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Role of Endoscopic Ultrasound for Evaluating Gastrointestinal Tract Disorders in Pediatrics: A Tertiary Care Center Experience

Al-Rashdan, Abdullah; LeBlanc, Julia; Sherman, Stuart; McHenry, Lee; DeWitt, John; Al-Haddad, Mohammad

Journal of Pediatric Gastroenterology and Nutrition: December 2010 - Volume 51 - Issue 6 - p 718–722
doi: 10.1097/MPG.0b013e3181dac094
Original Articles: Gastroenterology
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Background: Endoscopic ultrasound (EUS) with or without fine needle aspiration (FNA) has a well-established role in the evaluation of various gastrointestinal (GI) tract disorders in adults. The clinical impact of EUS on the management of the pediatric population remains less clear. This study evaluates the feasibility, safety, and applications of EUS ± FNA in pediatric GI tract disorders.

Patients and Methods: Using a prospectively maintained EUS database, all patients 18 years of age or younger referred for EUS at our institution were identified. Retrospective chart review was conducted to document procedure indications, type of anesthesia used, EUS findings, final FNA cytology results, and clinical impact of EUS ± FNA on the subsequent management of pediatric patients.

Results: Fifty-eight EUS procedures were performed in 56 patients (35 girls). Median age was 16 years (range 4–18 years). The main indications for EUS were acute or recurrent pancreatitis, abdominal pain of suspected pancreatobiliary origin, suspected biliary obstruction, upper GI mucosal/submucosal lesions, and evaluation of pancreatic abnormalities seen on prior imaging. Sedation used included nurse-administered propofol sedation in 38 (73%), general anesthesia in 9 (17%), and fentanyl with meperidine in 3 (6%). Five therapeutic procedures performed included celiac plexus blocks in 4 and 1 EUS-guided pancreatogram. In 44 (86%) patients, EUS provided a new diagnosis. The procedure was successfully completed in all patients with no reported complications.

Conclusions: EUS ± FNA is feasible and safe and makes a significant impact on most pediatric patients. Nurse-administered propofol sedation appears to be safe and well tolerated in this group.

From the Department of Gastroenterology & Hepatology, Indiana University/Clarian Health Partner, Indianapolis, IN, USA.

Received 30 October, 2009

Accepted 21 February, 2010

Address correspondence and reprint requests to Abdullah Al-Rashdan, MD, 550 N University Blvd, UH4100, Indianapolis, IN 46202 (e-mail: aalrashd@iupui.edu).

This article was presented at Digestive Diseases Week 2009 as topic forum “Advances in Pediatric Endoscopy” presentation.

The authors report no conflicts of interest.

Compared to their use in an adult population, advanced endoscopic procedures such as endoscopic ultrasound (EUS) are used less frequently in children. This is primarily due to a lower incidence of pancreaticobiliary disorders as well as less frequent gastrointestinal (GI) tract tumors in this age group. Although the role of EUS in adults has been well established, few reports have evaluated its utility in pediatric patients (1–7). Evaluation of pancreaticobiliary disorders is the most common indication for EUS referrals in a pediatric population (1–5). Most EUS procedures in children are performed by adult gastroenterologists and often at tertiary care centers (3,4,8). However, despite its safety and high diagnostic yield, the use of EUS and EUS-guided fine needle aspiration (EUS-FNA) in the pediatric population remains limited.

The primary aim of our single-center study was to report the feasibility, safety, and impact of EUS and EUS-FNA on the management of GI tract disorders in children at our institution. A secondary aim was to evaluate the safety of nurse-administered propofol sedation (NAPS) for EUS in this age group.

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PATIENTS AND METHODS

This study was approved by the institutional review board at Indiana University Medical Center/Clarian Health Partners. The EUS database at our hospital during an 8-year period (January 2000–October 2008) was searched for all patients 18 years of age or younger referred for EUS. Demographic, clinical, pathological, and radiographic data were recorded from existing medical records. The following clinical data were obtained: age, sex, indications of the EUS procedure, type of anesthesia used, EUS findings, any therapeutic interventions performed, procedure-related complications, and impact of EUS on patient's subsequent management.

Relevant data from EUS-FNA were abstracted and included site, size, structure and echogenicity of lesions biopsied, number of needle passes, and final cytology results. Pertinent follow-up data were obtained by review of existing medical records.

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Complications: Definitions and Assessment

For study purposes, procedure-related complications were defined as hypotension (absolute systolic blood pressure ≤80 mmHg) at any time during the procedure; hypoxia (oxygen saturation ≤85%); bradycardia (≤50 beats/min); need for supplemental oxygen above baseline supplementation, positive pressure ventilation, or endotracheal intubation; bleeding recognized during EUS or by subsequent imaging study; blood transfusion; and abdominal pain, fever, or requirement for hospitalization. All of the patients were monitored throughout the procedure and assessed immediately afterward before discharge from the laboratory. Per our department protocol, all of the patients were contacted by telephone 48 hours later to assess early postprocedural complications.

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EUS-FNA and Interventional Techniques

After written informed consent was obtained from parents or guardians, patients received general anesthesia: moderate or deep sedation using various combinations of intravenous midazolam, meperidine, fentanyl, or propofol under appropriate cardiorespiratory monitoring. In accordance with a hospital-approved deep sedation policy, registered nurse-administered propofol sedation (NAPS) was available in our endoscopy for all patients, beginning in 2001 (9). During the second half of the study period, commencement of deep sedation was usually initiated with a combination of midazolam and meperidine or fentanyl to minimize total requirements of propofol sedation (10). The choice of moderate or deep sedation was made at the discretion of the endosonographer; however, consultation with an anesthesiologist was routine for patients 14 years or younger to determine whether general anesthesia was appropriate.

All of the procedures were performed by or under the supervision of 1 of 6 experienced attending endosonographers. EUS examinations were classified into 2 major categories: upper EUS, when upper digestive tract, mediastinum, or proximal peritoneum was studied; and lower EUS, when the anorectal and the perirectal areas were studied. All of the examinations were usually initiated with an Olympus GF-UM20, GFUM-130, or GF-UM160 radial echoendoscope (Olympus America, Inc, Center Valley, PA). Curvilinear array endosonography was performed using the Pentax 32-UA, Pentax 36-UX (Pentax Medical Co, Montvale, NJ), Olympus GF-UC30P, or Olympus GF-UC140P-AL5 (Olympus America, Inc) echoendoscope. When indicated, EUS-FNA was performed using a 22-gauge EUSN-1, EUSN-2, EUSN-3, or Echotip Ultra needle (Cook Medical Inc, Winston-Salem, NC) or EZ-Shot needle (Olympus America, Inc). Core biopsies, if indicated, were performed using 19-gauge Trucut biopsy (TCB) device (Quick-Core, Cook Medical, Winston-Salem, NC), according to previously described techniques (11). A Doppler examination was used to ensure the absence of intervening vascular structures along the anticipated needle path. Depending on the amount of blood anticipated during tissue sampling, full, partial, or no suction was applied. Samples aspirated were expressed onto a glass slide and 2 smear preparations were made. One slide was air dried and stained with a modified Giemsa stain for rapid on-site interpretation, whereas the other slide was alcohol fixed and stained by the Papanicolaou method. A cytopathologist was available on-site for preliminary diagnostic interpretations and assessment of specimen adequacy on all of the procedures. EUS-FNA was repeated until a definitive diagnosis was made or the endosonographers felt that further sampling would not likely increase yield. Core biopsies were directly submitted in formalin without touch preparations. Definitive pathological diagnoses were given only after complete staining and subsequent final interpretation was provided.

Celiac plexus block was performed in 1 or 2 sites alongside the aorta using a combination of triamcinolone and bupivacaine as previously published. One dose of intravenous antibiotics (eg, ampicillin/sulbactam, fluoroquinolone) was given immediately following the procedure followed by 3 to 5 days of oral antibiotics (eg, amoxicillin/clavulanate, fluoroquinolone) if celiac plexus block was performed or cysts were aspirated (12). EUS was considered to have a significant impact on patient management if a new diagnosis was rendered, therapeutic intervention was performed, or the EUS findings altered subsequent treatment plans.

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RESULTS

Fifty-eight procedures (54 upper EUS, 4 lower EUS) were performed on 56 children (35 girls) with a median age of 16 years (range 4–18). Indications for the EUS examinations are demonstrated in Table 1. All of the patients underwent radial EUS. Fifteen underwent EUS-FNA (median passes 3; range 1–10) of pancreatic lesions (9), lymph nodes (2), and cysts/submucosal lesions (4). Three patients with recurrent abdominal pain and enlarged pancreas on computed tomography (CT) underwent successful transgastric core biopsy of pancreatic body or tail. Final histopathology in all 3 showed chronic idiopathic pancreatitis and thus precluded further diagnostic workup. Interventions were performed in 5 patients. Four patients with abdominal pain due to established chronic pancreatitis received celiac plexus blocks, and 1 EUS-guided pancreatogram was done after failed selective pancreatic duct cannulation during ERCP. All patients with abdominal pain of unknown etiology (n = 15) underwent upper endoscopy and abdominal cross-sectional imaging by CT scan or conventional ultrasound with unremarkable findings. Similarly patients with established pancreatitis (acute or recurrent, n = 13) were referred for EUS to investigate the underlying etiology of pancreatitis. Patients with abnormal pancreas on CT/MRI (magnetic resonance imaging) (n = 8) were referred for EUS-FNA of established mass lesions in 2, enlarged gland suspicious of neoplastic lesions in 3, and abnormal peripancreatic collections or cysts in 3. Overall, 44 (86%) patients received a new diagnosis following EUS, which influenced subsequent clinical management (Table 2). EUS was nondiagnostic in 7 patients (5 with abdominal pain of suspected pancreatobiliary etiology found to have normal sonographic imaging of the pancreas and bilary tree, 2 with idiopathic rectal pain found to have normal anorectal and perirectal sonograms). EUS was successfully completed in all of the patients with no immediate complications reported.

TABLE 1

TABLE 1

TABLE 2

TABLE 2

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Sedation, Anesthesia, and Complications

Data regarding sedation administered were available in 52 of 58 (90%) patients (Table 3). NAPS was given to 38 (73%) patients. When propofol was used alone (n = 15), a median dose of 365 mg (range 100–800 mg) was given; however, when propofol was combined with midazolam and fentanyl (n = 23), the median doses used were 290 mg (range 80–450), 2 mg (range 1–8), and 50 μg (range 50–200), respectively. Nine patients underwent general anesthesia. Three patients were sedated only with a combination of midazolam (median dose 9 mg, range 8–10) and fentanyl (median dose 150 μg, range 110–200). All of the procedures were successfully completed with no immediate complications related to sedation. No patient required positive pressure ventilation due to sedation administration. Two patients undergoing EUS for anorectal indications required no sedation.

TABLE 3

TABLE 3

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DISCUSSION

The present study demonstrates the feasibility and safety of diagnostic and therapeutic applications of EUS in the pediatric population. We found that pancreatobiliary disorders were the most common indication for EUS, which is similar to that reported in prior series (1–4). EUS has been shown to be of particular value in diagnosing conditions that are unique to or more commonly seen in children, such as congenital anomalies (4,7,13), tumors such as solid pseudopapillary tumor of the pancreas (14), as well as some anorectal disorders (1,4,15). In our study, 41(71%) procedures were performed to evaluate acute and or recurrent pancreatitis, suspected biliary obstruction, pancreatic abnormality detected by other imaging studies (CT/MRI), or upper abdominal pain of suspected pancreatobiliary origin (Table 1).

Overall, a new diagnosis was provided by EUS (Table 2) in 44 patients (86%). This high diagnostic yield is largely explained by establishing the diagnosis of chronic pancreatitis in 20 of 44 as well as other pancreatic pathologies such as congenital anomalies (pancreas divisum, n = 2) and pancreatic tumors/cysts (n = 9). EUS is known to be a sensitive tool to study the pancreas in particular and detect early pathological changes such as chronic pancreatitis due to proximity of the ultrasound probe to the entire gland in the stomach or duodenal bulb. This peculiar aspect with the ability of performing FNA gives this technique an advantage over other conventional cross-sectional imaging of the pancreas. Because of its ability to differentiate all 5 gut layers, EUS has emerged as a real-time imaging of choice to study mucosal or subepithelial esophageal, gastroduodenal, and anorectal lesions. In our series, EUS was indicated in 8 patients with mucosal/submucosal lesions seen on conventional endoscopy; all 8 patients had accurate diagnosis established by sonographic criteria. Similarly, Varadarajulu et al (2) and Attila et al (6) reported 71% and 84% diagnostic yield of EUS in their series, respectively.

We also found that EUS-guided therapeutic procedures can be performed in children as are routinely done in adults. We demonstrated the technical success and safety of celiac plexus block for pain control of established chronic pancreatitis in 4 patients. Another patient who previously underwent pancreaticoduodenectomy for a choledochal cyst had EUS-guided pancreatic duct puncture for contrast injection after failed cannulation of the pancreatic duct during ERCP.

Certain infrequent tumors of the pancreas that are peculiar to young individuals could be readily diagnosed with EUS-FNA (16,17). For example, 2 patients ages 15 and 16 years with solid pseudopapillary tumor were accurately diagnosed by EUS-FNA. Both patients underwent successful distal pancreatectomy. EUS-FNA also diagnosed a carcinoid tumor of the pancreas in a 12-year-old boy, which was inoperable due to mediastinal lymph node metastasis.

The present series demonstrated that EUS-FNA can be performed safely in children, with a high diagnostic accuracy, as previously reported (2,4,6,14). Three patients with pseuodcysts underwent diagnostic aspiration for persistent abdominal pain following acute pancreatitis, benign retroperitoneal cysts and hematoma in 2 patients, 1 gastric lipoma, 1 mediastinal lymphadenitis, and 3 duodenal duplication cysts, in which 1 was surgically removed due to preexisting infection and 2 suspected pancreatic head lesions were proved to be inflammatory fluid collection as a result of ongoing pancreatitis.

General anesthesia, in this series, was used particularly in younger patients. The patient's age, weight, comorbidities, anticipated procedural complexity and length, physician preferences, and institutional guidelines are important factors that influence the choice of sedation in advanced procedures, particularly for children (8). General anesthesia has been thought to be exclusively required for sedation of children undergoing advanced endoscopic procedures such as EUS due to certain physiological factors that predispose them to increased airflow resistance and airway occlusion (2,3). Propofol administered by an anesthesiologist without the need for endotracheal intubation or positive pressure ventilation has been shown to be a safe and effective agent for the induction and maintenance of sedation in children undergoing GI endoscopy while providing excellent amnesia during the procedure (1,18). Lightdale et al (19) reported that anesthesiologist-administered propofol sedation may not lead to faster sedation, recovery, or discharge times than endoscopist-administered sedation with midazolam and fentanyl. On the contrary, our group reported that using NAPS for adult EUS procedures offered a faster sedation induction and full recovery time, higher postprocedure patient satisfaction, and a quicker anticipated return to baseline function when compared with conscious sedation with midazolam and meperidine (20). Kaddu et al (21) showed in a randomized trial that the use of propofol for pediatric GI tract endoscopy resulted in less total time for anesthesia and recovery with an equally safe profile to general anesthesia. This study, however, did not include endoscopy procedures that required interventions such as EUS. In contrast to prior published series, the present series appears to be the first to report the safety and feasibility of NAPS for EUS procedures in children (Table 4). Although propofol sedation was not used for children younger than the age of 10, no adverse events directly related to anesthesia were reported in any age group.

TABLE 4

TABLE 4

This study has a few limitations that merit discussion. First, it is a retrospective study from a single tertiary referral center with no intermediate or long-term follow-up data. Second, the present study does not represent patients from all of the pediatric age groups evenly, particularly young children and infants in whom congenital disorders are more likely to be prevalent. The majority of our patients belonged to the teenage group, with median weight of 65 kg, which also limits generalizability of our findings regarding sedation to younger children. However, including patients from this young age group is technically challenging to perform with the presently available EUS instruments (1,3,22).

Our report highlights the important role of an adult gastroenterologist in the management of the pediatric population by providing the technical expertise needed to perform advanced endoscopy. This skill is infrequently available to pediatric gastroenterologists during their training (8). In conclusion, this study supports the applicability and safety of EUS with or without FNA for pediatric patients with a wide variety of GI tract disorders. We agree that EUS could replace ERCP as a diagnostic tool for evaluation of most pancreatobiliary disorders in children as previously anticipated (1–5). In fact, it has been the practice among our group for several years to consider EUS as the first tool for many pediatric ERCP referrals.

EUS as a noninvasive procedure has the potential to attract more pediatric gastroenterologists to consult with their counterpart adult gastroenterologist endosonographers and surgeons to minimize high-risk procedures to their patients. More studies are needed to evaluate the cost-effectiveness of industrial development of ultrasound imaging and scope design for children, particularly the young ones, who often require the assistance of anesthesia service when using standard-size equipments. The need for pediatric gastroenterologists to be trained in endosonography to meet the expected future rise in demand for these procedures remains to be determined.

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Keywords:

children; endoscopic ultrasound; fine needle aspiration; gastrointestinal tract disorders; nurse-administered propofol sedation

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