Clin J Gastroenterol DOI 10.1007/s12328-017-0750-3
CLINICAL REVIEW
Laparoscopic cholecystectomy for cholelithiasis in children with sickle cell disease Yousef Al Talhi1 • Bader Hamza Shirah1
•
Muteb Altowairqi2 • Yasmin Yousef1,3
Received: 24 February 2017 / Accepted: 14 May 2017 Japanese Society of Gastroenterology 2017
Abstract Patients with sickle cell disease (SCD) suffer from an increased incidence of gallstone formation due to hemolysis of sickled red blood cells; this leads to an increased level of bilirubin in secreted bile that becomes a nidus for pigment stone formation. Laparoscopic cholecystectomy (LC) is considered a standard operative procedure for gallstone disease mainly due to lower postoperative wound complaints, faster recovery, better postoperative cosmetic results, shorter hospital stay, and earlier return to work. Although numerous studies have been published addressing both the advantages and complications of LC in acute calcular cholecystitis, there is still limited evidence concerning the safety and efficacy of LC for the management of cholelithiasis in pediatric patients with SCD, and controversies remain unresolved. In this review, we aim to comprehensively study the available literature and propose evidence-based practice recommendations for the optimal management of gallstones in pediatric SCD patients. The current practice differs greatly depending on the prevalence of SCD in a particular geographic area. We acknowledge the limited number of patients reported, the lack of randomized control trials addressing the practice of specific recommendations, and the need for further evidence-based studies.
Keywords Sickle cell disease Sickle cell anemia Acute cholecystitis Cholelithiasis Laparoscopic cholecystectomy, pediatric
Introduction Laparoscopic cholecystectomy (LC) is currently considered the standard of care for managing gallstone disease. The worldwide acceptance of LC is mainly due to lower postoperative wound complaints, faster recovery, better postoperative cosmetic results, shorter hospital stay, and earlier return to work. Although numerous studies have been published addressing both the advantages and complications of LC in acute cholecystitis, there is still limited information concerning the safety and efficacy of LC in the management of acute cholecystitis for sickle cell disease (SCD) pediatric patients, and controversies remain unresolved [1]. Here, we aim to thoroughly review the literature and provide evidence-based recommendations for optimal management.
Epidemiology SCD
& Bader Hamza Shirah
[email protected] 1
King Abdullah International Medical Research Centre, King Saud bin Abdulaziz University for Health Sciences, P.O. Box: 65362, Jeddah 21556, Saudi Arabia
2
Taif University, Taif, Saudi Arabia
3
King Abdulaziz Medical City, Jeddah, Saudi Arabia
Among the world population, SCD is noticeably found among people from Asia, India, the Middle East, Africa, South and Central America, the Caribbean Islands, and the Mediterranean Sea area. However, migration has noticeably led to an increased prevalence of SCD in non-endemic areas such as European countries [2, 3]. Annually, around 312,000 newborns are homogenous for SCD, with the majority from developing countries. [3] For example,
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230,000 births with SCD occur in sub-Saharan Africa every year [3]. The early birth mortality rate of SCD has decreased vastly in affluent countries with improved diagnostic tools and clinical care; however, the opposite is found in non-affluent countries where the rate is still high [3]. Cholelithiasis among SCD patients Cholelithiasis is a well-known medical entity in pediatric patients with SCD. The reported prevalence rates range from 30-70%, depending on age and diagnostic criteria [4]. Curro et al. demonstrated that the chance of developing gallstones in SCD patients increases with age. For example, the chance for developing gallstones increases from 15% if the patient is aged \10 years to 50% when he/she reaches 22 years of age [5]. Therefore, cholelithiasis and biliary colic should be considered in the differential diagnosis for vaso-occlusive crisis (VOC) when a child or adult with SCD experiences an episode of abdominal pain.
Etiology and pathogenesis SCD occurs when valine is replaced with glutamic acid at the 6th position of the amino acid sequence representing one of the b-globin chains of the hemoglobin molecule due to a single gene mutation. HbS represents hemoglobin with the substituted valine (sickle cell carrier or heterozygous mutation), and HbSS designates the presence of both SCD recessive genes (SCD or the homozygous mutation). The mutated red blood cells (RBCs) in the oxygenated form stay in the normal biconcave disk shape and do not cause any problems. In contrast, in the deoxygenated form, the replaced amino acid forms a bond with the proximal b-globin molecules. This bond leads to polymerization of these molecules in a filamentlike structure which then accumulate to form inflexible rods, giving RBCs the sickle-like shape. Re-oxygenation reverses the shape of the RBCs to normal; however, shifting the shape back and forth ruptures the cell membrane, leading to hemolysis of RBCs [2]. The bilirubin is then conjugated by the liver and secreted in the gastrointestinal tract as urobilinogen. This is then absorbed and excreted several times through the enterohepatic circulation of bile. However, the abundance of urobilinogen in the excreted bile leads to sedimentation which may become calcified, leading to stone formation [6]. Furthermore, the sickled cells form microthrombi in the most peripheral blood vessels causing VOC and other complications related to SCD.
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Management options The management options include preoperative endoscopic retrograde cholangiopancreatography (PO-ERCP). Our literature review demonstrated that ERCP is a highly recommended valuable diagnostic and therapeutic tool in treating children with SCD suffering from cholelithiasis and/or choledocholithiasis with a success rate reaching 96.8% (n = 125) [1, 7–10]. Dan et al. suggested that ERCP reduces the operative time of subsequent LC with a mean of 27.9 min [11]. The reported indications for performing ERCP are jaundice, elevated alkaline phosphate and conjugated (direct) bilirubin [5 mg/dL, cholecystitis [1, 5, 9, 10, 12], former events of pancreatitis [1], abnormal liver function test (LFT) [13], and any ultrasound findings showing a dilated common bile duct (CBD) [7 mm and/or the presence of stones in the CBD [1, 5, 7, 9, 11]. With regard to previous indications, some studies demonstrated that the majority of patients have normal findings at ERCP, and this may be due to the high incidence of small CBD stones that pass spontaneously before ERCP. The formation of small CBD stones may reach up to 30% among SCD patients with cholelithiasis [1, 14, 15]. Therefore, these studies stressed the use of many powerful diagnostic tools such as endoscopic ultrasound and magnetic resonance cholangiopancreatography (MRCP) to identify CBD stones before performing ERCP [1, 8]. Issa et al. advised replacing ERCP with MRCP to reduce the complications of ERCP, especially for those with only a dilated CBD [9]. ERCP followed by LC was found to be the preferred option. The indications for LC were acute cholecystitis (fever [37.2C, positive Murphy’s sign, persistent right hypochondrial pain, leukocytosis [10 9 109/L), abnormal sonogram showing dilated, double-walled or thick cystic duct, pericholecystic fluid with the presence of gallstones, or any clinical findings confirming an acutely inflamed gallbladder [12]. Other indications include obstructive jaundice, biliary colic, gallstone pancreatitis, and identified cholelithiasis. Regarding preoperative care, along with simple blood transfusion or exchange transfusion if needed and POERCP only if indicated, there are some important measures that aim to reduce RBC sickling both intra- and postoperatively. These include hydration, oxygenation, keeping the patient warm, fasting orally [12, 16], maintaining normal acid–base balance, and infection control [5]. It could take more than one day to prepare the patient for surgery after admission [12]. It is also important to maintain proper analgesia since stress is a well-known risk factor for developing VOC [5, 12].
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Prophylactic antibiotics were also strongly indicated. It is important to minimize infections in patients with SCD with broad-spectrum antibiotics before pyrexia occurs [5]. The antibiotics used were cephalosporin alone or gentamycin and cephalosporin for three doses [1, 17]. Muroni et al. used amoxicillin or penicillin 1 h preoperatively and continued for 5 days after surgery [18]. Al-Mulhim et al. used ampicillin, metronidazole, and gentamicin prior to surgery [13]. We also found that the French National Authority for Health highlights the use of penicillin as a preoperative prophylaxis for children with SCD; however, the duration of treatment is variable [18]. Furthermore, Hirst et al. found that penicillin significantly reduces the risk of pneumococcal infection (odds ratio 0.37) [19]. Regarding intraoperative care, Muroni et al. reported using thermal cover at 40C to keep the patient warm [18]. In cases where stones are identified in the CBD, they should be removed by Dormia basket or any similar apparatus [18]. If this is not feasible, the operation should be converted to open surgery [18]. Complications during the operation can be transient acidosis, dehydration, or hypothermia, leading to VOC events such as acute chest syndrome (ACS), or even stroke intraoperatively or immediately postoperatively [20, 21]. With regard to postoperative care, it is important to maintain hydration postoperatively and administer oxygen therapy during recovery [12]. The hydration therapy should be continued until the patient shows proper oral intake
[20]. The use of antibiotics was uniform in the literature yet the duration and type of antibiotics was variable as it was found to be case-dependent ranging from 48 h to 5 days [12]. If acid–base balance disturbance is suspected, it is recommended to test atrial blood gas (ABG) every 6 h [12]. Diarra et al. suggested that the hospital stay should be extended whenever an SCD patient undergoes laparoscopic intervention [16]. However, Meshikhes disagreed with this suggestion and justified that prolonged hospital stay would not help prevent or reveal ACS [22], and would only trigger the risk of limited mobilization. He reported that the post-hospital stay at his institution was 23–48 h [22]. Therefore, we can recommend discharging the patient as soon as the patient tolerates oral intake, and pain is controlled by oral analgesics. With regard to postoperative complications, we reviewed all the complications detected among children who underwent LC in the literature. Any infection was treated with antibiotics [12]. Chest infections or shortness of breath were also treated with antibiotics along with steam inhalation, mucolytic drugs, and chest physiotherapy [11, 12]. VOC pain was relieved by using opioids [11]. Table 1 lists all the complications found among SCD patients as reported in the literature. Conversion to open cholecystectomy was a regularly reported occurrence; however, the conversion rate in the literature is variable. Table 2 shows the conversion rate in
Table 1 Reported complication rates for LC in the literature as well as the type of surgery, gender percentage, average age, operative time, and hospital stay Authors
N
Average age (years)
Male (%)
Female (%)
Type of surgery
Average operative time (min)
Average hospital stay (days)
Complication rate
Al-Salem et al. [1]
52
11.4
53.85
46.15
Elective
100
4.5
7.7%
Al-Mulhim et al. [13]
33
Reported complications 2 ACS 1 Fever 2 Bleeding (CA)
Al-Wabari et al. [17]
9.1
42.4
57.6
Emergency
91.3
8.5
18.18%
2 Wound infection 3 Chest infection
21
8.9
47
11.4
47.6
52.4
Elective
75.8
4.5
–
55
45
N/A
100
4.3
6.4%
1 lower limb VOC – 1 Mild ACS 1 Fever 1 Bleeding from an accessory cystic artery
Jawad et al. [32] SeguierLipszyc et al. [42]
5 11.2 29
9.9
20
80
Elective
80.6
1.9
N/A
5 Hypothermia
72.41
27.59
Elective
82.6
3
17%
N/A
ACS acute chest syndrome, CA cystic artery, VOC vaso-occlusive crisis
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Clin J Gastroenterol Table 2 Reported conversion rate from laparoscopic to open surgery and the underlying cause
Authors
N
Al-Salem et al. [1]
52
1 (1.93)
Severe adhesions
21
1 (4.76)
Severe adhesions Uncontrolled bleeding from the cystic artery
Al-Mulhim et al. [12]
35
2 (5.71)
Al-Mulhim et al. [13]
54
6 (11.11)
Not mentioned
Al-Wabari et al. [17]
47
1 (2.13)
Severe adhesions
Seguier-Lipszyc et al. [42]
29
1 (3.45)
Hemorrhaging of the cystic artery
Long-term effects of cholecystectomy We did not find any article in the literature discussing specifically the long-term effects of cholecystectomy among pediatric or even adult patients with SCD. However, the following points should be mentioned about the long-term effects of cholecystectomy in general:
•
•
CBD dilation: many studies investigated CBD dilation after cholecystectomy. The normal CBD diameter is \6 mm. However, this is not applicable to patients who underwent cholecystectomy. Resection of the gallbladder, which is the normal reservoir of bile, may cause a physiological compensation that results in dilation of the CBD to be the new reservoir of bile. Park et al. followed two groups of patients who underwent cholecystectomy with a preoperative CBD diameter \7 mm (i.e., those patients who did not have CBD disease and ERCP was not performed on both groups) for 6 and 12 months and concluded that a CBD diameter reaching up to 10 mm is considered a normal physiological compensation. No clinical manifestations were present, and patients remained asymptomatic with normal LFT. The increase of CBD diameter was found to be correlated with age [23]. Post-cholecystectomy syndrome (PCS): this can be defined as ‘recurrence of symptoms similar to those experienced before the cholecystectomy’, and includes dyspepsia and right upper-quadrant pain, with or without jaundice. The onset of PCS varies from 2-25 days post cholecystectomy. The incidence of PCS is 40%, and one study concluded that females are more prone (43%) than males (28%) for PCS. The etiology of PCS is variable and will not be discussed here [24]. Pigment stones in the CBD: 4–24% of patients who undergo cholecystectomy develop recurrence of CBD
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Reasons
Al-Salem et al. [7]
each study we reviewed. The variation between the studies may be due to the variability of experience among surgeons. The more recent studies have a lower conversion rate which may signify improvements in laparoscopy techniques and instruments.
•
Converted to open (%)
•
stones. This recurrence could be due to bile stasis or bacterobilia. CBD dilation [13 mm, biliary strictures, papillary stenosis, and stones in patients with gallbladder in situ are common risk factors [25]. Colorectal cancer: this concern was not discussed or investigated in patients with pigment stones such as patients with SCD. It was mainly investigated in patients with cholesterol stones, and a significant association was found [26], but no causation has been proven. Probably both conditions are related to the common etiology of high saturated fat consumption.
Challenges in management options Acute chest syndrome ACS is defined as the onset of new lobar infiltration on chest X-ray, excluding atelectasis, accompanied by fever [38.5C, cough, dyspnea and commonly peluric pain [16]. The deoxygenated sickled cells will remain in the deoxygenated state due to endothelial cell activation; they then accumulate, leading to infection, inflammation, and lung infarction. According to Kokoska et al., ACS risk factors include operative blood loss, weight, age, and hypothermia during surgery [27]. Diarra et al. also mentioned that hypoventilation due to increased intra-abdominal pressure with a resultant raise of the diaphragm and CO2 insufflation during LC that may be partially absorbed can lead to metabolic acidosis. All these factors are associated with ACS development [16].
Controversial issues Preoperative blood transfusion (PBT) Many studies adopted PBT, whether it is simple or exchange, in order to increase the Hb level to around 10 g/ dL, hematocrit [30–40%, and reduce HbSS percentage to \50% [1, 5, 8, 10, 13, 15, 17, 18, 28–33]. Other studies argued that it minimized intra- and postoperative
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complications such as VOC, intraoperative hypoxia, bleeding, and ACS [4, 5, 12, 33–35]. For example, a study in 1995 of 3765 patients showed PBT is a significant factor in lowering postoperative complications (p value = 0.009) [36]. Interestingly, as PBT elevates oxygen transportation and supply, Kokoska et al. suggested that PBT may explain the low incidence of ACS in their sample (sample size 60, ACS incidence 6%) [27]. Despite all the favorable outcomes mentioned above for PBT, some studies refused to consider PBT as a prophylactic standard or even to perform it. Aziz and Meshikhes claimed that postoperative complications in transfused patients (n = 16, 31.25%) are high compared to nontransfused patients (n = 24, 0%) with a p value = 0.002 [37]. The authors also showed a concern for transfusionrelated complications such as hyperhemolysis and delayed hemolysis. Moreover, the authors strengthened the findings with the results from other observational studies that shared the same goal as theirs and another study conducted in Saudi Arabia with a p value = 0.002 [38]. It also has to be mentioned that the use of PBT was reduced only for necessary cases by some authors such as Diarra et al. [16]. In contrast, multiple studies highly recommend the use of PBT as a prophylactic technique [5, 12, 18, 29, 39], and Marakis et al. considered it as a standard of care for patients with SCD [40]. Some essential notes were found while reviewing the literature. Al-Mulhim et al. noted that there is no significant difference between exchange PBT and simple PBT [12]. Poffenberger et al. highlighted that an elevation in pigment load leading to stone configuration and mud-like derivations from the bile may be a result of repeated blood transfusions [39]. If Hg is \10 mg/dL, it is advised to transfuse multiple but not too many dosages of packed erythrocytes at 10–15 days before surgery [14]. AlMulhim et al. highlighted the fact that PBT improves anesthesia methods [13]; however, prolonged anesthesia should not be allowed in order to avoid ACS [41]. We believe that PBT is strongly indicated and should be one of the standards of care for SCD patients suffering from gallstones to obtain at least 10 mg/dL Hb. PO-ERCP or intraoperative cholangiography (IOC) A discussion was found focusing on the need for preoperative ERCP rather than IOC. The different points of view behind preferring PO-ERCP were (1) the difficulty in deciding whether to choose postoperative ERCP or switch to open surgery, (2) IOC has a false-positive rate of 25% which may result in needless exploration of CBD, (3) IOC requires experienced surgeons, and (4) IOC will result in prolonged operative time [1, 9]. The authors of one study stated that IOC is not performed in their hospital as it raises the operation cost and time, without minimizing the risk of
biliary duct injury. Nevertheless, Al-Salem et al. linked biliary duct injury with surgeon experience [7]. Johna et al. declared that the valves of Heister and cystic duct angulation and/or size might lead to failure of IOC [10]. On the other hand, pre- or post-ERCP reported no mortality and slight morbidity. Bleeding, pancreatitis, cholangitis, and retroperitoneal perforation have been reported as complications of ERCP [8]. Thus, there is no need to perform IOC or CBD exploration, if ERCP is available and the patient’s size allows it [1, 7, 10, 11]. Nevertheless, Bonatsos et al. reported that ERCP was performed in five patients— three had CBD stones and two did not. One of the two had a stone while performing IOC [14]; however, this stone could have passed to the CBD after ERCP. For that reason, even if CBD stones are found during surgery, it is highly recommended to perform postoperative ERCP [17]. Another practical option is to convert the operation to an open procedure as it has lower morbidity (7%) than postoperative ERCP (13.5%); this approach avoids second anesthesia which carries its own risk for patients with SCD [18]. LC as a prophylactic procedure for cholelithiasis The French National Authority for Health has advised LC for children with SCD who are diagnosed with cholelithiasis, even if they are asymptomatic [18]. Repeated hemolytic crises among patients with SCD increase bilirubin level and lead to the formation of gallstones [5]. Curro et al. said that children under consideration for cholecystectomy have a significantly higher risk of developing complications [5]. Therefore, we found that many studies recommended LC in asymptomatic patients with SCD. Furthermore, it was found that the number of hospital visits doubled for patients with symptomatic gallstones compared to asymptomatic ones [5]. More importantly, the chance of gallstone complications among the asymptomatic patients is 50% within 3–5 years [5]. One of the surprising findings was that the gallbladders of symptomatic patients were found to be inflamed and infected at histopathologic examination [5]. Inflammation and infection of the gallbladder are well-recognized causes of reducing the survival rate of RBCs and increasing the chance of a hemolytic crisis [5]. Since the RBCs of SCD patients are unstable, cholelithiasis prophylactic surgery aims to reduce the hospital stay and the probability of developing complications. Hendricks-Ferguson et al. said that most surgeons nowadays perform elective LC in SCD children with asymptomatic gallstones to avoid the complications of urgent LC [20]. Table 3 shows the significant outcomes of prophylactic surgery regarding operative time, complications, and postoperative stay as reported by Curro et al. [5].
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Clin J Gastroenterol Table 3 Comparison between pediatric SCD patients with symptomatic and asymptomatic gallstones as reported by Curro et al. Author
Variables
Patients with symptomatic gallstones
Patients with asymptomatic gallstones
Curro et al. [5]
Number Age
10 x = 16.7
16 x = 13.1
N/A
Operative time in minutes
x = 90
x = 65
0.002
Postoperative stay in days
7.4 (4–10)
3 (2–4)
Overall complications Fever
3
1
Wound infection SCC
2 3
1 0
•
All the reviewed articles had some points in common, and we would like to recommend an outline for managing gallstones in patients with SCD.
• •
•
•
•
•
•
All pediatric patients with SCD should undergo an abdominal ultrasound annually for the presence of gallstones. This is supported by the fact that elective LC has less morbidity and less total hospital stay. In addition, asymptomatic gallstones are thought to cause symptoms in 50% of patients within 3–5 years. Pediatric SCD patients who are found to have gallstones should be evaluated for LC on elective basis. Pediatric SCD patients presenting with abdominal pain resembling VOC associated with jaundice or fever should be evaluated for acute cholecystitis. Patients presenting with CBD stones (obstructive jaundice) or biliary pancreatitis should undergo ERCP after adequate fluid management and antibiotic coverage. MRCP is a non-invasive diagnostic tool that can be utilized if ultrasound findings do not give adequate information. Furthermore, MRCP is highly recommended in patients who are too small for ERCP. Perioperative preparation and management should be undertaken using a multi-disciplinary approach including a hematologist, a surgeon, and an anesthetist to ensure patient safety and to avoid perioperative complications (e.g., VOC, ACS, and stroke). Blood transfusion (simple blood transfusion or exchange transfusion) is highly recommended to improve oxygen-carrying capacity and decrease total HbSS concentration. A Hb level of approximately 10 mg/dL is adequate to improve oxygenation and decrease sickling without increasing the risk of hypercoagulability and hemolysis that may occur with overtransfusion. Adequate analgesia, oxygen therapy, and fluid management must be continued 1–2 days postoperatively.
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0.0001 0.03
Recommendations
•
Significance level (p value)
•
IOC is recommended as indicated if ERCP is not feasible and the patient has CBD stones on ultrasound or MRCP. CBD stones found by IOC must be extracted either laparoscopically or via open surgery at the time of cholecystectomy. World-wide, little is known about the long-term outcomes of prophylactic LC for cholelithiasis in pediatric patients with SCD. We recommend conducting further research to evaluate the long-term outcomes of perfuming prophylactic LC for cholelithiasis in pediatric patients with SCD.
Conclusion Of all hemoglobinopathies, SCD is the most common. With the improvements in healthcare, patients with SCD are expected to have a near-normal life expectancy. From our review, we found that there is a lack of consensus or evidence-based treatment guidelines addressing gallstones associated with SCD pediatric patients. None of the recommendation reached level I or II evidence. Thus, for the previous recommendations to be guidelines, they need to be discussed by expert panel consensus that includes pediatric surgeons, hematologists, and anesthetists. Current practice differs greatly depending on the prevalence of SCD in a geographic area. We acknowledge the limited number of patients reported, the lack of randomized control trials addressing the practice of specific recommendations, and the need for further evidence-based studies. Compliance with ethical standards Conflict of interest: Yousef M. Al Talhi, Bader Hamza Shirah, Muteb Altowairqi, and Yasmin Yousef declare that they have no conflict of interest. Human Rights: All procedures followed have been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
Clin J Gastroenterol Informed Consent: This study does not involve human subjects and informed consent is not required.
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