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Highly clarithromycin-resistant Helicobacter pylori infection in asymptomatic children from a rural community of Cajamarca-Peru

BMC Research Notes volume 11, Article number: 809 (2018) Cite this article

Abstract

Objective

The objective of this study was to determine the prevalence of clarithromycin-resistant Helicobacter pylori in asymptomatic children in a rural community of Cajamarca (northern Peru).

Results

Helicobacter pylori was detected in 17.2% (49/285) of the samples. Unboiled water consumption the most frequent associated factor in patients with positive PCR for H. pylori infection (93.9%). Clarithromycin resistant mutations were found in 79.6% (39/49) of the positive samples for H. pylori. The most frequent mutation was A2142G (46.9%), followed by the double-mutation A2142G–A2143G (28.6%).

Introduction

Helicobacter pylori is one of the most prevalent human pathogens and the major cause of chronic gastritis, peptic ulcer disease, gastric adenocarcinoma and mucosa-associated lymphoid tissue lymphoma in children and adults [1, 2]. More than half of the world’s population is infected, with approximately 4.4 billion individuals in 2015 [3]. Infection is related mainly to socioeconomic status and living conditions so higher prevalence rates (more than 40%) are predominantly seen in low or low-to-middle-income areas [4].

Helicobacter pylori infection is generally acquired during childhood and persists throughout life if untreated. The continuous exposure is associated with the presence of gastritis and other severe complications [2]. Virulence factors, host gastric mucosal factors and patient’s environment are associated with clinical outcomes [5].

No clinical manifestations and especially not recurrent abdominal pain, have been shown to be specific to H. pylori infection in children [2, 6, 7]. Both invasive and non-invasive methods have been described for the H. pylori detection [8]. Invasive tests require an endoscopic sample and include: histologic analysis, rapid urease test and cultures. On the other hand, the urea breath test, serologic tests and the antigen detection in feces are non-invasive methods with limited applications [9]. In that sense, a positive serologic result cannot differentiate between a current and a past infection and the urea breath test requires very sophisticated equipment that usually is not available in the low-income settings [9].

In children, the collection and analysis of stool samples can be of special interest, due to their easy and fast sample collection. However, few methods are used for H. pylori detection in feces, including bacterial cultures, polymerase chain reaction (PCR) and enzymatic immunoassays [10,11,12].

In 1992, a Peruvian study showed extremely high levels of by H. pylori infection in all natural regions of the country, with regions that registered a prevalence higher than 80% [13]. Most recently an analysis of 1711 patients diagnosed with H. pylori by 13C-urea breath test showed a prevalence of 45.6% in Lima, the capital of Peru [14]. Also a local study associated the first H. pylori infection in infancy with more diarrheal episodes and diminished linear growth [15].

In the last few decades, non-invasive tests have been gaining importance for the early detection of H. pylori, especially in the following of treated infants [4, 11, 16]. The H. pylori eradication can drastically reduce both gastric and duodenal ulcers rates in children, as well as prevent further complications.

Most of the current regimens for the eradication of H. pylori include clarithromycin as main antibiotic. However, there are differences in the prevalence of clarithromycin-resistant strains of H. pylori among different countries [10]. It is also very worrying that the incidence of clarithromycin-resistant strains of H. pylori in children is increasing worldwide [10]. H. pylori clarithromycin resistance is related to the structural change of 23S rRNA because it is the target of clarithromycin [10]. This structural change of 23S rRNA is caused by the single nucleotide polymorphism (SNP) of the 23S rRNA gene, at the position of 2142 or 2143 in most cases [10, 17].

The main objective of this study is to determine the frequency of children infected with H. pylori, the presence of clarithromycin resistance strains and determine associated factors for this infection in a rural community of Cajamarca.

Main text

Methods

Study area

San Pablo district is a rural area located at the Peruvian North in the Cajamarca department. San Pablo has a population of 13,591 habitants, most of them having a low socioeconomic status [18].

Patients and ethics

Children between 5 and 12 years old from the single Primary School of San Pablo district who had lived for at least the previous 6 months in the study area were considered in this study. Children who had received antiparasitic treatment or laxatives in the previous 15 days from sample collection were excluded from the study.

The study protocol was approved by the Ethics committee of the Hospital Regional Docente de Cajamarca and performed according to the Helsinki declaration. Informed consent was obtained from the parents or guardians of the children before sample collection. Stool samples were stored by the Regional Laboratory of the DIRESA Cajamarca as part of their parasitic surveillance system. Permits were also requested from DIRESA Cajamarca for the use of this samples.

Sample preparation

One stool sample was obtained from each participant, they were collected in sterile containers and stored at − 20 °C.

DNA extraction

DNA was extracted from above mentioned sample aliquots using a commercial kit (High Pure Template Preparation Kit, Roche Applied Science, Germany) according to the manufacturer instructions.

PCR amplification for detection of H. pylori

Presence of H. pylori was determined by PCR amplification of the 23S rRNA gene and resistance mutation sequences for clarithromycin (A2142G and A2143G) were recognized by specific primers and conditions previously described [19].

Statistical analysis

The numbers of cases are given as frequencies and the graphics prepared with the Origin Pro software. Statistical difference in the frequency between the two different groups was assessed by normalized difference of two proportions test (Z-test) (Minitab® 18 Statistical Software). All p-values were two-tail and p < 0.05 were considered statistically significant.

Results

A cross-sectional study was conducted in the district of San Pablo in Cajamarca-Peru.

A total of 285 children from 6 to 14 years old were included in the study. None presented any suspicious symptom or diagnostic of H. pylori.

Helicobacter pylori was detected in 17.2% (49/285) of samples after PCR amplification and confirmed DNA sequencing. Demographic characteristics in the 285 children are summarized in Table 1. The population studied showed the same distribution by sex and the majority age group was in the range of 6–11 years. However, the frequency of male children infected (65.3%) with H. pylori was significantly higher (p = 0.013) than the cases of infected female children (34.7%). Both distribution of age and drainage systems in homes (e.g. bathroom and latrine) did not show an influence on the frequency of infected children (Table 1).

Table 1 Demographics characteristics in positives samples with diagnosis H. pylori by PCR from Cajamarca (Peru)
Full size table

Clinical symptoms were evaluated as shown in Fig. 1. The abdominal pain (65.3%) was the most frequent symptom, followed by weight loss (40.8%), diarrhea (26.5%), and nausea-vomiting (12.2%) in last 3 months in patients with positive PCR for H. pylori infection. However, the frequencies of these symptoms did not show significant differences with the cases of non-infected children (Fig. 1).

Fig. 1
figure 1

Risk factors and clinical symptoms during the last 3 months in the asymptomatic population of children

Full size image

On the other hand, factors associated with H. pylori infection were evaluated as shown in Fig. 1. Unboiled water (93.9%) and watercress (79.6%) consumptions were the most significant factors associated with H. pylori infection (with p = 0.028 and p = 0.006, respectively) in infected children compared to children who were not infected.

In addition, other habits such as vegetable consumption, hand washing before eating and boiled water consumption could favor non-infection by H. pylori (Fig. 1). In the samples that were positive for the presence of the H. pylori bacterium, the target gene (23S rRNA) sequence for the antibiotic clarithromycin was studied. Point mutations from adenine (A) to guanine (G) in the nucleotide 2142 or 2143 of this gene produce resistance to clarithromycin. A total of 79.6% (39/49) of the positive cases for H. pylori showed some clarithromycin-resistant mutation while 20.4% (10/49) of positive cases did not present mutations in this gene (wild-type in Fig. 2). The occurrence of single mutations (A2142G or A2143G) in children with clarithromycin-resistant H. pylori infection 51% (23/49) was significantly higher compared with the occurrence of double mutations (A2142G-2143G) 28.6% (14/49); (p = 0.02).

Fig. 2
figure 2

Frequency of clarithromycin-resistant mutations in the 23S rRNA gene of H. pylori in the children population

Full size image

Discussion

We observed a prevalence of 17.2% for H. pylori in our pediatric population, which is lower than previous reports in Peru [13, 14]. However, in this study we observed that the presence of the H. pylori bacterium is not clearly related to a clinical diagnosis of the infection (Fig. 1). In addition, in our population the 85% of cases with the presence of H. pylori are found in children with ages in the range of 6–11 years (Table 1), and it could be suggesting that infection may be age-dependent [20]. Although a previous study in Peru demonstrated a risk of early H. pylori infection in infants [21]. Other studies in Latin America, such as those conducted in Brazil, show a decrease in the prevalence of H. pylori infection in a period of 10 years in children under 18 years of age [22].

Recently, emphasis has been placed on the use of non-invasive diagnostic methods for the detection of H. pylori in pediatric population [23, 24]; however, their use is not yet standardized in routine clinical practice. The PCR is among the most promising techniques for being faster, more accurate and specificity [16, 25]. This method can detect H. pylori regardless of their viability with high sensitivity and specificity arriving to 95% [26]. PCR presents greater specificity than the rapid urease test (RUT) [25]. In addition, PCR has the advantage of identifying H. pylori with a limited quantity of bacterial load allowing to recognize the infection when other tests give negative results [27]. Thus, Montealegre et al. reported a prevalence of H. pylori of 78.3% using histological diagnosis and 68.3% by PCR [28]. In another study, ELISA detection of H. pylori antigen in stool samples was compared against other invasive methods, demonstrating the presence of the antigen with a 90% sensitivity and 100% specificity; and a positive predictive value of 100% [29]. In 2012, Smith et al. conducted a study in in dyspeptic patients comparing the detection of H. pylori by urease breath test (UBT) and PCR in stool samples, in this study a prevalence of 20.6% was reported and a specificity of 100% was calculated for the PCR when compared to the UBT as a gold standard [30].

Our study demonstrates the advantages of using the PCR as a method to detect the presence of H. pylori in stool samples. We found a prevalence of 17.2% and only found one study in Peru that used PCR to detect H. pylori in stool samples [31], while most of studies in the country focused on other methods as fast UBT [32].

For H. pylori eradication clarithromycin-based triple therapy has been recommended in children and adults by Maastricht Consensus, however the prevalence of resistant strains was higher in children and the frequent point mutations that are responsible for the clarithromycin resistance included A2143G, A2142G, A2142C and A2144G, and they varied geographically [10]. Rapid, reliable and non-invasive methods for detecting clarithromycin resistant H. pylori are needed [8, 10]. In this study clarithromycin resistant mutations were found in 79.6% (39/49) of the samples, which confirms the high prevalence in children. Most of the samples had one (51%) or two mutations (28.6%). The simple mutation most frequent was A2142G (46.9%), followed by A2143G (4.1%) (Fig. 2). However, the opposite happens in other reports for these mutations [10], which could suggest that these differences are due to different clones or simply that the bacteria are subjected to different environmental stresses that favors one or the other mutation; in any case, this requires further studies.

Since macrolide antibiotics show cross resistance, the higher clarithromycin resistance rates could be attributed to indiscriminate use of erythromycin and azithromycin in our population for respiratory infections [33]. Antibiotic resistance is an important conditioning factor for the success of H. pylori treatment. For this reason it is recommended in populations with a high rate of resistance to perform antibiotic sensitivity tests for clarithromycin before implementing the triple therapy [34].

The high prevalence of H. pylori in asymptomatic persons remains a special concern in our settings, considering the carcinogenic potential of H. pylori and the high prevalence of gastric cancer in Peru, which is estimated to be present in 15.8 per 100.000 inhabitants [35].

Limitations

The range of detection rates reported with molecular methods compared to conventional tests is very wide. This may be due to the fast degradation of the bacteria in the gastrointestinal tract which leads to a very low concentration of the H. pylori in the feces [11, 12]. This is a study in a small rural community in Peru and the results may differ from the reality of urban areas.

Abbreviations

PCR:

polymerase chain reaction

DNA:

deoxibonucleic acid

bp:

base pairs

H. Pylori :

Helicobacter pylori

rRNA:

RNA ribosomal ribonucleic acid

bp:

base pairs

References

  1. Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol. 2006;1:63–96.

    Article  CAS  Google Scholar 

  2. Kotilea K, Kalach N, Homan M, Bontems P. Helicobacter pylori infection in pediatric patients: update on diagnosis and eradication strategies. Paediatr Drugs. 2018;20(4):337–51.

    Article  Google Scholar 

  3. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153(2):420–9.

    Article  Google Scholar 

  4. Zabala Torrres B, Lucero Y, Lagomarcino AJ, Orellana-Manzano A, George S, Torres JP, et al. Review: prevalence and dynamics of Helicobacter pylori infection during childhood. Helicobacter. 2017;22(5):e12399.

    Article  Google Scholar 

  5. Bontems P, Aksoy E, Burette A, Segers V, Deprez C, Mascart F, et al. NF-kappaB activation and severity of gastritis in Helicobacter pylori-infected children and adults. Helicobacter. 2014;19(3):157–67.

    Article  CAS  Google Scholar 

  6. Pacifico L, Osborn JF, Tromba V, Romaggioli S, Bascetta S, Chiesa C. Helicobacter pylori infection and extragastric disorders in children: a critical update. World J Gastroenterol. 2014;20(6):1379–401.

    Article  Google Scholar 

  7. Dror G, Muhsen K. Helicobacter pylori infection and children’s growth: an overview. J Pediatr Gastroenterol Nutr. 2016;62(6):e48–59.

    Article  Google Scholar 

  8. Lopes AI, Vale FF, Oleastro M. Helicobacter pylori infection—recent developments in diagnosis. World J Gastroenterol. 2014;20(28):9299–313.

    PubMed  PubMed Central  Google Scholar 

  9. Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SS, et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol. 2015;21(40):11221–35.

    Article  CAS  Google Scholar 

  10. Xiong LJ, Tong Y, Wang Z, Mao M. Detection of clarithromycin-resistant Helicobacter pylori by stool PCR in children: a comprehensive review of literature. Helicobacter. 2013;18(2):89–101.

    Article  CAS  Google Scholar 

  11. Leal YA, Cedillo-Rivera R, Simon JA, Velazquez JR, Flores LL, Torres J. Utility of stool sample-based tests for the diagnosis of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr. 2011;52(6):718–28.

    Article  CAS  Google Scholar 

  12. Karakus C, Salih BA. Comparison of the lateral flow immunoassays (LFIA) for the diagnosis of Helicobacter pylori infection. J Immunol Methods. 2013;396(1–2):8–14.

    Article  CAS  Google Scholar 

  13. Escala Perez-Reyes AY, Jimenez Carranza AE, Bussalleu Rivera A. How do gastroenterologists in Peru deal with Helicobacter pylori infection? Study based on a survey conducted in 2014. Rev Gastroenterol Peru. 2015;35(4):295–305.

    PubMed  Google Scholar 

  14. Castillo Contreras O, Maguina Quispe J, Benites Goni H, Chacaltana Mendoza A, Guzman Calderon E, Davalos Moscol M, et al. Prevalence of Helicobacter pylori in symptomatic outpatients in Red Rebagliati (EsSalud) from 2010 to 2013, Lima, Peru. Rev Gastroenterol Peru. 2016;36(1):49–55.

    PubMed  Google Scholar 

  15. Jaganath D, Saito M, Gilman RH, Queiroz DM, Rocha GA, Cama V, et al. First detected Helicobacter pylori infection in infancy modifies the association between diarrheal disease and childhood growth in Peru. Helicobacter. 2014;19(4):272–9.

    Article  Google Scholar 

  16. Khadangi F, Yassi M, Kerachian MA. Review: diagnostic accuracy of PCR-based detection tests for Helicobacter Pylori in stool samples. Helicobacter. 2017;22(6):e12444.

    Article  Google Scholar 

  17. Mahmoudi S, Mamishi S, Banar M, Keshavarz Valian S, Bahador A, Najafi M, et al. Antibiotic susceptibility of Helicobacter pylori strains isolated from Iranian children: high frequency of A2143G point mutation associated with clarithromycin resistance. J Glob Antimicrob Resist. 2017;10:131–5.

    Article  Google Scholar 

  18. (INEI) INdEeI. Población 2000–2015. Consulted: 21/Jun/2018.

  19. Furuta T, Soya Y, Sugimoto M, Shirai N, Nakamura A, Kodaira C, et al. Modified allele-specific primer-polymerase chain reaction method for analysis of susceptibility of Helicobacter pylori strains to clarithromycin. J Gastroenterol Hepatol. 2007;22(11):1810–5.

    Article  CAS  Google Scholar 

  20. Muhsen K, Lagos R, Reymann MK, Graham DY, Pasetti MF, Levine MM. Age-dependent association among Helicobacter pylori infection, serum pepsinogen levels and immune response of children to live oral cholera vaccine CVD 103-HgR. PLoS ONE. 2014;9(1):e83999.

    Article  Google Scholar 

  21. Ramirez-Ramos ASSR. Contribución de Latinoamérica al estudio del Helicobacter pylori. Acta Gastroenterol Latinoam. 2009;39:197–218.

    PubMed  Google Scholar 

  22. Kawakami E, Machado RS, Ogata SK, Langner M. Decrease in prevalence of Helicobacter pylori infection during a 10-year period in Brazilian children. Arq Gastroenterol. 2008;45(2):147–51.

    Article  Google Scholar 

  23. Queiroz DM, Saito M, Rocha GA, Rocha AM, Melo FF, Checkley W, et al. Helicobacter pylori infection in infants and toddlers in South America: concordance between [13C]urea breath test and monoclonal H. pylori stool antigen test. J Clin Microbiol. 2013;51(11):3735–40.

    Article  CAS  Google Scholar 

  24. Calik Z, Karamese M, Acar O, Aksak Karamese S, Dicle Y, Albayrak F, et al. Investigation of Helicobacter pylori antigen in stool samples of patients with upper gastrointestinal complaints. Braz J Microbiol. 2016;47(1):167–71.

    Article  CAS  Google Scholar 

  25. Jalalypour F, Farajnia S, Somi MH, Hojabri Z, Yousefzadeh R, Saeedi N. Comparative evaluation of RUT, PCR and ELISA tests for detection of infection with cytotoxigenic H. pylori. Adv Pharm Bull. 2016;6(2):261–6.

    Article  CAS  Google Scholar 

  26. Castro-Munoz LJ, Gonzalez-Diaz CA, Munoz-Escobar A, Tovar-Ayona BJ, Aguilar-Anguiano LM, Vargas-Olmos R, et al. Prevalence of Helicobacter pylori from the oral cavity of Mexican asymptomatic children under 5 years of age through PCR. Arch Oral Biol. 2017;73:55–9.

    Article  CAS  Google Scholar 

  27. Garza-Gonzalez E, Perez-Perez GI, Maldonado-Garza HJ, Bosques-Padilla FJ. A review of Helicobacter pylori diagnosis, treatment, and methods to detect eradication. World J Gastroenterol. 2014;20(6):1438–49. https://0-doi-org.brum.beds.ac.uk/10.3748/wjg.v20.i6.1438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Montealegre O, Camila M, Jaramillo CA, Montealegre G, Parra G, Delgado P, del Pilar M. Detección histológica y molecular de Helicobacter pylori y genotipificación con base en los genes de virulencia babA2 e iceA en pacientes con patología gástrica benigna. Revista chilena de infectología. 2010;27(2):112–8.

    Article  Google Scholar 

  29. Falsafi T, Lavasani P, Basardeh I, Massarrat S, Landarani Z. Evaluation of an Iranian home-made Helicobacter pylori stool antigen ELISA kit. Jundishapur J Microbiol. 2014;7(6):e10629.

    Article  Google Scholar 

  30. Smith SI, Fowora MA, Lesi OA, Agbebaku E, Odeigah P, Abdulkareem FB, et al. Application of stool-PCR for the diagnosis of Helicobacter pylori from stool in Nigeria—a pilot study. Springerplus. 2012;1(1):78.

    Article  Google Scholar 

  31. Roth DE, Velapatino B, Gilman RH, Su WW, Berg DE, Cabrera L, et al. A comparison of a string test-PCR assay and a stool antigen immunoassay (HpSA) for Helicobacter pylori screening in Peru. Trans R Soc Trop Med Hyg. 2001;95(4):398–9.

    Article  CAS  Google Scholar 

  32. Espinoza Ildefonso V, Tabori Peinado H, Meza Borja C, Bussalleu Cavero A, Vasquez Elera L, Aguilar Sanchez V, et al. Validation of the rapid urease test for the detection of Helicobacter pylori in a Peruvian hospital. Rev Gastroenterol Peru. 2017;37(1):53–7.

    PubMed  Google Scholar 

  33. Wani FA, Bashir G, Khan MA, Zargar SA, Rasool Z, Qadri Q. Antibiotic resistance in Helicobacter pylori: a mutational analysis from a tertiary care hospital in Kashmir, India. Indian J Med Microbiol. 2018;36(2):265–72.

    Article  Google Scholar 

  34. O’Morain NR, Dore MP, O’Connor AJP, Gisbert JP, O’Morain CA. Treatment of Helicobacter pylori infection in 2018. Helicobacter. 2018;23(Suppl 1):e12519. https://0-doi-org.brum.beds.ac.uk/10.1111/hel.12519.

    Article  PubMed  Google Scholar 

  35. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.

    Article  CAS  Google Scholar 

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Authors’ contributions

JV, MAAL, FPC, FER, ACR and CPR performed the PCR for pathogens; JdVM and LJdV designed the study protocol. JdVM, LJdV and MAAL responsible for obtaining funding and laboratory work supervision. WSC, ACT, SLB, JBM and VZG was responsible for the clinical assessment, samples collection and database completion. JV, LJdVM, SLB drafted the manuscript. All authors critically revised the manuscript for intellectual content. All authors read and approved the final manuscript.

Acknowledgements

This study has been funded by the 4th Incentives for Research of the Peruvian University of Applied Sciences, Lima-Peru. Grant Number: EXP004-2016.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

Abstraction format used in the study and dataset are available and accessible from the corresponding author upon request in the link: https://figshare.com/articles/Dataset_HP_2018/7051613.

Consent to publish

Not applicable.

Ethics approval and consent to participate

The study protocol was approved by the Ethics committee of the Hospital Regional Docente de Cajamarca and performed according to the Helsinki declaration. Informed consent was obtained from the parents or guardians of the children before sample collection. Stool samples were stored by the Regional Laboratory of the DIRESA-Cajamarca as part of their parasitic surveillance system. Permits were also requested from DIRESA Cajamarca for the use of this samples.

Funding

This work was supported by Grants 4th Incentive for Research of the Universidad Peruana de Ciencias Aplicadas. Grant: UPC-EXP 004-2016. Lima-Peru. The funding body did not have any role in the design of the study and collection, analysis, and interpretation of data and in writing up process of the manuscript.

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Authors and Affiliations

  1. School of Medicine, Research and Innovation Center of the Health Sciences Faculty, Universidad Peruana de Ciencias Aplicadas, Av. San marcos Cdra 2, Chorrillos, Lima, Peru

    Miguel Angel Aguilar-Luis, Fernando Palacios-Cuervo, Fátima Espinal-Reyes, Andrea Calderón-Rivera, Saúl Levy-Blitchtein, Wilmer Silva-Caso, Angela Cornejo-Tapia & Juana del Valle-Mendoza

  2. Laboratorio de Biología Molecular, Instituto de Investigación Nutricional, Lima, Peru

    Miguel Angel Aguilar-Luis, Carlos Palomares-Reyes & Juana del Valle-Mendoza

  3. Dirección Regional de Salud de Cajamarca (DIRESA-Cajamarca), Cajamarca, Peru

    Victor Zavaleta-Gavidia & Jorge Bazán-Mayra

  4. Barcelona Research Center for Multiscale Science and Engineering, Departament d’Enginyeria Química, EEBE, Universidad Politecnica de Catalunya (UPC), Barcelona Tech, Barcelona, Spain

    Luis J. del Valle

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Correspondence to Juana del Valle-Mendoza or Luis J. del Valle.

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Aguilar-Luis, M.A., Palacios-Cuervo, F., Espinal-Reyes, F. et al. Highly clarithromycin-resistant Helicobacter pylori infection in asymptomatic children from a rural community of Cajamarca-Peru. BMC Res Notes 11, 809 (2018). https://0-doi-org.brum.beds.ac.uk/10.1186/s13104-018-3919-z

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