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doi:10.1111/jpc.13235

ORIGINAL ARTICLE

Risk factors, complications and outcome of cholelithiasis in children:

A retrospective, single-centre review
Ceyda Tuna Kirsaclioglu,1 Bahar Çuhacı Çakır,2 Gulsah Bayram,3 Fatih Akbıyık,4 Pamir Işık5 and Bahattin Tunç5
Departments of 1Pediatric Gastroenterology, 2Well Child Clinic, 3Radiology, 4Pediatric Surgery and 5Pediatric Hematology, Ankara Child Health and Diseases
Hematology-Oncology Research and Training Hospital, Ankara, Turkey

Aim: The aim of this study was to evaluate the clinical presentation, risk factors, complications, treatment and outcomes of cholelithiasis in children.
Methods: Children with cholelithiasis were reviewed for demographic information, predisposing factors, presenting symptoms, laboratory find-
ings, complications, treatment and outcome, retrospectively.
Results: A total of 254 children with cholelithiasis (mean age: 8.9 ± 5.2 years) were recruited to the study. Girls (52.8%) were significantly older than
boys (P < 0.001). Symptomatic patients (59%) were significantly older than asymptomatic patients (P = 0.002). Abdominal pain was the most frequent
symptom. No risk factors were identified in 56.6% of the patients. Ceftriaxone (20%) was the most commonly associated risk factor. At presentation, at
least one of the following complications was seen in 14.1% of patients: cholecystitis (10.9%), obstructive jaundice (2.7%), pancreatitis (1.96%) and
cholangitis (1.2%). There was no relationship between gallstone size and symptoms, aetiological factors and complications. The cholelithiasis disso-
lution rate was higher in younger children (P = 0.032), in those with biliary sludge (P < 0.0001) and ceftriaxone-related cholelithiasis (P < 0.001).
Haemolytic anaemia (P = 0.001) and older age (P = 0.002) were associated with stable stones. Ursodeoxycholic acid was administered to 94.4% of
patients at presentation. Twenty-nine patients underwent cholecystectomy, and seven patients underwent endoscopic retrograde
cholangiopancreotography. Patients who were symptomatic at presentation had significantly more frequent symptoms at follow-up (P < 0.001)
Conclusions: Dissolution rate of cholelithiasis was higher in younger children, biliary sludge formation and ceftriaxone-related cholelithiasis but
lower in older children and haemolytic anaemia-related cholelithiasis.
Key words: aetiology; children; cholelithiasis; treatment.

What is already known on this topic What this paper adds

1 Cholelithiasis in children may be asymptomatic or presented 1 High dissolution rate of gallstones may be associated with
with different symptoms. younger age, ceftriaxone-related cholelithiasis and billiary
2 Cholecystectomy is recommended for symptomatic and com- sludge form under ursodeoxycolic treatment.
plicated cases. 2 Cholecystectomy should be considered especially in older chil-
3 There is no consensus on follow-up care and treatment. dren who have more complicating disease and more frequent
symptoms.
3 Cholecystectomy should be considered in patients with hemolytic
anaemia-related cholelithiasis who have more stable gallstones.

Cholelithiasis has been diagnosed more frequently in recent years factors.1,2,6–9 Cholelithiasis may be asymptomatic, or it may present
because of the widespread use of ultrasonography in children. with nonspecific symptoms, cholecystitis, pancreatitis and obstruc-
The prevalence of cholelithiasis among children is 0.13–0.3%.1–3 tive jaundice in children.1,2,4,6–9 There is no consensus on follow-up
However, in obese children and adolescents, the prevalence of care and management of cholelithiasis in children. The aim of this
cholelithiasis is as high as 2–6.1%.4,5 The aetiology remains study was to evaluate the clinical presentation, risk factors,
idiopathic in 30–54% of children. Haemolytic disease and non- complications, treatment and outcomes of cholelithiasis in children.
haemolytic disorders, such as cystic fibrosis, obesity, drugs and total
parenteral nutrition (TPN), are common associated risk
Methods
A retrospective study was performed on children with cholelithia-
Correspondence: Dr Ceyda Tuna Kırsaclıoglu, Ankara Child Health and
Diseases Haematology-Oncology Research and Training Hospital, Ankara,
sis in the paediatric gastroenterology outpatient clinic of the
Turkey. Fax: +90 312 3472330; email: [email protected] Turkish Ministry of Health Ankara Child Health and Disease
Haematology Oncology Training and Research Hospital from June
Conflict of interest: None declared.
2008 to December 2013. Patients were either diagnosed in our out-
Accepted for publication 14 March 2016. patient clinic or referred to us from other departments for

Journal of Paediatrics and Child Health (2016) 1

© 2016 Paediatrics and Child Health Division (The Royal Australasian College of Physicians)
Cholelithiasis in children C Tuna Kirsaclioglu et al.

cholelithiasis. The records of patients with cholelithiasis were Table 1 Cholelithiasis related conditions and complications
reviewed for demographic information; medical history; family
history of cholelithiasis; predisposing factors; presenting symp- Number of patients who
toms; laboratory findings (alanine amino transferase (ALT), aspar- Number of had complications (%)
tate amino transferase (AST), gamma-glutamyl transferase (GGT), patients (%) (complication)
alkaline phosphatase (AP), total and direct bilirubin, sweat chloride Idiopathic 144 (56.6) 21 (14.5) (cholecytitis,
test, celiac disease screening and ceruloplasmin); abdominal ultra- cholangitis, pancreatitis)
sound findings; complications; treatment; follow-up period; and Drugs 64 (25.1) 7 (10.9) (cholecystitis)
outcome. We calculated body mass index (BMI) as weight in Ceftriaxone 51 (20) 7 (13.7) (cholecystitis)
kilogrammes divided by height in metres squared (kg/m2). Accord- Furosemid 5 (1,96) —
ing to age and gender charts of BMI from the World Health Orga- Antiepileptic drugs 7 (2.75) —
nisation, a BMI in the ≥85th to <95th percentile is considered Octreotide 1 (0.4) —
overweight, and a BMI in the ≥95th percentile is considered Obesity/overweight 34 (13.3) 2 (5.8) (cholangitis and
obese.10 Malnutrition was defined if the relative weight was cholecystitis)
<89%. The relative weights calculated by dividing the actual Hemolytic anaemia 31 (11.8) 8 (25.8) (cholecytitis,
weight by the estimated weight for their height, then multiplying cholangitis and pancreatitis)
by 100.11,12 Parameters were defined as increased according to Herediter 20 (7.5) 6 (30) (cholecytitis,
the following criteria: ALT, AST, GGT and AP >1.5 × the upper spherocytosis cholangitis and pancreatitis)
Sickle cell disease 5 (1,96) —
limit of normal; total or direct bilirubin levels >2 mg/dL; total
βThalessemia 5 (1,96) 1 (20) (cholecytitis)
cholesterol >200 mg/dL; and serum triglyceride level >200 mg/dL.
Glucose-6-phosphate 1 (0.4) 1 (100) (cholecytitis)
Data analysis was performed using the Statistical Package for So-
dehydrogenase deficiency
cial Sciences (SPSS) software 17.0. Initially, all variables were
Hypertriglyceridemia 15 (7) —
analysed descriptively. The non-parametric Mann–Whitney test
(>200 mg/dL)
and the chi-squared test were used.
Hypercholesterolemia 15 (7) —
The Ethics Committee of our hospital approved the study (pro- (>200 mg/dL)
tocol number 2014/024). Anorexia 3 (1.2) 1 (33.3) (cholecystitis)
Total parenteral nutrition 3 (1.2) —
Cardiac surgery 1 (0.4) —
Results Celiac disease 1 (0.4) —
Demographic and laboratory findings Wilson disease 1 (0.4) —
Cystic fibrosis 1 (0.4) —
A total of 254 children, with a mean age of 8.9 ± 5.2 years (age range
of 0.08–18 years), were diagnosed with cholelithiasis. Of these, 134
(52.8%) were female. Girls were significantly older than boys (mean
age 10 ± 4.8 years and 7.7 ± 5.4 years, respectively) (P < 0.001). factors associated with cholelithiasis in 144 (56.9%) patients.
At the time of diagnosis, 150 (59%) patients were symptomatic Among these groups, the percentage of symptomatic patients
(86 female, 57.3%), and 104 (41%) patients were asymptomatic (101, 70.1%) was significantly higher than the percentage of
(48 female, 46.1%). There was no statistically significant difference asymptomatic patients (P < 0.001).
in gender between asymptomatic and symptomatic patients. Patients with ceftriaxone-related cholelithiasis (mean age 7
Symptomatic patients were significantly older than asymptomatic ± 5.1 years) were significantly younger than the other patients
patients (mean age 9.8 ± 4.9 years and 7.7 ± 5.4 years, respectively) (mean age 9.5 ± 5.1 years) (P = 0.01). Patients with haemolytic
(P = 0.002). anaemia-related cholelithiasis (mean age 11.3 ± 4.2 years) were
Asymptomatic patients were incidentally diagnosed with chole- older than the other patients (mean age 8.6 ± 5.2 years) (P = 0.002).
lithiasis while evaluating for hepatosteatosis, splenomegaly, uri- The family history of 62 patients (24.4%) revealed the presence
nary infections or congenital anomalies with abdominal of cholelithiasis in first-degree and/or second-degree family
ultrasonography. members.
At presentation, symptomatic patients had at least one of the fol- Twenty-four (9.5%) patients were malnourished according to
lowing symptoms: chronic abdominal pain (125 patients, 83.3%); their relative weight (<89%). According to age-related and
nausea (90 patients, 60%); vomiting (82 patients, 54.6%); upper gender-related BMI, 10 (3.9%) patients were overweight and 24
right quadrant pain (23 patients, 15.3%); and icterus (7 patients, (9.5%) patients were obese. There was no difference between
4.6%). The children with abdominal pain and upper right quad- symptomatic and asymptomatic patients with respect to BMI
rant pain were older than the children without pain in the symp- (P > 0.05).
tomatic group (P < 0.001 and P < 0.001, respectively). Laboratory findings at presentation revealed elevation of ALT
Cholelithiasis-related conditions are given in Table 1. Further- and/or AST in 22 (8.8%) patients, GGT in 14 (6.2%) patients, AP
more the medical history of the patients revealed Down syndrome in 19 (8.5%) patients, total bilirubin in 10 (4.2%) patients and di-
(three patients, 1.2%); malignancy (three patients, 1.2%); familial rect bilirubin in 7 (2.9%) patients.
Mediterranean fever (two patients, 0.8%); cerebral palsy (one pa- Tissue transglutaminase IgA and total IgA were negative for all
tient, 0.4%); hydrocephalus (one patient, 0.4%); and cardiac sur- 165 patients assessed for celiac disease, with the exception of one
gery (1 patient, 0.4%). There were not any recognised risk patient who had previously been diagnosed with celiac disease.

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C Tuna Kirsaclioglu et al. Cholelithiasis in children

Ceruloplasmin levels were in the normal range in all 141 patients nausea and/or vomiting, 5 patients with abdominal discomfort and
assessed for Wilson’s disease, with the exception of one patient 3 patients with diarrhoea), and in 4 cases, the family refused to ad-
who had been previously diagnosed with Wilson’s disease. The minister the drug. Patients with a complicating disease at presenta-
sweat chloride test was positive in only one patient (1/72), who tion were also referred to paediatric surgery for cholecystectomy
also had chronic diarrhoea and malnutrition. even though they were prescribed UDCA. On follow-up, UDCA
was administered for a median of 3 months (range 1–60 months).
Abdominal ultrasound findings Dissolution rates of cholelithiasis did not statistically differ between
the UDCA treated group and the spontaneous resolution group
At presentation, gallstones with a diameter of ≥5 mm were the (P > 0.05) (Fig. 1).
most common (Table 2). There were no associations between The patients whose gallstones dissolved were significantly
gallstone size and symptoms, obesity, drug use, haemolytic younger (mean age 8 ± 5.2 years) than the other patients (mean
anaemia and complications (Table 2). age 9.5 ± 5 years) (P = 0.03). Biliary sludge was the most dissolving
Abdominal ultrasound revealed hepatosteatosis in 30 (11.8%) form of cholelithiasis when compared with the other forms
patients, hepatomegaly in 47 (18.5%) patients and splenomegaly (P < 0.0001) (Table 2).
in 31 (12.2%) patients. Ceftriaxone-related cholelithiasis was significantly more prone
to dissolve when compared with the other aetiologies
Complications (P < 0.001). In contrast, gallstones due to haemolytic disease were
At presentation, 36 (14.1%) patients had at least one of the the most stable gallstones when compared with those of other ae-
following complications: acute cholecystitis (29 patients, tiologies (P = 0.001) (Table 3).
10.9%); obstructive jaundice (7 patients, 2.7%); acute pancre- On-follow up, 168/216 (77.7%) patients remained asymptom-
atitis (5 patients, 1.9%); or cholangitis (3 patients, 1.2%). atic. Patients who were symptomatic at presentation had signifi-
The patients with complicating diseases (mean age of 12.4 cantly more frequent symptoms on follow-up (P < 0.001) (Fig. 2).
± 4.1 years) were significantly older than the other patients (mean
age 8.4 ± 5.1 years) (P < 0.001).
Patients with complicating disease and possible associated
risk factors are shown in Table 1. There was no relationship
between complicating disease and aetiological factors,
gallstone size or gallstone dissolution (P > 0.05) (Table 2).

Treatment, follow-up and resolution of cholelithiasis

Two hundred sixteen patients were followed for a median of
6 months (range 1–66 months). Resolution of cholelithiasis was
determined in 37% of patients at a median of 2 months (range
1–24 months) independent of ursodeoxycholic acid (UDCA)
treatment.
Ursodeoxycholic acid was prescribed to all patients at
presentation. However, 18 (7%) of them did not use UDCA: 14
discontinued the treatment because of side effects (6 patients with Fig. 1 Resolution of cholelithiasis due to ursodeoxycholic acid treatment.

Table 2 Relation of gallstone size and symptoms, complications, aetiology and dissolving rates

Number of patients (%)

Gallstone size ≥5 mm Gallstone size <5 mm Biliary sludge P-value*

Number of patients (%) 150 (59.1) 49 (19.3) 55 (21.7) —

Symptomatic patients 88 (58.7) 28 (18.7) 34 (22.7) NS
Asymptomatic patients 62 (59.6) 21 (20.1) 21 (20.1) NS
Complication 21 (61.8) 6 (17.6) 7 (20.6) NS
Aetiology
Idiopathic 83 (57.6) 29 (20.1) 32 (22.2) NS
Ceftriaxone 29 (56.8) 11 (21.5) 11 (21.5) NS
Hemolytic anaemia 21 (67) 3 (9.7) 7 (22.6) NS
Obesity and overweight 17 (68) 8 (32) 9 (3.5) NS
Dissolving rates of cholelithiasis 32 (26) 12 (27.9) 36 (72) <0.0001**; <0.0001***

*P-value > 0.05; NS. **P-value < 0.001; Significant difference between biliary sludge and <5-mm gallstone. ***P-value < 0.0001; Significant difference between
biliary sludge and ≥5-mm gallstone. NS, not significant.

Journal of Paediatrics and Child Health (2016) 3

© 2016 Paediatrics and Child Health Division (The Royal Australasian College of Physicians)
Cholelithiasis in children C Tuna Kirsaclioglu et al.

All patients with a complicating disease were referred to paediat- TPN, cardiac surgery, cystic fibrosis, obesity, prematurity and
ric surgery at presentation. Cholecystectomy had been performed congenital biliary malformations) and drug use.1,2,6,8,9,14 In our
in 29 (12.1%) patients at follow-up. The median duration time of study, we could not identify any risk factors in 56.6% of patients.
cholecystectomy was 5.5 months (range 1–60 months). Indications Ceftriaxone was the most common associated risk factor in our
for cholecystectomy were shown in Figure 2. Endoscopic retro- study. The incidence of ceftriaxone-associated cholelithiasis has
grade cholangiopancreotography (ERCP) was performed in seven been defined as 15–46% in previous reports.6,8,15,16 We
(2.8%) patients with obstructive jaundice due to choledocal stones. determined that ceftriaxone-related cholelithiasis was most likely
There were no complications related to cholecystectomy and ERCP. to dissolve. On the other hand, we observed that ceftriaxone could
lead to stable gallstones and complicating diseases such as
cholecystitis. Obesity-related non-alcoholic steatohepatitis and
Cholelithiasis in infants
cholelithiasis share common risk and pathogenic factors.
Our study included 19 (7.4%) infants (≤1 year age) with a median According to previous studies, the rate of cholelithiasis among
age of 5 months (age range 1–11 months). Five (26%) patients obese adolescents is 2–6.4%.4,5 Obesity prevalence ranges from
were symptomatic, and they presented with vomiting. 3.7% to 4.5% in Turkish school children.17–19 In our study, obesity
Ten (52.6%) infants had no recognised risk factors. Ceftriaxone and overweight together was the second most common risk factor.
(four patients, 21.4%), furosemide (two patients, 10.5%), TPN The obesity rate of children with cholelithiasis was 9.5%, which is
(two patients, 10.5%) and octreotide (one patient, 5.3%) were higher than the rate reported for our population and in previous
the cholelithiasis-associated risk factors. studies.
There were no complications at presentation and follow-up. The Our hospital is a general child health and disease hospital,
median follow-up period was 6 months (range 1–52 months). despite its name. Thus, the rate of haemolytic disease-related
Cholelithiasis dissolved in seven (36.8%) patients at a median of cholelithiasis (11.8%) was not higher than that previously re-
2.5 months (range 1–24 months) under UDCA treatment. ported in our study.
Aetiology, complications and cholelithiasis dissolution rates did Various studies have reported that as many as 50.5% of
not differ between infants and children >1 year old (Table 3). No children with cholelithiasis are asymptomatic.2,6,8,9 Typical
infants underwent cholecystectomy or ERCP. biliary symptoms (upper right quadrant or epigastric pain,
vomiting and nausea) are observed in 40–50% of children with
Discussion gallstones. In several studies, abdominal pain was the most
common symptom, present in as many as 94% of symptomatic
With the widespread use of abdominal ultrasonography, diagnosis patients.1,2,6,9 In our study, 83.3% of symptomatic patients had
of cholelithiasis in children has grown. Biliary sludge, which consists abdominal pain, similar to the findings of previous studies. In
of 1–3-mm microliths, is accepted as the intermediate step in gall- addition, the children who had abdominal pain were
stone development. The microliths can resolve spontaneously or significantly older than the other symptomatic children.
cause abdominal pain, cholecystitis, cholangitis, obstructive jaundice In previous studies, cholelithiasis-related complications such as
and pancreatitis.13 Given the risk of these complications and the pos- acute cholecystitis, cholangitis and acute pancreatitis were ob-
sibility of larger gallstone formation, we included biliary sludge in served in 12.9–25% of patients.2,7,20 The presence of at least one
our study. gallstone smaller than 5 mm in diameter increased the risk of de-
Previous reports have shown female predominance,6,7 but in veloping pancreatitis fourfold.21 Our total complication rate was
some studies, female predominance was observed mainly in 14.1%. Complicating diseases were observed in older patients.
adolescents.1–3 In our study group, there was no gender difference. The rate of complicating disease was higher in patients with
As in other studies, the girls were older than the boys in our study. haemolytic anaemia-related cholelithiasis (25.8%), but it was not
This has been attributed to the effects of hormonal changes during statistically different from the rate observed in other patients. In
puberty on biliary cholesterol saturation.6 addition, there was no correlation between complications and gall-
In children, the aetiology of cholelithiasis remains idiopathic in stone size in our study.
30–54% of cases. Roughly 12.9–30% are due to haemolytic Ursodeoxycholic acid markedly decreases biliary cholesterol sat-
disease, while 40–50% are due to non-haemolytic disease (e.g. uration by 40–60% by inhibiting cholesterol absorption in the

Table 3 Dissolving rates of gallstones according to aetiology and age

Number of gallstones dissolved patients (%)

Number of patients Total Idiopathic Ceftriaxone Hemolytic anaemia Obesity and overweight
underwent control ultrasound n = 204 (%) n = 106 (%) n = 40 (%) n = 28 (%) n = 30 (%)

All ages 76 (37.2) 31 (29.2) 31 (77.5) 3 (10.7) 11 (36.6)

>12 months 69 (33.8) 26 (27.1) 29 (70.2) 3 (10.7) 11 (36.6)
≤12 months 7 (3.4) 5 (4.7) 2 (5) — —
P-value* NS NS NS

*Dissolution percentages according to age: P-value > 0.05, not significant (NS).

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C Tuna Kirsaclioglu et al. Cholelithiasis in children

Fig. 2 Symptoms of patients on follow-up and indications for non-medical interventions.

intestine and cholesterol secretion into bile. In adults, clinical stud- especially in older children with cholelithiasis, independent of gall-
ies have demonstrated a dissolution rate of 30–60% and complete stone size and aetiological factors. These findings might support an
disappearance of small stones (<5 mm) and biliary sludge with eligible treatment option at presentation. Cholecystectomy should
UDCA treatment.22 In our study, 94.4% of patients were treated be considered in older children and in those with haemolytic
with UDCA, with a total resolution rate of 37%, which was higher anaemia-related gallstones.
than the rate observed in previous studies (19–29.4%) of chil-
dren.2,9 Our high resolution rate may be related to the high per-
centage of UDCA treatment. On the other hand, there was no
difference in the resolution rates of the UDCA-treated and non-
treated groups. Because the non-treated group was small in size, References
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