- Original research article
- Open Access
A survey of primary-care pediatricians regarding the management of Helicobacter pylori infection and celiac disease
Israel Journal of Health Policy Research volume 8, Article number: 88 (2019)
Adherence of primary-care pediatricians to guidelines in pediatric gastroenterology is essential to achieve optimal clinical outcomes. The study aim was to examine adherence of primary-care pediatricians to the European and North American Societies for Pediatric Gastroenterology, Hepatology and Nutrition guidelines on the management of Helicobacter pylori (H. pylori) infection and celiac disease.
We conducted a cross-sectional study during March–July 2017 using the survey platform of Maccabi Healthcare Services, the second largest state-mandated health organization in Israel. We sent the study questionnaire to a random sample of 300 pediatricians via electronic mails and to increase the response rate, we performed a telephone interview. Overall, 108 (36%) pediatricians provided completed questionnaires.
Using professional guidelines for the management of H. pylori infection and celiac disease was reported by 34 and 37% of pediatricians, respectively. Referral to H. pylori testing was reported by 78 and 52% of pediatricians in children with suspected duodenal ulcer and unexplained iron deficiency anemia, respectively, with the stool antigen enzyme immunoassay being mostly (51%) used as the first choice diagnostic test. Most pediatricians reported prescription of triple therapy; proton pump inhibitors/clarithromycin/amoxicillin (59%) or metronidazole (21%). For celiac disease, overall adherence to all guidelines was high both for initial evaluation and for confirmation of diagnosis.
Adherence to the guidelines on management of H. pylori infection was low, while adherence to the guidelines on celiac disease management was high among primary-care pediatricians. Educational interventions are needed to improve H. pylori infection management among primary-care pediatricians.
Gastrointestinal complaints such as abdominal pain, nausea, and diarrhea are common in the pediatric practice . Clinical guidelines based on synthesis of evidence by experts in the field of pediatric gastroenterology and nutrition provide high-quality summary of recommendations on testing, treatment and follow-up of pediatric patients with various gastrointestinal conditions such as Helicobacter pylori (H. pylori) infection [2, 3], celiac disease , and other conditions. These guidelines aimed to create a standard of care based on best available evidence with emphasis on the diagnostic process in each condition.
According to the European Society for Pediatric Gastroenterology Hepatology and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN and NASPGHAN) guidelines, esophagogastroduodenoscopy is recommended as a first choice for the diagnosis of H. pylori infection. The recommended first-line eradication regimens included triple therapy with a PPI/amoxicillin/clarithromycin or an imidazole or bismuth saltsamoxicillinan imidazole or sequential therapy. Confirmation of H. pylori eradication using non-invasive reliable tests such as the urea breath test (UBT) and stool antigen detection enzyme immunoassays (EIA) should be done 4–8 weeks after completing therapy. According to the 2012 ESPGHAN guidelines , the serological assays constitute the first step in the diagnosis of celiac disease. Patients testing positive for specific tissue transglutaminase type 2 (TG2) antibody should be referred to a pediatric gastroenterologist for further diagnostic workup that might include anti-endomysium antibodies and biopsy, depending the serology results.
Primary-care pediatricians usually are the first to be contacted by parents regarding their child’s illness. These physicians make most of the decisions regarding referral to diagnostic tests and treatment of children with gastrointestinal illnesses. Primary-care pediatricians vary according to their education, sub-specialty and experience. Adherence to guidelines created by professional societies regarding the diagnosis and treatment of children with gastrointestinal illnesses is expected to ensure safe and optimal treatment and achieve satisfactory clinical endpoints. However, utilization and adherence of these guidelines by primary-care pediatricians remains unclear. The aim of the current study was to examine adherence of primary-care pediatricians to the ESPGHAN/NASPGHAN guidelines for the diagnosis and treatment H. pylori infection [2, 3] and the ESPGHAN guidelines on celiac disease , as models for infectious and non-infectious chronic gastrointestinal illnesses, respectively.
Study design and population
We conducted a cross-sectional study during March–July 2017 using the survey platform of Maccabi Healthcare Services (MHS), the second largest state-mandated health organization in Israel. A random sample of 300 primary care pediatricians was selected among all pediatrician’s employees of MHS. Overall, 113 pediatricians agreed to participate in the study, of those 73 were successfully contacted by the email messages and 40 by telephone, while five pediatricians did not complete the survey, thus leaving 108 (36%) participants in the analysis.
The study team constructed a questionnaire (Additional file 1). For some Likert scale survey’s questions, we constructed a dichotomous variable by combining the categories (always and usually-yes) into one category and the other categories (usually-no and never) to the second category. The questionnaire consisted of questions on the utilization of professional guidelines in the diagnosis and treatment of H. pylori infection and celiac disease and the physicians’ referral patterns to diagnostic tests and treatment of these conditions. We used The 2011 ESPGHAN/NASPGHAN guidelines on H. pylori infection  and the 2012 ESPGHAN guidelines of celiac disease  as the reference in our study. Information on characteristics of all selected pediatricians was obtained from the MHS database on the physician’s age in years, sex, the year in which he/she began to work at MHS and type of employment/contract with MHS [being a contractor vs. employee of MHS). Information on number of years since board certification of the participating physicians was obtained through the questionnaire.
We sent the questionnaire to the physicians in the study sample via the electronic mail system of MHS. To increase the response, we sent two messages in different occasions 3–4 weeks apart. The study team contacted physicians who did not open the survey link by phone; and interviewed those who were successfully reached and agreed to participate in the survey.
We examined differences between responders and non-responders in background characteristics using the chi-square test or Fisher’s exact test for categorical variables and Student’s t test for continuous variables. Categorical variables were described using frequencies and percentages and continuous variables were described using means and standard deviation (SD). Results from unweighted and weighted analyses are presented. The weights were determined using the inverse probability weighting method . The probability to participate in the study was obtained from multiple logistic regression model in which the dependent variable was participating on the study (yes or no, coded 1 and 0, respectively) and the independent variables were age, sex and the year of starting to work at MHS. The inverse of this probability was used as the weight. P < 0.05 was considered statically significant. We analyzed the data using SPSS version 25 (IBM, New York, United States).
There were no significant differences in age, sex, years since board certification, employment contract and the year of beginning working at MHS between responders and non-responders (Table 1).
H. pylori infection
Among 103 participants who replied to the question regarding using guidelines, 35 (34%) reported utilization of any guidelines for the diagnosis of H. pylori infection.
Testing for H. pylori infection in patients with suspected duodenal ulcer was reported by 78% of the participants compared to 52 and 47% in patients with unexplained/ refractory iron deficiency anemia (IDA) and first-degree relatives of gastric cancer patients, respectively. All of these conditions should promote testing for H. pylori according to the guidelines. However 44% reported testing of children with recurrent abdominal pain to the diagnosis of H. pylori infection, where there is a recommendation not to test. Nearly half of the participants reported testing for stool antigen detection EIA as their first-choice diagnostic test, followed by the UBT (27%).
Most (59%) participants reported that they would prescribe triple therapy with proton pump inhibitors (PPIs)/clarithromycin/amoxicillin as first-line treatment, 21% reported prescription of triple therapy, but using metronidazole instead of clarithromycin. Forty percent reported prescription of anti-H. pylori therapy for 10 days, and 34% for 14 days. More than half reported that they do not refer their patients to follow-up examination after H. pylori treatment if symptoms resolved. In case of treatment failure, most participants (71%) reported that they would refer their patient to a specialist in gastroenterology. The weighted analysis yielded similar results (Table 2).
Forty (37%) participants reported using professional guidelines for the diagnosis and treatment of celiac disease.
Most participants (93%) reported that they suspect their patient to have celiac disease if he/she had chronic/intermittent diarrhea, growth impairment (97%), IDA (94%) or complaints of abdominal pain (85%). The majority of the participants reported recommending screening for celiac disease for patients with autoimmune disease and first-degree relatives of celiac disease patients: 92 and 98%, respectively. All participants reported recommending their patient gluten-free diet only after final diagnosis of celiac disease, 98% reported recommending their celiac disease patients an annual follow-up to monitor physical growth and disease complications, while 84% reported recommending a follow-up by a specialist in gastroenterology (Table 3). The weighted analysis yielded similar results (Table 3).
The main findings of this survey are that (a) only 34 and 37% of the participants reported using the ESPGHAN/NASPGHAN guidelines on the diagnosis and treatment of H. pylori infection and the ESPGHAN guidelines on celiac disease, respectively, and (b) there was a high adherence to the guidelines for the management and treatment of celiac disease, but not of H. pylori infection.
Overall, the reported management of suspected celiac disease was consistent with the ESPGHAN guidelines . All participants relied on serological assays for the initial diagnosis of celiac disease, and 89% would refer patients with positive celiac serology to a gastroenterology consultant for making the final diagnosis either by performing duodenal biopsies, or by immunoglobulin A TG2 antibody titers (> 10 times more than the upper normal limit), endomysial antibodies and human leukocyte antigen (HLA)-DQ2 and/or HLA-DQ8 .
On the other hand, testing for H. pylori infection in children with suspected duodenal ulcer, unexplained iron deficiency anemia and recurrent abdominal pain was reported by 78, 52 and 44% of the participants, respectively. Commonly, non-invasive testing (stool EIA and UBT) was the first choice for H. pylori infection, even though the guidelines recommend gastrointestinal endoscopy with biopsies for culture and histology [2, 3]. Similar to Chang et al. , we found that 79% of the participants recommended triple treatment for H. pylori infection, and 74% would prescribe it for 10–14 days, as currently recommended . However, most participants prescribed clarithromycin, even though small-scale studies in Israeli children found high clarithromycin resistance in H. pylori isolates [7, 8]. This is inconsistent with the guideline to consider the local prevalence of antibiotic resistance of H. pylori strains.
In our study, 71% of the participants would refer to a consultant in gastroenterology incase of treatment failure. This finding might be consistent with the guideline  to individualize rescue therapy by considering antibiotic susceptibility, age of the child, and available antimicrobial options.
The main strengths of this study are its utilization of a questionnaire that was constructed by experts in epidemiology, survey methods and pediatric gastroenterology, and its being the first survey in Israel of the clinical practices primary-care pediatricians regarding the diagnosis and treatment of H. pylori infection and celiac disease. The main limitation of our study is its reliance on self-reported data that may not reflect actual practice. However, a reporting bias is unlikely to be different for the two illnesses assessed in the survey. A second limitation is the low response rate of the invited participants. Even though responders and non-responders were similar in demographic characteristics, we cannot rule out the possibility that they differed in practice habits.
Future research should explore the causes of the limited adherence to practice guidelines for suspected H. pylori infection by Israeli primary-care pediatricians. Possible causes for this limited adherence are (a) Deficient understanding and implementation of the practice guidelines; this would require educational interventions. (b) Difficulties in implementing the practice guidelines in the Israeli primary care setting; this would require a review of the current guidelines with a view of their amendment. (c) Disagreement within the pediatric gastroenterology community; this would similarly require a review of the current guidelines for the management of suspected H. pylori infection with a view of forging a consensus on these guidelines.
Availability of data and materials
Individual level data from this study cannot be made publically available due to legal and ethical restrictions.
European Society for Pediatric Gastroenterology, Hepatology and Nutrition
- H. pylori :
Human leukocyte antigen
Iron deficiency anemia
Maccabi Healthcare Services
North American Society for Pediatric Gastroenterology, Hepatology and Nutrition
Proton pump inhibitors
Urea breath test
Lewis ML, Palsson OS, Whitehead WE, van Tilburg MAL. Prevalence of functional gastrointestinal disorders in children and adolescents. J Pediatr. 2016;177:39–43 e3. https://doi.org/10.1016/j.jpeds.2016.04.008.
Koletzko S, Jones NL, Goodman KJ, Gold B, Rowland M, Cadranel S, et al. Evidence-based guidelines from ESPGHAN and NASPGHAN for helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr. 2011;53:230–43. https://doi.org/10.1097/MPG.0b013e3182227e90.
Jones NL, Koletzko S, Goodman K, Bontems P, Cadranel S, Casswall T, 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. https://doi.org/10.1097/MPG.0000000000001594.
Husby S, Koletzko S, Korponay-Szabo IR, Mearin ML, Phillips A, Shamir R, et al. European Society for Pediatric Gastroenterology, Hepatology, and nutrition guidelines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012;54:136–60. https://doi.org/10.1097/MPG.0b013e31821a23d0.
Harkanen T, Kaikkonen R, Virtala E, Koskinen S. Inverse probability weighting and doubly robust methods in correcting the effects of non-response in the reimbursed medication and self-reported turnout estimates in the ATH survey. BMC Public Health. 2014;14:1150. https://doi.org/10.1186/1471-2458-14-1150.
Chang HY, Sharma VK, Howden CW, Gold BD. Knowledge, attitudes, and practice styles of north American pediatric gastroenterologists: helicobacter pylori infection. J Pediatr Gastroenterol Nutr. 2003;36:235–40.
Zevit N, Levy I, Shmuely H, Samra Z, Yahav J. Antibiotic resistance of helicobacter pylori in Israeli children. Scand J Gastroenterol. 2010;45:550–5. https://doi.org/10.3109/00365521003663688.
Khoury J, Geffen Y, Shaul R, Sholy H, Chowers Y, Saadi T. Secondary antibiotic resistance of helicobacter pylori isolates in Israeli children and adults. J Glob Antimicrob Resist. 2017;10:182–5. https://doi.org/10.1016/j.jgar.2017.05.017.
This study was funded by the Israel National Institute for Health Policy research (KM-PI, GH Co-PI 17/2014-R).
Ethics approval and consent to participate
The Helsinki committee of Bayit Balev Medical Center of MHS (number 47/2014) and the ethics committee of Tel Aviv University approved the study protocol. Informed consent was obtained from all participants included in the study.
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Ben Tov, A., Na’amnih, W., Bdair-Amsha, A. et al. A survey of primary-care pediatricians regarding the management of Helicobacter pylori infection and celiac disease. Isr J Health Policy Res 8, 88 (2019). https://doi.org/10.1186/s13584-019-0357-x
- Helicobacter pylori
- Celiac disease