ABSTRACT
Objectives
The 2023 joint North American Society for Pediatric Gastroenterology, Hepatology & Nutrition/European Society for Pediatric Gastroenterology, Hepatology & Nutrition guidelines for Helicobacter pylori infection management continue recommending initial diagnosis via endoscopy with biopsies, and obtaining a gastric biopsy culture. We previously reported on a quality improvement (QI) initiative to improve the rate of successful gastric biopsy culture at our hospital. We present 5‐year follow‐up data and describe implementation strategies that may guide similar efforts at other centers.
Methods
Interventions were conducted using the plan‐do‐study‐act (PDSA) framework to: (1) consolidate specialty laboratory processing to a single outside laboratory, and (2) educate and provide reminders to gastroenterologists, endoscopy suite personnel, and laboratory staff. Descriptive statistics were performed on all collected variables. Differences in culture positivity by year, and before and after consolidation to a single specialty laboratory, were assessed using logistic regression, and a p‐chart was constructed to determine variation. All analyses were conducted using R (version 2025.05).
Results
Between November 1, 2019, and March 31, 2025, we observed a consistent increase in the number of gastric biopsy cultures obtained by gastroenterologists each year. Among patients with positive histology, a logistic regression model demonstrated a significant association between calendar year and the odds of a positive culture (odds ratio [OR]: 2.19, 95% confidence interval [CI]: 1.7–2.9, p < 0.001). A marked improvement in culture positivity was observed following the intervention to consolidate specialty laboratory processing.
Conclusion
The implemented interventions, such as staff education, standardized checklists, and processing consolidation, may have led to sustained improvements in the success of primary gastric biopsy cultures.
Keywords: agar dilution, antimicrobial susceptibility, endoscopy, guided therapy
What is Known
Standardized checklists for endoscopy suite staff and educational activities directed at healthcare providers increase the use of gastric biopsy culture in patients with suspected Helicobacter pylori infection.
Proper specimen handling by endoscopy and laboratory staff increases culture yield in patients with positive H. pylori histology.
What is New
Embedding educational reminders into existing scheduled activities (e.g., grand rounds, administrative conferences) for healthcare providers, along with procedural prompts for endoscopy nursing and laboratory staff, promotes sustained use of primary gastric biopsy culture in patients with suspected H. pylori infection.
Consolidation of specimen processing to a single specialty laboratory led to marked improvement in culture yield in patients with positive H. pylori histology.
1. INTRODUCTION
Helicobacter pylori infection continues to be an important etiology of gastrointestinal disease worldwide. Current estimates show that the global prevalence has declined sharply, particularly over the past few decades, with lower rates observed in younger individuals and high‐income countries. 1 , 2 The bacterium is associated with well‐documented complications, including chronic gastritis, which is common in children, and gastric and duodenal ulcer disease, which are less frequently observed in pediatric population. 3 , 4 , 5
The diagnostic and management approach to H. pylori infection continues to focus on treating the condition as we treat other infections, guided by the principles of antimicrobial stewardship 6 , 7 High resistance rates to commonly used antimicrobials in both adults 8 , 9 , 10 , 11 and pediatric 3 , 12 , 13 , 14 , 15 , 16 , 17 , 18 treatment regimens have rendered these therapies no longer acceptable for empirical use. These findings have led to changes in the recommendations in recent clinical practice guidelines for both populations. 7 , 19 The 2023 updated joint North American Society for Pediatric Gastroenterology, Hepatology & Nutrition/European Society for Pediatric Gastroenterology, Hepatology & Nutrition guidelines for the management of H. pylori infection once again emphasize the importance of making the initial diagnosis via upper endoscopy with biopsies when there is a valid clinical indication for the procedure. Additionally, obtaining a gastric biopsy culture during endoscopy to confirm diagnosis and guide treatment is strongly encouraged.
Changing provider attitudes and clinical practices, particularly standardizing care across large clinical groups, can be challenging. At our own large tertiary care pediatric center, we found inconsistent adherence to expert guideline recommendations, especially regarding gastric biopsy culture. Additionally, culture yield was low in patients with histologically confirmed H. pylori infection, highlighting the need for process improvement. 20 In response, we previously conducted a quality improvement (QI) project to standardize the gastric biopsy culture process and increase the rate of successful primary gastric biopsy culture at our hospital. 20 We found that using a standardized checklist, in combination with educational initiatives for staff physicians and collaborative efforts with endoscopy and laboratory teams, were effective strategies to increase the use of gastric biopsy culture as a diagnostic tool for H. pylori infection and, to a lesser extent, to improve culture yield in patients with positive histology.
The availability of antibiotic susceptibility data is essential for understanding local and regional resistance patterns and for informing future guidelines on optimal treatment regimens for children. Building on our prior QI efforts, we now present 5‐year follow‐up data from this initiative and describe the changes implemented to maintain consistent use of gastric biopsy culture and improve culture yield in patients with positive histology, findings that may support similar efforts at other centers.
2. METHODS
2.1. Ethics statement
An exception waiver was granted by the Boston Children's Hospital Institutional Review Board for this QI initiative.
2.2. Context
This QI initiative was implemented in the Division of Pediatric Gastroenterology, Hepatology, and Nutrition at Boston Children's Hospital and involved physicians, endoscopy staff, and laboratory staff. Our hospital‐based gastroenterology (GI) practice currently comprises 70 pediatric gastroenterologists (60 at the onset of the initiative). Of these, 52 physicians perform endoscopic procedures in our endoscopy unit (48 at the onset of the initiative). Each procedure room is staffed by one anesthesia provider and two endoscopy personnel (one nurse and one technician), who assist the physician with multiple tasks, including retrieving the container for gastric biopsy specimens collected for culture and ensuring timely and temperature‐appropriate transport to the hospital laboratory. The endoscopy unit is located on the fourth floor of the hospital. The laboratory was originally located on the seventh floor of the same building but later moved to the basement level of a different building. Culture specimens are either hand‐delivered or transported via the hospital's pneumatic tube system by endoscopy staff. The study period was from November 1, 2019, to March 31, 2025.
2.3. Interventions
From the inception of the QI initiative, we worked collaboratively with individuals representing physicians, the endoscopy leadership (including the physician director of endoscopy and the endoscopy nursing leader and charge nurses), and the leadership of the Department of Laboratory Medicine. We identified deficiencies in the process for obtaining H. pylori cultures, as previously described in our initial paper. These deficiencies included the use of incorrect culture media, incorrect number of gastric biopsies, inadequate specimen temperature after collection, and improper transportation from the endoscopy suite to the hospital laboratory. The plan‐do‐study‐act (PDSA) QI project interventions from November 1, 2019 to July 31, 2020 are illustrated in Figure 1. 20 For the subsequent part of the initiative, which involved data‐driven decision‐making following interventions, we engaged additional leadership from Laboratory Medicine, including the Codirector of Infectious Diseases, a Senior Laboratory Quality Analyst, and laboratory staff and supervisors. We used PDSA cycles directed at staff education and procedural prompting for endoscopy nursing and laboratory personnel.
Figure 1.
PDSA QI project interventions. PDSA, plan‐do‐study‐act; QI, quality improvement.
2.4. Implementation of interventions
2.4.1. GI Provider Education (PDSA #1)
A presentation was given as part of Divisional Grand Rounds to inform physicians about the results of the QI initiative from July 31, 2020, to April 2022, and to discuss plans based on the data. These included the potential consolidation to a single laboratory for culture processing and the importance of submitting specimens in patients with relevant endoscopic findings.
2.4.2. Transition to Single Specialty Laboratory for Culture and Susceptibility Testing (PDSA #2)
On September 1, 2022, following presentation of the data and discussions with Laboratory Medicine leadership, a formal change was made to the previous protocol, which had involved using two separate outside laboratories (ARUP for culture and Mayo Clinic Laboratories for susceptibility testing), consolidating both tests to a single laboratory (Mayo Clinic Laboratories). A divisional email was sent to notify physicians, endoscopy leadership, and endoscopy suite personnel of the change. Emails were sent quarterly thereafter to notify new endoscopy and laboratory personnel.
2.4.3. Endoscopy Staff Education (PDSA #3)
We completed endoscopy staff education on changes to the specimen collection process, which involved simplifying the procedure by using a sterile container with the sample moistened with saline, eliminating the need for special culture media. We emphasized the importance of prompt transportation on ice, as had been done previously, and the need to avoid missing the laboratory's cutoff time for specimen reception to meet same‐day send‐out requirements from Mayo Laboratories. Procedural prompts were delivered during the pre‐procedure “time‐out” briefing, which is standard practice at our institution. As part of the checklist, the endoscopy nurse routinely asked whether the physician planned to submit specimens (e.g., disaccharidases, duodenal aspirate), and H. pylori culture was incorporated into this list. When a culture was planned in advance, nurses prepared ice, saline, and a sterile container before scope insertion. If the decision was made intraprocedurally based on endoscopic findings, the workflow was unchanged, and the physician entered the order postprocedure. After our institution transitioned to the EPIC electronic health record in June 2024, a divisional gastroenterology pre‐procedure order template was developed, enabling physicians to order several tests, including H. pylori culture, in advance. This order then appears as an intraprocedural alert for the endoscopy nurse, ensuring timely specimen handling and reinforcing reproducibility.
2.4.4. GI Provider Update (PDSA #4)
Results and updates were provided to physicians during a monthly divisional QI meeting following the change in laboratories. The session also included education and suggestions for re‐educating new laboratory personnel and creating an alternate pathway for patients undergoing endoscopy with positive histology whose cultures did not meet the laboratory cutoff and therefore could not be sent out.
2.4.5. Laboratory Staff Education (PDSA #5)
Review of the send‐out process to the specialized external laboratory with hospital laboratory staff, specifically for onboarding new personnel.
2.4.6. Addition of a Process for Positive H. pylori Patients with Cultures That Missed the Cutoff (PDSA #6)
The process was reviewed with hospital laboratory leadership to incorporate molecular testing for cases with no culture growth but positive histology, to obtain susceptibility data for all patients with biopsy‐proven H. pylori. All patients with positive biopsies who either had no growth on culture or whose samples were rejected for not meeting the laboratory cutoff qualify to proceed with antimicrobial susceptibility molecular testing on formalin‐fixed paraffin‐embedded (FFPE) tissue scrolls from the pathology archive.
2.5. Measures
The primary outcome measure was the proportion of gastric biopsy cultures obtained in patients with suspected H. pylori infection. The secondary outcome measure was the rate of culture growth in patients with H. pylori identified on histology. The process measure was compliance with obtaining H. pylori culture in patients with suspected infection. The balancing measure was the perceived increase in procedure time or workflow burden for endoscopy and laboratory staff due to additional steps in specimen collection, handling, and transport. A list of patients with gastric biopsy cultures was generated monthly and plotted on a process control chart (p‐chart) at quarterly intervals over the study period. Demographic data (age, gender, race, and ethnicity), endoscopic and histologic findings, prescribed treatment, and eradication results were also collected for analysis.
2.6. Statistical analysis
Descriptive statistics were used to summarize patient demographics and clinical features. Quantitative results were reported as the mean and standard deviation (SD). Categorical data were summarized as frequencies and percentages. A logistic regression model was employed to evaluate the association between year and the likelihood of obtaining positive gastric biopsy cultures among patients with biopsy‐confirmed H. pylori infection with p < 0.01 considered statistically significant. Additionally, we used statistical process control charts to monitor culture positivity rates, assessing the impact of the PSDA QI intervention. All statistical analyses were conducted using R statistical software (version 2025.05).
3. RESULTS
During the timeframe of the QI initiative, from November 1, 2019, to March 31, 2025, a total of 690 gastric biopsy cultures were sent, of which 681 were sent in patients aged 21 years or younger. The mean age was 13.0 ± 4.8, with the majority (53%) being adolescents aged 12–17. Overall, 51% of patients were male; 65% were white and 28% of our cohort identified as Hispanic or Latino. A prior history of H. pylori treatment and proton pump inhibitors (PPIs) use at the time of endoscopy was each reported in 11% of patients. Endoscopic findings were notable for nodular gastropathy in 51%, gastric erosions or ulcers in 14%, and duodenal erosions or ulcers in 8.5% (Table 1).
Table 1.
Patient characteristics overall and per year.
| Characteristic | Overall N = 681a | 2019 N = 10a | 2020 N = 58a | 2021 N = 101a | 2022 N = 116a | 2023 N = 164a | 2024 N = 172a | 2025 N = 60a |
|---|---|---|---|---|---|---|---|---|
| Age at procedure (years) | ||||||||
| Mean ± SD | 13.0 ± 4.8 | 12.8 ± 5.2 | 12.4 ± 5.1 | 13.2 ± 4.8 | 12.3 ± 5.1 | 13.1 ± 4.7 | 13.5 ± 4.8 | 13.3 ± 4.2 |
| Median [Q1, Q3] | 14.0 [10, 17] | 13.0 [9, 17] | 13.0 [10, 17] | 15.0 [11, 17] | 14.0 [9.5, 16] | 14.0 [9.5, 17] | 15.0 [10.5, 17] | 14.0 [12, 16] |
| [Min, Max] | [0, 21] | [5, 20] | [2, 21] | [1, 21] | [0, 21] | [2, 21] | [1, 21] | [3, 21] |
| Age group | ||||||||
| 0–2 | 20 (2.9%) | 0 (0%) | 1 (1.7%) | 4 (4.0%) | 6 (5.2%) | 3 (1.8%) | 6 (3.5%) | 0 (0%) |
| 3–6 | 68 (10.0%) | 1 (10%) | 10 (17%) | 9 (8.9%) | 13 (11%) | 14 (8.5%) | 15 (8.7%) | 6 (10%) |
| 7–11 | 131 (19%) | 3 (30%) | 12 (21%) | 17 (17%) | 25 (22%) | 40 (24%) | 26 (15%) | 8 (13%) |
| 12–17 | 360 (53%) | 4 (40%) | 26 (45%) | 58 (57%) | 59 (51%) | 81 (49%) | 92 (53%) | 40 (67%) |
| 18–21 | 102 (15%) | 2 (20%) | 9 (16%) | 13 (13%) | 13 (11%) | 26 (16%) | 33 (19%) | 6 (10%) |
| Sex | ||||||||
| Male | 344 (51%) | 5 (50%) | 28 (48%) | 43 (43%) | 62 (53%) | 91 (55%) | 81 (47%) | 34 (57%) |
| Race | ||||||||
| White | 444 (65%) | 7 (70%) | 40 (69%) | 75 (74%) | 83 (72%) | 101 (62%) | 108 (63%) | 30 (50%) |
| Asian | 83 (12%) | 1 (10%) | 13 (22%) | 13 (13%) | 19 (16%) | 13 (7.9%) | 17 (9.9%) | 7 (12%) |
| Black or African American | 79 (12%) | 2 (20%) | 3 (5.2%) | 5 (5.0%) | 12 (10%) | 25 (15%) | 23 (13%) | 9 (15%) |
| Other | 71 (10%) | 0 (0%) | 2 (3.4%) | 8 (7.9%) | 2 (1.7%) | 21 (13%) | 24 (14%) | 14 (23%) |
| Unknown | 4 (0.6%) | 0 (0%) | 0 (0%) | 0 (0%) | 0 (0%) | 4 (2.4%) | 0 (0%) | 0 (0%) |
| Hispanic or Latino | 194 (28%) | 2 (20%) | 9 (16%) | 32 (32%) | 31 (27%) | 62 (38%) | 42 (24%) | 16 (27%) |
| Prior Helicobacter pylori treatment | 72 (11%) | 2 (20%) | 10 (17%) | 13 (13%) | 12 (10%) | 16 (9.8%) | 11 (6.4%) | 8 (13%) |
| Proton pump inhibitor use at time of endoscopy | 73 (11%) | 3 (30%) | 15 (26%) | 9 (8.9%) | 15 (13%) | 10 (6.1%) | 16 (9.3%) | 5 (8.3%) |
| Endoscopic findingsb | ||||||||
| Nodular gastropathy | 346 (51%) | 6 (60%) | 31 (53%) | 53 (52%) | 54 (47%) | 84 (51%) | 87 (51%) | 31 (52%) |
| Gastric erosion/ulcer | 92 (14%) | 0 (0%) | 3 (5.2%) | 11 (11%) | 15 (13%) | 24 (15%) | 29 (17%) | 10 (17%) |
| Duodenal erosion/ulcer | 58 (8.5%) | 1 (10%) | 7 (12%) | 7 (6.9%) | 5 (4.3%) | 11 (6.7%) | 25 (15%) | 2 (3.3%) |
| Duodenitis | 5 (0.7%) | 0 (0%) | 0 (0%) | 0 (0%) | 1 (0.9%) | 1 (0.6%) | 3 (1.7%) | 0 (0%) |
| Other | 91 (13%) | 1 (10%) | 12 (21%) | 11 (11%) | 13 (11%) | 20 (12%) | 24 (14%) | 10 (17%) |
| Normal | 136 (20%) | 3 (30%) | 10 (17%) | 24 (24%) | 34 (29%) | 29 (18%) | 26 (15%) | 10 (17%) |
| Histologic findingsb | ||||||||
| Chronic gastritisc | 374 (55%) | 6 (60%) | 28 (48%) | 56 (55%) | 71 (61%) | 93 (57%) | 88 (51%) | 32 (53%) |
| Duodenitis | 57 (8.4%) | 1 (10%) | 7 (12%) | 11 (11%) | 5 (4.3%) | 10 (6.1%) | 16 (9.3%) | 7 (12%) |
| Esophagitis | 112 (16%) | 0 (0%) | 6 (10%) | 17 (17%) | 17 (15%) | 31 (19%) | 27 (16%) | 14 (23%) |
| Normal | 166 (24%) | 3 (30%) | 14 (24%) | 25 (25%) | 22 (19%) | 43 (26%) | 40 (23%) | 19 (32%) |
| Other | 56 (8.2%) | 1 (10%) | 9 (16%) | 8 (7.9%) | 10 (8.6%) | 10 (6.1%) | 14 (8.1%) | 4 (6.7%) |
Note: 2019 and 2025 data are partial and include only some months. No formal statistical comparison was performed due to unequal group.
Abbreviation: SD, standard deviation.
n (%).
Some patients had more than one finding.
Chronic gastritis (active or inactive).
We observed a consistent increase in the number of gastric biopsy cultures obtained by gastroenterologists each year. The most common reasons for sending cultures included endoscopic findings, a positive noninvasive test such as a stool antigen before the procedure, risk factors such as race/ethnicity or socioeconomic status, family history of gastric cancer, and confirmation of eradication.
Of all the patients that had a gastric biopsy culture sent, 194/691 (28.1%) had positive histology for H. pylori. Of note, two patients had negative histology (did not have the bacteria identified on gastric biopsy) but did have positive culture growth. Among patients with positive histology, a logistic regression model demonstrated a significant association between calendar year and the odds of a positive culture (odds ratio [OR]: 2.19 times, 95% confidence interval [CI]: 1.7–2.9, p < 0.001) (Table S1). A marked improvement in culture yield in H. pylori positive histology patients was observed following the intervention to consolidate specialty laboratory processing.
Overall, antimicrobial resistance was highest for metronidazole (27.5%) and clarithromycin (18.7%), and lower for rifampin (12.2%), levofloxacin (10.1%), and amoxicillin (4.3%). Only one isolate showed resistance to tetracycline. The most common dual resistance pattern was clarithromycin‐metronidazole (5%) (Table S2). Eradication data were available for 75.6% of all patients treated, and successful eradication was observed to increase during the QI initiative period (Figure 2, Table S3).
Figure 2.
Helicobacter pylori diagnosis and eradication rate overview by year: Rate of culture positivity (defined as positive culture growth in a patient with a gastric biopsy that demonstrated H. pylori organisms on pathology). Bars represent the total number of patients with biopsy‐proven H. pylori infection (outlined), and within these, the subset with culture‐confirmed infection (shaded). The overlaid line shows the eradication rate over time.
Before this QI initiative, the process of obtaining gastric biopsy cultures was not standardized due to a lack of awareness of this diagnostic tool. Only a modest number of cultures (28 in the year before the initiative, representing approximately 35% of potentially eligible patients) were sent by a limited number of providers. Frustration with the poor culture yield, as previously reported, further discouraged its use. 21 Subsequent PDSA cycles focused on education consistently increased the frequency of gastric biopsy cultures obtained by gastroenterologists each year. More importantly, they improved the culture yield in patients with positive H. pylori histology from 21% at baseline to nearly 90% at the end of the intervention, approaching our target, as shown in the P‐chart (Figure 3). The goal of ≥90% was achieved in the quarter following the intervention to consolidate specialty laboratory processing, indicating the effectiveness and sustainability of the implemented quality improvement interventions. Following this change, the positivity rates on positive histology patients consistently remained high and stable. To evaluate the balancing measure of perceived increases in procedure time or workflow burden for endoscopy and laboratory staff, meetings were held with both groups to streamline the processes of specimen collection, handling, and transport.
Figure 3.
P‐chart: quarterly culture positivity rate among histology positive patients CL shown in purple. QI interventions (project launch, education, protocol change) are annotated, showing a sustained increase in positivity rate. CL center line; QI, quality improvement; UCL, upper control limit.
4. DISCUSSION
Antimicrobial susceptibility data for H. pylori is essential for understanding local and regional resistance patterns and informing future guidelines on optimal treatment regimens for children. Our QI initiative successfully standardized the process of obtaining gastric biopsy cultures at our institution, resulting in an increased number of cultures sent by gastroenterologists and improved culture yield in patients with positive H. pylori histology. This standardization allows more patients to benefit from susceptibility‐guided treatment, with the ultimate goal of improving eradication rates.
Lack of awareness is one of the main drivers of physician nonadherence to clinical guidelines. 21 For our first outcome, we found that targeted educational interventions can positively influence clinician attitudes and improve quality of care. Embedding educational reminders into existing scheduled activities (e.g., grand rounds, administrative conferences) that were already part of providers' routines anddid not require additional time, proved effective in reaching a large number of clinicians. Feedback was positive, with providers reporting that they learned something new and did not feel the reminders were burdensome. Collaborating with endoscopy nursing and laboratory staff was at times challenging due to high turnover in both groups. This was mitigated by encouraging direct email communication with a designated point person on the QI team, who served as a liaison between both groups. We also found that frequent procedural prompts for endoscopy and laboratory staff, particularly after consolidating processing to a single specialty laboratory, helped keep new personnel informed and engaged.
Multiple factors affect the successful isolation and culture of H. pylori. Among the various interventions implemented during the QI project, the one that appears to have contributed most significantly to the dramatic improvement in culture yield among patients with H. pylori‐positive histology was the consolidation of specimen processing to a single specialty laboratory. Before this change, we were unable to achieve a culture yield higher than 55% in these patients, despite addressing factors related to specimen handling by our endoscopy and laboratory staff. We speculate that handling by specialty laboratories may have been a major contributor to the poor culture growth, as H. pylori is known to have limited survival during transport. 22 Additionally, eliminating the need for a specialized transport medium and instead using a simple sterile container with saline‐moistened tissue significantly streamlined the process and removed a key logistical barrier. Conversely, the change in specialty laboratories also introduced some challenges. Because samples had to be sent out the same day, they needed to be received by our lab before a specific cutoff time. Feedback from providers was helpful and led to creating an alternate pathway for patients whose cultures could not be sent due to missing the laboratory cutoff, via antimicrobial susceptibility molecular testing using FFPE tissue scrolls from the pathology archive. 18
Limitations of the study include the unique tertiary care center population, which may limit the generalizability of our findings to other clinical settings, particularly those with fewer resources or different patient demographics. As a QI initiative, this study was not designed to establish causal relationships but rather to observe process changes over time. Additionally, while improvements in culture yield were demonstrated, eradication outcomes were not available for all patients. Finally, the reliance on provider documentation for culture indications may introduce reporting bias or variability in interpretation.
5. CONCLUSION
Embedding educational activities and reminders into existing scheduled sessions for healthcare providers, along with procedural prompts for endoscopy nursing and laboratory staff, promoted sustained use of gastric biopsy culture in patients with suspected H. pylori infection. Consolidation of specimen processing to a single specialty laboratory led to a marked improvement in culture yield among patients with positive H. pylori histology. Successful gastric biopsy culture enables susceptibility‐guided treatment, contributes to local antimicrobial resistance surveillance, and informs future guidelines on optimal empiric regimens for children. In settings where culture is not feasible, molecular methods represent a viable alternative for obtaining antimicrobial susceptibility data.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Supporting information
Supplemental‐Table‐1.
Supplemental‐Table‐2.
Supplemental‐Table‐3.
Arellanos KR, Cardini J, Joerger J, Estrella‐Pimentel L, Goldsmith JD, Bonilla S. Standardizing a protocol for Helicobacter pylori gastric biopsy culture: from implementation to sustained practice. JPGN Rep. 2026;7:19‐27. 10.1002/jpr3.70097
[Correction added on 06 January 2026, after the first online publication: Article format has been updated.]
REFERENCES
- 1. Li Y, Choi H, Leung K, Jiang F, Graham DY, Leung WK. Global prevalence of Helicobacter pylori infection between 1980 and 2022: a systematic review and meta‐analysis. Lancet Gastroenterol Hepatol. 2023;8:553‐564. [DOI] [PubMed] [Google Scholar]
- 2. Yuan C, Adeloye D, Luk TT, et al. The global prevalence of and factors associated with Helicobacter pylori infection in children: a systematic review and meta‐analysis. Lancet Child Adolesc Health. 2022;6:185‐194. [DOI] [PubMed] [Google Scholar]
- 3. Kori M, Le Thi TG, Werkstetter K, et al. Helicobacter pylori infection in pediatric patients living in Europe: results of the EuroPedHP registry 2013 to 2016. J Pediatr Gastroenterol Nutr. 2020;71:476‐483. [DOI] [PubMed] [Google Scholar]
- 4. Bonilla S, Mitchell PD, Mansuri I. Low adherence to society guidelines for the management of Helicobacter pylori among pediatric gastroenterologists. J Pediatr Gastroenterol Nutr. 2021;73:178‐183. [DOI] [PubMed] [Google Scholar]
- 5. Nguyen TC, Tang NLC, Le GKN, et al. Helicobacter pylori infection and peptic ulcer disease in symptomatic children in Southern Vietnam: A prospective multicenter study. Healthcare. 2023;11:1658. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Jones NL, Koletzko S, Goodman K, et al. Joint ESPGHAN/NASPGHAN guidelines for the management of Helicobacter pylori in children and adolescents (update 2016). J Pediatr Gastroenterol Nutr. 2017;64:991‐1003. [DOI] [PubMed] [Google Scholar]
- 7. Homan M, Jones NL, Bontems P, et al. Updated joint ESPGHAN/NASPGHAN guidelines for management of Helicobacter pylori infection in children and adolescents (2023). J Pediatr Gastroenterol Nutr. 2024;79:758‐785. [DOI] [PubMed] [Google Scholar]
- 8. Duck WM, Sobel J, Pruckler JM, et al. Antimicrobial resistance incidence and risk factors among Helicobacter pylori–infected persons, United States. Emerging Infect Dis. 2004;10:1088‐1094. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Mosites E, Bruden D, Morris J, et al. Antimicrobial resistance among Helicobacter pylori isolates in Alaska, 2000‐2016. J Glob Antimicrob Resist. 2018;15:148‐153. [DOI] [PubMed] [Google Scholar]
- 10. Argueta EA, Alsamman MA, Moss SF, D'Agata EMC. Impact of antimicrobial resistance rates on eradication of Helicobacter pylori in a US population. Gastroenterology. 2021;160:2181‐2183.e1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Mégraud F, Graham DY, Howden CW, et al. Rates of antimicrobial resistance in Helicobacter pylori isolates from clinical trial patients across the US and Europe. Am J Gastroenterol. 2023;118:269‐275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Le Thi TG, Werkstetter K, Kotilea K, et al. Management of Helicobacter pylori infection in paediatric patients in Europe: results from the EuroPedHp registry. Infection. 2023;51:921‐934. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Crone J, Granditsch G, Huber W‐D, et al. Helicobacter pylori in children and adolescents: increase of primary clarithromycin resistance, 1997‐2000. J Pediatr Gastroenterol Nutr. 2003;36:368‐371. [DOI] [PubMed] [Google Scholar]
- 14. Kato S, Fujimura S, Udagawa H, et al. Antibiotic resistance of Helicobacter pylori strains in Japanese children. J Clin Microbiol. 2002;40:649‐653. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Seo J‐H, Jun J‐S, Yeom JS, et al. Changing pattern of antibiotic resistance of Helicobacter pylori in children during 20 years in Jinju, South Korea. Pediatr Int. 2013;55:332‐336. [DOI] [PubMed] [Google Scholar]
- 16. Serrano CA, Leon MA, Palma C, Vera M, Hernandez C, Harris PR. Helicobacter pylori‐clarithromycin resistance in symptomatic pediatric patients in a high prevalence country. J Pediatr Gastroenterol Nutr. 2017;64:e56‐e60. [DOI] [PubMed] [Google Scholar]
- 17. Sholeh M, Maleki F, Krutova M, et al. The increasing antimicrobial resistance of Helicobacter pylori in Iran: A systematic review and meta‐analysis. Helicobacter. 2020;25:e12730. [DOI] [PubMed] [Google Scholar]
- 18. Herzlinger M, Dannheim K, Riaz M, Liu E, Bousvaros A, Bonilla S. Helicobacter pylori antimicrobial resistance in a pediatric population from the New England region of the United States. Clin Gastroenterol Hepatol. 2023;21:3458‐3460.e2. [DOI] [PubMed] [Google Scholar]
- 19. Chey WD, Howden CW, Moss SF, et al. ACG clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol. 2024;119:1730‐1753. [DOI] [PubMed] [Google Scholar]
- 20. Bonilla S, Bousvaros A, Cardini J, et al. Lessons from a quality improvement project to standardize the process of gastric biopsy culture for Helicobacter pylori . JPGN Rep. 2021;2:e116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Cabana MD, Rand CS, Powe NR, et al. Why don't physicians follow clinical practice guidelines?A framework for improvement. JAMA. 1999;282:1458‐1465. [DOI] [PubMed] [Google Scholar]
- 22. Heep M, Scheibl K, Degrell A, Lehn N. Transport and storage of fresh and frozen gastric biopsy specimens for optimal recovery of Helicobacter pylori . J Clin Microbiol. 1999;37:3764‐3766. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
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Supplementary Materials
Supplemental‐Table‐1.
Supplemental‐Table‐2.
Supplemental‐Table‐3.