ORIGINAL ARTICLE

Laparoscopic Cholecystectomy in the Pediatric Population: A Single-center Experience Moiz M. Zeidan, MBBS, T.K. Pandian, MD, Khalid A. Ibrahim, MBBS, Christopher R. Moir, MD, Michael B. Ishitani, MD, and Abdalla E. Zarroug, MD, FACS, FAAP

Objective: We aimed to review our experience with laparoscopic cholecystectomy in the pediatric population to better understand the associated complications and outcomes. Methods: We performed a retrospective chart review of children below 18 years of age who underwent laparoscopic cholecystectomy at a single academic institution between the years 1990 and 2010. Results: Of the 325 cases of cholecystectomy, 202 (62.2%) were performed laparoscopically. The primary indication for surgery was symptomatic cholelithiasis (45.5%, n = 92). Preoperative endoscopic retrograde cholangiopancreatography (ERCP) was performed in 25 (12.4%) patients. Variations in anatomy and technical difficulties (eg, presence of adhesions) were observed in 45 (22.3%) patients. Intraoperative cholangiogram was performed in 20 (9.9%) patients and 16 (7.9%) underwent concomitant splenectomy. Only 8 (4%) of the cases were converted to an open approach because of lack of anatomic clarity. There were zero common bile duct injuries; however, spillage of bile was present in 12 (5.9%) patients. Postoperative complications including wound infection, retained stones, abdominal abscess, and biloma, were observed in 9 patients (4.5%). The median operative time was 117.5 minutes. The median postoperative hospital stay was 1 day. Nineteen (9.4%) patients had recurrence of abdominal pain without associated pathology. Three patients (1.5%) required postoperative ERCP. The average follow-up period was 54 months. Conclusions: Laparoscopic cholecystectomy in the pediatric population results in short postoperative hospital stay and has low complication rates. In particular, zero bile duct injuries were noted. Key Words: laparoscopic, cholecystectomy, pediatric, bile duct

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significant role in the formation of gallbladder stones.3 Less common etiologies include metabolic disorders, immunoglobulin deficiency, opioids, ceftriaxone, furosemide, parenteral nutrition, and premature birth.4–7 Laparoscopic cholecystectomy was first performed in adults in 1989.8,9 Although no major randomized controlled trials have been performed, it currently is the gold standard for gallbladder removal. Similar to adults, laparoscopic cholecystectomy performed in children has proven to result in short postoperative hospital stay and has low complication rates10,11 in a few small studies. In addition, it is superior to traditional open cholecystectomy in terms of cosmesis, analgesic requirement, and respiratory-associated morbidity.12 However, because of the relative infrequency of gallbladder pathology in children compared with adults, there is a paucity of data on the laparoscopic approach in the nonadult population. In this study, we aimed to review our experience with laparoscopic cholecystectomy in children, to better understand the associated complications and outcomes.

METHODS We performed an IRB approved, HIPAA compliant retrospective chart review of children below 18 years of age who underwent cholecystectomy at a single, academic institution between the years 1990 and 2010. Data categories analyzed included patient demographics, clinical history, indication for cholecystectomy, imaging studies, operative time and technique, pathologic diagnosis, complications, and recovery. The medical record of each patient was reviewed for this information. Data analysis was performed only on patients who underwent laparoscopic cholecystectomy. All cases in which the laparoscopic method was the initial approach were included.

C

holelithiasis and other gallbladder diseases requiring cholecystectomy are less common in children compared with adults. Recently, however, rising rates of obesity in the pediatric population have led to a rise in gallbladder pathology.1,2 Studies have suggested prevalence rates between 0.1% and 0.6% in children and adolescents.1,2 Sickle cell disease is considered to be the most important cause of cholelithiasis in children.3 Other hematological diseases such as spherocytosis, elliptocytosis, stomatocytosis, thalassemia, and hemoglobin C disease, also play a

Received for publication April 27, 2013; accepted July 11, 2013. From the Department of Surgery, Division of Pediatric Surgery, Mayo Clinic, Rochester, MN. The authors declare no conflicts of interest. Reprints: Abdalla E. Zarroug, MD, FACS, FAAP, Department of Surgery, Division of Pediatric Surgery, Mayo Clinic, 200 First Street, SW, Rochester, MN 55905 (e-mail: zarroug.abdalla@ mayo.edu). Copyright r 2014 by Lippincott Williams & Wilkins

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RESULTS Our search yielded a total of 325 cases of cholecystectomy during the study period. Of these, 202 (62.2%) were performed laparoscopically. The open approach was utilized more frequently in the early study period (56.5%, between the years 1990 and 1995); however, the laparoscopic approach became more common with every 5-year advancement (69.3%, between the years 2006 and 2010). The majority (89%) of open cases were combined procedures and included operations such as liver transplantation, liver resection, pancreaticoduodenectomy, and gastric bypass. Demographics and clinical history for our laparoscopic cohort are included in Table 1. The majority of our patients were girls (72.3%, n = 146) with a median age of 162 months (13.5 y). Nearly all patients were white (75%, n = 149). The median body mass index was 23.4 kg/m2 (range, 12.9 to 47.6 kg/m2). Table 2 displays the characterization of gallbladder stones.

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The primary indication for surgical intervention was symptomatic cholelithiasis (45.5%, n = 92). Other indications included the diagnoses of cholecystitis (n = 14), biliary colic (n = 15), gallbladder polyps (n = 1), and biliary dyskinesia (n = 2). Preoperative endoscopic retrograde cholangiopancreatography (ERCP) was performed in 25 (12.4%) patients because of suspicion of common bile duct stones. Variations in anatomy and technical difficulties (eg, presence of adhesions) were observed in 45 (22.3%) patients. Only a small minority (12.4%, n = 25) of patients had any previous abdominal surgical history. Intraoperative cholangiogram was performed in 20 (9.9%) patients and 16 (7.9%) underwent concomitant splenectomy. Only 8 (4%) of the cases were converted to an open approach because of lack of anatomic clarity. There were 0 common bile duct injuries; however, spillage of bile was present in 12 (5.9%) patients. Postoperative complications including wound infection (n = 4), retained stones (n = 4), abdominal abscess (n = 1), and biloma (n = 0), were observed in 9 patients (4.5%). The median operative time was 117.5 minutes. The median postoperative hospital stay was 1 day, and 19 (9.4%) patients had recurrence of abdominal pain without associated pathology. Three patients (1.5%) required postoperative ERCP because of retained stones. In our cohort, the average follow-up period was 54 months.

DISCUSSION Recently, the number of laparoscopic cholecystectomies performed in the pediatric population has been on the rise. This has been largely linked to the increasing prevalence of cholelithiasis in children.2 In the adult population, cholecystectomy is performed laparoscopically in >90% of patients.13 The laparoscopic approach is employed in >80% of children on the basis of a 2006 study using the National Inpatient Sample data.14 Although we demonstrate a lower rate of laparoscopic cholecystectomy at our institution (62%), we attribute this to the very large number of open cases we perform in a combined (89%) manner (liver transplant, liver resection,

TABLE 1. Patient Characteristics

n (%) Age (mo) Body mass index (BMI) (kg/m2) Sex Male Female Race/ethnicity White Black/African American Hispanic Others Presence of comorbidities Surgical history Abdominal Others Total bilirubin on admission (mg/dL)* Amylase on admission (U/L)w

Range

163.2 23.4

6-216 12.9-47.6

1.5

0.2-22.8

94.4

18-1184

56 (27.7) 146 (72.3) 149 4 9 5 52

(75) (2) (5) (3) (25.7)

25 (12.4) 32 (15.8)

*Reference range: 0.1 to 1.0 mg/dL. wReference range: 0 to 6 U/L.

r

Mean

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Laparoscopic Cholecystectomy in the Pediatric Population

TABLE 2. Type of Stone by Percentage

% Mixed Pigment Cholesterol Sludge No abnormalities

45 18 15 5 17

pancreaticoduodenectomy, etc.) and a relatively small patient sample. In our series, symptomatic cholelithiasis was the primary indication for surgery in nearly half (45.5%) of the patients, which is consistent with rates of 23% to 52% reported in other series.10 There is at least 1 single-institution study, however, in which the most common indication for cholecystectomy was biliary dyskinesia.15 It is still unclear what specific etiologies are contributing to the pediatric gallbladder disease burden. Risk factors for the development of gallbladder stones in adults include female sex, age, obesity, and family history. Of these, female sex is one of the largest contributors. In our cohort, 72.3% (n = 146) of the patients who underwent laparoscopic cholecystectomy were female. Other analyses found a more balanced distribution between sexes16–18 in the pediatric population. With respect to family history, our data showed only 31 (15.3%) patients with a positive family history of gallbladder stones or biliary diseases. Studies on obese individuals have demonstrated increased cholesterol saturations in bile, which can lead to the formation of cholesterol stones.19 In children, pigment stones are still more common, mainly because of the higher prevalence of hemoglobinopathies such as sickle cell disease.20 The majority of our patients had mixed or pigment stones and findings of cholesterol stones did not differ between normal, overweight, and obese individuals. Gallbladder sludge is also frequently reported with sickle cell anemia; therefore, elective cholecystectomy has been recommended when evidence suggests the presence of sludge.21 In this cohort, ERCP was performed in 25 (12.4%) patients because of suspected common bile duct stones. Intraoperative cholangiogram was performed in 20 (9.9%) patients. Only 3 patients (1.5%) required postoperative ERCP. Although pediatric intraoperative cholangiography and ERCP are not widely available techniques for the diagnosis and removal of common bile duct stones outside of major centers, we used them successfully on a case-bycase basis. Previous studies do not recommend routine intraoperative cholangiography because of the low incidence of subclinical common bile duct stones in children.10,22–25 Previously, our institution has published studies on the safety of ERCP in the pediatric population and overall, we favored preoperative ERCP and/or intraoperative cholangiogram for the management of suspected preoperative choledocholithiasis.26 Overall, our intraoperative and postoperative complication rates were low. The most common intraoperative complications were bile spillage (5.9%) and conversion to an open procedure (4.0%). Our study reported no common bile duct injuries; this continues to be a rare complication from this procedure.11,27 The most common postoperative complications were wound infections and retained stones. Although the profile of complications in the pediatric www.surgical-laparoscopy.com |

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laparoscopic cholecystectomy has not been thoroughly delineated in the literature, our rates are similar to those described in previous studies.11,15,27,28 We also noted that despite an average of 10 laparoscopic cholecystectomies per year over 20 years, in our practice bile duct injury rate was zero. Despite relatively low numbers of this specific procedure, we conclude that pediatric surgeons can perform this procedure with minimal morbidity. Our review has a number of limitations. First, this is a retrospective review with inherent biases. Second, this is a tertiary hospital with referral biases and this manuscript may not be reflective of other practices. Third, analysis over a large time period introduces the potential for a skewed view of clinical practice as it evolves over time, resulting in information bias. However, there remain no randomized controlled studies for evaluating laparoscopic pediatric cholecystectomy and therefore our cohort, even with its limitations, adds to the literature that pediatric laparoscopic cholecystectomy remains safe. In particular, our lack of bile duct injuries over 20 years attests to the safety of the procedure. To date, there are a number of small-sized to moderate-sized case series that describe single-institution experiences with laparoscopic cholecystectomy. Our postoperative rate of recurrent abdominal pain without associated pathology (9.4%) continues to plague pediatric surgeons, especially with regard to patients with biliary dyskinesia. Although our study and others have shown favorable results with this procedure in the pediatric population, larger, prospective, randomized trials are required to truly elucidate which patient will or will not benefit from gallbladder removal, no matter how safe it remains. In addition, with the rising incidence of obesity, further evaluation is needed to better assess the impact of risk factors associated with gallbladder pathology in children. Although our cohort did not include single-site procedures, future emphasis should also be placed on the single-site approach to ensure continued safety, as this technique is growing in popularity with respect to the pediatric population.29

CONCLUSIONS Laparoscopic cholecystectomy in the pediatric population is a safe procedure that results in short postoperative hospital stay with low complication rates. No common bile duct injuries were reported in our cohort of over 200 patients in 20 years. In our follow-up of 4.5 years, approximately 9% still had some abdominal pain without associated pathology. Further studies are required to elucidate which pediatric patient will benefit the most from gallbladder removal. REFERENCES 1. Kaechele V, Wabitsch M, Thiere D, et al. Prevalence of gallbladder stone disease in obese children and adolescents: influence of the degree of obesity, sex, and pubertal development. J Pediatr Gastroenterol Nutr. 2006;42:66–70. 2. Garey CL, Laituri CA, Keckler SJ, et al. Laparoscopic cholecystectomy in obese and non-obese children. J Surg Res. 2010;163:299–302. 3. Curro G, Meo A, Ippolito D, et al. Asymptomatic cholelithiasis in children with sickle cell disease: early or delayed cholecystectomy? Ann Surg. 2007;245:126–129. 4. Angelico M, Gandin C, Canuzzi P, et al. Gallstones in cystic fibrosis: a critical reappraisal. Hepatology. 1991;14:768–775. 5. Bunyapen C, Howell CG, Kanto WP Jr. Cholecystitis in a preterm infant. Clin Pediatr (Phila). 1986;25:96–97.

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6. Danon YL, Dinari G, Garty BZ, et al. Cholelithiasis in children with immunoglobulin A deficiency: a new gastroenterologic syndrome. J Pediatr Gastroenterol Nutr. 1983;2:663–666. 7. Stabile A, Ferrara P, Marietti G, et al. Ceftriaxone-associated gallbladder lithiasis in children. Eur J Pediatr. 1995;154:590. 8. Dubois F, Icard P, Berthelot G, et al. Coelioscopic cholecystectomy. Preliminary report of 36 cases. Ann Surg. 1990; 211:60–62. 9. Reddick EJ, Olsen DO. Laparoscopic laser cholecystectomy. A comparison with mini-lap cholecystectomy. Surg Endosc. 1989;3:131–133. 10. Gowda DJ, Agarwal P, Bagdi R, et al. Laparoscopic cholecystectomy for cholelithiasis in children. J Indian Assoc Pediatr Surg. 2009;14:204–206. 11. St Peter SD, Keckler SJ, Nair A, et al. Laparoscopic cholecystectomy in the pediatric population. J Laparoendosc Adv Surg Tech. Part A. 2008;18:127–130. 12. Davenport M. Laparoscopic surgery in children. Ann R Coll Surg Engl. 2003;85:324–330. 13. Kaafarani HM, Smith TS, Neumayer L, et al. Trends, outcomes, and predictors of open and conversion to open cholecystectomy in Veterans Health Administration hospitals. Am J Surg. 2010;200:32–40. 14. Balaguer EJ, Price MR, Burd RS. National trends in the utilization of cholecystectomy in children. J Surg Res. 2006; 134:68–73. 15. Siddiqui S, Newbrough S, Alterman D, et al. Efficacy of laparoscopic cholecystectomy in the pediatric population. J Pediatr Surg. 2008;43:109–113; discussion 113. 16. Reif S, Sloven DG, Lebenthal E. Gallstones in children. Characterization by age, etiology, and outcome. Am J Dis Child. 1991;145:105–108. 17. Kumar R, Nguyen K, Shun A. Gallstones and common bile duct calculi in infancy and childhood. Aust N Z J Surg. 2000;70:188–191. 18. Henschke CI, Teele RL. Cholelithiasis in children: recent observations. J Ultrasound Med. 1983;2:481–484. 19. Bennion LJ, Grundy SM. Effects of obesity and caloric intake on biliary lipid metabolism in man. J Clin Invest. 1975;56:996–1011. 20. Suell MN, Horton TM, Dishop MK, et al. Outcomes for children with gallbladder abnormalities and sickle cell disease. J Pediatr. 2004;145:617–621. 21. Winter SS, Kinney TR, Ware RE. Gallbladder sludge in children with sickle cell disease. J Pediatr. 1994;125(pt 1):747–749. 22. Williams GL, Vellacott KD. Selective operative cholangiography and perioperative endoscopic retrograde cholangiopancreatography (ERCP) during laparoscopic cholecystectomy: a viable option for choledocholithiasis. Surg Endosc. 2002; 16:465–467. 23. Tham TC, Lichtenstein DR, Vandervoort J, et al. Role of endoscopic retrograde cholangiopancreatography for suspected choledocholithiasis in patients undergoing laparoscopic cholecystectomy. Gastrointest Endosc. 1998;47:50–56. 24. Prasil P, Laberge JM, Barkun A, et al. Endoscopic retrograde cholangiopancreatography in children: a surgeon’s perspective. J Pediatr Surg. 2001;36:733–735. 25. Mah D, Wales P, Njere I, et al. Management of suspected common bile duct stones in children: role of selective intraoperative cholangiogram and endoscopic retrograde cholangiopancreatography. J Pediatr Surg. 2004;39:808–812; discussion 808-12. 26. Iqbal CW, Baron TH, Moir CR, et al. Post-ERCP pancreatitis in pediatric patients. J Pediatr Gastroenterol Nutr. 2009;49:430–434. 27. Raval MV, Lautz TB, Browne M. Bile duct injuries during pediatric laparoscopic cholecystectomy: a national perspective. J Laparoendosc Adv Surg Tech. Part A. 2011;21:113–118. 28. Esposito C, Alicchio F, Giurin I, et al. Lessons learned from the first 109 laparoscopic cholecystectomies performed in a single pediatric surgery center. World J Surg. 2009;33:1842–1845. 29. Garey CL, Laituri CA, Ostlie DJ, et al. Single-incision laparoscopic surgery in children: initial single-center experience. J Pediatr Surg. 2011;46:904–907. r

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Laparoscopic cholecystectomy in the pediatric population: a single-center experience.

We aimed to review our experience with laparoscopic cholecystectomy in the pediatric population to better understand the associated complications and ...
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