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Laparoscopic management of choledochal cyst in children: Lessons learnt from low-middle income countries


1 Department of Pediatric Surgery, National Children Hospital, Hanoi; Department of Pediatric Surgery, Vinmec Research Institute of Stemcell and Gene Technology, Hà Nôi, Vietnam
2 Department of Surgery, Division of Pediatric Surgery, Netaji Subhash Chandra Bose Medical College, Jabalpur, Madhya Pradesh, India
3 Department of Pediatric Surgery, Philippine Children's Medical Center, Quezon City, Philippines

Date of Submission22-May-2020
Date of Decision22-Jun-2020
Date of Acceptance24-Jun-2020
Date of Web Publication08-Sep-2020

Correspondence Address:
Vikesh Agrawal,
Department of Surgery, Division of Pediatric Surgery, Netaji Subhash Chandra Bose Medical College, Jabalpur, Madhya Pradesh
India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmas.JMAS_114_20

PMID: 32964871

  Abstract 

Choledochal cyst (CC) is a disease with a strong Asian preponderance. As laparoscopic surgery has become mainstay in its treatment, the experience in these countries has been phenomenal. However, there are many contentious issues related with the laparoscopic management of CC. In this review article, we will try to answer the contentious questions related to the laparoscopic management of CC. The issues related to aetiology, classification, surgical technique, type of biliary anastomosis, intrahepatic stones and malignancy are discussed. We also discuss the current and future considerations of laparoscopic management with reference to it becoming a gold standard. This article describes the standard surgical approach and will discuss its technical nuances. This article will also discuss the outcome of treatment in different settings of low- and middle-income countries based on lessons learnt by the authors from their experience and research.


Keywords: Choledochal cyst, laparoscopy, low- and middle-income countries, outcomes



How to cite this URL:
Liem NT, Agrawal V, Aison DS. Laparoscopic management of choledochal cyst in children: Lessons learnt from low-middle income countries. J Min Access Surg [Epub ahead of print] [cited 2020 Oct 29]. Available from: https://www.journalofmas.com/preprintarticle.asp?id=294571



  Introduction Top


Choledochal cysts (CCs) are cystic dilatations of the extra-hepatic and/or intrahepatic biliary system. Owing to variation in the involvement of the biliary tree amongst subtypes and new insights into epithelial markers, the more recent term for this condition is choledochal malformation.[1] This congenital disease is more common in the Asian population with an incidence ranging from 1 in 13,000 live births in South Asia to 1:1000 live births in Japan as compared to 1 in 100,000–150,000 live births in Western population.[2] Nearly 80% of CC is diagnosed as jaundice in the early infancy or non-specific abdominal pain in older children.[3] The treatment for CC includes total cyst excision and restoration of the biliary-enteric system, either by hepatico-duodenostomy (HD) or hepatico-jejunostomy (HJ) and laparoscopy is becoming its mainstay approach. Minimising the surgical complications such as post-operative cholangitis, duodenal–pancreatic reflux, anastomotic leaks and strictures, pancreatitis, perforation, adhesive intestinal obstruction, iatrogenic portal vein injury, intra-hepatic stones (IHS), biliary reflux and late malignant transformation along with early recovery have been the focus of newer strategies.[4] Although laparoscopic management has become a standard procedure for the management of CC, there remain many old questions that are looking for new answers.

The Asian preponderance has led to extensive experience amongst paediatric surgeons of these countries and has found quite a few differences as compared to western literature.[5] In order to match the state of the art status in the management of CC, despite limited resources, these countries have modernised the management of CC. This article shall provide answers related to the contentious issues of laparoscopic management of CC, current standards of what is being done/can be done and the outcome which has been achieved in the low/middle income settings based on authors' experience and research.


  Aetiology of Choledochal Cyst-Has the Postulate Changed? Top


The aetiology of CC remains disputed but the 'the obstructing segment hypothesis' and 'the pancreatic reflux hypothesis' are the most commonly accepted hypotheses.[6],[7],[8] The latter hypothesis is more widely accepted which states that reflux into the bile duct through long common channel due to anomalous pancreaticobiliary duct junction expose biliary epithelium to the destructive effects of activated proteolytic pancreatic enzymes, thus causing weakness and then dilatation of the common bile duct, however, it is found in only 50%–80% of cases.[8],[9] A significant role of reflux and pressure has been demonstrated based on raised bile amylase levels (as a surrogate marker of reflux), intra-choledochal pressure and biliary epithelial histology.[10] However, so far, there is little evidence at basic research and molecular level which can be mentioned.[11]


  Classification of Choledochal Cyst-Are There Newer Developments? Top


Various morphological classifications of CC have been described. The original classification was described by Alonso-Lej et al.[12] The most widely accepted classification remains the one by Todani et al. including eight variants (Type Ia, b and c; II; III; IVa and IVb and V CC).[13] It is worth mentioning that 'Caroli's disease' (alternatively syndrome if involving the entire intrahepatic tree and coexisting with congenital hepatic fibrosis) remains apart from most choledochal classifications but it is a hepatic manifestation of a genetic disease affecting the basement membrane of other organs (mainly the kidney, presenting as autosomal polycystic kidney disease [dominant and recessive], medullary sponge kidney and medullary cystic disease).[14] Recently, as there has been a lot of emphasis on an anomalous pancreaticobiliary junction and pancreatic reflux in the aetiology of CC, few authors have classified variants of the common channel based on the angle of insertion, etc., but these do not seem to have much relevance in decision making.[15],[16]

A further pancreaticobiliary variant is the 'forme fruste' which is not included in any one of the above-stated classification systems. This term was first coined by Lilly et al., in 1985, and used to describe an entity without (cystic) extra-hepatic bile duct dilatation but with a long common channel.[17] This variant is associated with recurrent biliary pain, cholangitis and pancreatitis. Complete relief after disconnection surgery is reported.[18]


  Laparoscopic Cystectomy: Is it a State of the Art Procedure? Top


For many years, complete removal of the CC with HJ by open technique has been the standard approach. In 1994, the first laparoscopic cystectomy (LC) and HJ were described by Farello et al. and years later, Tan et al. described LC with HD.[19],[20] With the growing experience of paediatric laparoscopic surgery, LC has become a state of the art approach in the management of CC. The biggest advantages of LC, which makes it eligible to become future-standard, is magnification, reduced bleeding, lesser surgical complications, better anastomosis and early recovery apart from cosmetic benefits.[21] Therefore, countries with higher volumes have been able to standardise the operation technique of LC and achieve better outcomes. As a result, the effective learning of the procedure has been translated into efficient teaching, which further strengthens the above fact.[22] However, there have been various questions related to the nuances of the procedure which will be addressed in this review.


  Standard Operative Technique: How Far Have We Reached? Top


The technique of LC has never been standardised and the time has come to take the call. The growing publications in this field have substantiated the experience-based learning in evidence-based surgery.[23] Authors would like to describe their standard approach which allows the procedure to be effective, safe and reproducible.

Laparoscopic cystectomy

LC is carried out using four ports. A nasogastric tube, rectal tube and Foley urinary catheter are used to decompress the stomach, the colon and bladder, respectively. The patient is placed in a 30° head up supine position. The surgeon stands at the lower end of the operating table [Figure 1]. A 10 mm trocar is inserted through the umbilicus for the telescope. A carbon dioxide pneumoperitoneum is established and maintained at a pressure of 8–12 mm Hg. Three additional 5 mm or 3 mm trocars are placed for instrumentation at the right flank, left flank and left hypochondrium [Figure 2]. The liver is hitched to the anterior abdominal wall by the first percutaneous suspension suture placed at the falciform ligament allowing good exposure to the upper part of the CC. The cystic artery and cystic duct are identified, isolated, clipped, and divided. A second percutaneous suspension suture is placed at the distal cystic duct and the gallbladder to elevate the liver and expose the liver hilum [Figure 3]a and [Figure 3]b. These two suspension sutures are important heuristic steps for better exposure and avoiding extra ports. The duodenum is retracted downward using a dissector through the left hypochondrium trocar while flank trocars are used for dissection. The middle portion of the cyst is dissected circumferentially. With a large cyst, the dissection is started a little higher than usual and then proceeds distally. Separation of the cyst from the hepatic artery and portal vein is carried out meticulously until a dissector can be passed through the space between the posterior wall of the cyst and portal vein proceeding from left to right. The cyst is then divided at this site. The lower part of the cyst is dissected from the pancreatic tissue down to the common pancreaticobiliary junction using a 3 mm dissector mounted with cautery. The distal part of the cyst is removed progressively. Protein plugs or calculi within the distal cyst and common channel are washed and sucked out. The distal part of the cyst is opened longitudinally [Figure 4]a and [Figure 4]b. The inspection of the lumen is carried out to identify the orifice of the common pancreaticobiliary junction. A small catheter is inserted into the common channel. Irrigation with normal saline via this catheter is performed to eliminate any protein plug until the catheter can be passed down to the duodenum. The distal CC is clipped and divided at the level of the orifice of the common channel. Consequently, the upper part of the cyst is dissected up to the common hepatic duct and then divided from it. The cyst is initially divided below the level of the cystic duct, and after identifying the orifice of the right and left hepatic ducts, definitive resection is performed preserving the adequate length of the hepatic duct for anastomosis. When the cyst is intensely inflamed and extensive peri-cystic adhesions are present, the dissection of the cyst wall from the portal vein is carried out carefully while viewing the cyst internally and externally. After excision, the common hepatic duct and hepatic ducts are irrigated with normal saline to wash out biliary debris and stones. Irrigation with normal saline is done through a 6 Fr catheter inserted into the right followed by the left hepatic duct to wash out the protein plugs or calculi until the effluent is clear [Figure 5]a and [Figure 5]b. The inspection and irrigation at both ends can be performed through a rigid paediatric cystoscope if the common channel is big enough. The gallbladder is dissected from its bed and surrounding tissues. The excised specimen is removed through the umbilicus [Supplementary Material, Video 1, https://drive.google.com/file/d/1r1TrZywXVjfsUi0pkyI2Gnq7_cGOSs4j/view?usp=sharing].
Figure 1: Ergonomic layout

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Figure 2: Port placement

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Figure 3: Figures demonstrating suspension sutures at falciform ligament (a, suspension suture-1) and gallbladder (b, suspension suture-2)

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Figure 4: Figures demonstrating laying open of distal cut-end of bile duct (a) and its irrigation (b)

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Figure 5: Figures demonstrating hepatic-end of duct and both ductal openings (a) and their irrigation (b)

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Hepatico-jejunostomy

After completion of LC, the ligament of Treitz is identified and a 5/0 silk stay-suture is placed 30 cm distal to the ligament of Treitz. A second 5/0 PDS suture is placed 2.0 cm below the first sutures to mark the jejunal limb, which will be anastomosed to the hepatic duct. The jejunal segment with 2 sutures is grasped with an intestinal grasper. The trans-umbilical vertical incision is extended 1.0 cm above the umbilicus. The jejunum is exteriorized, Roux limb is constructed and the jejunojejunostomy is completed extra-corporeally. The jejunum is then reposited back into the abdominal cavity. The extended umbilical incision is closed to make it small enough to accommodate a 10 mm trocar without gas leakage. The laparoscopic instruments are now repositioned. The Roux limb is passed through a window in the transverse mesocolon to the porta hepatis. The jejunum is opened longitudinally on the anti-mesenteric border a few millimetres from the closed end of the Roux. HJ is fashioned using 2 running sutures of 5/0 PDS (Interrupted sutures are used when the diameter of the common hepatic duct is <1.0 cm). Sutures are inserted from the left to right with 3 mm instruments. Ducto-plasty is performed by opening the common hepatic duct by incising the left hepatic duct longitudinally for a variable distance if the common hepatic duct is too narrow. Mesenteric defects in the transverse mesocolon and small bowel mesentery are closed with sutures. The operative field is washed with warm saline. A sub-hepatic drain is inserted and closure is performed.[24]

Hepatico-duodenostomy

After LC, the duodenum is mobilised using Kocher's manoeuvre, and a HD is constructed 2.0 cm distal to the pylorus using 2 running sutures of 5/0 PDS. Interrupted sutures are used when the diameter of the common hepatic duct is <1.0 cm. The rest of the operation is performed the same as described previously.[25]

Single-incision laparoscopic cystectomy for choledochal cyst

The single-incision LC is performed using conventional instruments of laparoscopy avoiding additional expenditure involved in specially designed single incision ports suiting the needs of low and middle income countries. A peri-umbilical incision is made and the peri-umbilical skin is separated from the fascia. Two 5-mm trocars (one long and one short) and a short 3-mm trocar are placed in a triangular fashion within the range of the exposed fascia. A trans-abdominal suspension suture is made to lift the falciform ligament to the anterior abdominal wall. A second suspension suture is taken to lift the gallbladder to the abdominal wall on the right. The cystic artery and cystic duct are exposed, clipped and divided. A third suspension suture is taken to lift the anterior wall of the cyst to the abdominal wall. The distal part of the cyst is dissected and dissection proceeds, more suspension sutures can be added to facilitate dissection. The rest of the operation is performed similarly to the conventional LC. With experienced surgeons outcomes of single incision laparoscopic surgery is similar to conventional laparoscopic surgery.[26],[27],[28] The only benefit of this approach is the cosmetic aspect, therefore it is advisable to perform single-incision LC only by experienced surgeons who have a high volume of patients with CC and have performed a definite number of LCs.

Robotic-assisted laparoscopic cystectomy

The operation is carried out using five ports. First, a 12-mm port is placed through the umbilicus for endo-vision. Then, a 5-mm port is placed lateral to the midclavicular line on each side, and an 8-mm port was placed in the upper far-right lateral position. The last 5-mm port is placed in the far-left position for surgical assistance [Figure 5]. The details of the operation performed are similar to conventional LC as described above. The outcome of robotic surgery is not different from LC or open surgery. However, higher cost remains a contentious issue in the developing world.[29],[30],[31]


  Hepatico-Jejunostomy Versus Hepatico-Duodenostomy: Does This Settle the Debate? Top


HJ has been the preferred reconstructive method in the era of open surgery after LC because it has minimal chances of bile reflux and associated complications.[32] However, when LC started becoming popular the logical advantage of HD in terms of its simplicity rekindled the debate. More studies started coming up stating that even HJ is associated with complications including stone formation in the elongated blind pouch or intrahepatic bile duct stones caused by bile stasis, bowel obstruction, duodenal obstruction caused by compression by a tight RY limb vascular arch, and abnormally elongated RY jejunal limb.[33] Few authors recommend a minimum length of 30 for Roux limb, end-to-end HJ, and longer jejunojejunostomy to avoid complications related to Roux stasis syndrome.[33] On the contrary, a shorter loop individualised for the patient's age was recommended by Diao et al.[34] We recommend that the HJ loop should be shorter and individualised according to the patient age to avoid its twist, adhesion and stasis of bile.

The biggest advantage of HD in LC, which was overlooked in the era of open surgery, and got the special consideration was the ease of the anastomosis in laparoscopy, reduced operative time and future endoscopic access; these led to the reinvention of its role in LC.[35] The debates surrounded the biliary reconstruction between HJ versus HD and the critics of HD questioned it for its high incidence of bile reflux predisposing to gastritis, cholangitis and potentially higher on-going risk of cholangiocarcinoma. The real impact of bile reflux in terms of clinical relevance did not get much space in the medium-term follow-up studies.[36] Most reports of intrahepatic carcinoma after complete excision of CC are associated with intrahepatic ductal dilation, stones, strictures, and/or recurrent cholangitis despite a Roux-en-Y HJ reconstruction in several cases, suggesting a high possibility of field-risk as a determinant of future malignancy rather than the type of reconstruction.[13]

In the authors' view, HJ and HD are equally good options, while in place of HJ, HD provides added advantage of its simplicity, reduced operative duration and future endoscopic access for IHS/stricture management. However, long-term assessment is awaited before we reach a conclusion and settle this debate.


  Intrahepatic Stones in Choledochal Cyst: Seeing the Unseen? Top


The identification and management of IHS associated with CC are challenging. The reported incidence of post-operative IHSs varies between 2.7% and 10.7%, and their formation has been reported to occur between 3 and 20 years after CC excision.[15],[37],[38] The causes of post-operative IHSs are usually missed/residual debris/stones, missed intrahepatic biliary duct (IHBD) stenosis, biliary stasis due to stricture of the anastomosis or congenitally dilated IHBD. Advanced imaging procedures, such as virtual endoscopy and per-operative cholangioscopy, are recommended by many authors to identify IHSs and IHBD stenosis associated with CC, so their simultaneous management can be done.[39],[40] As we have understood that post-operative IHS are not real post-operative stones and are avoidable to a large extent, the use of paediatric size cystoscope/ureteroscope for routine per-operative 'pre-emptive' cholangioscopy is advocated by few authors which allow identification of IHS and intrahepatic bile duct stenosis followed by their redressal. Intraoperative cholangioscopy using a paediatric cystoscope has been described by Takahashi et al., and Agrawal et al., for irrigating and clearing IHBD debris, stones, and dilatation of stenosis during CC surgery which can reduce incidence of post-operative IHS.[41],[42],[43]

Routine intraoperative thorough irrigation of proximal and distal ends of CC plus pre-emptive cholangioscopy and hepatic dichotomy in case of stenosis avoids residual stones and can reduce incidence of post-operative stones. This step has been elaborated in the technique described by the authors.

The management of post-operative IHS is always challenging. As we discussed before, even though R-en-Y HJ is considered as the gold standard for reconstruction after CC excision, recent literature has rekindled the popularity of HD over R-en-Y HJ.[34],[44] Here, lies the significance of HD over HJ due to easy endoscopic access to the anastomosis, ease of endoscopic retrograde cholangiography, access to a non-dilated system for retrieval of recurrent stones and dilatation of IHBD stenosis.[45] Other therapeutic modalities for post-operative IHSs include extracorporeal shock wave lithotripsy, percutaneous transhepatic cholangioscopic lithotomy, double-balloon endoscopy, Roux-en-Y limb enterotomy and rarely revision hepaticoenterostomy and even liver resection.[46],[47]


  Malignancy in Choledochal Cyst: Is it a Problem Anymore in the Era of Complete Excision? Top


Malignancies develop in 25%–26% of patients with CC.[48] It is speculated that prolonged reflux of pancreatic secretions into the biliary tract occurs in Todani Types I and IV, which frequently present with abnormal pancreaticobiliary duct junctions.[7] The situation is different in Types II and III choledochal malformations, which might be true congenital malformations in which reflux is absent.[49] A systematic review conducted by Ten Hove et al. established above facts and complete cyst excision followed by the construction of a bilio-enteric anastomosis is therefore recommended to protect the patient from developing malignancy, while a drainage procedure like cystojejunostomy is disregarded as it is associated with a higher incidence of malignancy. The evidence is enough to suggest that chances of developing malignancy in CC after complete excision is negligible and no screening is recommended.[50]


  Long-Term Outcome After Laparoscopic Cystectomy in Low and Middle-Income Countries: What Is the Level of Evidence? Top


Outcomes from Vietnam

From January 2007 to October 2012, 547 patients with CC underwent conventional LC at the National Children Hospital, Hanoi, Vietnam, and 353 patients with the removal of dilated choledochus plus HD and 194 with the removal of dilated choledochus plus HJ. The mean operative time for HD and HJ was 156 ± 47 min and 210 ± 56 min, respectively. Conversion to open surgery was required in two patients. Intraoperative complications included the transection of two hepatic ducts in three patients, perforation of the right portal vein in one patient, and perforation of the right hepatic duct in another. The repair was successful in all patients through laparoscopy. Early postoperative complications included biliary fistula in nine patients (1.6%), with one patient requiring reoperation. Pancreatic fistula occurred in five patients (0.9%). No patients required reoperation. The mean post-operative hospital stay was 6.2 ± 0.3 days for HD and 6.6 ± 0.5 days for HJ. Follow-up from 1 to 57 months was obtained in 453 patients. Eight patients had cholangitis (1.4%), six patients in the HD group (2%) and two patients in the HJ group (1.3%). The rate of gastritis due to bilious reflux in HD group was 6.8%. Three patients required reoperation, two due to anastomotic stricture and another due to stenosis at the bifurcation of hepatic ducts.[51]

From September 2012 to December 2013, 86 patients received single incision LC. HJ was performed in 84 cases and HD in two cases. Additional trocars were needed in just 1.2% of cases. There was no conversion to open surgery. The median operative time was 195 min. There was no anastomotic leakage. Mild umbilical infection was noted in 2.3%. The median postoperative hospital stay was 5 days. At a follow-up of 4–18 months, one patient needed a redo surgery for anastomotic stenosis; all other patients were in good health.[26] Between February 2013 and August 2016, 39 patients underwent robotic-assisted surgery for CC. The mean patient age was 40.2 months (range 5–108 months). The mean operating time was 192.7 min (range 150–330 min). There were no intraoperative complications; no conversions to laparoscopic or open surgery; and no post-operative complications, including cholangitis, cholelithiasis or anastomotic stenosis.[29]

Outcomes from the Philippines and other parts of Asia

In a 14-year retrospective cohort study of Guzman et al., 122 patients underwent CC excision with biliary-enteric reconstruction at the Philippine Children's Medical Center, of which 68 (56%) HD and 54 (44%) HJ (Roux en Y). Only three cases were done laparoscopically with HD repair, with the majority cases were done by the open technique. Although there was no report of the size of the fusiform (Type I) CCs encountered during the study, it is very common among Filipinos to have a late diagnosis thus with a big cyst size and perhaps not amenably safe for a laparoscopic approach.[52]

Laparoscopic CC excision and repair has so much room for improvement in the Philippines. It may be facilitated further by an early diagnosis of CC among Filipino children, as most of the diagnosed cases are considered late with cyst sizes extremely large. In other parts of the developing world like India, the incidence of CC is not very high. The surprising fact revealed from Indian studies is up to 50% of CC undergoing LC belonged to adulthood which was mostly diagnosed incidentally.[53] Overall, long-term outcomes after eliminating the learning curve issue are no different for laparoscopy with higher radiological evidence of contrast reflux into the biliary tree in HD which has little clinical implications.[36],[44]


  Can Laparoscopic Cystectomy Be the New Gold Standard for Choledochal Cyst? Top


From its first description in 1994, LC is routinely performed in many centres from east to west. We found 85 original articles published on Medline with 3455 patients who underwent laparoscopic operations. Different questions need to be answered before LC can be considered as a new gold standard approach for CC.

First, is laparoscopic operation feasible for choledochal cyst?

The published data demonstrated that LC is feasible. The rate of conversion to operation surgery is minimal which is documented by centres with a small volume of patients or who are at the beginning of the learning curve.

Second, is the laparoscopic approach safe?

That is the main concern for surgeons who are used to perform an open operation. Results from publications showed that this approach is safe and the complications are as low as in open operation or even lower. In a meta-analysis of 1408 patients (611 in the laparoscopic operation group, 797 in the open operation group) from 7 studies showed that the incidences of complications including intra-abdominal fluid collection, anastomotic stenosis, bile leak, IHS formation, intrahepatic reflux, cholangitis, pancreatic leak, pancreatic calculi formation, pancreatitis, adhesive intestinal obstruction, Roux loop obstruction and gastrointestinal bleeding were similar. The LC group had a significantly lower rate in intraoperative blood transfusion, re-intervention and adhesive intestinal obstruction. Only one disadvantage of LC is longer operation time. However, it had a shorter duration of recovery of bowel function and hospital stay.[54]

Third, Is it reproducible and easy to teach?

The learning curve of minimum 37 cases is essential for a safe surgery and it has been shown that with a learning curve of 67 cases surgery-specific outcome improves remarkably.[55]


  Conclusion Top


LC is a state of the art procedure for CC in children. The high volume centres perform LC from trainer to trainee levels and have decoded the procedure along with its nuances, quite well. Given the trifecta of qualities – feasibility, safety and reproducibility – LC can be considered as the gold standard for CCs.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]



 

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2004 Journal of Minimal Access Surgery
Published by Wolters Kluwer - Medknow
Online since 15th August '04