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Table of Contents   
ORIGINAL ARTICLE
Year : 2023  |  Volume : 28  |  Issue : 2  |  Page : 137-143
 

Prevalence of pancreato-biliary maljunction in children with choledochal cyst – A prospective observational study


1 Department of Paediatric Surgery, All India Institute of Medical Sciences, Bhubaneswar, Odisha, India
2 Department of Pathology, All India Institute of Medical Sciences, Bhubaneswar, Odisha, India
3 Department of Radiology, All India Institute of Medical Sciences, Bhubaneswar, Odisha, India
4 Department of Paediatric Surgery, All India Institute of Medical Sciences, Mangalagiri, Andhra Pradesh, India

Date of Submission29-Jul-2022
Date of Decision13-Oct-2022
Date of Acceptance26-Oct-2022
Date of Web Publication30-Nov-2022

Correspondence Address:
Bikasha Bihary Tripathy
Department of Paediatric Surgery, All India Institute of Medical Sciences, Bhubaneswar, Odisha
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiaps.jiaps_104_22

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   Abstract 


Background: Pancreatico-biliary maljunction (PBM) is often found to be associated with choledochal cysts (CCs). According to a European multicenter study, the prevalence of PBM in cases of CC is found to be 72.2%, however, there is no Indian study depicting the prevalence of PBM in Indian children with CCs, which is one of the main postulated factors in the etiopathogenesis of CC. In this study, we have attempted to observe prospectively the prevalence of PBM in children with CC and correlate this to its morphological and biochemical parameters. The association between the presence of PBM and histopathological findings such as epithelial changes of the mucosa of the CC, inflammation, metaplasia or dysplasia, and histopathology of the liver has also been evaluated.
Materials and Methods: We carried out a single center, prospective observational study with a single arm study group. We prospectively selected all patients of CC admitted for surgery from November 2018 to October 2020. Data on biochemical, radiological, and histopathological parameters were collected and analyzed.
Results: We included a total of 20 patients in our study. The mean age of the participants was 6.22 ± 4.32 years. Among them, 11 (55.0%) were male and 9 (45%) were female. Abdominal pain was the most common presenting complaint among our patients (75.0%) and had a significant association with the presence of a PBM (P = 0.001). In symptomatic children, the mean duration of symptoms was 4.50 ± 2.26 months for jaundice, 4.50 ± 1.98 months for abdominal distension, and 5.07 ± 2.02 months for abdominal pain. Among the 3 children with cholangitis, the mean number of episodes was 3.33 ± 2.08, with a median of four episodes. Fourteen (70.0%) of the children had type I a CC, 1 (5.0%) participant each for types I b, I c, II and IV a and 2 (10.0%) of them had type IV b cyst. The mean size of the cyst (cm) was 7.41 ± 3.03 with a median of 6.85 cm. Among the children, 9 (45%) showed the presence of PBM on magnetic resonance cholangiopancreatography (MRCP), with 7 (77.8%) showing Komi's C-P type and 2 (22.2%) showing Komi's PC type. The mean common channel length (mm) on MRCP was 8.11 ± 2.47 with a median length of 8.00 mm. The biochemical analysis of a bile fluid amylase and lipase is the functional indicator of the presence of a PBM. Histopathological examination showed the presence of ulceration in the walls of the CC in 10 (50.0%) of the specimens. There was a significant association of the presence of PBM and ulceration in the mucosa of the CC (P ≤ 0.001), with the median levels being the highest in the PBM present group.
Conclusion: Abdominal pain is the most common complaint in a child with CC, and when present, it is significantly associated with the presence of a PBM. MRCP is the gold standard tool to detect CCs and find out the morphology of PBM. The prevalence of PBM in children with CC of 45% with a mean common channel length of 8.11 mm. The biochemical analysis of a bile amylase and lipase is the functional indicator of the presence of a PBM and there is a significant association of their higher levels and presence of PBM. The presence of chronic inflammation and microscopic ulcers is significant histologic parameters depicting the presence of a PBM.


Keywords: Magnetic resonance cholangiopancreatography, hepaticojejunostomy, hepatobiliary


How to cite this article:
Manekar AA, Tripathy BB, Sahoo SK, Sable MN, Naik S, Janjala N, Mohanty MK. Prevalence of pancreato-biliary maljunction in children with choledochal cyst – A prospective observational study. J Indian Assoc Pediatr Surg 2023;28:137-43

How to cite this URL:
Manekar AA, Tripathy BB, Sahoo SK, Sable MN, Naik S, Janjala N, Mohanty MK. Prevalence of pancreato-biliary maljunction in children with choledochal cyst – A prospective observational study. J Indian Assoc Pediatr Surg [serial online] 2023 [cited 2023 Mar 29];28:137-43. Available from: https://www.jiaps.com/text.asp?2023/28/2/137/362387





   Introduction Top


Choledochal cyst (CC) is a pathologic condition characterized by varying degrees of congenital dilatation of the biliary system, including the common hepatic, intrahepatic, and retropancreatic bile ducts. It is common in the Asian population, especially in infants and females.[1],[2],[3],[4],[5],[6],[7],[8] Pancreatico-biliary maljunction (PBM), a congenital anomaly of the junction between pancreatic and bile ducts,[9] is often found to be associated with CCs.[1],[10],[11],[12],[13] PBM is defined as an abnormal union between the pancreatic and the biliary ducts located outside the duodenal wall with a long common channel. It is postulated that reflux of pancreatic juice is caused by the presence of PBM and is an etiological factor in the pathogenesis of CC and the development of subsequent biliary cancer, especially in dilated segments.[14] This reflux causes damage to the mucosa of common bile duct (CBD) as well as to its musculature leading to its dilatation and the cyst formation. The presence of PBM is evident from the preoperative imaging and a raised amylase and lipase levels in the cyst fluid.[14],[15],[16],[17]

However, there is no Indian study available on literature search, depicting the prevalence of PBM in cases of CCs, which is one of the main postulated factors in the etiopathogenesis of CC and also depicting the association of the PBM with other related parameters. In our study, we have attempted to observe the prevalence of PBM in children with CC and correlate this to its morphological and biochemical parameters and its influence on the surgical outcome. The association between the presence of PBM and histopathological findings such as epithelial changes of the mucosa of the CC, inflammation, metaplasia or dysplasia, and histopathology of the liver has also been evaluated.


   Materials and Methods Top


The study was done in the department of pediatric surgery at a tertiary care hospital of Eastern India. Approval was obtained from the Institutional Ethics Committee. The duration of the study was from November 2018 to October 2020. This is a prospective observational study with a single arm study group. All diagnosed cases of CCs admitted for surgery in the Department of Pediatric Surgery, AIIMS Bhubaneswar were included in our study. The children presenting with clinical symptoms and signs of CC were evaluated using imaging (ultrasonography and magnetic resonance cholangiopancreatography [MRCP]) and pathological investigations. After all preoperative preparation, patients underwent surgery, as indicated for the type of CC. During surgery, cyst fluid was collected and was sent for the estimation of amylase and lipase levels. Surgery was performed as per the standard institutional protocol. We did not use a choledochoscope in our study. Liver core needle biopsies were collected at the end of surgery and the excised cyst along with liver cores in formalin were sent for histopathological examination where gross and histopathological analysis of the cyst was done. Statistical analysis was performed using the SPSS software version 23 (IBM Corp).


   Results Top


Only 20 patients were recruited during this period due to restrictions imposed by the COVID pandemic. The mean age of the participants was 6.22 ± 4.32 years, with the youngest participant being 2 months old and the oldest being 13 years old. Among them, 11 (55.0%) were male and 9 (45%) were female with male-to-female ratio being 1.2:1. Abdominal pain was the most common presenting complaint among our patients (15; 75.0%), followed by abdominal distension seen in 12 children (60.0%), jaundice in 6 children (30.0%), and previous episodes of cholangitis in 3 children (15.0%).

Majority (14; 70.0%) of the children had type Ia CC, 1 (5.0%) participant each for types Ib, Ic, II and IVa and 2 (10.0%) of them had type IVb cyst. The mean size of the cyst (cm) was 7.41 ± 3.03 with a median of 6.85 cm. Only 9 (45%) showed the presence of PBM on MRCP, with 7 (77.8%) showing Komi's C-P type and 2 (22.2%) showing Komi's P-C type. The mean common channel length (mm) on MRCP was 8.11 ± 2.47, with a median length of 8.00 mm [Figure 1].
Figure 1: Representative MRCP picture showing the CC (red arrow) and the PBM (yellow arrow). MRCP: Magnetic resonance cholangiopancreatography, CC: Choledochal cysts, PBM: Pancreatico-biliary maljunction

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A roux-en-Y hepatico-jejunostomy was performed in all our patients (100.00%). Only 2 (10.0%) of our children showed the presence of a cirrhotic liver intra-operatively. The mean intra-operative cyst size was 6.79 ± 3.14 cm (median 6.00 cm). A visible common channel was not seen intra-operatively in any of our operated patients 0 (0.00%).

The mean bile fluid amylase level was 5114.95 ± 9669.91 IU/L with a median value of 40.50 IUL/and that of bile fluid lipase was 4375.10 ± 8029.30 IUL/with a median value of 71.50 IUL/. These values ranged from 8.0–35523.0 to 10.0–28343.0 for bile fluid amylase and lipase levels.

There was no statistically significant correlation between MRCP: Common Channel Length (mm) and Age (Years) [r = −0.23, P = 0.555, [Figure 2]].
Figure 2: The correlation between age and the common channel length. MRCP: Magnetic resonance cholangiopancreatography

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Histopathological examination showed the presence of ulceration in the walls of the CC in 10 (50.0%) of the specimens. No dysplasia was seen among all excised specimens. The changes were seen in the histopathology of the liver with cholestasis and hepatocellular damage seen in 3 (15.0%) of the liver biopsies taken, parenchymal inflammation, bile duct proliferation, bile duct inflammation and central venous distension seen in 2 (10.0%) of the liver biopsy specimens, and fibrosis seen in 4 (20.0%) specimens. In 80.0% of the specimens, no fibrosis on histopathological examination was seen. Of those 4 who had fibrosis, Grades of 1, 2, 3, 4 was observed in 1 specimen each.


   Discussion Top


CCs are rare congenital anomalies of the bile duct system. They consist of a distinctive dilatation of the intra- andor/extra-hepatic bile ducts most common being types I and IVa. These have a common association with PBMs.[18] PBM are congenital anomalies of the junction between CBD and the pancreatic duct; defined by a “union between the pancreatic and the biliary ducts located outside the duodenal wall with a common channel.” This maljunction induces the reflux of pancreatic juice into the biliary tract, which causes the intermixing of the juices. This participates in damage to the wall of the cyst and the dilatation of the CBD and the development of biliary cancer, especially in dilated segments.[19],[20],[21]

Although PBM has been described to have significant influence in the etiopathogenesis and long-term consequences of CC, there are very few literatures available describing the prevalence of PBM in CCs in children and none in Indian children to best of our knowledge. In an exclusive pediatric case series by Singhavejsakul and Ukarapol[4] CCs were predominant in females, and 38% of the patients were younger than 2 years of age. They had 32 patients (25 female) with a mean age at diagnosis of 4.1 years (range: 1 month to 14.8 years) in their study. Jaundice was the most common presenting complaint in this study, followed by abdominal pain, abdominal mass. Three amongst the 32 patients had a history of previous cholangitis.[4] A comparison with similar other studies of CC and PBM is shown in [Table 1].
Table 1: Comparison between the parameters of various other studies

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Similar results were also seen in a mixed group (pediatric and adult patients) as studied by Lipsett et al.,[8] and Chijiiwa and Koga.[22] Our study had only paediatric patients with a mean age of presentation at 6.22 years and female-to-male ratio being 1:1.2. The male predominance in our study population might be due to the small sample size and the social practice of preferential hospital visit for male child prevalent in our society.

Abdominal pain (75%) was the most common presenting complaint in our study similar to other studies with a mean duration of 5.07 months. In our study, abdominal pain (χ2 = 5.455, P = 0.038) was significantly associated with the presence of PBM (P < 0.05). However, there was no significant association of other symptoms; jaundice (χ2 = 0.087, P = 1.0000), abdominal distension (χ2 = 1.650, P = 0.362), and cholangitis episodes (χ2 = 4.314, P = 0.074). There are no other studies available in the literature depicting this association.

MRCP is the “gold standard” for the diagnosis of CCs and describing its morphology. It has a reported sensitivity of 90%–100%, but a low sensitivity for delineating the common channel and pancreatic duct (46%) as compared to computed tomography cholangiography (64%).[21] MRCP avoids ionizing radiation and is also noninvasive when compared with ERCP with no complications of pancreatitis or cholangitis. MRCP with magnetic resonance imaging (MRI) can also image surrounding structures, stones, and malignancy.[21] It detects the morphological presence of PBM extraduodenally, between the choledochus and the MPD even in apparently normal children, with the rate of detection being as high as 82% to 100%.[21] It is reported in the anatomical studies that a short common channel (4.6 ± 2.2 mm) is present in only 80%–85% of CCs in adults.[20] This suggests the proposal of Kamisawa et al.,[23] where the length of the common channel was taken as the main anatomical diagnostic parameter for the PBM. There is however no study about the consensus for the “cut-off” limits of the long common channel; the length being variable in 1st year of life. Almost 90% of the patients of CCs (adult and infants) showed a mean length of the common channel of 10 mm (considering >8 mm as the cut-off limit).[20],[24]

Our study used MRCP as the diagnostic tool for the diagnosis of CC, more specifically for finding the anatomy of PBM. Only 45% of our patients had the presence of PBM. This is in contrast to the higher prevalence of PBM in children of CCs in Japan and Europe.[20] Comparing with other studies, as demonstrated in Table, type 1 cyst was the most common variety of CCs followed by type IV, as shown in [Table 2]. Similar results were achieved by us in our study.
Table 2: Comparison between similar studies for type of cyst, pancreatico-biliary maljunction and its type, common channel length (percentage)

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According to Komi's classification, there are 3 types of PBM, the C-P type, the P-C type and the complex type. This was the classification used by Ragot et al.,[20] in their European multicenter study and the same has been incorporated in our study. A PBM was found in 72.2% cases in their study with a C-P type junction in 57.2% participants, 34.5% had a P-C junction and the remaining 8.3% had a complex junction. The median length of the common channel among the participants was 15.8 ± 6.8 mm (range 5–40 mm).[20] However, their study included adults too, along with pediatric patients. Our study consisted of only pediatric patients with the presence of a PBM in 45% patients, with C-P junction in 77.8% cases and a P-C junction in 22.2% cases. The median common channel length in our study was 8 mm (range 6–10).

Ragot et al.[20] in their multicenter European study described that there was a higher mean bile fluid amylase level when PBM was present than those where PBM was absent. Literature analysis depicted that a raised bile amylase level of more than 10,000 IUL/indicates the presence of a functional PBM [Table 3].[20],[25] Kamisawa et al.[23] showed that the length of a common channel more than 5 mm gives rise to levels of bile fluid amylase more than 1000 IUL/. A slight fusiform dilated CBD with raised bile fluid amylase is an evidence of the presence of a PBM.[20]
Table 3: Comparison between Ragot et al.[20] and our study

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Our study confirmed the morphological presence of the PBM by the use of MRCP, which was reconfirmed functionally by the biochemical picture of raised bile fluid amylase and lipase levels from the intra-operative samples. The mean (standard deviation [SD]) of bile fluid amylase in the PBM present group was 11333.78 (11957.16) and in absent group was 26.82 (11.21) with a median (IQR) 8498 (1774–13327) and 29 (20.5–34.5) in each group, respectively, and a range of 498– 35523 and 8–41, respectively. There was a significant difference between the two groups in terms of bile fluid amylase (W = 99.000, P ≤ 0.001), with the median bile fluid amylase being highest in the PBM present group. Similarly, the mean (SD) of bile fluid lipase in the PBM present group was 9679.11 (9776.04) and in absent group was 35.45 (23.31) with a median (IQR) 6387 (1427–16598) and 28 (17.5–49.5), respectively, in each group, and a range of 391–28343 and 10,–82 respectively. There was a significant difference between the two groups in terms of bile fluid lipase (W = 99.000, P ≤ 0.001), with the median bile fluid lipase being highest in the PBM present group.

There was a weak positive correlation between bile fluid amylase and common channel length (mm), and this correlation was not statistically significant (rho = 0.08, P = 0.846). Furthermore, there was a weak positive correlation between bile fluid lipase and common channel length (mm), and this correlation was not statistically significant (rho = 0.08, P = 0.846) [Figure 3]. This may be due to the smaller sample size. Histopathological changes of varying severity were evident in all patients in the preoperative liver biopsy in a study by Sugandhi et al,[26] and hepatocellular damage was the most widespread parameter noted with all patients showing at least some degree of parenchymal damage. Majority of patients demonstrated Grade 1–2 changes across all histological parameters. A significant association was found with the presence of PBM and hepatocellular damage on histopathology of liver. In the postoperative liver biopsies, it was seen that all the histopathological changes either resolved completely or decreased in severity except portal fibrosis which did not show any significant reduction and central venous distension which was rather aggravated.[26] There was no significance found among all other parameters of liver histology.
Figure 3: (a) Correlation of common channel length with bile fluid amylase, (b) Correlation of common channel length with bile fluid lipase. MRCP: Magnetic resonance cholangiopancreatography

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In our study, 80.0% of children in the PBM present group showed the presence of ulceration in the mucosa of the CC which was a statistically significant association (χ2 = 9.899, P = 0.005). Our study showed no significance association between the presence of PBM and histopathological changes in the liver.

Sharma et al.[27] have correlated the intracystic pressure with cyst volume, length of common channel, biochemical changes in bile, and histopathological changes in the liver in CC. This is a similar to our study. However, the length of the common channel has been correlated with histopathological parameters in our study.


   Conclusion Top


PBM has a significant role in the etiopathogenesis and long-term consequences of CCs. However, there is a paucity in the literature documenting its prevalence in paediatric CC patients. We found the prevalence of PBM in children with CC of 45% with a mean length of 8.11 mm in our part of the world. We documented abdominal pain to be the most common complaint and when present, it was significantly associated with presence of a PBM. MRCP is the gold standard tool to detect CCs and find out the morphology of PBM. The biochemical analysis of a bile fluid amylase and lipase is the functional indicator of the presence of a PBM. There was a significantly raised bile fluid amylase and lipase in PBM patients in our study. The presence of chronic inflammation and microscopic ulcers were significant histologic parameters depicting the presence of a PBM. However, we did not find any significant association of postoperative complications in cases of CC with a PBM. To the best of our knowledge, this is the only study of its kind in Indian children.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

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