximum transverse and longitudinal diameters of gallbladder, liver and spleen, the diameters of choledochal cysts at transverse, coronal and sagittal planes and the maximum diameters of portal vein) were recorded. The features in two groups were then analyzed.

Results

A total of 139 fetuses were included, 100 in the healthy fetuses and 39 in the type I choledochal cysts. We found a nonlinear relationship between gestational weeks and gallbladder size with two inflection points of 27 and 34 in fetuses with type I choledochal cyst, after adjusting for potential confounders. In normal fetuses, however, the relationship is linear.

Conclusions

The relationship between gestational weeks and gallbladder size is non-linear in fetuses with type I choledochal cyst, with gallbladder size shrinking and spleen enlargement compared to healthy fetuses.

Fetuses

Gallbladder

Gestational weeks

Magnetic resonance imaging

Type I congenital choledochal cyst

Early detection and diagnosis of fetal choledochal cyst is of great significance for postnatal treatment. Due to the presence of cysts, gallbladder size will atrophy to a certain extent compared with normal fetuses.

What is New

The size of the gallbladder in fetuses with type I choledochal cyst is non-linear in relation to gestational weeks.
The relationship between gallbladder size and gestational weeks in healthy fetuses is linear.
The gallbladder volume of the fetus with type I choledochal cyst is smaller than that of the normal fetus at the same gestational week.

Choledochal cysts are congenital disease with dilatation of the biliary tree [1]. The incidence of choledochal cysts is higher in the Asian population than in European that more commonly found among females [2; 3]. Although the pathogenesis of choledochal cysts remains speculative, it has been suggested that pancreaticobiliary maljunction, bile duct dysplasia, and lack of ganglion cells in the distal common bile duct wall may lead to bile duct dilatation [4]. Todani et al. [5] modified the original Alonso-Lej [6] anatomic classifications into five forms, of which type I accounts for up to 50–80% of cases of choledochal cyst [7]. Type I choledochal cysts are fusiform or spherical dilatations of the extrahepatic biliary tree [8].

Diagnosis of choledochal cysts occurs during the first decade of life [9; 10], with most being diagnosed in childhood [2]. Early diagnosis and treatment of choledochal cysts can help avoid possible complications such as chronic inflammation and worsening lesions in the long term [8]. Therefore, prenatal diagnosis of fetal choledochal cyst has important significance for clinical intervention decision and follow-up treatment. Fetal choledochal cysts should be distinguished from congenital biliary atresia, hepatic cyst, ovarian cyst, biliary lithiasis, duodenal obstruction, cystic biliary atresia, among others [2]. It is especially difficult to distinguish from congenital cystic biliary atresia [11]. Observation of morphology of the fetal biliary tract and its anatomic variations of gallbladder and cysts is helpful for differentiation [12]. On the one hand, previous literatures have shown that choledochal cyst was considered if the cystic mass grow larger as the pregnancy progresses and the normal size of gallbladder [13–17]. However, there are a few reports of choledochal cysts with a stable size [12; 18]. On the other hand, the size and morphology of the gallbladder are also significant in the differential diagnosis of choledochal cysts. Koukoura O [12] et al. mentioned that the gallbladders of fetuses with choledochal cysts were smaller than that of normal fetuses. Therefore, the diameter or volume and morphological changes of gallbladders, cysts and surrounding tissues are of great help to improve the diagnostic accuracy of fetal congenital choledochal cyst.

At present, the diagnosis of fetal choledochal cyst mainly relies on ultrasound and magnetic resonance imaging (MRI) [19]. However, prenatal ultrasound is affected by many factors, such as maternal obesity, fetal position, skeletal sound shadow, amniotic fluid volume, etc., resulting in missed diagnosis or misdiagnosis. With the development of MRI techniques in recent years, such as rapid imaging sequences and black blood sequences, MRI has shown a more favorable prospect than ultrasound for a clearer overview of the biliary system, such as intrahepatic bile duct dilatation [20]. Therefore, we conducted a retrospective case-control study to evaluate the differences in gallbladders, livers, spleens, and common bile duct diameters at different gestational weeks between fetuses with type I choledochal cyst and normal fetuses, specifically to investigate the factors influencing gallbladder size in fetuses with choledochal cysts.

Patients

From January 2018 to March 2022, a retrospective analysis was performed on healthy fetuses and fetuses diagnosed with type I choledochal cyst after surgery, which were examined by prenatal MRI in the Second Hospital of Hebei Medical University. The source of MRI images of healthy fetuses was that there were abnormal signals in the abdomen ultrasound of the fetus and the MRI examination showed no abnormality. Or fetal MRI images showed abnormalities elsewhere but no developmental abnormalities in the abdomen. Demographic data at the time of MRI were recorded through medical chart review. This study was approved by the hospital Ethics Committee. Because the study was retrospective, informed consent was waived for this study.

Mri Protocol

MRI protocol

All fetuses underwent a 1.5 T MR (Signa, General Electric Company, Grandview Blvd, Waukesha, USA). Abdominal surface receiving coils were used for signal acquisition. Two-dimensional Balanced-Steady State Free Precession (B-SSFP) sequence, T2WI Single Shot-Fast Spin Echo (SS-FSE) sequence, Fast Inversion Recovery Motion Inhibition (FIRM) sequence and Diffusion-Weighted Imaging (DWI) sequence were included for MR examination. The specific parameters were as follows, B-SSFP sequence: TR = 4.78 ms, TE = 2.16 ms, Field of view (FOV) = 38cm×38cm, matrix = 256×224, layer thickness 6mm; T2WI SSFSE sequence: TR = 2000 ms, TE = 159.71 ms, FOV = 38 cm×38 cm, matrix = 256×256, layer thickness 5mm; FIRM sequence: TR = 50 ms, TE = 4.2 ms, FOV = 38 cm×38 cm, matrix = 288×180, layer thickness 5mm; DWI sequence: b = 700 s/mm², TR = 3274 ms, TE = 77.7 ms, FOV = 38 cm×38 cm, matrix = 128×128, layer thickness 5mm. Axial, sagittal and coronal images of the upper abdomen were acquired after the pre-scanning. The scanning time was about 18 ~ 30 minutes due to fetal changes in position and other factors.

Measurement Of Gallbladder Size And Other Imaging Indicators

The maximum cross-section of the gallbladder was found in the sagittal position of the SS-FSE sequence, and the maximum transverse and longitudinal diameters were measured both in the healthy fetuses and fetuses with type I choledochal cyst. The gallbladder size was expressed as the multiplication of the orthogonal diameters (OD) of the gallbladder.

The maximum transverse and longitudinal diameters of liver and spleen were measured similarly to those of the gallbladder in the coronal position of the B-SSFP sequence and transverse position of the DWI sequence, respectively. Similarly, the size of the liver and spleen was expressed as their OD values.

The maximum longitudinal diameters, maximum transverse diameters, and maximum antero-posterior diameters of the cysts in the fetuses with type I choledochal cyst were measured in the coronal, transverse and sagittal planes of B-SSFP sequence. Cysts volume [14; 16] (mm³) = 4/3 × π × maximum longitudinal diameter (mm)/2 × maximum transverse diameter (mm)/2 × maximum transverse diameter (mm)/2.

The maximum diameters of portal vein were measured in transverse position of B-SSFP sequence both in the healthy fetuses and fetuses with type I choledochal cyst. A diagram of the measurement process was shown in supplementary data figure S1.

Statistical analysis

Statistical analysis was performed using the SPSS 27.0 (IBM, Chicago, IL, USA). Continuous variables if conform to normal distribution were expressed as mean ± standard deviation or median (Quartile: Q1-Q3) which conform to skewed distribution. Categorical variables were expressed in frequency. The T test (normal distribution), Mann-Whitney (skewed distribution) and chi-square tests (categorical variables) were used to determine any statistical difference between the means and proportions of the type I congenital choledochal cysts group and healthy group. Univariate linear regression models were adopted to evaluate the associations between demographic information (gender and gestational weeks), relevant imaging-measurement values (maximum transverse and longitudinal diameters of liver and spleen, OD values of liver and spleen, volumes of choledochal cysts, and maximum diameters of portal vein) and gallbladders size. Multiple regression models were used to evaluate the associations between gestational weeks and gallbladder size in two groups respectively. Non-adjusted and slightly adjusted, and multivariate adjusted models were present as recommended by the Strengthening the Reporting of Observational studies in Epidemiology (STROBE) guide. Generalized additive models (GAM) were used to identify non-linear relationships between gestational weeks and gallbladder size in two groups. The threshold effect of gestational weeks on gallbladder size were calculated by smoothing plots that gave the maximum model likelihood.

Of the 42 fetuses with type I choledochal cyst over the study period, 3 were excluded. Of the 3 excluded fetuses, 2 were ruled out due to operations at other hospitals, image quality was poor in 1, leaving 39 for study analysis. (Supplementary Fig. S2).

Magnetic resonance imaging was performed on 1367 healthy fetuses in our hospital during the same period. 1267 were excluded. Of the 1267 excluded fetuses, 1171 were examined for other body parts other than the abdomen, image quality was poor in 35 fetuses, the incomplete sequences were in 35, 5 were twins, leaving 100 for study analysis. (Supplementary Fig. S3).

In summary, a total of 39 fetuses with type I choledochal cysts and 100 healthy controls were included in this study.

Baseline Characteristics Of The Study Population

Demographic characteristics and imaging findings of the participants were summarized in Table 1. There was no statistically significant difference in liver length, liver width and liver OD values among the healthy fetuses and fetuses with type I choledochal cysts. Compared with healthy fetuses, patients had significantly lower of the gallbladder length, width and OD in the type I choledochal cysts group. Compared with healthy fetuses, patients had significantly lower of the gallbladder length, width and OD in the type I choledochal cysts group. The portal vein diameter, spleen length, spleen width and spleen OD was greater in the type I choledochal cysts group than in the healthy group. Although there was no difference in liver morphological changes between the two groups, we found that liver fibrosis was confirmed by postoperative pathology in 18 of the 39 cases, as shown in supplementary Fig. S4.

Table 1

Baseline Characteristics of participants.
	Healthy fetuses (n = 100)	Fetuses with Type I choledochal cysts (n = 39)	P-value
Gender(male/female)	66(34.00%)/34(66.00%)	8(20.51%)/31 (79.49%)	< 0.001
Gestational weeks	28.84 ± 3.94	26.63 ± 4.09	0.004
Portal vein diameter (mm)	2.34 ± 0.19	2.47 ± 0.34	0.007
Gallbladder length (mm)	17.18 ± 3.10	12.84 ± 5.00	< 0.001
Gallbladder width (mm)	5.77 ± 1.26	5.03 ± 2.75	0.033
Gallbladder OD (mm²)	93.28 (75.50-123.42)	55.08 (37.05–75.60)	< 0.001
Liver length (mm)	60.15 ± 9.84	58.93 ± 10.08	0.51
Liver width (mm)	42.16 ± 6.33	43.19 ± 9.13	0.45
Liver OD (mm²)	2565.61 (2033.62-3106.55)	2401.33 (1888.51-3342.47)	0.86
Spleen length (mm)	19.66 ± 4.62	23.07 ± 5.74	< 0.001
Spleen width (mm)	8.21 ± 2.44	9.38 ± 3.48	0.026
Spleen OD (mm²)	153.93 (101.16-216.95)	207.68(141.69-245.56)	0.003
Cyst volume (mm³)	——	931.91(342.69-2195.20)	< 0.001
OD: multiplication of orthogonal diameter

Univariate Analysis For Gallbladder Size

The results of univariate analysis for gallbladder size were shown in Table 2. The results of univariate analysis showed that gestational weeks were positively correlated with gallbladder size (β = 6.47, p = 0.0002) and the same results were observed for liver width, liver OD, and spleen length (β = 1.89, p = 0.022; β = 0.02, p = 0.042; β = 3.04, p = 0.017, respectively). We also found that gender, portal vein diameter, liver length, spleen width, spleen OD and the cyst volume were not associated with gallbladder size.

Table 2

The results of univariate analysis for Gallbladder OD values in fetuses with Type I choledochal cysts.
	Statistics	β(95%CI)	p-value
Gender
Female	31 (79.49%)	ref
Male	8 (20.51%)	8.69 (-27.30, 44.68)	0.64
Gestational weeks	26.63 ± 4.09	6.47 (3.44, 9.51)	0.0002
Portal vein diameter (mm)	2.47 ± 0.34	11.21 (-32.70, 55.12)	0.62
Liver length (mm)	58.93 ± 10.08	1.15 (-0.28, 2.58)	0.13
Liver width (mm)	43.19 ± 9.13	1.89 (0.35, 3.43)	0.022
Liver OD (mm²)	2611.83 ± 953.17	0.02 (0.00, 0.03)	0.042
Spleen length (mm)	23.07 ± 5.74	3.04 (0.67, 5.41)	0.017
Spleen width (mm)	9.38 ± 3.48	2.07 (-2.23, 6.38)	0.35
Spleen OD (mm²)	207.68 (141.69-245.56)	0.08 (-0.03, 0.19)	0.15
Cyst volume (mm³)	931.91 (342.69-2195.20)	-0.00 (-0.01, 0.01)	0.82
OD: multiplication of orthogonal diameter; ref: reference.

The Relationship Between Gestational Weeks And Gallbladder Size In Different Models

Univariate linear regression models were used to evaluate the associations between gestational weeks and gallbladder size in fetuses with type I choledochal cysts in different models. Meanwhile, the non-adjusted and adjusted models were showed in Table 3. In the non-adjusted model, gestational weeks showed positive correlation with gallbladder OD (β = 6.47, 95%CI: 3.44 to 9.51, P = 0.0002). In the minimally adjusted model (adjusted gender), the effect size was an obvious positive correlation (β = 7.28, 95%CI: 3.99 to 10.56, P = 0.0001). After adjusting for other covariates, the effect size was also positive (β = 13.47, 95%CI: 6.83 to 20.10, P = 0.0005).

Table 3

Relationship between gestational weeks and gallbladder OD of fetuses with Type I choledochal cysts in different models.
Variable	Non-adjusted (β, 95%CI, P)	Adjust I (β, 95%CI, P)	Adjust II (β, 95%CI, P)
Gestational weeks	6.47 (3.44, 9.51) 0.0002	7.28 (3.99, 10.56) 0.0001	13.47 (6.83, 20.10) 0.0005
Non-adjusted model: All of the covariants were not adjusted.
Adjust I model: We adjusted gender.
Adjust II model: We adjusted gender, portal vein diameter, liver length, liver width, liver OD, spleen length, spleen width, spleen OD, cyst volume.
CI: confidence interval; OD: multiplication of orthogonal diameter

The analyses of non-linear relationship and threshold analysis was performed between gallbladder size with gestational weeks

We analyzed the non-linear relationship between gallbladder OD with gestational weeks (Fig. 1). We found that the relationship between gallbladder OD and gestational weeks was non-linear (after adjusting gender, portal vein diameter, liver length, liver width, liver OD, spleen length, spleen width, spleen OD, cyst volume). By using a two-piecewise linear regression model, we calculated that the two inflection points were 27 and 34. On the right of the first inflection point, the effect size was 32.31 with 95%CI (7.23, 57.38), p = 0.021. On the left of the second inflection point, we also observed a positive relationship between gallbladder OD and gestational weeks (27.23, 4.62 to 49.84, p = 0.05) (Table 4).

Table 4

The results of two-piecewise regression model in fetuses with Type I choledochal cysts.
Inflection points of gestational weeks (Per 1 change)	Effect size β (95%CI)		P value
Inflection point 27
< 27	3.92 (-1.94, 9.78)		0.20
> 27	32.31 (7.23, 57.38)		0.021
Log likelihood ratio test			0.012
Inflection point 34
< 34	27.23 (4.62, 49.84)		0.05
> 34	-17.90 (-53.07, 17.26)		0.35
Log likelihood ratio test		0.032
Effect: Gestational weeks
Cause: Gallbladder OD
Adjusted: gender, portal vein diameter, liver length, liver width, liver OD, spleen length, spleen width, spleen OD, cyst volume.
CI: confidence interval; OD: multiplication of orthogonal diameter

Comparison of gallbladder size with gestational age between healthy fetuses and type I choledochal cysts group

Similarly, we found that gallbladder OD changes with gestational weeks in normal fetuses as shown by the solid line after adjusting for gender, portal vein diameter, liver length, liver width, liver OD, spleen length, spleen width, spleen OD (Fig. 2). Compared with normal fetuses, the overall trend in gallbladder OD was lower in the type I choledochal cysts group than in the normal fetuses. The change of gallbladder OD with gestational weeks in normal fetuses was shown in Supplementary Fig. S5.

This study was to examine the relationship between gestational weeks on gallbladder size among participants especially in fetuses with type I choledochal cyst. As was shown in adjusted II model, the gallbladder size continued to increase with gestational weeks after adjusting for all covariates. However, the trend of gallbladder growth was curvilinear rather than linear throughout the gestational period due to the presence of type I choledochal cysts. There were two inflection points in the curve (gestational weeks were 27 and 34). Gestational weeks was positively associated with gallbladder size on the right side of 27 gestational weeks and the left side of 24 gestational weeks.

Previous studies reported that type I choledochal cyst was higher in females than in males [3]. In the 39 cases of fetal type I choledochal cyst included in this study, 31 were female and 8 were male, which was consistent with previous studies.

This study showed that the gallbladder size of fetuses with type I choledochal cyst was significantly smaller than that of normal fetuses. This is because most of the bile is stored in the choledochal cyst instead of the normal bile duct. Due to cholestasis, gallstones and the formation of protein particles on the cystic duct has a certain degree of obstruction. Both conditions lead to the collapse of the gallbladder.

In this study, it was also found that the portal vein diameter of fetuses with type I choledochal cyst was larger than that of healthy fetuses. Previous literature has reported that dilation of type I choledochal cysts and narrowing of ducts can lead to gallstones, the formation of cholestasis, and infection of the biliary system [21], leading to secondary biliary cirrhosis in 40%-50% of children with associated signs and symptoms. This study found that portal vein diameter widened in fetuses with type I choledochal cysts. It is speculated that the widening mechanism is as follows. First, choledochal cysts cause cholestasis in the liver, which aggravates the direct damage to the liver, leading to higher portal pressure and a corresponding increase in the diameter of the portal vein. This was confirmed by the pathological results of intraoperative puncture showing the formation of liver pseudolobular and fibrosis at the torcular confluence [22]. Second, large cysts can even mechanically block the portal vein, and portal hypertension can occur even in the absence of cirrhosis [23].

In addition, it has been reported that choledochal cysts caused hepatosplenomegaly from a case report [24; 25]. In this study, we also found that the transverse diameter, short diameter and OD value of spleen of fetuses with type I choledochal cyst were greater than those of normal fetuses. As mentioned above, choledochal cysts can cause increased portal vein pressure, which can affect the return of the spleen. Therefore, the spleen can enlarge due to congestion. In this study, no differences in liver morphology were found between the two groups, which may be due to the limited influence of choledochal cysts on the liver during the fetal period, leading to pathological changes, namely liver fibrosis, but no morphological enlargement. As the fetus grows, the diet after birth can accelerate cholestasis and cause liver fibrosis.

There are some limitations in our study. First, the sample size of fetuses with type I choledochal cyst was small and it was a single-center study. Second, this study was a case-control study. Therefore, only weak evidence between exposure and outcome could be provided. Third, the follow-up time war short, and the prognosis of neonates who underwent surgery after birth should be followed up continuously.

The gallbladder of the fetuses with type I congenital choledochal cyst was smaller than that of the normal fetuses, and the gallbladder increased in a curve rather than a straight line with the increase of gestational weeks. In addition, type I choledochal cysts of the fetuses caused portal vein dilation and spleen enlargement.

B-SSFP Balanced-Steady State Free Precession

DWI Diffusion-Weighted Imaging

FIRM Fast Inversion Recovery Motion Inhibition

FOV Field of view

GAM Generalized additive models

MRI Magnetic Resonance Imaging

OD The multiplication of the orthogonal diameters

STROBE Strengthening the Reporting of Observational studies in Epidemiology SS-FSE Single Shot-Fast Spin Echo

Statement of Ethics

The study was approved by the Ethics Committee of the Second Hospital of Hebei Medical University. Written parental informed consent was waived because the study was retrospective.

Conflict of Interest Statement

The authors have no conflicts of interest to disclose.

Funding Sources

For this study, a grant was obtained from the foundation of the Second Hospital of Hebei Medical University (2HC202125).

Author Contributions

Lixia Zhou and Zuojun Geng designed the study. Duo Gao, Liyi Jia, Jianxiong Zheng, Yingchao Li, Chengxiang Zhang, Yimin Cao and Zexi Yi contributed to the data acquisition of the study. Duo Gao and Lixia Zhou performed the analyses. Duo Gao has written the manuscript. Lixia Zhou and Zuojun Geng critically reviewed the manuscript. All authors have contributed to the final version of the manuscript.

Data Availability Statement

The data used to support the findings of this study are available from the corresponding author upon request.

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MRI analysis of gallbladder changes with gestational weeks between fetuses with type I congenital choledochal cyst and healthy fetuses

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Abstract

Purpose

Methods

Results

Conclusions

Figures

What Is Known

Introduction

Patients And Methods

Patients

Mri Protocol

Measurement Of Gallbladder Size And Other Imaging Indicators

Statistical analysis

Results

Baseline Characteristics Of The Study Population

Univariate Analysis For Gallbladder Size

The Relationship Between Gestational Weeks And Gallbladder Size In Different Models

Discussion

Conclusion

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

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