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Keywords:

  • functional dyspepsia;
  • functional gastrointestinal disorders;
  • gastric electric stimulation;
  • gastroparesis

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

Background

Our objective is to evaluate the effect of gastric electrical stimulation (GES) on symptoms and quality of life for pediatric patients with functional dyspepsia (FD).

Methods

Twenty-four patients (16 female, median 15 years) were treated with GES for FD after a median of 24 months of symptoms (3 months–14 years). At baseline, 46% required tube feeds and 25% parenteral nutrition. Sixty percent had gastroparesis. The PedsQL GI Module (PedsQL) was completed for 18/24 both pre-/post-GES after a median of 8 months. Patients also completed the Symptom Monitor Worksheet (SMW) pre-/post-GES after a median of 6 months. Pre-/post-GES global health was also assessed.

Key Results

Significant improvements were seen in multiple areas of the PedsQL, including stomach pain/upset, food/drink limits, heartburn/reflux, gas/bloating, patient worry, medication tolerance, and constipation (P < 0.05). A decrease was found in combined symptom severity/frequency based on SMW (P < 0.01). Improvements were made in all categories, including vomiting, nausea, early satiety, bloating, fullness, epigastric pain, and burning (P < 0.01). Improvements in PedsQL/SMW scores remained when analysis was limited to normal or delayed gastric emptying (P < 0.05, P < 0.05). Thirteen percent needed tube feeds and 13% parenteral nutrition after GES. Sixty-five percent reported that their health was much improved after GES vs 15% the same or worse. Five patients experienced complications, primarily mild abdominal discomfort.

Conclusions & Inferences

In the largest series to date of pediatric patients who have undergone GES for FD, we found significant improvements in upper gastrointestinal symptoms, quality of life, and perception of global health. Patients were less dependent on tube feeding or parenteral nutrition.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

Functional dyspepsia (FD) in children is defined by the pediatric Rome III criteria as upper abdominal pain or discomfort not associated with alteration in defecation, stool frequency or form that occurs at least once per week for at least 2 months. These symptoms must occur without evidence of organic disease.[1] Other symptoms commonly associated with FD include postprandial fullness, early satiety, and nausea. Functional dyspepsia has been found to be associated with anxiety and depression.[2] The prevalence of FD in children remains unclear. A recent survey of children in a developing country showed a prevalence of 2.5%, whereas studies in adults have described rates as high as 29%.[3, 4] Patients with FD can have delayed, normal, or accelerated gastric emptying. Traditional medical treatment for FD includes tricyclic antidepressants, proton-pump inhibitors, H2 antagonists, and prokinetic agents.

Symptoms of FD can overlap with other upper gastrointestinal disorders, including gastroparesis (GP), a condition characterized by delayed gastric emptying in the absence of mechanical obstruction. Patients with GP typically experience nausea, vomiting, early satiety, and upper abdominal pain. The true prevalence of GP is difficult to estimate, but a recent study estimates that delayed gastric emptying occurs in 1.8% of individuals in the community.[5] The prevalence of delayed gastric emptying seems to be higher in adolescents with FD than those in healthy control subjects.[6] Medical treatment for GP includes prokinetic agents, antiemetic medications, and dietary modifications with intake of small, frequent, low-fat meals. Side effects prevent as many as 40% of adult patients from tolerating chronic use of prokinetic agents.[7]

For patients with FD or GP refractory to medical and dietary therapy, further treatment options are limited and include the use of jejunal feeding, intrapyloric botulinum toxin injections, and gastric electrical stimulation (GES), a therapy commonly known as a ‘gastric pacemaker’. Gastric electrical stimulation therapy consists of an implanted neurostimulator that delivers high-frequency, low-energy electrical stimulation through electrodes implanted in the muscle wall of the antrum.[8] An implantable gastric electrical stimulator was approved by the United States Food and Drug Administration in 2000 as a humanitarian use device for treatment of diabetic and idiopathic GP. Over the past decade, GES therapy has been shown to consistently provide significant and sustained symptomatic improvement in adult patients with FD with both normal and delayed gastric emptying. Improvements in quality of life, nutritional status, and overall functioning have been documented, as well as a decreased need for hospitalization.[9-11] A recent meta-analysis of 13 studies showed significant decreases in symptom severity scores and improved quality of life after GES therapy, and also demonstrated low heterogeneity between studies for most outcomes.[12]

Despite these encouraging results in adults, information on GES therapy in pediatric patients is very limited. This article describes the effect of GES therapy on a series of pediatric patients with FD. The primary aims of our study were: (i) to evaluate the effect of GES therapy on FD symptoms and quality of life in pediatric patients with and without GP and (ii) to assess the feasibility and safety of GES therapy in the pediatric population.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

Approval was obtained from the Nationwide Children's Hospital Institutional Review Board prior to initiation of this study.

Subjects

Our study includes patients referred to the Motility Clinic at Nationwide Children's Hospital in Columbus, OH with symptoms of FD from 2009 to 2011 who were treated with GES therapy. Gastric electrical stimulation therapy was offered to each patient after failure of medical treatment. If the patient was felt to be a suitable candidate for GES therapy based on an initial evaluation, an inpatient stay was scheduled during which GES therapy was to be initiated. Most patients underwent endoscopic placement of electrodes to provide temporary GES therapy prior to initiation of permanent GES therapy. Patients who underwent temporary GES therapy were observed for an improvement in abdominal pain, nausea, and overall comfort of at least 50% for 2–4 days. Those who did not experience symptomatic improvement with temporary GES therapy subsequently had the electrodes removed and did not go on to have permanent GES therapy placed. Patients who did experience at least 50% improvement in their clinical symptoms underwent surgical implantation of the permanent GES device and electrodes. Each device was initially programmed according to a standard set of parameters. After discharge, patients were followed in clinic every 3 months. Device parameters were subsequently adjusted based on each patient's clinical response.

Outcome measures

Our primary outcome measure was the Symptom Monitor Worksheet (SMW), a one-page questionnaire asking each patient to rate the severity and frequency of several gastrointestinal symptoms on a scale of 0–4. These gastrointestinal symptoms included vomiting, nausea, early satiety, bloating, postprandial fullness, epigastric pain, and epigastric burning. Severity was reported using the following scale: (0) absent; (1) mild or not influencing normal activities; (2) moderate or diverting from, but not urging modification of, usual activities; (3) severe or influencing usual activities severely enough to urge modifications; (4) extremely severe or requesting bed rest. Frequency was reported using the following scale: (0) absent; (1) rare or 1 time per week; (2) occasional or 2–4 times per week; (3) frequent or 5–7 times per week; (4) extremely frequent or greater than 7 times per week.

Patients also completed the PedsQL GI Symptoms Module (PedsQL), a more extensive survey that collects information on the following areas: stomach pain and hurt, stomach upset, food and drinks limits, trouble swallowing, heartburn and reflux, gas and bloating, constipation, diarrhea, worry, medicines, and communication. Each area is comprised a number of more specific complaints, and responders were asked to rate each complaint using the following scale: (0) it is never a problem, (1) it is almost never a problem, (2) it is sometimes a problem, (3) it is often a problem, (4) it is almost always a problem.[13] We also monitored patients' route of nutrition, specifically whether or not gastric/jejunal feeding or parenteral nutrition were needed. Finally, subjects were also asked about their perception of their global health before and after GES initiation.

Data collection and analysis

The SMW was completed prior to GES placement and at each follow-up visit. Pre-GES and post-GES data were collected for 22 patients. The follow-up SMW was completed after a median of 6 months, with a range of 1–20 months. The PedsQL was completed both at follow-up and retrospectively to assess symptoms prior to GES initiation in 18 patients. The follow-up PedsQL was completed a median of 8 months after GES initiation, with a range of 2–30 months. Questionnaires were completed by either the patient or a parent, depending on the patient's age.

Pre-GES and post-GES data were compared using the paired t-test and Wilcoxon signed-rank test. Statistical significance is defined as having a P-value < 0.05. Analysis was conducted by SAS 9.2 (by SAS Institute Inc., Cary, NC, USA).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

Patient characteristics

Twenty-six patients received GES therapy. Twenty-three patients (88%) underwent temporary GES therapy prior to permanent GES therapy. Two of these 23 patients did not experience symptomatic improvement and subsequently did not have permanent GES therapy initiated. Three patients directly received permanent GES placement. Thus, a total of 24 patients received permanent GES.

Among the 24 patients who underwent permanent GES placement, 16 patients were female and the median age of our subjects was 15 years, with a range of 4–19 years. The GES therapy was started after a median of 24 months of symptoms, with a range from 3 months to 14 years. At baseline, 11 patients (46%) required either gastric or jejunal feeding and six patients (25%) required parenteral nutrition. Twelve patients (60%) had documented delayed gastric emptying and eight patients (33%) had documented normal gastric emptying. Gastric emptying studies were not available for the other four patients. Three patients had type 1 diabetes mellitus. Two of the three diabetic patients had normal baseline gastric emptying and one had delayed emptying. At the time of GES initiation, patients were receiving an average of 6.7 medications each.

Symptom monitoring

Significant improvement in symptom severity was found in all symptoms assessed by the SMW, including nausea (P < 0.001), fullness (P < 0.001), early satiety (P = 0.003), bloating (P = 0.002), epigastric pain (P < 0.001), vomiting (P < 0.001), and burning (P = 0.002), as shown in Fig. 1. The largest improvement was seen in nausea, which was also the predominant symptom in our patients by both severity and frequency. The average severity score for nausea prior to GES therapy was greater than three, which is defined as severe and causing modification of usual activities. The average score at follow-up was less than one, which is defined as mild and not influencing normal activities. The five most severe symptoms by decreasing severity were nausea, postprandial fullness, early satiety, bloating, and epigastric pain.

image

Figure 1. Symptom severity. Symptom severity rated using the following scale: (0) absent; (1) mild or not influencing normal activities; (2) moderate or diverting from, but not urging modification of, usual activities; (3) severe or influencing usual activities severely enough to urge modifications; (4) extremely severe or requesting bed rest. Bars represent standard deviation.

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Symptom frequency was also significantly decreased for all symptoms assessed by the SMW, which include nausea (P < 0.001), fullness (P < 0.001), early satiety (P = 0.01), bloating (P = 0.001), epigastric pain (P = 0.003), burning (P < 0.001), and vomiting (P < 0.001), as shown in Fig. 2. Again, the largest improvement was seen in nausea. The average frequency score for nausea prior to GES therapy was nearly four, which is defined as extremely frequent and greater than 7 times per week. The average score at follow-up was just above one, which is defined as rare or occurring about 1 time per week.

image

Figure 2. Symptom frequency. Symptom frequency rated using the following scale: (0) absent; (1) rare or 1 time per week; (2) occasional or 2–4 times per week; (3) frequent or 5–7 times per week; (4) extremely frequent or greater than 7 times per week. Bars represent standard deviation.

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Improvements in symptom severity and frequency persisted when patients were divided based on the presence (N = 11) or absence (N = 7) of GP based on documented gastric emptying studies. However, a number of categories lose statistical significance. These results are shown in Table 1.

Table 1. Symptom Monitor Worksheet severity and frequency in patients with delayed vs normal emptying
 Pre-GES score (SD)Post-GES score (SD)% Change in scoreP-value
  1. SD = standard deviation, *denotes statistical significance.

Delayed emptying (N = 11)
Severity
Vomiting2.5 (1.6)0.8 (1.4)−680.01*
Nausea3.6 (0.7)1.5 (1.2)−570.002*
Early satiety2.4 (1.4)1.6 (1.3)−380.1
Bloating2.6 (1.0)1.0 (1.1)−620.004*
Postprandial fullness2.3 (0.9)1.4 (1.2)−390.06
Epigastric pain2.6 (1.4)1.5 (1.6)−420.04*
Epigastric burning2.2 (1.3)0.9 (1.1)−590.03*
Frequency
Vomiting2.6 (1.8)0.7 (1.1)−720.02*
Nausea3.8 (0.4)1.8 (1.3)−530.002*
Early satiety2.6 (1.5)1.6 (1.6)−380.2
Bloating2.9 (1.1)1.3 (1.5)−550.02*
Postprandial fullness3.1 (1.2)1.6 (1.4)−480.05*
Epigastric pain2.8 (1.4)1.6 (1.6)−460.06
Epigastric burning2.4 (1.4)1.0 (1.4)−580.02*
Normal emptying (N = 9)
Severity
Vomiting2.0 (1.6)0.3 (0.5)−850.06
Nausea3.3 (1.1)0.3 (0.8)−910.02*
Early satiety2.6 (1.3)1.0 (1.2)−620.06
Bloating1.9 (1.5)1.1 (1.7)−420.4
Postprandial fullness2.6 (1.6)0.7 (1.0)−730.03*
Epigastric pain1.7 (1.6)0.7 (1.5)−590.1
Epigastric burning1.6 (1.0)0.7 (1.5)−560.2
Frequency
Vomiting1.7 (1.4)0.3 (0.5)−820.1
Nausea3.1 (1.1)0.3 (0.8)−900.02*
Early satiety3.3 (1.5)1.4 (1.6)−580.06
Bloating2.3 (1.8)1.0 (1.4)−570.2
Postprandial fullness2.9 (1.7)0.6 (0.8)−790.03*
Epigastric pain1.7 (1.6)1.1 (2.0)−350.5
Epigastric burning2.0 (1.3)1.1 (2.0)−450.2

PedsQL GI Symptoms Module

Significant improvements were seen in most areas of the PedsQL, including stomach pain (P = 0.001), stomach upset (P < 0.001), heartburn (P < 0.001), food and drink limits (P < 0.001), gas and bloating (P = 0.01), constipation (P = 0.04), patient worry (P = 0.003), and medication tolerance (P = 0.03), as shown in Fig. 3. We did not find significant improvements in ability to swallow, diarrhea, or the ability of our patients to communicate their symptoms.

image

Figure 3. PedsQL GI Symptoms Module. Score represents the sum total of responses to each section of the PedsQL GI Symptoms Module questionnaire. Bars represent standard deviation.

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When patients were divided based on the presence (N = 9) or absence (N = 6) of GP, improvement in PedsQL remains in the majority of areas assessed but a number of categories lose statistical significance. Among patients with GP, significant improvement remained in stomach upset (P = 0.03), heartburn (P = 0.03), food and drink limits (P = 0.04), and stomach pain (P = 0.03). Among patients with normal gastric emptying, significant improvement remained in stomach upset (P = 0.01) and food and drink limits (P = 0.02). These results are shown in Table 2.

Table 2. PedsQL GI Symptoms Module in patients with delayed vs normal emptying
 Pre-GES score (SD)Post-GES score (SD)% Change in scoreP-value
  1. SD = standard deviation, *denotes statistical significance.

Delayed emptying (N = 9)
 Stomach pain and hurt11.4 (5.0)7.1 (4.8)−370.03*
 Stomach upset28.2 (3.5)18.6 (8.7)−340.03*
 Food and drinks limits19.2 (6.3)12.3 (9.4)−360.04*
 Trouble swallowing1.0 (1.3)0.8 (1.2)−25na
 Heartburn and reflux25.2 (5.2)15.9 (9.0)−370.03*
 Gas and bloating17.2 (5.7)11.4 (9.5)−340.1
 Constipation11.1 (12.9)6.8 (6.5)−390.3
 Diarrhea8.6 (7.6)5.5 (5.6)−360.2
 Worry8.5 (2.7)5.6 (3.6)−340.02*
 Medicines4.4 (3.6)3.1 (3.8)−290.2
 Communication7.5 (4.2)7.3 (4.2)−30.4
Normal emptying (N = 6)
 Stomach pain and hurt7.2 (5.1)4.3 (1.8)−400.1
 Stomach upset25.2 (8.0)12.7 (8.4)−500.01*
 Food and drinks limits19.0 (7.4)9.3 (6.6)−510.02*
 Trouble swallowing2.4 (2.5)1.2 (2.7)−500.2
 Heartburn and reflux18.8 (4.9)13.0 (7.7)−310.1
 Gas and bloating10.0 (10.1)8.5 (10.5)−150.4
 Constipation12.7 (15.7)6.7 (10.4)−470.1
 Diarrhea3.2 (3.6)2.3 (3.7)−260.4
 Worry8.0 (3.0)4.4 (3.1)−450.1
 Medicines7.2 (3.0)5.4 (4.3)−250.2
 Communication8.0 (6.7)5.6 (7.4)−300.2

Route of nutrition

Fewer patients required gastric/jejunal feeding or parenteral nutrition after GES therapy. The number of patients requiring gastric or jejunal feeding decreased from 11 to 3. The number of patients requiring parenteral nutrition decreased from 6 to 3.

Global health

Patients were asked about their global health after GES therapy compared with prior to GES. Thirteen patients (65%) reported that their overall health was ‘much better’. Four patients (20%) reported that overall health was better. One patient (5%) reported that overall health was the same and two patients (10%) that overall health was worse. One of the patients who reported that her global health was worse afterward was subsequently diagnosed with an eating disorder and her symptoms improved with appropriate treatment.

Complications

Among the 24 patients we studied, five patients reported complications after GES placement. Four had mild discomfort or tenderness at the implantation site. Another was found to have a failed battery that required replacement during a second procedure less than 1 year after initial placement.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

In this largest series to date of pediatric patients who have undergone permanent GES therapy for FD and/or GP, we report significant improvement not only in gastrointestinal symptom severity and frequency but also in quality of life and perception of global health. Improvement was observed as long as 30 months after GES initiation. We were also able to show a decrease in dependence on gastric or jejunal feeding and parenteral nutrition, which is perhaps a more tangible indicator of the impact GES therapy had on many of our patients. Although prior pediatric studies have shown improvement in upper gastrointestinal symptoms, we observed improvement in a number of areas that had not been previously evaluated. For example, a significant improvement was seen in constipation. Although not a symptom typically associated with FD or GP, it could be postulated that improvement in dietary intake may lead to more regular bowel function.

Islam et al. published an article in 2008 describing a series of nine adolescent patients with refractory nausea and vomiting who responded well to GES treatment. Significant symptomatic improvement was observed with follow-up ranging from 8 to 42 months.[14] A second case series of three patients between 2 and 3 years of age showed improvement in weekly vomiting frequency with temporary and permanent GES therapy. Other outcome variables were difficult to assess given the young ages of the subjects.[15] In both case series, neurostimulator implantation and GES therapy were generally well-tolerated and investigators concluded that GES therapy is a promising option for medically refractory nausea and vomiting.[14, 15] Our study confirms these findings and in addition demonstrates that the benefits of GES therapy extend beyond symptomatic improvement alone.

Improvements in gastrointestinal symptoms and quality of life were shown in both patients with normal and delayed gastric emptying. This improvement regardless of the presence or absence of GP is consistent with prior studies showing that GES therapy does not have a consistent effect on gastric emptying.[16] While we did not systematically perform gastric emptying studies after GES initiation in this study, four patients did have studies performed both before GES therapy and afterward as clinically indicated. Two patients had normal emptying at baseline and remained normal afterward. Two patients had delayed emptying at baseline and one had normal emptying afterward while the other continued to demonstrate delayed emptying.

The mechanism behind the improvement seen with GES therapy remains unclear. Gastric electrical stimulation has not been shown to affect gastric emptying in a consistent manner. Although some studies have shown improvement in gastric emptying with GES, one study of patients with normal gastric emptying time at baseline described a slowing of gastric emptying after GES therapy in nearly a third of subjects despite improvements in symptoms.[16] Gastric electrical stimulation has not been shown to stimulate gastric muscle contraction or entrain the gastric slow wave.[17, 18] A number of other possible mechanisms have been proposed, including improved gastric accommodation and changes in vagal tone.[19] A multifactorial explanation is most likely. Patients with FD or GP often have baseline impairment in gastric accommodation[20, 21] and GES therapy has been shown to affect gastric tone in animals.[19] A study by McCallum et al. showed an improved discomfort threshold for intragastric pressure as well as increased gastric accommodation with GES therapy. The study also used analysis of heart rate variability to demonstrate increased vagal efferent activity with GES and postulated that thalamic activation observed on positron emission tomography after GES could suggest increased vagal afferent activity, thus concluding that the mechanism of GES therapy could be a result of increased vagal autonomic function.[22] This effect is supported by a canine study that observed a decrease in the gastric relaxation seen as a result of GES therapy after truncal vagotomy.[19]

Our study suggests that GES therapy is generally well-tolerated in the pediatric population. In the prior pediatric study by Islam et al., two of nine subjects ultimately required removal of GES. One case was because of recurrent symptoms and eventual diagnosis of an absence of gastric and duodenal interstitial cells of Cajal, and the other case was due to breakdown of the skin overlying the implanted neurostimulator resulting from trauma.[14] This is in contrast with adults, where in one study of 221 patients, 7% had their implanted neurostimulator removed due to local infection.[9]

Three of our patients continued to require parenteral nutrition after GES therapy. The first patient had a history of intestinal pseudo-obstruction and although she continues to require parenteral nutrition, her overall health was felt to be much improved after GES initiation. The second patient has short bowel syndrome secondary to gastroschisis and experienced a small bowel obstruction a few months after GES initiation. She was restarted on parenteral nutrition after her bowel obstruction. The third patient has an extensive psychiatric history and has ongoing difficulty communicating his symptoms.

Although our study is the largest series of pediatric patients with FD and/or GP treated with GES therapy to date, our sample size still remains limited. This particularly limits our ability to draw conclusions when we divide our sample into smaller groups, for example, those with normal vs delayed gastric emptying. Our length of follow-up was also limited, ranging from a month to over 2 years. The adult literature includes studies demonstrating improvement at up to 10 years after GES initiation, but such information is not yet available in children.[9] Although we were able to show a significant improvement in symptom scores and quality of life, more evidence is needed before we can conclude that these changes will be sustained in the pediatric population. A longer length of follow-up is particularly important in the pediatric population to learn more about the effect of physical growth on electrode placement and efficacy of GES therapy.

The design of our study has inherent limitations as well. A major limitation for many studies on GES therapy is the lack of a true placebo group, particularly as the mechanism of GES therapy remains unclear. A 2003 study incorporated a 1-month observation period after GES implantation with subjects randomized to having the pacemaker turned on or off and reported a preference for having the pacemaker turned on.[8] However, more recent controlled trials using temporary GES therapy did not show a statistically significant improvement in symptoms when implanted electrodes delivered stimulation vs when they did not.[23-25] This suggests that placebo effect, or perhaps the placement of electrodes in the gastric musculature, may play a significant role in the symptomatic improvement observed with GES therapy. No such information is available in children. Future research is needed before this promising therapy can be more widely accepted in the pediatric population.

Our results also highlight the importance of establishing well-defined patient selection criteria. Preoperative predictors of outcomes after GES therapy are particularly relevant to children as they may prevent unnecessary surgical procedures in a vulnerable patient population. Proposed predictors of symptomatic improvement in the adult literature include severe symptoms, nausea and vomiting-predominant symptoms, and diabetic GP. Characteristics associated with a poor response to GES include pain-predominant symptoms, idiopathic GP, prior gastric surgery, and dependence on narcotic pain medications.[26-28] Larger samples of pediatric patients are needed before such conclusions can be made in children. As described earlier, one of our patients who did not improve and remains on parenteral nutrition has an extensive psychiatric history that may be limiting the efficacy of GES therapy. Another patient who did not improve with GES therapy was subsequently diagnosed with an eating disorder. On the basis of our experience thus far, we have begun to regularly provide mental health evaluation as part of each patient's initial screening prior to GES initiation.

In summary, GES therapy seems to be a promising option for pediatric patients with FD and/or GP refractory to medical treatment. Our experience suggests that GES is not only effective in improving symptoms and quality of life but is also generally well-tolerated with few serious complications.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

We would like to acknowledge Wei Wang for her assistance with statistical analysis of our data.

Author Contributions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References

PLL designed the study, performed data collection and analyses, drafted initial manuscript, revised, and approved final manuscript as submitted; ST and CDL conceptualized and designed the study, critically reviewed manuscript and approved the final manuscript as submitted; BS and MA designed the study, performed data collection, critically reviewed manuscript, and approved the final manuscript as submitted; HMM: Conceptualized and designed the study, supervised data collection and analyses, critically reviewed manuscript, and approved the final manuscript as submitted.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Funding
  9. Disclosures
  10. Author Contributions
  11. References
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