Survey on the Knowledge and the Management of Helicobacter pylori Infection by Italian General Practitioners and Doctors in General Practice Training
by
, ,
Cesare Tosetti
*,
Enzo Ubaldi
,
Edoardo Benedetto
,
Luciano Bertolusso
,
Luigi Napoli
,
Carmelo Cottone
,
Riccardo Scoglio
,
Alessandra Belvedere
,
Giovanni Casella
,
Maurizio Mancuso
,
Gennaro Abagnale
,
Guido Sanna
and
Rudi De Bastiani
Italian Group for Primary Care Gastroenterology (GIGA-CP), Via Piave 4/A, 32032 Feltre, Italy
*
Author to whom correspondence should be addressed.
Gastrointest. Disord. 2024, 6(2), 421-430; https://doi.org/10.3390/gidisord6020028
Submission received: 7 March 2024
/
Revised: 26 April 2024
/
Accepted: 28 April 2024
/
Published: 30 April 2024
(This article belongs to the Special Issue Feature Papers in Gastrointestinal Disorders in 2023-2024)
Abstract
:The management of gastric Helicobacter pylori (H. pylori) infection represents a significant concern in primary healthcare. This survey evaluates the approaches, attitudes, and knowledge regarding gastric H. pylori infection among Italian general practitioners (GPs) and young doctors undergoing general practice training (ITGPs). The survey enrolled 466 GPs and 70 ITGPs. Among GPs, specialist recommendations and the Maastricht–Florence guidelines were frequently referenced sources, while ITGPs relied more on the Maastricht–Florence guidelines and internet resources. ITGPs demonstrated more proactive approaches than GPs in investigating and treating conditions such as gastric ulcers, atrophic gastritis, and iron-deficiency anemia. However, there was limited attention given to the role of H. pylori treatment in first-degree relatives of gastric cancer patients. The most used diagnostic methods were the urea breath test and fecal test. Triple therapy was the most frequently chosen initial treatment regimen, with quadruple bismuth therapy becoming the primary option after initial treatment failure, followed by quinolone therapy and concomitant therapy. This survey underscores a disparity between real-world practices and the recommendations outlined in current guidelines, indicating a need for improved understanding of H. pylori guidelines among both GPs and ITGPs.
Keywords:
Helicobacter pylori; dyspepsia; primary care; general practice; guidelines; diagnosis; treatment1. Introduction
Gastric Helicobacter pylori (H. pylori) infection is one of the most common bacterial infections worldwide, usually transmitted in childhood, and persists for life if untreated [1].
Its prevalence varies significantly between different geographical regions, influenced by socioeconomic, environmental, and hygienic factors, reaching up to 50–80% of the general population in developing countries, while in industrialized countries the prevalence generally varies between 20% and 50% of the population [1,2,3]. In Italy, the prevalence is estimated at approximately one-third of the population [2].
It has been demonstrated that gastric H. pylori infection plays an important role not only in the pathogenesis of gastritis and peptic ulcers, but also in oncological pathologies such as gastric cancer or gastric mucosa-associated lymphoid tissue lymphoma, and it is also believed to be associated with numerous extra-gastric pathologies [1].
For these reasons, H. pylori infection has a significant impact not only on individual health, but also on public health, in terms of both morbidity and economic cost, posing a clinical challenge for healthcare providers.
The management of H. pylori infection is an important part of clinical practice both in specialist medicine and in primary care, taking on particular importance regarding the appropriateness of diagnostic tests and, above all, the management of therapies based on the growing resistance to antibiotics [1].
To support appropriate decisions on the management of H. pylori infection, several guidelines have been developed internationally. Among these, the guidelines of the European H. pylori and Microbiota Study Group, known as the Maastricht–Florence guidelines, now in their sixth draft [4,5], are of particular importance, especially for European countries. Like all international guidelines, the Maastricht–Florence guidelines need to be adapted to national and local organizational models in the implementation process.
In Italy, neither the Maastricht–Florence guidelines nor those developed by a national expert consensus report in 2007 [6] have been officially implemented. Instead, the clinical practice of Italian general practitioners (GPs) has been governed by the reimbursement regulations of the healthcare system for drug prescriptions.
In 2022, an official guideline developed by the Italian Society of Gastroenterology and the Italian Society of Digestive Endoscopy was released [7]. The difficulty of implementing the guidelines is a complex problem that involves economic, managerial, and relational aspects [8]. Knowledge of the aspects of daily clinical practice that most deviate from the guidelines represents a key factor in setting up a virtuous implementation process.
This study aims to evaluate the approaches, attitudes, and knowledge regarding H. pylori gastric infection among Italian GPs in comparison to a group of young doctors undergoing specific training for general practice (ITGPs).
2. Results
2.1. Questionnaire Response Rate
A cohort of 910 doctors was invited to participate in the survey, comprising 800 GPs and 110 ITGPs. The survey enrolled 466 GPs, representing 58.3% of the 800 GPs invited, and 70 ITGPs, representing 63.6% of the 110 ITGPs invited.
2.2. Characteristics of Participants
In comparison to ITGPs, GPs exhibited a higher average age (57.4 ± 9.8 years vs. 32.6 ± 6.1 years; p = 0.001) and were predominantly male (61.4% vs. 38.6%, p = 0.002). Most GPs (63.3%) reported over 20 years of active service in the National Health Service (NHS), with an average patient load of 1274.8 ± 327.9. Approximately 36.7% of GPs had pursued specialization, with only 4.1% specializing in gastroenterology. Regarding knowledge about H. pylori, 58.2% of GPs deemed their understanding adequate, compared to 45.7% of ITGPs (p = 0.032).
2.3. Sources of Information on the Management of H. pylori Infection
Specialist recommendations and the Maastricht–Florence guidelines were the most frequently cited sources among GPs, whereas ITGPs relied more on the Maastricht–Florence guidelines and the internet (Table 1).
2.4. Clinical Conditions of Interest in the Search for Gastric H. pylori Infection
Although both groups recognized H. pylori infection as a significant risk factor for gastric cancer (81.6% for GPs and 91.4% for ITGPs), ITGPs were more inclined to believe that eradicating the infection could prevent cancer (92.9% vs. 86.8%, p = 0.017).
Table 2 provides insights into the search for and treatment of H. pylori infection. Key indications for investigation among GPs included uninvestigated dyspepsia in young subjects without alarm symptoms, gastric ulcer, duodenal ulcer, chronic non-atrophic gastritis, and atrophic gastritis. ITGPs demonstrated greater attention than GPs to gastric ulcer and atrophic gastritis.
Limited attention was observed towards the role of H. pylori treatment in patients with gastric cancer, first-degree relatives of gastric cancer patients, and functional dyspepsia, with ITGPs showing more interest in patients with iron-deficiency anemia compared to GPs.
2.5. Diagnostic Methods for Gastric H. pylori Infection
The most utilized diagnostic methods (Table 3) were the urea breath test and fecal test. Both groups relied on bacterium detection during esophagogastroduodenoscopy, with no significant differences observed.
2.6. Post-Treatment Control of Gastric H. pylori Infection
Most GPs (76.4%) and ITGPs (72.9%) reported always checking for eradication after treatment completion; 14.2% of GPs and 11.4% of ITGPs indicated that they only ensure eradication if the patient remains symptomatic, while 9.3% of GPs and 11.4% of ITGPs based the control on the patient’s pathology. ITGPs tended to perform eradication control earlier, with 28.4% scheduling it after at least 2 weeks and 71.6% after at least 4 weeks, compared to GPs (11.8% and 88.2%, respectively; p = 0.001).
In post-treatment evaluation, GPs more frequently utilized the fecal test, while ITGPs preferred the urea breath test (Table 3).
2.7. Therapeutic Choices for the Treatment of Gastric H. pylori Infection
Most GPs (83.9%) and ITGPs (82.9%) reported treating all patients with H. pylori infection, with a small percentage preferring selective treatment based on patient pathology.
Regarding treatment frequency, many GPs (49.1%) reported treating 5–15 cases per year: 34.1% treated fewer than 5 cases per year, 49.1% between 5 and 15 cases per year, and 10.1% more than 15 cases per year, while 6.7% were unable to quantify the number of treatments. GPs more frequently personally administered eradication therapy (76.6% almost always or often, 20.4% rarely, 3.0% never). Approximately one-third of both GPs and ITGPs were aware of the frequency of clarithromycin resistance in their area (35.4% of GPs and 38.6% of ITGPs).
Table 4 outlines the treatment regimens that participants identified as their first choice. Triple therapy emerged as the most frequently selected initial treatment regimen by both GPs and ITGPs, albeit with some variations in duration. Quadruple therapy and concomitant therapy were more commonly utilized by ITGPs.
After treatment failure, quadruple bismuth therapy emerged as the predominant option for both groups, followed by quinolone therapy and concomitant therapy (Table 5). ITGPs exhibited a greater preference for quinolone therapy than GPs.
3. Discussion
Our survey’s findings offer valuable insights into the knowledge, attitudes, and practices surrounding the management of H. pylori infection among GPs and ITGPs in Italy. The number of participating GPs was consistent with figures from several other international surveys [9,10,11]. Notably, the survey successfully captured a significant portion of the invited GPs and ITGPs, providing a comprehensive understanding of their approaches to H. pylori management.
Demographic data regarding the sex and age distribution of GPs reflect the reality of Italian general practice. In comparison to other international surveys, Italian GPs were found to be more frequently male [12] and older [9,12], which may be attributed to the delayed generational turnover in Italian primary care. This is confirmed by the fact that ITGPs were more frequently female than GPs, and that a notable proportion of GPs reported extensive experience within the National Health Service.
The survey uncovered disparities in knowledge regarding H. pylori infection between GPs and ITGPs, with a larger percentage of GPs expressing confidence in their knowledge compared to ITGPs. The Maastricht–Florence guidelines, in whose drafting Italian experts participated, are a point of reference, especially for Western European countries. The most recent Italian guidelines on H. pylori infection are substantially aligned with the Maastricht–Florence guidelines as regards indications and methods of investigation to search for infection.
Although both groups referenced established guidelines like the Maastricht–Florence guidelines, ITGPs demonstrated a greater dependency on internet sources for information, suggesting a potential preference for digital resources among younger medical practitioners. In a survey conducted in Hungary [11], postgraduate training emerged as the most favored source of information, whereas in Israel 50% of respondents reported relying on professional guidelines [13]. Knowledge of the Maastricht–Florence guidelines in Spain was found to be below 50% [12].
The survey underscored disparities in clinical focus and treatment preferences between GPs and ITGPs. ITGPs displayed greater proactivity in investigating and treating conditions like gastric ulcer, atrophic gastritis, and iron-deficiency anemia. The strategy of testing and treating H. pylori infection in uninvestigated dyspepsia among young subjects without alarm symptoms aligned with findings from surveys conducted in Israel [13] and Hungary [11]. However, this approach was not extensively promoted in Italy until the release of the recent 2022 guidelines, nor was it reimbursed by the National Health System. A substantial proportion of GPs did not mention peptic ulcer as a target of treatment for H. pylori infection, highlighting potential gaps in clinical awareness.
Both GPs and ITGPs acknowledged H. pylori infection as a significant risk factor for gastric cancer; however, ITGPs demonstrated a stronger belief in the preventive role of eradicating the infection.
The findings of this study are similar to those obtained in Croatia [10] but differ from those in Israel, where only 45.0% of respondents believed that the organism is carcinogenic, and only 65.0% agreed that H. pylori eradication reduces the risk of developing gastric cancer [9]. Despite the recognized pathogenetic role of cancer, there was limited attention to the eradication of H. pylori infection in patients with gastric cancer, mirroring the practices in Israel [9,13] and contrasting with data from Hungary [11]. Similarly, scarce emphasis was placed on the investigation and treatment of first-degree relatives of patients with gastric cancer. In Israel, this practice was more frequent, albeit not optimal [9].
Over 30% of participants indicated gastroesophageal reflux disease as a condition warranting the eradication of the infection, despite current guidelines not considering it to be an indication for treatment unless the patient with reflux disease is a candidate for prolonged gastric acid suppression therapy. Italian GPs demonstrated minimal interest in the role of gastric H. pylori infection in irritable bowel syndrome, a condition not typically associated with such an infection [14,15].
The structure of this study does not allow us to understand why family doctors show less interest in the eradication of gastric H. pylori infection in various pathologies. The fault could lie with a certain therapeutic inertia that can develop over the course of the profession, due, among other things, to the large number of pathologies to be addressed.
Both GPs and ITGPs relied on non-invasive diagnostic methods, such as the urea breath test and fecal test, with minimal differences observed between the two groups. The preference of GPs for the fecal test may be pragmatically attributable to the greater territorial availability of this test. This approach aligns with the recommendations outlined in both the Maastricht–Florence and Italian guidelines. Comparisons with other countries may be influenced by varying national and local organizational contexts. For instance, in Spain, 16% of respondents reported having no direct access to any validated diagnostic method, with only 44% having access to the urea breath test [12].
Most participants reported treating all patients diagnosed with H. pylori infection. In contrast, in Croatia, only 59.0% of general practitioners indicated that they would treat all patients [10].
Less than 40% of both GPs and ITGPs indicated awareness of the frequency of local resistance of H. pylori to antibiotics. This lack of awareness could present a challenge in treatment settings, particularly in regions like Southern Europe, known for high rates of H. pylori resistance to clarithromycin [16,17]. The reasons for lack of awareness regarding the rates of local antibiotic resistance can be many, including poor diffusion of antibiotic susceptibility tests in the case of gastric H. pylori infection, scarce availability of specific local resistance registers, and poor dissemination of available data, especially among general practitioners. Certainly, a lack of awareness regarding local rates of antibiotic resistance can lead to the use of inappropriate therapies and, therefore, limited effectiveness and a further increase in resistance. It is advisable to implement a specific program for monitoring the rates of resistance to H. pylori as part of the collaboration between GPs, specialists, and the National Health Service, as already frequently happens for urinary tract infections, for example.
As regards therapeutic choices, the Italian guidelines also include sequential therapy among the first-choice therapies, which has demonstrated good results in this country. In terms of second-line therapies in case of failure of the initial therapy, the Maastricht–Florence guidelines and the Italian ones coincide. Despite the good results obtainable overall in the European region from triple therapy based on clarithromycin, as highlighted by a recent review [18], the situation in Southern Europe, characterized by high (>15%) resistance to clarithromycin, suggests using this therapy only in areas with demonstrated low resistance [16,17,19]. The treatment approaches in our study exhibited variations, with triple therapy emerging as the preferred initial regimen for both groups. Clarithromycin resistance in H. pylori infection is notably high and increasing in Italy [17,20,21], rendering standard triple therapy potentially ineffective [22]. The overall efficacy of triple therapies has significantly declined in Italy, prompting calls to abandon them altogether due to their consistently low success rates [23]. Both the Maastricht–Florence guidelines and recent Italian guidelines advise against triple therapy as a first-line choice; however, clarithromycin-based standard triple therapy is the most preferred regimen in several European primary care settings [8,9,10]. Notably, triple therapy with amoxicillin and clarithromycin is also commonly prescribed by European gastroenterologists [24], with a slow adaptation to current recommendations by specialists as well [24,25,26]. Recent data suggest satisfactory eradication rates in Italy with bismuth-based regimens and quadruple therapies [17,23], and prescriptions for triple therapy have decreased [24].
Most participants affirmed that they consistently verify eradication, with ITGPs conducting post-treatment assessments earlier than GPs.
Although the frequency of post-therapy control aligned with findings from other countries [9,11,12], the importance of a confirmatory test after H. pylori treatment must be underlined, since it confirms effectiveness both at the individual level and for epidemiological purposes [27]. The post-treatment confirmation of eradication is recommended in all sets of published guidelines on the topic; however, retesting rates remain poor, ranging from 30% to 70% in different studies [28,29]. The importance of post-treatment confirmation appears intuitive based on the risk of disease recurrence, persistence, or development of future complications (e.g., gastric cancer), but it is also driven by concerns over emerging antimicrobial resistance and declining global eradication rates of traditional treatment regimens [29]. The data from our survey show that cases of failure to retest are linked to a choice not to retest patients with resolution of symptoms or pathologies considered minor, unlike studies in which the reasons were mainly organizational in the absence of a continuum of care [29]. These results confirm the need for the dissemination of guidelines aimed at achieving the best clinical practice. Moreover, the study revealed disparities in post-treatment evaluation practices, with GPs showing a preference for the fecal test while ITGPs leaned towards the urea breath test. The choice of test may be influenced by specific local organizational protocols.
Quadruple bismuth therapy emerged as the most prescribed second-line treatment, followed by quinolone therapy and concomitant therapy. These findings align more closely with international guidelines and national recommendations, as well as with the literature from Italy [17] and Europe [30]. Studies from European countries have shown that this second-line regimens offer optimal effectiveness [25,30].
As regards therapeutic choices, Italian GPs seem to pay for the lack of dissemination of guidelines, continuing to favor triple therapy with clarithromycin as the initial test. The ITGPs instead showed that they are aware of the most recent guidelines in their preferences for both initial and second-line treatments.
This study has several limitations. The sample of doctors examined, although large, did not include all Italian regions and was not selected with specific representativeness criteria. In a healthcare system like the Italian one, which is fragmented into regional realities, local organizational aspects, especially regarding diagnostic tests, can represent a factor influencing the activities of doctors, irrespective of their desire to adhere to the guidelines.
4. Materials and Methods
4.1. Participants
Doctors from 8 different regions across Italy were invited to participate in the survey. The GPs invited were randomly chosen from the list of doctors registered with the National Health Service of one of the provinces of each of the 8 Italian regions involved (3 in the north, 2 in the center, and 3 in the south and islands). The cohort of ITGPs was chosen by inviting all of the doctors participating in the last year of the specific training course in general medicine from the schools of 3 of the 8 Italian regions involved (1 in the north, 1 in the center, and 1 in the south). GPs were contacted via email and provided with a link to an anonymous survey form, while ITGPs were asked to complete the survey anonymously after a day of unrelated teaching activities. The ITGPs invited were still partly engaged in an educational framework, with limited direct prescribing responsibilities.
4.2. Questionnaire
The survey questionnaire covered various topics, including participants’ demographic and professional backgrounds, their approaches to managing H. pylori infections, sources of information, knowledge adequacy, oncological considerations, patient demographics, diagnostic methodologies, and pharmaceutical interventions. Responses were collected anonymously and stored in an electronic database.
4.3. Statistical Analysis
Categorical data were summarized using absolute and relative frequencies, while continuous data were presented as means and standard deviations. Qualitative factors were analyzed via chi-squared or z-tests for proportions, and quantitative factors were assessed using Mann–Whitney U tests, with significance set at 0.05. Statistical analyses were conducted utilizing STATA version 16 (Stata Corp, College Station, TX, USA).
The survey adhered to the principles outlined in the Declaration of Helsinki. Since it involved anonymous participation by professionals, it did not require review by an ethics committee. However, prior to participation, each physician provided individual consent for the anonymous utilization of the data that they provided in the questionnaire.
5. Conclusions
Our survey highlights a need for improvement in the knowledge of H. pylori guidelines among both GPs and ITGPs. Like other countries, there exists a gap between real-world practices and the recommendations provided in the current guidelines. Research has shown that adherence to guidelines can be influenced by several factors, including younger age, practicing in central urban clinic locations, and encountering a high volume of H. pylori patients [9]. However, it is crucial to prioritize the implementation of guidelines, especially among younger healthcare professionals.
Simplifying the guidelines and identifying barriers to their implementation are essential steps forward. An online survey conducted among Italian gastroenterologists and gastroenterology fellows indicated that specialists generally adhere more closely to guideline recommendations than gastroenterology fellows, but the adherence to the recommended first-line treatment regimen remains suboptimal for both groups [31]. Addressing gaps in awareness, adopting evidence-based treatment approaches, and promoting interdisciplinary collaboration are crucial measures to optimize patient care and reduce the burden of H. pylori-related diseases.
In summary, the results of our survey underscore the importance of continuous education and training initiatives to improve knowledge and clinical practices related to H. pylori management among healthcare professionals in Italy. Further research is needed to evaluate the impact of educational interventions and strategies for disseminating guidelines on clinical outcomes and healthcare delivery in this field.
Author Contributions
Conceptualization, C.T., E.U., E.B. and R.D.B.; methodology, C.T. and E.U.; formal analysis, C.T. and E.U.; investigation, C.T., E.U., E.B., L.B., L.N., C.C., R.S., A.B., G.C., M.M., G.A., G.S. and R.D.B.; writing—original draft preparation, C.T. and E.U.; writing—review and editing, C.T. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
Ethical review and approval were waived for this study because it was an anonymous professional survey.
Informed Consent Statement
Each physician provided individual consent for the anonymous utilization of the data given in the questionnaire.
Data Availability Statement
The raw data supporting the conclusions of this article will be made available by the authors on request.
Acknowledgments
This study is dedicated to the memory of Enzo Pirrotta, who played an active role in this working group.
Conflicts of Interest
The authors declare no conflicts of interest.
References
- Malfertheiner, P.; Camargo, M.C.; El-Omar, E.; Liou, J.M.; Peek, R.; Schulz, C.; Smith, S.I.; Suerbaum, S. Helicobacter pylori infection. Nat. Rev. Dis. Primers 2023, 9, 19. [Google Scholar] [CrossRef]
- Hooi, J.K.Y.; Lai, W.Y.; Ng, W.K.; Suen, M.M.Y.; Underwood, F.E.; Tanyingoh, D.; Malfertheiner, P.; Graham, D.Y.; Wong, V.W.S.; Wu, J.C.Y.; et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology 2017, 153, 420–429. [Google Scholar] [CrossRef]
- Zamani, M.; Ebrahimtabar, F.; Zamani, V.; Miller, W.H.; Alizadeh-Navaei, R.; Shokri-Shirvani, J.; Derakhshan, M.H. Systematic review with meta-analysis: The worldwide prevalence of Helicobacter pylori infection. Aliment. Pharmacol. Ther. 2018, 47, 868–876. [Google Scholar] [CrossRef]
- Malfertheiner, P.; Megraud, F.; O’Morain, C.A.; Gisbert, J.P.; Kuipers, E.J.; Axon, A.T.; Bazzoli, F.; Gasbarrini, A.; Atherton, J.; Graham, D.Y.; et al. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut 2017, 66, 6–30. [Google Scholar] [CrossRef]
- Malfertheiner, P.; Megraud, F.; Rokkas, T.; Gisbert, J.P.; Liou, J.M.; Schulz, C.; Gasbarrini, A.; Hunt, R.H.; Leja, M.; O’Morain, C.; et al. Management of Helicobacter pylori infection: The Maastricht VI/Florence consensus report. Gut 2022, 71, 1724–1762. [Google Scholar] [CrossRef] [PubMed]
- Caselli, M.; Zullo, A.; Maconi, G.; Parente, F.; Alvisi, V.; Casetti, T.; Sorrentino, D.; Gasbarrini, G.; Working Group of the Cervia II Meeting. “Cervia II Working Group Report 2006”: Guidelines on Diagnosis and Treatment of Helicobacter pylori Infection in Italy. Dig. Liver Dis. 2007, 39, 782–789. [Google Scholar] [CrossRef]
- Romano, M.; Gravina, A.G.; Eusebi, L.H.; Pellegrino, R.; Palladino, G.; Frazzoni, L.; Dajti, E.; Gasbarrini, A.; Di Mario, F.; Zagari, R.M.; et al. Management of Helicobacter pylori infection: Guidelines of the Italian Society of Gastroenterology (SIGE) and the Italian Society of Digestive Endoscopy (SIED). Dig. Liver Dis. 2022, 54, 1153–1161. [Google Scholar] [CrossRef] [PubMed]
- Fahim, C.; Prashad, A.J.; Silveira, K.; Chandraraj, A.; Thombs, B.D.; Tonelli, M.; Thériault, G.; Grad, R.; Riva, J.; Colquhoun, H.; et al. Dissemination and implementation of clinical practice guidelines: A longitudinal, mixed-methods evaluation of the Canadian Task Force on Preventive Health Care’s knowledge translation efforts. Can. Med. Assoc. Open Access J. 2023, 11, E684–E695. [Google Scholar] [CrossRef]
- Boltin, D.; Kimchi, N.; Dickman, R.; Gingold-Belfer, R.; Niv, Y.; Birkenfeld, S. Attitudes and practice related to Helicobacter pylori infection among primary care physicians. Eur. J. Gastroenterol. Hepatol. 2016, 28, 1035–1040. [Google Scholar] [CrossRef] [PubMed]
- Jukic, I.; Vukovic, J.; Rusic, D.; Bozic, J.; Bukic, J.; Leskur, D.; Seselja Perisin, A.; Modun, D. Adherence to Maastricht V/Florence consensus report for the management of Helicobacter pylori infection among primary care physicians and medical students in Croatia: A cross-sectional study. Helicobacter 2021, 26, e12775. [Google Scholar] [CrossRef]
- Márkus, B.; Herszényi, L.; Matyasovszky, M.; Vörös, K.; Torzsa, P.; Rurik, I.; Tulassay, Z.; Kalabay, L. The Diagnosis and Therapy of Helicobacter pylori Infection in Hungary: Comparison of Strategies Applied by Family Physicians and Internists. Dig. Dis. 2019, 37, 434–443. [Google Scholar] [CrossRef] [PubMed]
- McNicholl, A.G.; Amador, J.; Ricote, M.; Cañones-Garzón, P.J.; Gene, E.; Calvet, X.; Gisbert, J.P. Spanish Primary Care Survey on the Management of Helicobacter pylori Infection and Dyspepsia: Information, Attitudes, and Decisions. Helicobacter 2019, 24, e12593. [Google Scholar] [CrossRef] [PubMed]
- Na’amnih, W.; Ben Tov, A.; Bdair-Amsha, A.; Cohen, S.; Tsamir, J.; Chodick, G.; Muhsen, K. Physicians’ adherence to management guidelines for H. pylori infection and gastroesophageal reflux disease: A cross-sectional study. Isr. J. Health Policy Res. 2020, 9, 28. [Google Scholar] [CrossRef]
- Li, L.; Tan, J.; Liu, L.; Li, J.; Chen, G.; Chen, M.; Xie, J.; Song, Q.; Huang, X.; Xie, S. Association between H. pylori infection and health outcomes: An umbrella review of systematic reviews and meta-analyses. BMJ Open 2020, 10, e031951. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Zhang, J.; Han, F.; Liu, D.; Han, Y. No evidence for a causal link between Helicobacter pylori infection and irritable bowel syndrome: A Mendelian randomization study. Front. Microbiol. 2024, 14, 1268492. [Google Scholar] [CrossRef] [PubMed]
- Megraud, F.; Bruyndonckx, R.; Coenen, S.; Wittkop, L.; Huang, T.D.; Hoebeke, M.; Bénéjat, L.; Lehours, P.; Goossens, H.; Glupczynski, Y.; et al. Helicobacter pylori resistance to antibiotics in Europe in 2018 and its relationship to antibiotic consumption in the community. Gut 2021, 70, 1815–1822. [Google Scholar] [CrossRef]
- Nista, E.C.; Pellegrino, A.; Giuli, L.; Candelli, M.; Schepis, T.; De Lucia, S.S.; Ojetti, V.; Franceschi, F.; Gasbarrini, A. Clinical Implications of Helicobacter pylori Antibiotic Resistance in Italy: A Review of the Literature. Antibiotics 2022, 11, 1452. [Google Scholar] [CrossRef] [PubMed]
- Zamani, M.; Alizadeh-Tabari, S.; Zamani, V.; Shokri-Shirvani, J.; Derakhshan, M.H. Worldwide and Regional Efficacy Estimates of First-line Helicobacter pylori Treatments: A Systematic Review and Network Meta-Analysis. J. Clin. Gastroenterol. 2022, 56, 114–124. [Google Scholar] [CrossRef] [PubMed]
- Thung, I.; Aramin, H.; Vavinskaya, V.; Gupta, S.; Park, J.Y.; Crowe, S.E.; Valasek, M.A. Review article: The global emergence of Helicobacter pylori antibiotic resistance. Aliment. Pharmacol. Ther. 2016, 43, 514–533. [Google Scholar] [CrossRef]
- Saracino, I.M.; Zullo, A.; Holton, J.; Castelli, V.; Fiorini, G.; Zaccaro, C.; Ridola, L.; Ricci, C.; Gatta, L.; Vaira, D. High prevalence of primary antibiotic resistance in Helicobacter pylori isolates in Italy. J. Gastrointest. Liver Dis. 2012, 21, 363–365. [Google Scholar]
- Saracino, I.M.; Fiorini, G.; Zullo, A.; Pavoni, M.; Saccomanno, L.; Vaira, D. Trends in Primary Antibiotic Resistance in H. pylori Strains Isolated in Italy between 2009 and 2019. Antibiotics 2020, 9, 26. [Google Scholar] [CrossRef] [PubMed]
- Rokkas, T.; Gisbert, J.P.; Malfertheiner, P.; Niv, Y.; Gasbarrini, A.; Leja, M.; Megraud, F.; O’Morain, C.; Graham, D.Y. Comparative Effectiveness of Multiple Different First-Line Treatment Regimens for Helicobacter pylori Infection: A Network Meta-Analysis. Gastroenterology 2021, 161, 495–507. [Google Scholar] [CrossRef] [PubMed]
- De Francesco, V.; Zullo, A.; Manta, R.; Pavoni, M.; Saracino, I.M.; Fiorini, G.; Giostra, F.; Monti, G.; Vaira, D. First-line therapies for H. pylori infection in Italy: A pooled-data analysis. Acta Gastro-Enterol. Belg. 2022, 85, 295–299. [Google Scholar] [CrossRef] [PubMed]
- Nyssen, O.P.; Vaira, D.; Tepes, B.; Kupcinskas, L.; Bordin, D.; Pérez-Aisa, Á.; Gasbarrini, A.; Castro-Fernández, M.; Bujanda, L.; Garre, A.; et al. Room for Improvement in the Treatment of Helicobacter pylori Infection: Lessons from the European Registry on H. pylori Management (Hp-EuReg). J. Clin. Gastroenterol. 2022, 56, e98–e108. [Google Scholar]
- Nyssen, O.P.; Vaira, D.; Pérez Aísa, Á.; Rodrigo, L.; Castro-Fernandez, M.; Jonaitis, L.; Tepes, B.; Vologzhanina, L.; Caldas, M.; Lanas, A.; et al. Empirical Second-Line Therapy in 5000 Patients of the European Registry on Helicobacter pylori Management (Hp-EuReg). Clin. Gastroenterol. Hepatol. 2022, 20, 2243–2257. [Google Scholar] [CrossRef] [PubMed]
- Graham, D.Y.; El-Serag, H.B. European Registry on Helicobacter pylori management shows that gastroenterology has largely failed in its efforts to guide practitioners. Gut 2021, 70, 1–2. [Google Scholar] [CrossRef] [PubMed]
- Ariño-Pérez, I.; Martínez-Domínguez, S.J.; Alfaro Almajano, E.; Carrera-Lasfuentes, P.; Lanas, Á. Mistakes in the diagnosis and treatment of Helicobacter pylori infection in daily clinical practice. Helicobacter 2023, 28, e12957. [Google Scholar] [CrossRef] [PubMed]
- O’Connor, A.; O’Moráin, C. Mistakes in the management of Helicobacter pylori infection and how to avoid them. UEG Educ. 2017, 17, 42–44. [Google Scholar]
- Sharara, A.I. Confirmatory Testing for Eradication of Helicobacter pylori: Challenges and Opportunities. Clin. Gastroenterol. Hepatol. 2021, 19, 232–234. [Google Scholar] [CrossRef]
- De Francesco, V.; Zullo, A.; Manta, R.; Gatta, L.; Fiorini, G.; Saracino, I.M.; Vaira, D. Helicobacter pylori eradication following first-line treatment failure in Europe: What, how and when chose among different standard regimens? A systematic review. Eur. J. Gastroenterol. Hepatol. 2021, 33 (Suppl. S1), e66–e70. [Google Scholar] [CrossRef]
- Zagari, R.M.; Romano, M.; Frazzoni, L.; Marasco, G.; Dajti, E.; Arcidiacono, P.G.; Armuzzi, A.; Biagi, F.; Cannizzaro, R.; Cavestro, G.M.; et al. Adherence to international guidelines for the management of Helicobacter pylori infection among gastroenterologists and gastroenterology fellows in Italy: A Survey of the Italian Federation of Digestive Diseases-FISMAD. Helicobacter 2022, 27, e12862. [Google Scholar] [CrossRef] [PubMed]
Table 1.
Differences in sources of information on the management of gastric H. pylori infection between GPs and ITGPs (multiple answers possible).
Table 1.
Differences in sources of information on the management of gastric H. pylori infection between GPs and ITGPs (multiple answers possible).
| Sources | GPs n (%) | ITGPs n (%) | p-Values |
|---|---|---|---|
| Recommendations from specialists | 178 (38.2%) | 20 (28.6%) | n.s. |
| Maastricht–Florence guidelines | 165 (35.1%) | 28 (40.0%) | n.s. |
| Professional journals (printed or online) | 126 (27.0%) | 15 (21.4%) | n.s. |
| Directives from national/local health system | 114 (24.5%) | 14 (20.0%) | n.s. |
| Educational courses on H. pylori or dyspepsia | 112 (24.0%) | 22 (31.4%) | n.s. |
| Other international guidelines | 102 (21.9%) | 18 (25.7%) | n.s. |
| Other internet resources | 70 (15.0%) | 24 (34.3%) | 0.002 |
| Advice from a colleague general practitioner | 49 (10.5%) | 19 (27.1%) | 0.002 |
GPs = general practitioners; ITGPs = doctors in training for general practice; n.s. = not significant.
Table 2.
Differences in clinical conditions of interest in the search for gastric H. pylori infection between GPs and ITGPs (multiple answers possible).
Table 2.
Differences in clinical conditions of interest in the search for gastric H. pylori infection between GPs and ITGPs (multiple answers possible).
| Clinical Conditions | GPs n (%) | ITGPs n (%) | p-Values |
|---|---|---|---|
| Uninvestigated dyspepsia in patients aged < 50 years | 313 (67.2%) | 52 (74.3%) | n.s |
| Gastric ulcer | 304 (65.2%) | 58 (82.9%) | 0.005 |
| Duodenal ulcer | 237 (50.9%) | 44 (62.9%) | n.s |
| Chronic non-atrophic gastritis | 196 (42.1%) | 27 (38.6%) | n.s |
| Chronic atrophic gastritis | 170 (36.5%) | 41 (58.6%) | 0.011 |
| Gastroesophageal reflux disease | 142 (30.5%) | 32 (45.7%) | 0.032 |
| Functional dyspepsia (EGD negative) | 121 (26.0%) | 22 (31.4%) | n.s |
| First-degree family members of patients with gastric cancer | 120 (25.6%) | 19 (27.1%) | n.s |
| Gastric cancer | 86 (18.5%) | 26 (37.1%) | 0.012 |
| Iron-deficiency anemia of unknown origin | 81 (17.4%) | 22 (31.4%) | 0.007 |
| Start of long-term therapy with proton-pump inhibitors | 52 (11.2%) | 10 (14.3%) | n.s |
| Start of long-term therapy with NSAIDs * | 50 (10.7%) | 3 (4.3%) | n.s |
| Patient request | 46 (9.9%) | 6 (8.6%) | n.s |
| Dermatitis of unknown origin | 32 (6.9%) | 4 (5.4%) | n.s |
| Irritable bowel syndrome | 18 (3.9%) | 6 (8.6%) | n.s |
GPs = general practitioners; ITGPs = doctors in training for general practice. * NSAIDs = non-steroidal anti-inflammatory drugs; n.s. = not significant.
Table 3.
Differences in the tests utilized for the diagnosis of H. pylori infection and the control after treatment between GPs and ITGPs (multiple answers possible).
Table 3.
Differences in the tests utilized for the diagnosis of H. pylori infection and the control after treatment between GPs and ITGPs (multiple answers possible).
| Test | First Diagnosis of H. pylori Infection | Control after Treatment | ||||
|---|---|---|---|---|---|---|
| GPs n (%) | ITGPs n (%) | p-Values | GPs n (%) | ITGPs n (%) | p-Values | |
| Urea breath test | 311 (66.7%) | 55 (78.6%) | n.s | 212 (45.6%) | 45 (67.2%) | 0.002 |
| Fecal antigen test | 314 (67.4%) | 48 (68.6%) | n.s | 298 (64.1%) | 33 (49.3%) | 0.027 |
| Serology | 68 (14.7%) | 17 (24.3%) | n.s | 69 (14.8%) | 5 (7.5%) | n.s |
| Histology/rapid urease test | 176 (37.8% | 33 (47.1%) | n.s | 29 (6.2%) | 6 (9.0%) | n.s |
GPs = general practitioners; ITGPs = doctors in training for general practice; n.s. = not significant.
Table 4.
Differences in the use of first-line therapies for H. Pylori infection between GPs and ITGPs.
Table 4.
Differences in the use of first-line therapies for H. Pylori infection between GPs and ITGPs.
| Regimen | GPs n (%) | ITGPs n (%) | p-Values |
|---|---|---|---|
| Dual therapy | |||
| 7 days | 21 (4.5%) | 0 (0.0%) | n.s |
| 10 days | 7 (1.5%) | 1 (0.1%) | n.s |
| 14 days | 9 (1.9%) | 2 (0.3%) | n.s |
| Triple therapy | |||
| 7 days | 136 (29.2%) | 10 (14.3%) | 0.014 |
| 10 days | 109 (23.4%) | 21 (30.0%) | 0.010 |
| 14 days | 82 (17.6%) | 22 (31.4%) | 0.001 |
| Quadruple therapy | |||
| 10 days | 69 (14.8%) | 22 (31.4%) | 0.001 |
| Concomitant therapy | |||
| 7 days | 49 (10.5%) | 7 (10.0%) | n.s |
| 10 days | 46 (9.9%) | 14 (20.0%) | 0.021 |
| Sequential therapy | |||
| 10 days | 79 (17.0%) | 9 (12.9%) | n.s |
| 14 days | 52 (11.2%) | 12 (17.1%) | n.s |
| Quinolone therapy | |||
| 10 days | 39 (8.4%) | 5 (7.1%) | n.s |
GPs = general practitioners; ITGPs = doctors in training for general practice; Dual therapy = amoxicillin + PPI; Triple therapy = amoxicillin + clarithromycin + PPI; Concomitant therapy = amoxicillin + clarithromycin + metronidazole/tinidazole + PPI; Sequential therapy = amoxicillin + PPI (5 days), followed by clarithromycin + metronidazole/tinidazole + PPI (5 days); Quadruple therapy = bismuth + tetraciclin + metronidazole/tinidazole + PPI; Quinolone therapy = amoxicillin + levofloxacin + PPI; PPI = proton-pump inhibitor; n.s. = not significant.
Table 5.
Differences in the use of second-line therapies for H. Pylori infection between GPs and ITGPs.
Table 5.
Differences in the use of second-line therapies for H. Pylori infection between GPs and ITGPs.
| Regimen | GPs n (%) | ITGPs n (%) | p-Values |
|---|---|---|---|
| Dual therapy | |||
| 7 days | 7 (1.5%) | 0 (0.0%) | n.s |
| 10 days | 6 (1.3%) | 0 (0.0%) | n.s |
| 14 days | 7 (1.5%) | 1 (0.1%) | n.s |
| Triple therapy | |||
| 7 days | 17 (3.6%) | 2 (0.3%) | n.s |
| 10 days | 16 (3.4%) | 1 (0.1%) | n.s |
| 14 days | 30 (6.4%) | 3 (4.3%) | n.s |
| Quadruple therapy | |||
| 10 days | 150 (32.2%) | 26 (37.1%) | n.s |
| Concomitant therapy | |||
| 7 days | 49 (10.5%) | 5 (7.1%) | n.s |
| 10 days | 79 (17.0%) | 19 (27.1%) | n.s |
| Sequential therapy | |||
| 10 days | 64 (13.7%) | 8 (11.4%) | n.s |
| 14 days | 73 (15.7%) | 16 (22.9%) | n.s |
| Quinolone therapy | |||
| 10 days | 85 (18.2%) | 22 (31.4%) | 0.016 |
GPs = general practitioners; ITGPs = doctors in training for general practice; Dual therapy = amoxicillin + PPI; Triple therapy = amoxicillin + clarithromycin + PPI; Concomitant therapy = amoxicillin + clarithromycin + metronidazole/tinidazole + PPI; Sequential therapy = amoxicillin + PPI (5 days), followed by clarithromycin + metronidazole/tinidazole + PPI (5 days); Quadruple therapy = bismuth + tetraciclin + metronidazole/tinidazole + PPI; Quinolone therapy = amoxicillin + levofloxacin + PPI; PPI = proton-pump inhibitor; n.s. = not significant.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Tosetti, C.; Ubaldi, E.; Benedetto, E.; Bertolusso, L.; Napoli, L.; Cottone, C.; Scoglio, R.; Belvedere, A.; Casella, G.; Mancuso, M.; et al. Survey on the Knowledge and the Management of Helicobacter pylori Infection by Italian General Practitioners and Doctors in General Practice Training. Gastrointest. Disord. 2024, 6, 421-430. https://doi.org/10.3390/gidisord6020028
AMA Style
Tosetti C, Ubaldi E, Benedetto E, Bertolusso L, Napoli L, Cottone C, Scoglio R, Belvedere A, Casella G, Mancuso M, et al. Survey on the Knowledge and the Management of Helicobacter pylori Infection by Italian General Practitioners and Doctors in General Practice Training. Gastrointestinal Disorders. 2024; 6(2):421-430. https://doi.org/10.3390/gidisord6020028
Chicago/Turabian StyleTosetti, Cesare, Enzo Ubaldi, Edoardo Benedetto, Luciano Bertolusso, Luigi Napoli, Carmelo Cottone, Riccardo Scoglio, Alessandra Belvedere, Giovanni Casella, Maurizio Mancuso, and et al. 2024. "Survey on the Knowledge and the Management of Helicobacter pylori Infection by Italian General Practitioners and Doctors in General Practice Training" Gastrointestinal Disorders 6, no. 2: 421-430. https://doi.org/10.3390/gidisord6020028
