Next Article in Journal
Healthcare Service Efficiency: An Empirical Study on Healthcare Capacity in Various Counties and Cities in Taiwan
Previous Article in Journal
A Service Reconfiguration Bundle for Expanding Access to Peritoneal Dialysis Including for Older Frailer Patients
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Healthcare
Volume 11
Issue 11
10.3390/healthcare11111658
healthcare-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Helicobacter pylori Infection and Peptic Ulcer Disease in Symptomatic Children in Southern Vietnam: A Prospective Multicenter Study

by
Tu Cam Nguyen
1,2,*,†,
Ngoc Le Chau Tang
3,
Giao Kim Ngoc Le
4,
Vy Thuy Nguyen
5,
Khuong Hoang Gia Nguyen
6,
Thai Hoang Che
6,
Van Thi Tuong Phan
1,
Ngoc Minh Nguyen
3,
Dinh Quang Truong
7,
Xuan Minh Ngo
8,
Hiep Thanh Nguyen
9,
Annie Robert
10,
Patrick Bontems
2,11 and
Phuong Ngoc Van Nguyen
6,†
1
Department of Gastroenterology, City Children’s Hospital, Ho Chi Minh City 700000, Vietnam
2
Faculty of Medicine, Université Libre de Bruxelles, 1020 Brussels, Belgium
3
Department of Gastroenterology, Children’s Hospital 2, Ho Chi Minh City 700000, Vietnam
4
Department of Microbiology and Parasitology, University of Medicine and Pharmacy, Ho Chi Minh City 700000, Vietnam
5
Department of Genetics, University of Science—Vietnam National University Ho Chi Minh City, Ho Chi Minh City 700000, Vietnam
6
Department of Biostatistics and Informatics, Pham Ngoc Thach University of Medicine, Ho Chi Minh City 700000, Vietnam
7
Department of Surgery, City Children’s Hospital, Ho Chi Minh City 700000, Vietnam
8
Faculty of Medicine, Pham Ngoc Thach University of Medicine, Ho Chi Minh City 700000, Vietnam
9
Faculty of Public Health, Pham Ngoc Thach University of Medicine, Ho Chi Minh City 700000, Vietnam
10
Institut de Recherche Expérimentale et Clinique, Pôle d’Épidémiologie et Biostatistique, Université Catholique de Louvain, 1200 Brussels, Belgium
11
Department of Gastroenterology, Hôpital Universitaire des Enfants Reine Fabiola, 1020 Brussels, Belgium
 
add Show full affiliation list
 
remove Hide full affiliation list
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Healthcare 2023, 11(11), 1658; https://doi.org/10.3390/healthcare11111658
Submission received: 19 April 2023 / Revised: 24 May 2023 / Accepted: 31 May 2023 / Published: 5 June 2023
Browse Figures
Versions Notes

Abstract

:
Background: Helicobacter pylori (H. pylori) remains a major cause of gastroduodenal diseases. We aimed to evaluate the burden of this infection, particularly peptic ulcer disease in Vietnamese children. Methods: We enrolled consecutive children referred for esophagogastroduodenoscopy at two tertiary children’s hospitals in Ho Chi Minh City, from October 2019 to May 2021. Children treated with proton pump inhibitors during the last two weeks or antibiotics for four weeks, and those having a previous or interventional endoscopy were excluded. H. pylori infection was diagnosed with either a positive culture or positive histopathology combined with a rapid urease test, or with a polymerase chain reaction of the urease gene. The study was approved by the Ethics Committee and written informed consent/assent was obtained. Results: Among 336 enrolled children aged 4–16 (mean: 9.1 ± 2.4 years; 55.4% girls), H. pylori infection was positive in 80%. Peptic ulcers were detected in 65 (19%), increasing with age, and 25% with anemia. cagA+ strains were detected at a higher rate in children with ulcers. Conclusions: Prevalence of H. pylori and peptic ulcers is high among symptomatic Vietnamese children. It is crucial to have a program for early detection of H. pylori to reduce ulcer risk and gastric cancer later.

1. Introduction

Helicobacter pylori (H. pylori) infection remains a significant cause of human gastroduodenal diseases, especially in highly prevalent countries. It is commonly acquired during childhood and can have long-term consequences. H. pylori may cause chronic gastritis and gastroduodenal ulcers, affecting both children and adults [1,2]. It can sometimes progress to stomach cancer decades later [3]. Although rare, H. pylori infection can also lead to gastric mucosa-associated lymphoid tissue lymphoma, particularly in children [4]. Furthermore, it may be associated with certain extra-intestinal diseases such as chronic idiopathic thrombocytopenic purpura, iron deficiency anemia, Henoch–Schonlein purpura, and nutritional status [5].
Its clinical manifestations are diverse, nonspecific, and can be asymptomatic. Diagnosis of H. pylori infection in children relies on an upper gastrointestinal (GI) endoscopy using biopsy-based diagnostic tests [6], with acceptable indications for upper GI endoscopies described by Tringali et al. [7].
Vietnam is regarded as an emerging country, but H. pylori prevalence in the community remains high [8,9]. H. pylori infection was estimated at 70.3% of the Vietnamese population in 2017 [8]. In 2022, the prevalence of H. pylori was reported at 87.7% in school-aged children in Ho Chi Minh City [10].
Clinical data in symptomatic, scoped, Vietnamese children are rare. Recent clinical series have reported an increase in H. pylori-induced gastritis and peptic ulcer disease (PUD) among children over the past decade [11,12,13,14]. However, comparing across centers is difficult because diagnostic tests depend upon local resources, not always aligned with international standards. Therefore, extensive hospital-based, prospective, multicenter studies are needed to determine the infection rate, clinical features, and endoscopic findings of H. pylori infection in symptomatic Vietnamese children. We conducted such a study in two pediatric reference endoscopic facilities in Ho Chi Minh City, Vietnam’s largest city.

2. Materials and Methods

2.1. Study Population and Design

The study was conducted at two pediatric hospitals in Ho Chi Minh City (HCMC), from October 2019 to May 2021. The 1400-bed Children’s Hospital 2 and the 1000-bed City Children’s Hospital serve as primary facilities for the local population in HCMC and as the tertiary referral centers for children from 18 southern provinces, with a catchment population of over 2.4 million children [15]. We recruited consecutive children aged 4 to 16 years assigned to upper GI endoscopy due to alarm symptoms according to the guidelines of the European Society of Gastrointestinal Endoscopy (ESGE) and European Society for Pediatric Gastroenterology Hepatology and Nutrition (ESPGHAN) [6]. Alarm symptoms include persistent right upper quadrant pain, dysphagia, odynophagia, persistent vomiting, GI blood loss, and weight loss. Children underwent therapeutic endoscopic procedures; those with a previous history of upper GI endoscopy; those who had taken proton-pump inhibitors (PPIs), 2-histamine receptor antagonists, antacids, and bismuth salts within two weeks, or antibiotics within four weeks before endoscopy, were excluded from the study. Data on demographic characteristics, history of H. pylori infection, underlying diseases, clinical symptoms, and endoscopic findings were collected. Nutritional status was determined using anthropometric measurements and classified as underweight, normal weight, overweight, and obesity according to the World Health Organization Child Growth Standards Chart.
Written informed consent of parents/legal guardians was obtained before data and sample collection. Children older than 12 years also signed informed assent. The study was approved by the Scientific Council of the Pham Ngoc Thach University of Medicine (No 2683/QĐ-TĐHYKPNT) and the local Ethics Committees of two hospitals (No 37/QĐ-BVNĐTP).

2.2. Gastrointestinal Endoscopy and H. pylori Tests

Each patient underwent an upper GI endoscopy, with macroscopic findings recorded for the esophagus, gastric corpus, gastric antrum, and duodenum. Endoscopic lesions were categorized based on the most severe lesion in ascending order of erythema, nodularity, erosion, and ulceration if both gastric and duodenal lesions were present, using Minimal Standard Terminology for Digestive Endoscopy [16]. The Los Angeles Classification [17] was used for grading erosive esophagitis. The Forrest classification was used for peptic ulcers with spurting hemorrhage (Forrest Ia), oozing hemorrhage (Forrest Ib), non-bleeding visible vessel (Forrest IIa), adherent clotting (Forrest IIb), flat pigmented hematin on an ulcer base (Forrest IIc), and a clean base ulcer (Forrest III) [18]. Following ESPGHAN recommendations [7], three antrum and two corpus biopsy specimens were taken routinely, whenever not contra-indicated, for H. pylori culture, histopathology, rapid urease test (RUT), and polymerase chain reaction (PCR) assay of urease gene-ureA, cytotoxin-associated gene A (cagA) gene, and vacuolating cytotoxin A (vacA) genotypes during the endoscopy.
Two biopsies (one antrum, one corpus) for H. pylori culture were preserved separately in specialized carrying media, brain heart infusion broth, with 1% agar at 4 °C. They were transported within 4 h to the laboratory. Plates were incubated for up to 14 days at 35 °C under microaerophilic conditions. Positive reactions for oxidase, catalase, and urease identified isolates of H. pylori.
Two other biopsies (one antrum, one corpus) were preserved in a 10% formalin solution and stained with Hematoxylin-Eosin and Giemsa. Histological classification was defined using the updated Sydney classification system [19].
The remaining gastric antrum biopsy was used for on-site RUT (Urease NS, Vieta Corporation, Ho Chi Minh City, Vietnam) and PCR assays for the urease gene-ureA, as well as virulence factors, such as cagA gene and vacA genotypes. Real-time PCR was performed using the AccuPid H. pylori Detection Kit (KT Biotech, Ho Chi Minh City, Vietnam) for urease gene detection. Urease PCR-positive samples were further genotyped for cagA and vacA genes using Multiplex PCR with the AccuLite H. pylori Genotyping Kit (KT Biotech, Ho Chi Minh City, Vietnam) and primer sequences from a previous Vietnamese study [20]. After that, they were then synthesized using Integrated Device Technology. Multiplex PCR was performed in Biometra (Tprofessional Thermocycler Family). PCR products for each reaction were electrophoresed on 5% agarose gel, stained with ethidium bromide, and visualized under UV light.
The diagnosis of H. pylori infection was based on either a positive culture or the combination of histological examination with at least one other positive biopsy-based test (RUT or PCR), following ESPGHAN/NASPGHAN criteria [6]. H. pylori status was defined as doubtful if the culture was negative with one other positive biopsy test.

2.3. Statistical Analysis

Data were coded and recorded using EpiData software version 4.6.0 (EpiData Association, Odense, Denmark), with encoding performed by two data managers. Data monitoring was conducted by the first author (T.C.N.), and additional plausibility checks were performed before exporting to StataSE 17.0 (Stata Corporation, College Station, TX, USA) for analysis. Initially, a descriptive analysis was performed to determine the H. pylori infection rate. Subsequently, a univariable analysis was performed using the chi-square test (or Fisher’s exact test) to compare H. pylori infection between the categories of variables (gender, living area, history of gastroduodenal disease, history of H. pylori infection, nutritional status, clinical manifestations, endoscopic findings, cagA status, and vacA genotypes). For ordered categorical variables such as age subgroups, the Cochran–Armitage test for trend was used. In the multivariable logistic regression model, variables were entered if they had a univariate p-value < 0.25. This model was built for identifying factors independently associated with H. pylori infection or with PUD. A p-value less than 0.05 was considered significant.

3. Results

3.1. Patient Characteristics

From October 2019 to May 2021, among 1461 consecutive children undergoing upper GI endoscopy at the two children’s hospitals in HCMC, 336 patients who met the criteria were included in the study (Figure 1).
The mean age was 9.1 ± 2.4 years (range: 4.2–15.3 years) and 55.4% (186/336) were girls. The proportion of boys increased significantly with age: 33.3% (8/24) were in the group under 6 years, 40.8% (97/238) in the group aged 6–11 years, and 60.8% (45/74) in the group above 11 years. Most children lived in HCMC (39.9%), followed by South-East provinces (28%), Mekong River Delta (22.9%), and other regions (9.2%). Children presented with an average of four GI symptoms at endoscopy. The most common symptoms were chronic abdominal pain (95.2%; 320/336) and epigastric pain (75.3%; 253/336). More than a third of patients showed accompanying symptoms (vomiting, constipation, regurgitation, weight loss, and loss of appetite).

3.2. H. pylori Infection Rate in Symptomatic Children

The positivity rate was 39.0% (131/336) for H. pylori culture, 79.7% (267/335) for histopathology, 83.6% (280/335) for PCR ureA, and 83.6% (281/335) for RUT. H. pylori status was confirmed positive in 80.1% of patients (269/336), doubtful in 9.2% (31/336), and negative in 10.7% (36/336). The prevalence of H. pylori infection was similar between age groups and gender but varied between boys and girls across different age groups (Figure 2).
Living in HCMC was associated with higher H. pylori infection rates in both univariable and multivariable logistic regression (OR = 4.28; 95% CI: [2.15–8.55]; p < 0.001), while there was no difference between urban and rural residents of HCMC.
No association was found between demographic characteristics, history of gastroduodenal diseases, history of H. pylori infection, nutritional status, clinical symptoms, and H. pylori infection (Table 1).

3.3. H. pylori Infection and Gastroduodenal Endoscopic Lesions

Among 336 symptomatic children, the most common mucosal abnormalities were nodularity, accounting for 60.7% (204/336), followed by ulcers (19.4%, 65/336), erythema (12.2%; 41/336) and erosion (7.7%; 26/336). Nodularity was commonly observed in the stomach. Ulcers were predominantly located in the duodenal bulb (93.9%, 61/65), both gastric and duodenal ulcers (4.6%, 3/65), and in the stomach (1.5%,1/65). Erosive esophagitis was reported in only 1.8% of the children (6/336) (Table 2).
Regarding peptic ulcers, the median diameter was 7 mm (IQR: 5–15 mm). Multiple ulcers were observed most frequently, accounting for 50.8% (33/65). Forrest classification was available in 37 out of 65 cases (Forrest class III: 91.9%; Forrest class IIb: 8.1%). Among the children with ulcers, nodular gastritis was found in 83.1% (54/65).
H. pylori infection was positive in 93.8% of children with ulcers (61/65) and in 76.8% of children without ulcers (208/271). There was a significant association between nodularity, PUD, and H. pylori infection. Ulcers appeared more commonly in boys and with increasing age. Children with ulcers presented frequently with anemia (15/32; 46.9%) and melena (11/20; 55%), but this significant association was not observed in multiple analysis. Table 3 provides further information on demographics, family history of PUD, nutritional status, clinical symptoms, and virulence factors of H. pylori-positive children with and without ulcers.

3.4. H. pylori Virulence Factors

PCR was successfully performed in 268 out of the 269 children diagnosed with H. pylori infection, and cagA was detected in 69% (185/268) of the cases. H. pylori isolates carrying the cagA gene had a higher risk of ulceration (OR: 3.25, (95% CI: 1.37–17.71); p = 0.008). vacA genotypes were associated with ulcers in univariable analysis, but not significantly different in the multivariable analysis. In children with ulcers, the vacA s1/m1m2 was higher while the vacA s1/m2 genotype was lower.

4. Discussion

The overall prevalence of H. pylori infection among symptomatic Vietnamese children was approximately 80%, much higher than that reported worldwide (21.9%) [21] and in Southeast Asia (48.4%) [21]. When confirmed and doubtful infections are pooled, the infection rate reached 89.2%. This infection rate is 1.8 to 2.3-fold higher than the rate observed in the communities in the Northern and central provinces of Vietnam such as Hanoi (34%) [22], TayNguyen (40%) [23], and HoaBinh (42.8%) [24], but it is close to the rate of 87.7% among school-aged children in HCMC [10] and of 90% among hospitalized children in Hanoi [25]. These findings indicate an alarming prevalence of H. pylori infection in symptomatic children in Southern Vietnam.
Interestingly, children living in HCMC had higher H. pylori infections than in neighboring provinces, which supports findings from a community-based study conducted in HCMC with school-aged children from 6 to 15 years (87.7%) [10]. The overcrowded living conditions explain this finding. HCMC has a high population density of 4375 people/km2, in contrast to lower population densities in the South-East regions (778 persons/km2), and the Mekong Delta region (426 persons/km2) [15]. However, the infection rate was similar between urban and rural areas, which is consistent with findings in a hospital-based study in Hanoi [22], but different from a community-based study in HCMC that showed higher infection rates in urban areas [10]. In Vietnamese tradition, living together across generations, and sharing beds, dishes, and food with chopsticks may increase H. pylori infection risk [22,24,26,27]. Regarding socioeconomic factors, in a community-based study in HCMC using a stool antigen test, all crowding factors such as population density, employee density, family size, and the number of children in a household were significantly associated with a high prevalence of H. pylori infection [28]. Age and gender were not associated with H. pylori infection in this study, which is in line with other research [21,29,30,31]. H. pylori infection typically increases with age, with a prevalence ranging from 31.6% in high-income countries to 54.7% in low-income countries [21,29,32]. This may be related to our study series being selective in hospitals while the community-based studies used random sampling and as such, are more representative. However, H. pylori transmission appeared to occur at an early age, as 79.2% of children between 4 and 5 years of age were already infected.
Children with H. pylori may exhibit GI symptoms or may only be diagnosed when complications occur, such as upper GI bleeding or perforation from peptic ulcers [1,2]. The main indications for upper GI endoscopy in our study were persistent abdominal pain (95.2%) and epigastric pain (75.3%). Although the association between clinical symptoms and H. pylori infection was not significant, these findings highlight the importance of clinicians considering H. pylori gastritis and PUD as potential organic causes in children with alarming GI symptoms.
Regarding endoscopic lesions, most patients had abnormal appearances in the stomach and duodenum. Despite all children being symptomatic and referred for endoscopy due to suspected organic causes, the diagnostic yield was remarkably high. The most common endoscopic lesions in children were nodularity (60.7%), of which 83.8% were positive for H. pylori. Nodularity has been reported in infected children, ranging from 21 to 93% [11,13,33,34,35,36]. It is a typical endoscopic finding in children with H. pylori infection [34,37]. However, it could be caused by other viral infections (CMV, EBV), autoimmune disorders, NSAIDs use, or gastric cancer [2,36]. Nodular gastritis may be a good predictor of H. pylori infection [35,37], with high specificity (99.7%) but low sensitivity (7.2%) [38]. However, antral nodularity was still present in some H. pylori-negative patients (16.2%), possibly due to the spontaneous elimination of H. pylori, which can occur in around 2% of infected children [39,40,41].
PUD, though uncommon in children, can lead to severe complications such as GI bleeding or perforation [2]. This study recorded a high frequency of ulcers (19.4%), mainly located in the duodenum. Our results exceed the global rates reported in the clinical series, which ranged from 1% to 13% [30,42,43]. Notably, PUD in Vietnamese children seems to be on the rise or better recognized. The prevalence of PUD in children was only 1% in 2011 [11] and increased by 14,1% in 2014 [12]. More recently, in 2022, the ulcer rate was alarmingly high (30.8%) in Can Tho City, a neighboring province of HCMC [14]. Improved socioeconomic conditions and advancements in Vietnam’s health sector have made healthcare services more accessible [15]. Endoscopy indications in children have also been extended based on international guidelines [6]. Moreover, H. pylori are considered a major cause of PUD, especially in children [2,44,45]. Interestingly, in univariate analysis, PUD showed a significant increase with age and predominantly in boys. Prolonged H. pylori infection may lead to the development of PUD. The proportion of boys in the older age group (≥11 years) was higher than in other age groups. However, in multiple analysis, only gender was associated with PUD. The higher prevalence among boys could be attributed to a combination of genetic, hormonal, and immune responses.
Most H. pylori isolates carried the cagA gene (69%) and vacA s1/m1 genotype (44.3%). These strains are known to have a higher risk of developing PUD, as documented in the literature, including in Southeast Asian countries [46,47,48,49] and Vietnamese adults [50,51,52]. Interestingly, we detected mixed infections of H. pylori strains, with one-third of patients having coexistence of both m1 and m2 alleles of vacA (34.4% s1/m1m2), possibly because the genotype of H. pylori was studied directly from the gastric biopsy, rather than from a single colony. Multiple colonization with different H. pylori genotypes have been associated with gastritis features and ulceration [53]. These reasons may have contributed to the high frequency of PUD in symptomatic Vietnamese children requiring prompt diagnostic endoscopy.
Our study has three main limitations. Firstly, the number of patients was lower than expected due to recruitment interruption and disruptions in medical services, caused by the COVID-19 pandemic in Vietnam since February 2020. The adequate follow-up of patients was hampered by confinement. Secondly, such a low frequency of H. pylori-negative patients was not expected (20%). This may affect the study’s statistical power in identifying factors associated with H. pylori infection. Finally, some data remained subjective since the medical history and clinical symptoms were reported by parents of the children involved in the study. However, this study’s strength lies in being the first prospective multicenter design based on the international standard criteria for H. pylori diagnosis and endoscopic observation. We also excluded cases that may lead to an incorrect diagnosis, such as prior antibiotics, PPIs use, or repeated endoscopy, to limit selection bias. Therefore, our results accurately reflect the alarming frequency of H. pylori infection and PUD in symptomatic children in Southern Vietnam.

5. Conclusions

Vietnamese symptomatic children undergoing upper GI endoscopy have an alarming rate of H. pylori infection, up to 80%, from the age of four years. PUD is common in children in Southern Vietnam and is strongly associated with H. pylori infection. Health education programs focusing on the prevention and early detection of H. pylori should be established in Vietnamese children to mitigate the risk of ulcers and future gastric cancer.

Author Contributions

Conceptualization, T.C.N. and P.N.V.N.; methodology, P.N.V.N. and A.R.; validation, T.C.N.; formal analysis, T.C.N. and P.N.V.N.; investigation, T.C.N., K.H.G.N., T.H.C., V.T.T.P., G.K.N.L. and V.T.N.; data curation, T.C.N. and P.N.V.N.; writing—original draft preparation, T.C.N.; writing—review and editing, T.C.N., A.R. and P.B.; visualization, T.C.N.; supervision, P.N.V.N., A.R. and P.B.; project administration, N.L.C.T., N.M.N., D.Q.T., X.M.N. and H.T.N.; funding acquisition, T.C.N. and P.B. All authors have read and agreed to the published version of the manuscript.

Funding

This work is part of a Belgian–Vietnamese research project for development (PRD2017-Bontems) supported by a grant from the Belgian government: Académie de Recherche et d’Enseignement Supérieur (Research Academy and Higher Education) (ARES-CCD, Brussels, Belgium).

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, approved by the Scientific Council of the Pham Ngoc Thach University of Medicine (No 2683/QĐ-TĐHYKPNT) and the local Ethics Committees of two hospitals (No 37/QĐ-BVNĐTP).

Informed Consent Statement

Written informed consent of parents/legal guardians was obtained before data and sample collection. Children older than 12 years also signed informed assent.

Data Availability Statement

The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.

Acknowledgments

We express our gratitude to all the children and their parents who participated in this study. Many thanks to our colleagues from the Department of Gastroenterology in two Children’s Hospitals, the Department of Biostatistics and Informatics at the Pham Ngoc Thach University of Medicine, the Department of Microbiology and Parasitology-University of Medicine and Pharmacy, the Department of Genetics-University of Science—Vietnam National University Ho Chi Minh City, for their invaluable support. Special thanks to Académie de Recherche et d’Enseignement Supérieur (ARES-CCD) for funding this work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hojsak, I. Helicobacter Pylori Gastritis and Peptic Ulcer Disease. In Textbook of Pediatric Gastroenterology and Nutrition: A Comprehensive Guide to Practice; Guandalini, S., Dhawan, A., Branski, D., Eds.; Taylor & Francis: Abingdon, UK, 2015. [Google Scholar]
  2. Blanchard, S.S.; Czinn, S.J. Peptic Ulcer Disease in Children. In Nelson’s Textbook of Pediatrics; Robert, M., Kliegman, B.S., Eds.; Saunders: Philadelphia, PA, USA, 2016. [Google Scholar]
  3. Conteduca, V.; Sansonno, D.; Lauletta, G.; Russi, S.; Ingravallo, G.; Dammacco, F.H. Pylori Infection and Gastric Cancer: State of the Art (Review). Int. J. Oncol. 2013, 42, 5–18. [Google Scholar] [CrossRef] [Green Version]
  4. Homan, M.; Hojsak, I.; Kolaček, S. Helicobacter Pylori in Pediatrics. Helicobacter 2012, 17, 43–48. [Google Scholar] [CrossRef]
  5. Sustmann, A.; Okuda, M.; Koletzko, S. Helicobacter Pylori in Children. Helicobacter 2016, 21, 49–54. [Google Scholar] [CrossRef] [PubMed]
  6. Jones, N.L.; Koletzko, S.; Goodman, K.; Bontems, P.; Cadranel, S.; Casswall, T.; Czinn, S.; Gold, B.D.; Guarner, J.; Elitsur, Y.; 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. [Google Scholar] [CrossRef] [PubMed]
  7. Tringali, A.; Thomson, M.; Dumonceau, J.M.; Tavares, M.; Tabbers, M.M.; Furlano, R.; Spaander, M.; Hassan, C.; Tzvinikos, C.; Ijsselstijn, H.; et al. Pediatric Gastrointestinal Endoscopy: European Society of Gastrointestinal Endoscopy (ESGE) and European Society for Paediatric Gastroenterology Hepatology and Nutrition (ESPGHAN) Guideline Executive Summary. Endoscopy 2017, 49, 83–91. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. 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] [PubMed] [Green Version]
  9. Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Che, T.H.; Nguyen, T.C.; Ngo, D.T.T.; Nguyen, H.T.; Vo, K.T.; Ngo, X.M.; Truong, D.Q.; Bontems, P.; Robert, A.; Nguyen, P.N.V. High Prevalence of Helicobacter Pylori Infection Among School-Aged Children in Ho Chi Minh City, VietNam. Int. J. Public Health 2022, 67, 1605354. [Google Scholar] [CrossRef]
  11. Nguyen, T.C.; Pham, T.N.T.; Nguyen, A.T. Helicobacter Pylori Induced Gastritis and Peptic Ulcer Disease in Children: Clinical Features, Endoscopic Findings and Efficacy of Oac Regimen in Eradication Therapy. Ho Chi Minh City J. Med. 2011, 1, 294–301. [Google Scholar]
  12. Nguyen, P.T.; Hoang, L.P.; Nguyen, V.T.; Pham, T.D.; Nguyen, A.T. Clinical Manifestations and Management of Peptic Ulcer Diseases in Children at Children’s Hospital 1 from June 2013 to January 2014. Ho Chi Minh City J. Med. 2014, 18, 41–47. [Google Scholar]
  13. Tho, L.; Bang, N.V.; Hang, H.M.; Toan, N.V.; Ha, H.T.T. Epidemiological characteristics; clinical manifestations of gastritis and peptic ulcer disease caused by Helicobacter pylori in children at the National Pediatric Hospital. Vietnam. J. Med. Res. 2016, 101, 71–81. [Google Scholar]
  14. Le, L.T.T.; Nguyen, T.A.; Nguyen, N.A.; Nguyen, Y.T.H.; Nguyen, H.T.B.; Nguyen, L.T.; Vi, M.T.; Nguyen, T. Antibiotic Resistance of Helicobacter Pylori in Children with Gastritis and Peptic Ulcers in Mekong Delta, Vietnam. Healthcare 2022, 10, 1121. [Google Scholar] [CrossRef]
  15. General Statistics Office of Vietnam. Statistical Yearbook of Viet Nam 2021; Statistical Publishing House: Hanoi, Vietnam, 2021; ISBN 978-604-75-1873-9. [Google Scholar]
  16. Delvaux, M.; Crespi, M.; Armengol-Miro, J.R.; Hagenmuller, F.; Teuffel, W.; Spencer, K.B.; Stettin, J.; Zwiebel, F.M. Minimal Standard Terminology for Digestive Endoscopy: Results of Prospective Testing and Validation in the GASTER Project. Endoscopy 2000, 32, 345–355. [Google Scholar] [CrossRef]
  17. Lundell, L.R.; Dent, J.; Bennett, J.R.; Blum, A.L.; Armstrong, D.; Galmiche, J.P.; Johnson, F.; Hongo, M.; Richter, J.E.; Spechler, S.J.; et al. Endoscopic Assessment of Oesophagitis: Clinical and Functional Correlates and Further Validation of the Los Angeles Classification. Gut 1999, 45, 172–180. [Google Scholar] [CrossRef] [Green Version]
  18. Forrest, J.A.; Finlayson, N.D.; Shearman, D.J. Endoscopy in Gastrointestinal Bleeding. Lancet 1974, 304, 394–397. [Google Scholar] [CrossRef]
  19. Dixon, M.F.; Genta, R.M.; Yardley, J.H.; Correa, P. Classification and Grading of Gastritis: The Updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am. J. Surg. Pathol. 1996, 20, 1161–1181. [Google Scholar] [CrossRef]
  20. Trung, T.T.; Minh, T.A.; Anh, N.T. Value of CIM, CLO Test and Multiplex PCR for the Diagnosis of Helicobacter Pylori Infection Status in Patients with Gastritis and Gastric Ulcer. Asian Pac. J. Cancer Prev. APJCP 2019, 20, 3497–3503. [Google Scholar] [CrossRef] [PubMed]
  21. Yuan, C.; Adeloye, D.; Luk, T.T.; Huang, L.; He, Y.; Xu, Y.; Ye, X.; Yi, Q.; Song, P.; Rudan, I. 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. [Google Scholar] [CrossRef] [PubMed]
  22. Nguyen, V.; Nguyen, K.; Phung, C.; Kremp, O.; Kalach, N.; Dupont, C.; Raymond, J.; Vidal-Trecan, G. Prevalence of and Factors Associated with Helicobacter Pylori Infection in Children in the North of Vietnam. Am. J. Trop. Med. Hyg. 2006, 74, 536–539. [Google Scholar] [CrossRef] [PubMed]
  23. Tho, L.; Bang, N.V.; Hang, H.M.; Toan, N.V.; Ha, H.T.T. Helicobacter Pylori Infection in Children From 6 Months To 15 Years In Western Highlands. Vietnam. J. Med. Res. 2012, 80, 17–21. [Google Scholar]
  24. Nguyen, T.V.H. Prevalence and Risk Factors of Helicobacter Pylori Infection in Muong Children in Vietnam. Ann. Clin. Lab. Res. 2017, 5, 159. [Google Scholar] [CrossRef] [Green Version]
  25. Dao, L.V.; Dao, H.V.; Nguyen, H.T.; Vu, V.T.; Tran, A.T.N.; Dat, V.Q.; Hoang, L.B.; Nguyen, H.T.V.; Nguyen, T.D. Helicobacter Pylori Infection and Eradication Outcomes among Vietnamese Patients in the Same Households: Findings from a Non-Randomized Study. PLoS ONE 2021, 16, e0260454. [Google Scholar] [CrossRef]
  26. Viet, T.; Nguyen, H.; Nguyen, V.; Thanh, T.; Phan, B.; Hoang, H.; Lan, T.; Le, A.; Phung-Dac, C. Epidemiology of Helicobacter Pylori Infection in Tay Children in Vietnam. Ann. Clin. Lab. Res. 2016, 4, 125. [Google Scholar] [CrossRef]
  27. Nguyen, V.B.; Nguyen, G.K.; Phung, D.C.; Okrainec, K.; Raymond, J.; Dupond, C.; Kremp, O.; Kalach, N.; Vidal-Trecan, G. Intra-Familial Transmission of Helicobacter Pylori Infection in Children of Households with Multiple Generations in Vietnam. Eur. J. Epidemiol. 2006, 21, 459–463. [Google Scholar] [CrossRef]
  28. Borka Balas, R.; Meliț, L.E.; Mărginean, C.O. Worldwide Prevalence and Risk Factors of Helicobacter Pylori Infection in Children. Children 2022, 9, 1359. [Google Scholar] [CrossRef]
  29. Che, T.H.; Nguyen, T.C.; Vu, V.N.T.; Nguyen, H.T.; Hoang, D.T.P.; Ngo, X.M.; Truong, D.Q.; Bontems, P.; Robert, A.; Nguyen, P.N.V. Factors Associated With Helicobacter Pylori Infection Among School-Aged Children From a High Prevalence Area in Vietnam. Int. J. Public Health 2023, 68, 1605908. [Google Scholar] [CrossRef]
  30. Biernat, M.M.; Iwanczak, B.; Binkowska, A.; Grabinska, J.; Gosciniak, G. The Prevalence of Helicobacter Pylori Infection in Symptomatic Children: A 13-Year Observational Study in the Lower Silesian Region. Adv. Clin. Exp. Med. 2016, 25, 303–308. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Tang, M.Y.L.; Chung, P.H.Y.; Chan, H.Y.; Tam, P.K.H.; Wong, K.K. Recent Trends in the Prevalence of Helicobacter Pylori in Symptomatic Children: A 12-Year Retrospective Study in a Tertiary Centre. J. Pediatr. Surg. 2019, 54, 255–257. [Google Scholar] [CrossRef] [PubMed]
  32. Galal, Y.S.; Ghobrial, C.M.; Labib, J.R.; Abou-Zekri, M.E. Helicobacter Pylori among Symptomatic Egyptian Children: Prevalence, Risk Factors, and Effect on Growth. J. Egypt. Public Health Assoc. 2019, 94, 17. [Google Scholar] [CrossRef] [PubMed]
  33. Zabala Torrres, B.; Lucero, Y.; Lagomarcino, A.J.; Orellana-Manzano, A.; George, S.; Torres, J.P.; O’Ryan, M. Review: Prevalence and Dynamics of Helicobacter Pylori Infection during Childhood. Helicobacter 2017, 22, e12399. [Google Scholar] [CrossRef]
  34. Kako, S.; Iwaya, Y.; Nagaya, T.; Hara, D.; Okamura, T.; Iwaya, M.; Kurasawa, S.; Kato, S.; Nakayama, Y.; Akamatsu, T.; et al. Clinicopathological Features of Nodular Gastritis in Three Classes of Age. Helicobacter 2021, 26, e12845. [Google Scholar] [CrossRef] [PubMed]
  35. Yorulmaz, A.; Emiroglu, H.H.; Gumus, M.D.; Emiroglu, M. The Relationship between Helicobacter Pylori Infection and Nodular Antral Gastritis in Pediatric Patients. J. Natl. Med. Assoc. 2022, 114, 440–450. [Google Scholar] [CrossRef] [PubMed]
  36. Urganci, N.; Kalyoncu, D.; Özgüven, B.H.Y. Pylori Infection and Antral Nodular Gastritis in Children. J. Contemp. Med. 2020, 10, 31–34. [Google Scholar] [CrossRef] [Green Version]
  37. Hojo, M.; Nagahara, A.; Kudo, T.; Takeda, T.; Ikuse, T.; Matsumoto, K.; Ueda, K.; Ueyama, H.; Matsumoto, K.; Asaoka, D.; et al. Endoscopic Findings of Helicobacter Pylori Gastritis in Children and Young Adults Based on the Kyoto Classification of Gastritis and Age-Associated Changes. JGH Open Open Access J. Gastroenterol. Hepatol. 2021, 5, 1197–1202. [Google Scholar] [CrossRef]
  38. Lazowska-Przeorek, I.; Kotowska, M.; Banasiuk, M.; Karolewska-Bochenek, K.; Banaszkiewicz, A.; Gawronska, A.; Albrecht, P. Value of Antral Nodularity for the Diagnosis of Helicobacter Pylori Infection in Children. Med. Sci. Monit. 2015, 21, 1827–1830. [Google Scholar] [CrossRef] [Green Version]
  39. Glover, B.; Teare, J.; Ashrafian, H.; Patel, N. The Endoscopic Predictors of Helicobacter Pylori Status: A Meta-Analysis of Diagnostic Performance. Ther. Adv. Gastrointest. Endosc. 2020, 13, 2631774520950840. [Google Scholar] [CrossRef]
  40. Miranda, A.C.; Machado, R.S.; Kawakami, E. Spontaneous Elimination of Helicobacter Pylori Infection in a Cohort of Asymptomatic School Children by Enzyme-Linked Immunosorbent Assay Polyclonal Antigen in Stool. J. Clin. Gastroenterol. 2008, 42, 143–146. [Google Scholar] [CrossRef] [PubMed]
  41. Xia, H.; Talley, N. Natural Acquisition and Spontaneous Elimination of Helicobacter Pylori Infection: Clinical Implications. Am. J. Gastroenterol. 1997, 92, 1780–1787. [Google Scholar] [PubMed]
  42. Zhou, Y.; Ye, Z.; Huang, J.; Huang, Y.; Yan, W.; Zhang, Y. High Prevalence and Low Spontaneous Eradication Rate of Helicobacter Pylori Infection among Schoolchildren Aged 7–12 Years. Acta Paediatr. 2018, 107, 1624–1628. [Google Scholar] [CrossRef]
  43. Hernandez, C.; Serrano, C.; Einisman, H.; Villagran, A.; Pena, A.; Duarte, I.; Torres, J.; Riera, F.; Harris, P.R. Peptic Ulcer Disease in Helicobacter Pylori-Infected Children: Clinical Findings and Mucosal Immune Response. J. Pediatr. Gastroenterol. Nutr. 2014, 59, 773–778. [Google Scholar] [CrossRef] [PubMed]
  44. Güven, B.; Sağ, E.; Usta, D.; İssi, F.; Çakir, M. Peptic Ulcer Disease in Children. Mucosa 2020, 3, 18–22. [Google Scholar] [CrossRef] [Green Version]
  45. Mhaskar, R.S.; Ricardo, I.; Azliyati, A.; Laxminarayan, R.; Amol, B.; Santosh, W.; Boo, K. Assessment of Risk Factors of Helicobacter Pylori Infection and Peptic Ulcer Disease. J. Glob. Infect. Dis. 2013, 5, 60–67. [Google Scholar] [CrossRef]
  46. Bontems, P.; Kalach, N.; Vanderpas, J.; Iwanczak, B.; Casswall, T.; Koletzko, S.; Oderda, G.; Martinez-Gomez, M.J.; Urruzuno, P.; Kindermann, A.; et al. Helicobacter Pylori Infection in European Children with Gastro-Duodenal Ulcers and Erosions. Pediatr. Infect. J. 2013, 32, 1324–1329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Nejati, S.; Karkhah, A.; Darvish, H.; Validi, M.; Ebrahimpour, S.; Nouri, H.R. Influence of Helicobacter Pylori Virulence Factors CagA and VacA on Pathogenesis of Gastrointestinal Disorders. Microb. Pathog. 2018, 117, 43–48. [Google Scholar] [CrossRef] [PubMed]
  48. Falsafi, T.; Khani, A.; Mahjoub, F.; Asgarani, E.; Sotoudeh, N. Analysis of VacA/CagA Genotypes/Status in Helicobacter Pylori Isolates from Iranian Children and Their Association with Clinical Outcome. Turk. J. Med. Sci. 2015, 45, 170–177. [Google Scholar] [CrossRef]
  49. Biernat, M.M.; Gosciniak, G.; Iwanczak, B. Prevalence of Helicobacter Pylori CagA, VacA, IceA, BabA2 Genotypes in Polish Children and Adolescents with Gastroduodenal Disease. Postepy Hig. Med. Dosw. Online 2014, 68, 1015–1021. [Google Scholar] [CrossRef]
  50. Sahara, S.; Sugimoto, M.; Vilaichone, R.K.; Mahachai, V.; Miyajima, H.; Furuta, T.; Yamaoka, Y. Role of Helicobacter Pylori CagA EPIYA Motif and VacA Genotypes for the Development of Gastrointestinal Diseases in Southeast Asian Countries: A Meta-Analysis. BMC Infect. Dis. 2012, 12, 223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. Uchida, T.; Nguyen, L.T.; Takayama, A.; Okimoto, T.; Kodama, M.; Murakami, K.; Matsuhisa, T.; Trinh, T.D.; Ta, L.; Ho, D.Q.; et al. Analysis of Virulence Factors of Helicobacter Pylori Isolated from a Vietnamese Population. BMC Microbiol. 2009, 9, 175. [Google Scholar] [CrossRef] [Green Version]
  52. Nguyen, T.H.; Ho, T.T.M.; Nguyen-Hoang, T.-P.; Qumar, S.; Pham, T.T.D.; Bui, Q.N.; Bulach, D.; Nguyen, T.-V.; Rahman, M. The Endemic Helicobacter Pylori Population in Southern Vietnam Has Both South East Asian and European Origins. Gut Pathog. 2021, 13, 57. [Google Scholar] [CrossRef]
  53. Ren, L.; Liao, Y.L.; Song, Y.; Guo, Y.; Mao, X.H.; Xie, Q.H.; Zhang, W.J.; Guo, G.; Zou, Q.M. High Frequency Variations of Helicobacter Pylori Isolates in Individual Hosts in a Chinese Population. Int. J. Infect. Dis. 2012, 16, e358–e363. [Google Scholar] [CrossRef] [Green Version]
Healthcare 11 01658 g001 550
Figure 1. Flowchart of the study series.
Figure 1. Flowchart of the study series.
Healthcare 11 01658 g001
Healthcare 11 01658 g002 550
Figure 2. Distribution of H. pylori infection according to age group and gender.
Figure 2. Distribution of H. pylori infection according to age group and gender.
Healthcare 11 01658 g002
Table
Table 1. Distribution of H. pylori infection according to characteristics of 336 symptomatic children.
Table 1. Distribution of H. pylori infection according to characteristics of 336 symptomatic children.
CharacteristicsH. pylori-Positive Children (n = 269)H. pylori-Negative Children (n = 67)p
Age group (years)—No (%) 0.96 *
  <6 19 (7.1)5 (7.5)
  6–11190 (70.6)48 (71.6)
  ≥1160 (22.3)14 (20.9)
Gender—No (%) 0.06
  Girls142 (52.8)44 (65.7)
  Boys127 (47.2)23 (34.3)
Living area—No (%) <0.001
  Other provinces146 (54.3)56 (83.6)
  - South-East provinces71 (26.4)23 (34.3)
  - Mekong Delta River50 (18.6)27 (48.2)
  - South Central Provinces13 (8.9)4 (7.1)
  Central Highlands10 (6.9)2 (3.6)
  - HCMC123 (45.7)11 (16.4)0.90
  - Rural76 (61.8)7 (63.6)
  - Urban47 (38.2)4 (36.4)
Family history of gastric cancer—No (%) >0.99
  First-degree00
  Second-degree8 (3.0)2 (3.0)
  No history261 (97.0)65 (97.0)
Family history of PUD (n = 335)—No (%) 0.74
  Yes150 (56.0)39 (58.2)
  No118 (44.0)28 (41.8)
Family history of H. pylori infection—No (%) 0.21
  Yes135 (50.2)27 (41.5)
  No134 (49.8)38 (58.5)
Living with an infected person (n = 325)—No (%) 0.20
  Yes119 (45.4)23 (36.5)
  No143 (54.6)40 (63.5)
  Nutritional status—No (%) 0.10
  Normal weight137 (50.9)33 (49.3)
  Underweight51 (19.0)20 (29.9)
  Overweight/Obesity81 (30.1)14 (20.9)
Signs and symptoms #—No (%)
  Persistent abdominal pain254 (94.4)66 (98.5)0.16
  Epigastric pain200 (74.4)53 (79.1)0.42
  Vomiting99 (36.8)25 (37.3)0.94
  Constipation (n = 335)90 (33.5)27 (40.9)0.26
  Regurgitation87 (32.3)21 (31.3)0.88
  Weight loss85 (31.6)23 (34.3)0.67
  Loss of appetite73 (27.1)18 (26.9)0.96
  Heartburn44 (16.4)9 (13.4)0.56
  Dyspepsia33 (12.3)8 (11.9)0.94
  Anemia32 (11.9)8 (11.9)0.99
  Melena/Hematemesis20 (7.4)6 (9.0)0.68
  Diarrhea20 (7.4)6 (9.0)0.68
* Cochran–Armitage test was used. # Children may have more than one symptom; So total percentage may exceed 100%. HCMC: Ho Chi Minh City. PUD: peptic ulcer disease.
Table
Table 2. Association between endoscopic findings and H. pylori infection.
Table 2. Association between endoscopic findings and H. pylori infection.
Endoscopic FindingsPositive H. pylori
N = 269		Negative H. pylori
N = 67		p **
Esophagus *
  Erosive oesophagitis6 (100)0 (0.0)NA
Stomach and Duodenum
  Erythema16 (6.0)25 (37.3)<0.001
  - GEt14 (5.2)25 (37.3)
  - GEt & DEt2 (0.8)0 (0.0)
  Nodularity171 (63.6)33 (49.3)0.03
  - GN69 (25.7)9 (13.4)
  - GN & DEt2 (0.8)1 (1.5)
  - DN & GEt6 (2.2)2 (3.0)
  - DN & GN94 (34.9)21 (31.3)
  Erosion21 (7.8)5 (7.5)0.93
  - GEs1 (0.4)0 (0.0)
  - GEs & DEt0 (0.0)1 (1.5)
  - GEs & DN1 (0.4)0 (0.0)
  - DEs & DEt1 (0.4)3 (4.5)
  - DEs & GN18 (6.7)1 (1.5)
  Peptic ulcer disease61 (22.7)4 (6.0)0.002
  - GU & DN1 (0.4)0 (0.0)
  - DU3 (1.1)0 (0.0)
  - DU & GEt3 (1.1)0 (0.0)
  - DU & GN50 (18.6)4 (6.0)
  - DU & GEs1 (0.4)0 (0.0)
  - DU & GU3 (1.1)0 (0.0)
* Patients may have simultaneous endoscopic lesions in the esophagus, stomach, and duodenum. ** Chi-square test on four categories. NA denotes not available. GEt: gastric erythema, GN: gastric nodularity, GEs: gastric erosion, GU: gastric ulcer. DEt: duodenal erythema, DN: duodenal nodularity, DEs: duodenal erosion, DU: duodenal ulcer.
Table
Table 3. Logistic regression to assess factors associated with peptic ulcers among 269 H. pylori-positive children.
Table 3. Logistic regression to assess factors associated with peptic ulcers among 269 H. pylori-positive children.
CharacteristicsnPUD
(%)		Univariable Analysis
OR (95% CI)		pMultivariable Analysis
OR (95% CI)		p
Age (years) 0.003 0.23
  <1120918.71 1
  ≥116036.72.52 (1.34–4.74) 1.55 (0.76–3.14)
Gender 0.003 0.04
  Girls14215.51 1
  Boy12730.72.42 (1.34–4.36) 1.94 (1.02–3.66)
Living area 0.14 0.26
  - Other provinces14619.21 1
  - HCMC12326.81.55 (0.87–2.74) 1.43 (0.77–2.68)
  - Rural7625.01 NI
  - Urban4729.81.27 (0.56–2.87)0.56
Family history of PUD * 0.18 0.36
  Yes15019.3 0.67 (0.38–1.20) 0.75 (0.40–1.40)
  No11826.31 1
Nutritional status 0.68NI
  Normal weight13724.81
  Underweight5119.60.74 (0.33–1.63)
  Overweight/Obesity8121.00.80 (0.42–1.56)
Signs and symptoms
  Anemia <0.001 0.13
  - Yes3246.93.66 (1.70–7.87) 1.99 (0.81–4.87)
  - No23719.41 1
  Melena/Hematemesis <0.001 0.07
  - Yes2055.04.86 (1.91–12.4) 2.85 (0.92–8.86)
  - No24920.11 1
cagA status * <0.001 0.008
  - Positive18529.24.48 (1.94–10.3) 3.25 (1.37–7.71)
  - Negative838.41 1
vacA genotypes ** <0.001 0.60
  - s1/m18631.41.83 (0.20–17.2) 0.74 (0.06–9.10)
  - s1/m210611.30.51 (0.05–4.95) 0.28 (0.03–3.14)
  - s2/m240.01 1
  - s1/m1m2 #5240.42.71 (0.28–26.0) 1.62 (0.13–20.2)
  - s1s2/m2 #520.0NA NA
  - s1s2/m1m2 #20.0NA NA
  - s2/m1m2 #10.0NA NA
  - incomplete vacA $80.0NA NA
* One missing data. ** Five missing data. # Multiple vacA genotypes. $ Incomplete vacA indicates only the s or m region was detected (7/8 vacA s1 was detected, 1/8 vacA m2 was detected). HCMC: Ho Chi Minh City. PUD: Peptic ulcer disease. NI: not included. NA denotes not available.
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.

Share and Cite

MDPI and ACS Style

Nguyen, T.C.; Tang, N.L.C.; Le, G.K.N.; Nguyen, V.T.; Nguyen, K.H.G.; Che, T.H.; Phan, V.T.T.; Nguyen, N.M.; Truong, D.Q.; Ngo, X.M.; et al. Helicobacter pylori Infection and Peptic Ulcer Disease in Symptomatic Children in Southern Vietnam: A Prospective Multicenter Study. Healthcare 2023, 11, 1658. https://doi.org/10.3390/healthcare11111658

AMA Style

Nguyen TC, Tang NLC, Le GKN, Nguyen VT, Nguyen KHG, Che TH, Phan VTT, Nguyen NM, Truong DQ, Ngo XM, et al. Helicobacter pylori Infection and Peptic Ulcer Disease in Symptomatic Children in Southern Vietnam: A Prospective Multicenter Study. Healthcare. 2023; 11(11):1658. https://doi.org/10.3390/healthcare11111658

Chicago/Turabian Style

Nguyen, Tu Cam, Ngoc Le Chau Tang, Giao Kim Ngoc Le, Vy Thuy Nguyen, Khuong Hoang Gia Nguyen, Thai Hoang Che, Van Thi Tuong Phan, Ngoc Minh Nguyen, Dinh Quang Truong, Xuan Minh Ngo, and et al. 2023. "Helicobacter pylori Infection and Peptic Ulcer Disease in Symptomatic Children in Southern Vietnam: A Prospective Multicenter Study" Healthcare 11, no. 11: 1658. https://doi.org/10.3390/healthcare11111658

APA Style

Nguyen, T. C., Tang, N. L. C., Le, G. K. N., Nguyen, V. T., Nguyen, K. H. G., Che, T. H., Phan, V. T. T., Nguyen, N. M., Truong, D. Q., Ngo, X. M., Nguyen, H. T., Robert, A., Bontems, P., & Nguyen, P. N. V. (2023). Helicobacter pylori Infection and Peptic Ulcer Disease in Symptomatic Children in Southern Vietnam: A Prospective Multicenter Study. Healthcare, 11(11), 1658. https://doi.org/10.3390/healthcare11111658

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop