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Laparoscopic cholecystectomy for symptomatic cholelithiasis in children and adolescents: analysis of 50 cases from a single institution

ABSTRACT

Purpose:

To investigate the clinical characteristics of symptomatic cholecystolithiasis and laparoscopic cholecystectomy complications in pediatric patients.

Methods:

The medical records of 50 children and adolescents who underwent laparoscopic cholecystectomy were analyzed. We evaluated gender, age, body mass index, preoperative clinical aspects, perioperative complications, and gallstone composition.

Results:

Among the patients, 33 (66%) were female, and 17 (34%) were male. The mean age was 11.4 ± 3.6. All patients were diagnosed with cholecystolithiasis by abdominal ultrasonography. Twelve patients (24%) had hematological disease: eight (16%) with sickle cell anemia and four (8%) with hereditary spherocytosis. Thirteen patients (26%) were obese. Twelve patients (24%) had complicated biliary disease. During the intraoperative period, three patients (6%) had excessive bleeding in the hepatic hilum, and one had an accidental injury to the common bile duct. Three (6%) postoperative complications (acute pancreatitis, common bile duct stenosis, and intestinal obstruction) were observed. Among 28 patients (56%), 25 (50%) had cholesterol gallstones, and three (6%) had bile pigment gallstones.

Conclusions:

The evolution of cholecystolithiasis in the pediatric population can present serious complications, emphasizing the need to avoid temporizing cholecystolithiasis in children and adolescents because laparoscopic cholecystectomy in this group is safe, with low complication rates.

Key words
Cholecystolithiasis; Cholecystectomy, Laparoscopic; Cholecystectomy; Child; Pediatric Obesity

Introduction

Cholecystolithiasis is a rare pediatric disease with a prevalence between 0.13 and 1.9%11 Gao K, Zheng C, Han H, Guo C. A Multicenter Randomized Prospective Study of Early Cholecystectomy for Pediatric Patients with Biliary Colic. J Gastrointest Surg. 2021;25(3):713–9. https://doi.org/10.1007/s11605-020-04700-9
https://doi.org/10.1007/s11605-020-04700...
. About 80% of pediatric patients with gallstones in the gallbladder remain asymptomatic during their lifetimes22 Doud A, Bond L, Downard C, Vitale G, Fallat M, Foley D, Wright T, Bond S. Management of complicated biliary disease in the pediatric population. Surgery. 2022;171(3):736–40. https://doi.org/10.1016/j.surg.2021.09.041
https://doi.org/10.1016/j.surg.2021.09.0...
44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. .

The increase in the incidence of cholecystolithiasis in the pediatric population was registered in studies carried out in the last three decades55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. 77 Greer D, Heywood S, Croaker D, Gananadha S. Is 14 the new 40: trends in gallstone disease and cholecystectomy in Australian children. Pediatr Surg Int. 2018;34(8):845–9. https://doi.org/10.1007/s00383-018-4300-y
https://doi.org/10.1007/s00383-018-4300-...
. The increased awareness of gallbladder disease as a cause of abdominal pain in children may be associated with the growing use of abdominal ultrasonography, consequently improving the diagnosis of cholecystolithiasis33 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. . However, in clinical practice, the diagnosis and treatment of this condition in children and adolescents are based on studies of small populations33 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. .

Although hemolytic diseases (sickle cell anemia, hereditary spherocytosis, and thalassemia) have been identified as risk factors, the prevalence of pediatric cholecystolithiasis has increased proportionally with the recent childhood obesity epidemic88 Frybova B, Drabek J, Lochmannova J, Douda L, Hlava S, Zemkova D, Mixa V, Kyncl M, Zeman L, Rygl M, Keil R. Cholelithiasis and choledocholithiasis in children; risk factors for development. PLoS One. 2018;13(5):e0196475. https://doi.org/10.1371/journal.pone.0196475
https://doi.org/10.1371/journal.pone.019...
,99 Tian Y, Ingram MCE, Raval M V. National Trends and Disparities in the Diffusion of Laparoscopic Surgery for Children in the United States. J Laparoendosc Adv Surg Tech. 2021;31(9):1061–6. https://doi.org/10.1089/lap.2021.0013
https://doi.org/10.1089/lap.2021.0013...
. The most likely cause for this increase in cholecystolithiasis in children and adolescents would be the rise in this population’s mean body mass index (BMI)66 Sarrami M, Ridley W, Nightingale S, Wright T, Kumar R. Adolescent gallstones—need for early intervention in symptomatic idiopathic gallstones. Pediatr Surg Int. 2019;35(5):569–74. https://doi.org/10.1007/s00383-019-04461-w
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,1010 Liebe HL, Phillips R, Handley M, Gastanaduy M, Burton JH, Roybal J. A pediatric surgeon’s dilemma: does cholecystectomy improve symptoms of biliary dyskinesia? Pediatr Surg Int. 2021;37(9):1251–7. https://doi.org/10.1007/s00383-021-04922-1
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,1111 Tannuri ACA, Leal AJG, Velhote MCP, Gonlçalves MEP, Tannuri U. Management of gallstone disease in children: a new protocol based on the experience of a single center. J Pediatr Surg. 2012;47(11):2033–8. https://doi.org/10.1016/j.jpedsurg.2012.06.010
https://doi.org/10.1016/j.jpedsurg.2012....
, with a third of children being overweight or obese, which is considered the cause of most cholecystectomies performed in pediatric patients1212 Diez S, Müller H, Weiss C, Schellerer V, Besendörfer M. Cholelithiasis and cholecystitis in children and adolescents: Does this increasing diagnosis require a common guideline for pediatricians and pediatric surgeons? BMC Gastroenterol. 2021;21(1):186. https://doi.org/10.1186/s12876-021-01772-y
https://doi.org/10.1186/s12876-021-01772...
. Other reasons for cholecystolithiasis have included a cholesterol-rich diet, cephalosporins, total parenteral nutrition, sepsis, congenital heart disease, prematurity, and intestinal malabsorption11 Gao K, Zheng C, Han H, Guo C. A Multicenter Randomized Prospective Study of Early Cholecystectomy for Pediatric Patients with Biliary Colic. J Gastrointest Surg. 2021;25(3):713–9. https://doi.org/10.1007/s11605-020-04700-9
https://doi.org/10.1007/s11605-020-04700...
.

Laparoscopic cholecystectomy (LC) has gradually become the primary technique for treating symptomatic gallstones in children55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. . Compared with open cholecystectomy, LC has several advantages, including less postoperative pain, an earlier recovery period, a quicker return to unrestricted activities, and better cosmetic outcomes33 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,99 Tian Y, Ingram MCE, Raval M V. National Trends and Disparities in the Diffusion of Laparoscopic Surgery for Children in the United States. J Laparoendosc Adv Surg Tech. 2021;31(9):1061–6. https://doi.org/10.1089/lap.2021.0013
https://doi.org/10.1089/lap.2021.0013...
. LC is considered a safe procedure with a low rate of complications. In adults, injury to the bile duct occurs in 0.85% of cases, but in children and adolescents no index has been defined1313 Treider M, Ohnesorge S, Bjørnland K. Few serious complications after cholecystectomy in paediatric patients. Acta Paediatr. 2020;109(3):630–1. https://doi.org/10.1111/apa.15081
https://doi.org/10.1111/apa.15081...
,1414 Babb J, Davis J, Tashiro J, Perez EA, Sola JE, Pandya S. Laparoscopic Versus Open Cholecystectomy in Pediatric Patients: A Propensity Score-Matched Analysis. J Laparoendosc Adv Surg Tech. 2020;30(3):322–7. https://doi.org/10.1089/lap.2019.0655
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. The most frequent causes of bile duct injury are inadequate exposure to the surgical field and failure to identify the hepatic hilum structures. Furthermore, acute or chronic gallbladder inflammation, obesity, anatomical variations, and bleeding also predispose patients to accidental injuries of the biliary tree during the surgical procedure, both in children and adults1313 Treider M, Ohnesorge S, Bjørnland K. Few serious complications after cholecystectomy in paediatric patients. Acta Paediatr. 2020;109(3):630–1. https://doi.org/10.1111/apa.15081
https://doi.org/10.1111/apa.15081...
,1414 Babb J, Davis J, Tashiro J, Perez EA, Sola JE, Pandya S. Laparoscopic Versus Open Cholecystectomy in Pediatric Patients: A Propensity Score-Matched Analysis. J Laparoendosc Adv Surg Tech. 2020;30(3):322–7. https://doi.org/10.1089/lap.2019.0655
https://doi.org/10.1089/lap.2019.0655...
.

Cholecystectomy is a surgical procedure not often performed in pediatric patients. Pediatric surgeons face difficulty gaining experience in this operation, which can have serious complications1515 Lee YJ, Park YS, Park JH. Cholecystectomy is Feasible in Children with Small-Sized or Large Numbers of Gallstones and in Those with Persistent Symptoms Despite Medical Treatment. Pediatr Gastroenterol Hepatol Nutr. 2020;23(5):430–8. https://doi.org/10.5223/pghn.2020.23.5.430
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16 Gupta V, Jain G. Safe laparoscopic cholecystectomy: Adoption of universal culture of safety in cholecystectomy. World J Gastrointest Surg. 2019;11(2):62–84. https://doi.org/10.4240/wjgs.v11.i2.62
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17 Suh SG, Choi YS, Park KW, Lee SE. Pediatric cholecystectomy for symptomatic gallstones unrelated to hematologic disorder. Ann Hepato-Biliary-Pancreatic Surg. 2016;20(4):187–90. https://doi.org/10.14701/ahbps.2016.20.4.187
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18 Kılıç ŞS, Özden Ö, Çolak ST. Comparative analysis of reliability and clinical effects of the critical view of safety approach used in laparoscopic cholecystectomy in the pediatric population. Pediatr Surg Int. 2021;37(6):737–43. https://doi.org/10.1007/s00383-021-04869-3
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-1919 Bhaumik K. Asymptomatic cholelithiasis in children: Management dilemma. J Indian Assoc Pediatr Surg. 2021;26(4):228–33. https://doi.org/10.4103/jiaps.JIAPS_107_20
https://doi.org/10.4103/jiaps.JIAPS_107_...
.

In this study, we retrospectively reviewed the clinical and sonographic data, histopathological findings, and the outcomes in patients with symptomatic cholecystic disease who underwent LCs.

Methods

The present study was conducted in accordance with the ethical principles of the Declaration of Helsinki and its amendments, and it was approved on December 22, 2020, by the institution’s Research Ethics Committee (Comitê de Ética e Pesquisa em Seres Humanos of the Centro Universitário of the Faculdade de Medicina do ABC, number 4.482.005).

This study is retrospective, cross-sectional, and descriptive, involving the medical records of 50 patients of both sexes aged younger than 18 years old, with symptomatic cholelithiasis, who underwent LC at the Pediatric Surgery Unit of Hospital Estadual Mário Covas (Santo André, SP, Brazil), from August 2008 to August 2019.

The primary outcome aimed to investigate the clinical characteristics and treatment of children and adolescents with symptomatic cholecystolithiasis undergoing LC at a single institution. The second outcome was to study the results of LC in children and adolescents with symptomatic cholecystolithiasis.

Routine demographic and clinical data were collected for all patients, including documented comorbidities. The clinical diagnoses of the cases included in this study were determined and classified into nonacute and acute conditions. Nonacute pathologies include biliary dyskinesia, symptomatic cholelithiasis, and others. Acute pathologies include cholecystitis and gallstone pancreatitis/choledocholithiasis. There were no cases of asymptomatic cholelithiasis. The cases of patients operated on for any other condition, such as polyps, abdominal trauma, transplantation, incidental cholecystectomy, or open cholecystectomy, or those aged 18 years old or older were not included in this series. A single surgeon performed all cases. Indication for intraoperative cholangiogram during this period was based on findings at an immediate preoperative ultrasound scanning (biliary dilatation or choledocholithiasis) or if a biliary duct anomaly was suspected but unable to be defined by magnetic resonance cholangiopancreatography (MRCP).

The indication for intraoperative cholangiogram during this period was based on findings at an immediate preoperative ultrasound scanning (the presence of biliary dilatation or the presence of choledocholithiasis) or if a biliary duct anomaly was suspected but unable to be defined by MRCP. The LC surgical procedure was performed with the standard four-port surgical approach with trans-umbilical open access, three trocars (two operative and one accessory), the cystic artery, and ligation of the duct with non-absorbable polymer clips (knots or Hem-o-lok clip), and the gallbladder removal through the umbilical access. A single surgeon performed all cases.

The variables studied were sex, age, BMI, hematological disease, and gallstone type (cholesterol or bile pigment). The BMI × age curve (z score) from the World Health Organization was adopted to determine whether a patient was obese or not. Patients with a z score greater than 3 were considered obese. The type of gallstone was identified in the anatomopathological examination report of the surgical specimen.

Considering the nature of the samples, quantitative variables were represented by absolute (n) and relative (%) frequency, median, and arithmetic mean with standard deviation.

Results

Among the 50 patients evaluated in the study, the mean age was 11.4 (± 3.6) (range = 3 to 17), with a median age of 12 years old (Table 1).

Table 1
Characteristics of children and adolescents with symptomatic cholelithiasis undergoing laparoscopic cholecystectomy.

Among patients with hematological disease, eight (16%) had sickle cell anemia, and four (8%) had hereditary spherocytosis. In the remaining 38 patients (76%), a specific cause of cholecystolithiasis could not be identified (Table 1). No comorbidities, except hematological diseases, were observed in the patients in this series.

No patient underwent clinical treatment for stone dissolution or had undergone any previous surgery. Among obese patients, nine (18%) were females, and four (8%) were males. Two obese patients (4%) had a hematologic disease. Familial hyperlipidemia or glucose-6-phosphate dehydrogenase deficiency was not observed.

In patients with a clinical picture of abdominal pain, symptoms occurred from one week to 24 months. Four patients (8%) had episodes of cholestatic jaundice: two due to acute cholecystitis, one due to choledocholithiasis, and one due to biliary pancreatitis, all without the hematological disease.

All patients underwent ultrasonography before LC, and one (2%) underwent MRCP. Preoperatively, six patients (12%) underwent endoscopic retrograde cholangiopancreatography (ERCP) with sphincterotomy (four for acute biliary pancreatitis and two for choledocholithiasis).

Thirty-eight patients (76%) underwent surgery for biliary colic or uncharacteristic abdominal pain: six (12%) for acute biliary pancreatitis, four (8%) for acute cholecystitis, and two (4%) for choledocholithiasis. All patients with acute cholecystitis underwent surgery eight weeks after the onset of symptoms. Only patients with acute biliary pancreatitis were operated on urgently.

All patients underwent LC without intraoperative cholangiography. Three cases (6%) resulted in conversion to open access due to excessive bleeding: two of them had acute cholecystitis with an intense inflammatory area between the gallbladder and the hepatic hilum, and the gallbladder firmly adhered to the liver and duodenum in the third case. In one case, an accidental lesion of the common bile duct was identified intraoperatively. This patient underwent end-to-end common bile duct anastomosis with drainage of the main bile duct with T-tube drainage. Postoperatively, the patient evolved into stenosis of the main bile duct. He underwent an ERCP, and a papillotomy with the placement of a self-expandable metallic biliary stent was performed. After 12 months, the patient was anicteric and without the biliary endoprosthesis. One patient (2%) was reoperated on for intestinal obstruction due to adhesions. Another patient (2%) had acute biliary pancreatitis and underwent an ERCP with sphincterotomy and the placement of a plastic biliary endoprosthesis. The mean length of stay was three days (range: one to 50 days).

The anatomopathological description of the gallbladder revealed the presence of chronic cholecystitis in all cases. In two cases (4%) with an initial clinical picture of acute cholecystitis, we observed the histopathological picture of an acute outbreak of chronic cholecystitis (Table 1).

There were no deaths. All patients underwent operations experience improvement or resolution of their biliary symptoms after the laparoscopic cholecystectomy.

Discussion

In this series, the pediatric patients with cholecystolithiasis and without hemolytic disease represented most cases compared to the patients with hemolytic diseases. This tendency was also observed by other authors33 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. ,66 Sarrami M, Ridley W, Nightingale S, Wright T, Kumar R. Adolescent gallstones—need for early intervention in symptomatic idiopathic gallstones. Pediatr Surg Int. 2019;35(5):569–74. https://doi.org/10.1007/s00383-019-04461-w
https://doi.org/10.1007/s00383-019-04461...
,1111 Tannuri ACA, Leal AJG, Velhote MCP, Gonlçalves MEP, Tannuri U. Management of gallstone disease in children: a new protocol based on the experience of a single center. J Pediatr Surg. 2012;47(11):2033–8. https://doi.org/10.1016/j.jpedsurg.2012.06.010
https://doi.org/10.1016/j.jpedsurg.2012....
,1313 Treider M, Ohnesorge S, Bjørnland K. Few serious complications after cholecystectomy in paediatric patients. Acta Paediatr. 2020;109(3):630–1. https://doi.org/10.1111/apa.15081
https://doi.org/10.1111/apa.15081...
,2020 Quiroz HJ, Valencia SF, Willobee BA, Ferrantella AR, Ryon EL, Thorson CM, Sola JE, Perez EA. Utility of routine intraoperative cholangiogram during cholecystectomy in children: A nationwide analysis of outcomes and readmissions. J Pediatr Surg. 2021;56(1):61–5. https://doi.org/10.1016/j.jpedsurg.2020.09.047
https://doi.org/10.1016/j.jpedsurg.2020....
2222 Miura da Costa K, Saxena AK. Complications in pediatric laparoscopic cholecystectomy: systematic review. Updates Surg. 2021;73(1):69–74. https://doi.org/10.1007/s13304-020-00888-2
https://doi.org/10.1007/s13304-020-00888...
. The hemolytic disease seems to make cholecystolithiasis manifest at an earlier age, unrelated to obesity, and more frequently in males2323 Lascano D, Lai R, Stringel G, Stewart FD. Weekend Admissions Associated with Increased Length of Stay for Children Undergoing Cholecystectomy. JSLS J Soc Laparosc Robot Surg. 2021;25(4):e2021.00047. https://doi.org/10.4293/JSLS.2021.00047
https://doi.org/10.4293/JSLS.2021.00047...
2626 Al Talhi Y, Shirah BH, Altowairqi M, Yousef Y. Laparoscopic cholecystectomy for cholelithiasis in children with sickle cell disease. Clin J Gastroenterol. 2017;10(4):320–6. https://doi.org/10.1007/s12328-017-0750-3
https://doi.org/10.1007/s12328-017-0750-...
. Interestingly, even patients with hematological disease can present cholesterol stones, which shows that factors may overlap in the formation of these stones in hemolytic anemias2525 Al Hindi S, Al Aradi H, Mubarak M. Laparoscopic cholecystectomy in children with sickle cell disease: A simple modified technique. Asian J Endosc Surg. 2020;13(4):514–8. https://doi.org/10.1111/ases.12789
https://doi.org/10.1111/ases.12789...
,2626 Al Talhi Y, Shirah BH, Altowairqi M, Yousef Y. Laparoscopic cholecystectomy for cholelithiasis in children with sickle cell disease. Clin J Gastroenterol. 2017;10(4):320–6. https://doi.org/10.1007/s12328-017-0750-3
https://doi.org/10.1007/s12328-017-0750-...
. Cholecystolithiasis was diagnosed in the majority in the age group of 8 to 12 years old, followed by the age group of 13 to 15, as observed in other series of cholecystectomy in children and adolescents33 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. ,66 Sarrami M, Ridley W, Nightingale S, Wright T, Kumar R. Adolescent gallstones—need for early intervention in symptomatic idiopathic gallstones. Pediatr Surg Int. 2019;35(5):569–74. https://doi.org/10.1007/s00383-019-04461-w
https://doi.org/10.1007/s00383-019-04461...
,1111 Tannuri ACA, Leal AJG, Velhote MCP, Gonlçalves MEP, Tannuri U. Management of gallstone disease in children: a new protocol based on the experience of a single center. J Pediatr Surg. 2012;47(11):2033–8. https://doi.org/10.1016/j.jpedsurg.2012.06.010
https://doi.org/10.1016/j.jpedsurg.2012....
,1313 Treider M, Ohnesorge S, Bjørnland K. Few serious complications after cholecystectomy in paediatric patients. Acta Paediatr. 2020;109(3):630–1. https://doi.org/10.1111/apa.15081
https://doi.org/10.1111/apa.15081...
,2020 Quiroz HJ, Valencia SF, Willobee BA, Ferrantella AR, Ryon EL, Thorson CM, Sola JE, Perez EA. Utility of routine intraoperative cholangiogram during cholecystectomy in children: A nationwide analysis of outcomes and readmissions. J Pediatr Surg. 2021;56(1):61–5. https://doi.org/10.1016/j.jpedsurg.2020.09.047
https://doi.org/10.1016/j.jpedsurg.2020....
,2222 Miura da Costa K, Saxena AK. Complications in pediatric laparoscopic cholecystectomy: systematic review. Updates Surg. 2021;73(1):69–74. https://doi.org/10.1007/s13304-020-00888-2
https://doi.org/10.1007/s13304-020-00888...
,2727 Lamberts MP. Indications of cholecystectomy in gallstone disease. Curr Opin Gastroenterol. 2018;34(2):97–102. https://doi.org/10.1097/MOG.0000000000000419
https://doi.org/10.1097/MOG.000000000000...
. In the present study, females had a significantly higher cholesterol stones than males.

The time elapsed between the onset of symptoms and the diagnosis is likely longer in children than in adults, probably due to the lower prevalence of the disease in this age group and consequent lower clinical suspicion44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. ,55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. ,77 Greer D, Heywood S, Croaker D, Gananadha S. Is 14 the new 40: trends in gallstone disease and cholecystectomy in Australian children. Pediatr Surg Int. 2018;34(8):845–9. https://doi.org/10.1007/s00383-018-4300-y
https://doi.org/10.1007/s00383-018-4300-...
. Biliary colic attacks are irregular, and the intensity can vary from one episode to another. In pediatric patients, vomiting is a common symptom in up to 60% of symptomatic cases88 Frybova B, Drabek J, Lochmannova J, Douda L, Hlava S, Zemkova D, Mixa V, Kyncl M, Zeman L, Rygl M, Keil R. Cholelithiasis and choledocholithiasis in children; risk factors for development. PLoS One. 2018;13(5):e0196475. https://doi.org/10.1371/journal.pone.0196475
https://doi.org/10.1371/journal.pone.019...
,1212 Diez S, Müller H, Weiss C, Schellerer V, Besendörfer M. Cholelithiasis and cholecystitis in children and adolescents: Does this increasing diagnosis require a common guideline for pediatricians and pediatric surgeons? BMC Gastroenterol. 2021;21(1):186. https://doi.org/10.1186/s12876-021-01772-y
https://doi.org/10.1186/s12876-021-01772...
. Abdominal pain, characteristic or not, has a higher incidence with advancing age. It can be expected that the increased prevalence of cholecystolithiasis risk factors in pediatric patients will improve the indication of cholecystectomy for conditions typically found in adult patients77 Greer D, Heywood S, Croaker D, Gananadha S. Is 14 the new 40: trends in gallstone disease and cholecystectomy in Australian children. Pediatr Surg Int. 2018;34(8):845–9. https://doi.org/10.1007/s00383-018-4300-y
https://doi.org/10.1007/s00383-018-4300-...
. Abdominal ultrasonography is the method of choice for diagnosing cholecystolithiasis in adults and children44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. ,55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. .

LC is the criterion standard for treating cholecystolithiasis in children and adolescents99 Tian Y, Ingram MCE, Raval M V. National Trends and Disparities in the Diffusion of Laparoscopic Surgery for Children in the United States. J Laparoendosc Adv Surg Tech. 2021;31(9):1061–6. https://doi.org/10.1089/lap.2021.0013
https://doi.org/10.1089/lap.2021.0013...
,1414 Babb J, Davis J, Tashiro J, Perez EA, Sola JE, Pandya S. Laparoscopic Versus Open Cholecystectomy in Pediatric Patients: A Propensity Score-Matched Analysis. J Laparoendosc Adv Surg Tech. 2020;30(3):322–7. https://doi.org/10.1089/lap.2019.0655
https://doi.org/10.1089/lap.2019.0655...
,1616 Gupta V, Jain G. Safe laparoscopic cholecystectomy: Adoption of universal culture of safety in cholecystectomy. World J Gastrointest Surg. 2019;11(2):62–84. https://doi.org/10.4240/wjgs.v11.i2.62
https://doi.org/10.4240/wjgs.v11.i2.62...
,1818 Kılıç ŞS, Özden Ö, Çolak ST. Comparative analysis of reliability and clinical effects of the critical view of safety approach used in laparoscopic cholecystectomy in the pediatric population. Pediatr Surg Int. 2021;37(6):737–43. https://doi.org/10.1007/s00383-021-04869-3
https://doi.org/10.1007/s00383-021-04869...
,2424 Dekonenko C, Holcomb GW. Laparoscopic Cholecystectomy in Children. J Laparoendosc Adv Surg Tech. 2021;31(10):1180–4. https://doi.org/10.1089/lap.2021.0397
https://doi.org/10.1089/lap.2021.0397...
,2828 Mattson A, Sinha A, Njere I, Borkar N, Sinha CK. Laparoscopic cholecystectomy in children: A systematic review and meta-analysis. Surg. 2022;21(3):e133–41. https://doi.org/10.1016/j.surge.2022.09.003
https://doi.org/10.1016/j.surge.2022.09....
. It is associated with less postoperative pain, shorter hospital stays, a quicker return to unrestricted activities, lower risk of infection, and a less intrusive scar when compared to conventional surgery. As a rule, LC is considered a safe procedure with a low rate of complications33 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,99 Tian Y, Ingram MCE, Raval M V. National Trends and Disparities in the Diffusion of Laparoscopic Surgery for Children in the United States. J Laparoendosc Adv Surg Tech. 2021;31(9):1061–6. https://doi.org/10.1089/lap.2021.0013
https://doi.org/10.1089/lap.2021.0013...
,1414 Babb J, Davis J, Tashiro J, Perez EA, Sola JE, Pandya S. Laparoscopic Versus Open Cholecystectomy in Pediatric Patients: A Propensity Score-Matched Analysis. J Laparoendosc Adv Surg Tech. 2020;30(3):322–7. https://doi.org/10.1089/lap.2019.0655
https://doi.org/10.1089/lap.2019.0655...
,1616 Gupta V, Jain G. Safe laparoscopic cholecystectomy: Adoption of universal culture of safety in cholecystectomy. World J Gastrointest Surg. 2019;11(2):62–84. https://doi.org/10.4240/wjgs.v11.i2.62
https://doi.org/10.4240/wjgs.v11.i2.62...
,2424 Dekonenko C, Holcomb GW. Laparoscopic Cholecystectomy in Children. J Laparoendosc Adv Surg Tech. 2021;31(10):1180–4. https://doi.org/10.1089/lap.2021.0397
https://doi.org/10.1089/lap.2021.0397...
,2525 Al Hindi S, Al Aradi H, Mubarak M. Laparoscopic cholecystectomy in children with sickle cell disease: A simple modified technique. Asian J Endosc Surg. 2020;13(4):514–8. https://doi.org/10.1111/ases.12789
https://doi.org/10.1111/ases.12789...
,2929 Zilberstein B, Eshkenazy R, Ribeiro Jr. MAF, Sallet JA, Ramos AC. Laparoscopic cholecystectomy in children and adolescents. Sao Paulo Med J. 1996;114(6):1293–7. https://doi.org/10.1590/S1516-31801996000600002
https://doi.org/10.1590/S1516-3180199600...
.

Managing incidentally diagnosed and asymptomatic gallstones in the pediatric age group poses a dilemma1010 Liebe HL, Phillips R, Handley M, Gastanaduy M, Burton JH, Roybal J. A pediatric surgeon’s dilemma: does cholecystectomy improve symptoms of biliary dyskinesia? Pediatr Surg Int. 2021;37(9):1251–7. https://doi.org/10.1007/s00383-021-04922-1
https://doi.org/10.1007/s00383-021-04922...
,3030 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8:203. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,3131 Bhaumik K. Asymptomatic Cholelithiasis in Children: Management Dilemma. J Indian Assoc Pediatr Surg. 2021;26(4):228–33. https://doi.org/10.4103/jiaps.JIAPS_107_20
https://doi.org/10.4103/jiaps.JIAPS_107_...
. Long-term follow-up studies have consistently shown that only a minority of asymptomatic gallstones lead to the development of symptoms or complications which makes performing LC challenging55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. ,66 Sarrami M, Ridley W, Nightingale S, Wright T, Kumar R. Adolescent gallstones—need for early intervention in symptomatic idiopathic gallstones. Pediatr Surg Int. 2019;35(5):569–74. https://doi.org/10.1007/s00383-019-04461-w
https://doi.org/10.1007/s00383-019-04461...
. However, surgical intervention is appropriate with the presence of a clinical picture compatible with gallstone disease22 Doud A, Bond L, Downard C, Vitale G, Fallat M, Foley D, Wright T, Bond S. Management of complicated biliary disease in the pediatric population. Surgery. 2022;171(3):736–40. https://doi.org/10.1016/j.surg.2021.09.041
https://doi.org/10.1016/j.surg.2021.09.0...
,55 Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaţă R. Biliary Lithiasis with Choledocolithiasis in Children. Chirurgia (Bucur). 2015;110(6):559–61. ,66 Sarrami M, Ridley W, Nightingale S, Wright T, Kumar R. Adolescent gallstones—need for early intervention in symptomatic idiopathic gallstones. Pediatr Surg Int. 2019;35(5):569–74. https://doi.org/10.1007/s00383-019-04461-w
https://doi.org/10.1007/s00383-019-04461...
,1919 Bhaumik K. Asymptomatic cholelithiasis in children: Management dilemma. J Indian Assoc Pediatr Surg. 2021;26(4):228–33. https://doi.org/10.4103/jiaps.JIAPS_107_20
https://doi.org/10.4103/jiaps.JIAPS_107_...
,2222 Miura da Costa K, Saxena AK. Complications in pediatric laparoscopic cholecystectomy: systematic review. Updates Surg. 2021;73(1):69–74. https://doi.org/10.1007/s13304-020-00888-2
https://doi.org/10.1007/s13304-020-00888...
. In our opinion, the disadvantage of expectant treatment is that complications may develop, which leads to more morbidity, whereas routine cholecystectomy can avoid those complications.

In the present series, complications of cholecystolithiasis were observed, such as acute cholecystitis, biliary pancreatitis, and choledocholithiasis, indicating that this condition in the pediatric population can progress to severe illnesses88 Frybova B, Drabek J, Lochmannova J, Douda L, Hlava S, Zemkova D, Mixa V, Kyncl M, Zeman L, Rygl M, Keil R. Cholelithiasis and choledocholithiasis in children; risk factors for development. PLoS One. 2018;13(5):e0196475. https://doi.org/10.1371/journal.pone.0196475
https://doi.org/10.1371/journal.pone.019...
,1313 Treider M, Ohnesorge S, Bjørnland K. Few serious complications after cholecystectomy in paediatric patients. Acta Paediatr. 2020;109(3):630–1. https://doi.org/10.1111/apa.15081
https://doi.org/10.1111/apa.15081...
,3030 Pelizzo G, Bussani R, De Silvestri A, Di Mitri M, Rosone G, Amoroso S, Milazzo M, Girgenti V, Mura GB, Unti E, Rozze D, Shafiei V, Calcaterra V. Laparoscopic Cholecystectomy for Symptomatic Cholecystic Disease in Children: Defining Surgical Timing. Front Pediatr. 2020;8:203. https://doi.org/10.3389/fped.2020.00203
https://doi.org/10.3389/fped.2020.00203...
,3232 Muñoz Abraham AS, Osei H, Bajinting A, Cowles RA, Greenspon J, Hosfield BD, Keller MS, Landman MP, Owens H, Shaughnessy MP, St. Peter SD, Sujka J, Vogel AM, Villalona GA. Index Admission Cholecystectomy and Recurrence of Pediatric Gallstone Pancreatitis: Multicenter Cohort Analysis. J Am Coll Surg. 2022;234(3):352–8. https://doi.org/10.1097/XCS.0000000000000062
https://doi.org/10.1097/XCS.000000000000...
. During an observation period of 17 years, Tannuri et al.1111 Tannuri ACA, Leal AJG, Velhote MCP, Gonlçalves MEP, Tannuri U. Management of gallstone disease in children: a new protocol based on the experience of a single center. J Pediatr Surg. 2012;47(11):2033–8. https://doi.org/10.1016/j.jpedsurg.2012.06.010
https://doi.org/10.1016/j.jpedsurg.2012....
verified that 25% of patients had complications from cholecystolithiasis. In the present series, in 11 years, 12 patients (24%) had complications from biliary disease: biliary pancreatitis, acute cholecystitis, and choledocholithiasis. These results emphasize the need to avoid temporizing cholecystolithiasis in that age group.

An LC with a preoperative or postoperative ERCP is at least a two-procedure process. In contrast, a cholecystectomy with a laparoscopic common bile duct exploration (LCBDE) can provide definitive treatment in a single procedure under one anesthetic3333 Bosley ME, Zamora IJ, Neff LP. Choledocholithiasis-a new clinical pathway. Transl Gastroenterol Hepatol. 2021;6:35. https://doi.org/10.21037/tgh-20-172
https://doi.org/10.21037/tgh-20-172...
,3434 Destro F, Pierucci UM, Durante E, Caruso AM, Girgenti V, Canonica CPM, Degrassi I, Campari A, Pellegrinelli A, Barisella M, Nebuloni M, Brunero M, Biganzoli EM, Calcaterra V, Pelizzo G. Laparoscopic Cholecystectomy in Children: The Experience of Two Centers Focusing on Indications and Timing in the Era of “New Technologies”. Children (Basel). 2023;10(11):1771. https://doi.org/10.3390/children10111771
https://doi.org/10.3390/children10111771...
. Exploration of the common bile duct and removal of stones by an LCBDE is safe and feasible in pediatric patients to treat choledocholithiasis. Through this procedure, choledocholithiasis and cholelithiasis can be treated in a single procedure without papillotomy or fluoroscopy. Compared with an LC and ERCP, an LCBDE is associated with a shorter hospital stay3434 Destro F, Pierucci UM, Durante E, Caruso AM, Girgenti V, Canonica CPM, Degrassi I, Campari A, Pellegrinelli A, Barisella M, Nebuloni M, Brunero M, Biganzoli EM, Calcaterra V, Pelizzo G. Laparoscopic Cholecystectomy in Children: The Experience of Two Centers Focusing on Indications and Timing in the Era of “New Technologies”. Children (Basel). 2023;10(11):1771. https://doi.org/10.3390/children10111771
https://doi.org/10.3390/children10111771...
3636 Pogorelić Z, Lovrić M, Jukić M, Perko Z. The Laparoscopic Cholecystectomy and Common Bile Duct Exploration: A Single-Step Treatment of Pediatric Cholelithiasis and Choledocholithiasis. Children (Basel). 2022;9(10):1583. https://doi.org/10.3390/children9101583
https://doi.org/10.3390/children9101583...
. Unfortunately, during the period in which the cases in this series were operated on, the Pediatric Surgery Unit did not have an LCBDE available.

Major postoperative complications in an LC are uncommon44 Pogorelić Z, Aralica M, Jukić M, Žitko V, Despot R, Jurić I. Gallbladder Disease in Children: A 20-year Single-center Experience. Indian Pediatr. 2019;56(5):384–6. ,1313 Treider M, Ohnesorge S, Bjørnland K. Few serious complications after cholecystectomy in paediatric patients. Acta Paediatr. 2020;109(3):630–1. https://doi.org/10.1111/apa.15081
https://doi.org/10.1111/apa.15081...
,2929 Zilberstein B, Eshkenazy R, Ribeiro Jr. MAF, Sallet JA, Ramos AC. Laparoscopic cholecystectomy in children and adolescents. Sao Paulo Med J. 1996;114(6):1293–7. https://doi.org/10.1590/S1516-31801996000600002
https://doi.org/10.1590/S1516-3180199600...
, and in this series they occurred in two patients: one patient had postoperative biliary pancreatitis, and the other one patient had a bile duct stenosis due to an intraoperative injury In both cases, the patients had a good recovery and no intercurrences.

Mattson et al.2828 Mattson A, Sinha A, Njere I, Borkar N, Sinha CK. Laparoscopic cholecystectomy in children: A systematic review and meta-analysis. Surg. 2022;21(3):e133–41. https://doi.org/10.1016/j.surge.2022.09.003
https://doi.org/10.1016/j.surge.2022.09....
performed a systematic review with meta-analysis through 114 studies and 76.524 patients. The authors found a rate of 3.4% for postoperative complications in children, slightly lower than that of the present series (4%). In their meta-analysis, the conversion rate to conventional surgery was 2 vs. 6% in our series. Despite the experience of the single surgeon, it is possible to speculate that, of the cases that were operated on urgently, they contributed to increasing the number of cases with complications or even the need to convert the LC to open access.

The main limitations of this study were its retrospective character and single-center design. Furthermore, due to the number of patients included, additional studies with a larger sample are needed to confirm the results obtained in the current series.

Conclusion

The natural evolution of cholecystolithiasis in the pediatric population can present serious complications, emphasizing the need to avoid temporizing cholecystolithiasis in children and adolescents because LC in this age group is a safe operation with low complication rates. When necessary, a cholecystectomy with a LCBDE can provide definitive treatment in a single procedure under one anesthetic, avoiding papillotomy or fluoroscopy.

Acknowledgements

Not applicable.

  • Research performed at Faculdade de Medicina do ABC, Santo André, SP, Brazil.
  • Funding

    Not applicable.

Data availability statement

All data were generated or analyzed in the current study.

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Edited by

Section editor: Gaspar Lopes Filho https://orcid.org/0000-0002-9344-6479

Publication Dates

  • Publication in this collection
    22 July 2024
  • Date of issue
    2024

History

  • Received
    19 June 2023
  • Accepted
    29 May 2024
Sociedade Brasileira para o Desenvolvimento da Pesquisa em Cirurgia https://actacirbras.com.br/ - São Paulo - SP - Brazil
E-mail: actacirbras@gmail.com