Skip to main content
Top
Published in: Antimicrobial Resistance & Infection Control 1/2018

Open Access 01-12-2018 | Research

Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk

Authors: Reza Ranjbar, Farid Yadollahi Farsani, Farhad Safarpoor Dehkordi

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2018

Login to get access

Abstract

Background

Foods with animal origins and particularly milk play a considerable role in transmission of Helicobacter pylori. The current study was performed to assess phenotypic characters of antibiotic resistance and genotyping pattern of vacA, cagA, iceA, oipA and babA2 alleles amongst the H. pylori strains isolated from raw milk.

Methods

Six-hundred and thirty raw milk samples were collected and cultured on Wilkins Chalgren anaerobe media. Antibiotic resistance and genotyping patterns were studied using disk diffusion and PCR, respectively.

Results

Sixty-seven out of 630 (10.63%) raw milk samples were positive for H. pylori. Ovine raw milk (17.27%) samples had the highest prevalence of H. pylori, while camel (5.00%) had the lowest. H. pylori strains harbored the highest prevalence of resistance against ampicillin (82.08%), tetracycline (76.11%), amoxicillin (74.62%), metronidazole (65.67%) and erythromycin (53.73%). Prevalence of resistance against more than 10 types of antibiotics was 17.91%. VacA s1a (83.58%), m1a (80.59%), s2 (77.61%) and m2 (68.65%), cagA (73.13%) and babA2 (44.77%) were the most commonly detected genotypes. We found that S1am1a (56.71%), s2m1a (56.71%), s1 am2 (43.28%) and s2 m2 (43.28%) were the most commonly detected genotyping pattern. Frequency of cagA-, oipA- and babA2- genotypes were 26.86%, 62.68% and 55.22%, respectively. We found that S1a/cagA+/iceA1/oipA−/babA2- (28.35%), m1a/cagA+/iceA1/oipA−/babA2- (28.35%) and s2/cagA+/iceA1/oipA−/babA2- (26.86%) were the most commonly detected combined genotyping pattern.

Conclusions

Simultaneous presence of vacA, cagA, iceA, oipA and babA2 genotypes in antibiotic resistant H. pylori strains indicates important public health issue regarding the consumption of raw milk. However, additional researches are required to find molecular genetic homology and other epidemiological aspects of H. pylori in milk.
Literature
1.
go back to reference Thorning TK, Raben A, Tholstrup T, Soedamah-Muthu SS, Givens I, Astrup A. Milk and dairy products: good or bad for human health? An assessment of the totality of scientific evidence. Food Nutr Res. 2016;60:32527.PubMed Thorning TK, Raben A, Tholstrup T, Soedamah-Muthu SS, Givens I, Astrup A. Milk and dairy products: good or bad for human health? An assessment of the totality of scientific evidence. Food Nutr Res. 2016;60:32527.PubMed
2.
go back to reference Safarpoor Dehkordi F, Valizadeh Y, Birgani T, Dehkordi K. Prevalence study of Brucella melitensis and Brucella abortus in cow's milk using dot enzyme linked immuno sorbent assay and duplex polymerase chain reaction. J Pure Appl Microbiol. 2014;8:1065–9. Safarpoor Dehkordi F, Valizadeh Y, Birgani T, Dehkordi K. Prevalence study of Brucella melitensis and Brucella abortus in cow's milk using dot enzyme linked immuno sorbent assay and duplex polymerase chain reaction. J Pure Appl Microbiol. 2014;8:1065–9.
3.
go back to reference Momtaz H, Safarpoor Dehkordi F, Taktaz T, Rezvani A, Yarali S. Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: serogroups, virulence factors, and antibiotic resistance properties. Sci World J. 2012;2012:1-9. Momtaz H, Safarpoor Dehkordi F, Taktaz T, Rezvani A, Yarali S. Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: serogroups, virulence factors, and antibiotic resistance properties. Sci World J. 2012;2012:1-9.
4.
go back to reference Rahimi E, Sepehri S, Dehkordi FS, Shaygan S, Momtaz H. Prevalence of Yersinia species in traditional and commercial dairy products in Isfahan Province, Iran. Jundishapur J Microbiol. 2014;7. Rahimi E, Sepehri S, Dehkordi FS, Shaygan S, Momtaz H. Prevalence of Yersinia species in traditional and commercial dairy products in Isfahan Province, Iran. Jundishapur J Microbiol. 2014;7.
5.
go back to reference Ranjbar R, Dehkordi FS, Shahreza MHS, Rahimi E. Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Infect Control. 2018;7:53.PubMedPubMedCentral Ranjbar R, Dehkordi FS, Shahreza MHS, Rahimi E. Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Infect Control. 2018;7:53.PubMedPubMedCentral
6.
go back to reference Safarpoor Dehkordi F, Barati S, Momtaz H, Hosseini Ahari SN, Nejat Dehkordi S. Comparison of shedding, and antibiotic resistance properties of listeria monocytogenes isolated from milk, feces, urine, and vaginal secretion of bovine, ovine, caprine, buffalo, and camel species in Iran. Jundishapur J Microbiol. 2013;6:284–94. Safarpoor Dehkordi F, Barati S, Momtaz H, Hosseini Ahari SN, Nejat Dehkordi S. Comparison of shedding, and antibiotic resistance properties of listeria monocytogenes isolated from milk, feces, urine, and vaginal secretion of bovine, ovine, caprine, buffalo, and camel species in Iran. Jundishapur J Microbiol. 2013;6:284–94.
7.
go back to reference Atapoor S, Dehkordi FS, Rahimi E. Detection of helicobacter pylori in various types of vegetables and salads. Jundishapur J Microbiol. 2014;7:e10013.PubMedPubMedCentral Atapoor S, Dehkordi FS, Rahimi E. Detection of helicobacter pylori in various types of vegetables and salads. Jundishapur J Microbiol. 2014;7:e10013.PubMedPubMedCentral
8.
go back to reference Ghorbani F, Gheisari E, Dehkordi FS. Genotyping of vacA alleles of helicobacter pylori strains recovered from some Iranian food items. Trop J Pharm Res. 2016;15:1631–6. Ghorbani F, Gheisari E, Dehkordi FS. Genotyping of vacA alleles of helicobacter pylori strains recovered from some Iranian food items. Trop J Pharm Res. 2016;15:1631–6.
9.
go back to reference Yahaghi E, Khamesipour F, Mashayekhi F, Safarpoor Dehkordi F, Sakhaei MH, Masoudimanesh M, et al. Helicobacter pylori in vegetables and salads: genotyping and antimicrobial resistance properties. Biomed Res Int. 2014;2014:1–11. Yahaghi E, Khamesipour F, Mashayekhi F, Safarpoor Dehkordi F, Sakhaei MH, Masoudimanesh M, et al. Helicobacter pylori in vegetables and salads: genotyping and antimicrobial resistance properties. Biomed Res Int. 2014;2014:1–11.
10.
go back to reference Mousavi S, Dehkordi FS, Rahimi E. Virulence factors and antibiotic resistance of helicobacter pylori isolated from raw milk and unpasteurized dairy products in Iran. J Venom Anim Toxins Incl Trop Dis. 2014;20:51.PubMedPubMedCentral Mousavi S, Dehkordi FS, Rahimi E. Virulence factors and antibiotic resistance of helicobacter pylori isolated from raw milk and unpasteurized dairy products in Iran. J Venom Anim Toxins Incl Trop Dis. 2014;20:51.PubMedPubMedCentral
11.
go back to reference Biernat MM, Gościniak G, Iwańczak B. Prevalence of helicobacter pylori cagA, vacA, iceA, babA2 genotypes in polish children and adolescents with gastroduodenal disease. Adv Hyg Experiment Med. 2014;68:1015–21. Biernat MM, Gościniak G, Iwańczak B. Prevalence of helicobacter pylori cagA, vacA, iceA, babA2 genotypes in polish children and adolescents with gastroduodenal disease. Adv Hyg Experiment Med. 2014;68:1015–21.
12.
go back to reference Alba C, Blanco A, Alarcón T. Antibiotic resistance in helicobacter pylori. Curr Opin Infect Dis. 2017;30:489–97.PubMed Alba C, Blanco A, Alarcón T. Antibiotic resistance in helicobacter pylori. Curr Opin Infect Dis. 2017;30:489–97.PubMed
13.
go back to reference Ranjbar R, Khamesipour F, Jonaidi-Jafari N, Rahimi E. Helicobacter pylori in bottled mineral water: genotyping and antimicrobial resistance properties. BMC Microbiol. 2016;16:40.PubMedPubMedCentral Ranjbar R, Khamesipour F, Jonaidi-Jafari N, Rahimi E. Helicobacter pylori in bottled mineral water: genotyping and antimicrobial resistance properties. BMC Microbiol. 2016;16:40.PubMedPubMedCentral
14.
go back to reference Ranjbar R, Khamesipour F, Jonaidi-Jafari N, Rahimi E. Helicobacter pylori isolated from Iranian drinking water: vacA, cagA, iceA, oipA and babA2 genotype status and antimicrobial resistance properties. FEBS Open Bio. 2016;6:433–41.PubMedPubMedCentral Ranjbar R, Khamesipour F, Jonaidi-Jafari N, Rahimi E. Helicobacter pylori isolated from Iranian drinking water: vacA, cagA, iceA, oipA and babA2 genotype status and antimicrobial resistance properties. FEBS Open Bio. 2016;6:433–41.PubMedPubMedCentral
15.
go back to reference Ho S-A, Hoyle J, Lewis F, Secker A, Cross D, Mapstone N, et al. Direct polymerase chain reaction test for detection of helicobacter pylori in humans and animals. J Clin Microbiol. 1991;29:2543–9.PubMedPubMedCentral Ho S-A, Hoyle J, Lewis F, Secker A, Cross D, Mapstone N, et al. Direct polymerase chain reaction test for detection of helicobacter pylori in humans and animals. J Clin Microbiol. 1991;29:2543–9.PubMedPubMedCentral
16.
go back to reference Andrews J. BSAC disc diffusion method for antimicrobial susceptibility testing. 2.1.4 ed. British Society for Antimicrobial Chemotherapy: Birmingham, UK; 2003. Andrews J. BSAC disc diffusion method for antimicrobial susceptibility testing. 2.1.4 ed. British Society for Antimicrobial Chemotherapy: Birmingham, UK; 2003.
17.
go back to reference NCCLS. Performance Standards for Antimicrobial Susceptibility Testing. Approved Standard M7-A5: Informational Supplement M100- S18. National Committee for Clinical Laboratory Standards: Wayne, PA; 2007. NCCLS. Performance Standards for Antimicrobial Susceptibility Testing. Approved Standard M7-A5: Informational Supplement M100- S18. National Committee for Clinical Laboratory Standards: Wayne, PA; 2007.
18.
go back to reference Glupczynski Y, Megraud F, Lopez-Brea M, Andersen L. European multicentre survey of in vitro antimicrobial resistance in helicobacter pylori. Eur J Clin Microbiol Infect Dis. 2001;20:820–3.PubMed Glupczynski Y, Megraud F, Lopez-Brea M, Andersen L. European multicentre survey of in vitro antimicrobial resistance in helicobacter pylori. Eur J Clin Microbiol Infect Dis. 2001;20:820–3.PubMed
19.
go back to reference Yamazaki S, Yamakawa A, Okuda T, Ohtani M, Suto H, Ito Y, et al. Distinct diversity of vacA, cagA, and cagE genes of helicobacter pylori associated with peptic ulcer in Japan. J Clin Microbiol. 2005;43:3906–16.PubMedPubMedCentral Yamazaki S, Yamakawa A, Okuda T, Ohtani M, Suto H, Ito Y, et al. Distinct diversity of vacA, cagA, and cagE genes of helicobacter pylori associated with peptic ulcer in Japan. J Clin Microbiol. 2005;43:3906–16.PubMedPubMedCentral
20.
go back to reference Wang J, Chi DS, Laffan JJ, Li C, Ferguson DA, Litchfield P, et al. Comparison of cytotoxin genotypes of helicobacter pylori in stomach and saliva. Digest Dis Sci. 2002;47:1850–6.PubMed Wang J, Chi DS, Laffan JJ, Li C, Ferguson DA, Litchfield P, et al. Comparison of cytotoxin genotypes of helicobacter pylori in stomach and saliva. Digest Dis Sci. 2002;47:1850–6.PubMed
21.
go back to reference Peek JR, Thompson SA, Donahue JP, Tham KT, Atherton JC, Blaser MJ, et al. Adherence to gastric epithelial cells induces expression of a helicobacter pylori gene, iceA, that is associated with clinical outcome. Proc Assoc Am Physicians. 1998;110:531–44.PubMed Peek JR, Thompson SA, Donahue JP, Tham KT, Atherton JC, Blaser MJ, et al. Adherence to gastric epithelial cells induces expression of a helicobacter pylori gene, iceA, that is associated with clinical outcome. Proc Assoc Am Physicians. 1998;110:531–44.PubMed
22.
go back to reference Sheu B, Sheu S, Yang H, Huang A, Wu J-J. Host gastric Lewis expression determines the bacterial density of helicobacter pylori in babA2 genopositive infection. Gut. 2003;52:927–32.PubMedPubMedCentral Sheu B, Sheu S, Yang H, Huang A, Wu J-J. Host gastric Lewis expression determines the bacterial density of helicobacter pylori in babA2 genopositive infection. Gut. 2003;52:927–32.PubMedPubMedCentral
23.
go back to reference Dore MP, Sepulveda AR, El-Zimaity H, Yamaoka Y, Osato MS, Mototsugu K, et al. Isolation of helicobacter pylori from sheep—implications for transmission to humans. Am J Gastroenterol. 2001;96:1396.PubMed Dore MP, Sepulveda AR, El-Zimaity H, Yamaoka Y, Osato MS, Mototsugu K, et al. Isolation of helicobacter pylori from sheep—implications for transmission to humans. Am J Gastroenterol. 2001;96:1396.PubMed
24.
go back to reference Bui D, Brown HE, Harris RB, Oren E. Serologic evidence for fecal–oral transmission of helicobacter pylori. Am J Trop Med Hyg. 2016;94:82–8.PubMedPubMedCentral Bui D, Brown HE, Harris RB, Oren E. Serologic evidence for fecal–oral transmission of helicobacter pylori. Am J Trop Med Hyg. 2016;94:82–8.PubMedPubMedCentral
25.
go back to reference Mard SA, Khadem Haghighian H, Sebghatulahi V, Ahmadi B. Dietary factors in relation to helicobacter pylori infection. Gastroenterol Res Pract. 2014;2014:1–5. Mard SA, Khadem Haghighian H, Sebghatulahi V, Ahmadi B. Dietary factors in relation to helicobacter pylori infection. Gastroenterol Res Pract. 2014;2014:1–5.
26.
go back to reference Stevenson TH, Bauer N, Lucia LM, Acuff GR. Attempts to isolate helicobacter from cattle and survival of helicobacter pylori in beef products. J Food Prot. 2000;63:174–8.PubMed Stevenson TH, Bauer N, Lucia LM, Acuff GR. Attempts to isolate helicobacter from cattle and survival of helicobacter pylori in beef products. J Food Prot. 2000;63:174–8.PubMed
27.
go back to reference Poms RE, Tatini SR. Survival of helicobacter pylori in ready-to-eat foods at 4 C. Int J Food Microbiol. 2001;63:281–6.PubMed Poms RE, Tatini SR. Survival of helicobacter pylori in ready-to-eat foods at 4 C. Int J Food Microbiol. 2001;63:281–6.PubMed
28.
go back to reference Meng X, Zhang H, Law J, Tsang R, Tsang T. Detection of helicobacter pylori from food sources by a novel multiplex PCR assay. J Food Safety. 2008;28:609–19. Meng X, Zhang H, Law J, Tsang R, Tsang T. Detection of helicobacter pylori from food sources by a novel multiplex PCR assay. J Food Safety. 2008;28:609–19.
29.
go back to reference Jiang X, Doyle MP. Optimizing enrichment culture conditions for detecting helicobacter pylori in foods. J Food Prot. 2002;65:1949–54.PubMed Jiang X, Doyle MP. Optimizing enrichment culture conditions for detecting helicobacter pylori in foods. J Food Prot. 2002;65:1949–54.PubMed
30.
go back to reference Herrera AG. Helicobacter pylori and food products. Public Health Microbiol. 2004:297–301. Herrera AG. Helicobacter pylori and food products. Public Health Microbiol. 2004:297–301.
31.
go back to reference Quaglia N, Dambrosio A, Normanno G, Parisi A, Firinu A, Lorusso V, et al. Survival of helicobacter pylori in artificially contaminated ultrahigh temperature and pasteurized milk. Food Microbiol. 2007;24:296–300.PubMed Quaglia N, Dambrosio A, Normanno G, Parisi A, Firinu A, Lorusso V, et al. Survival of helicobacter pylori in artificially contaminated ultrahigh temperature and pasteurized milk. Food Microbiol. 2007;24:296–300.PubMed
32.
go back to reference Fujimura S, Kawamura T, Kato S, Tateno H, Watanabe A. Detection of helicobacter pylori in cow's milk. Lett Appl Microbiol. 2002;35:504–7.PubMed Fujimura S, Kawamura T, Kato S, Tateno H, Watanabe A. Detection of helicobacter pylori in cow's milk. Lett Appl Microbiol. 2002;35:504–7.PubMed
33.
go back to reference Vale F, Vítor J. Transmission pathway of helicobacter pylori: does food play a role in rural and urban areas? Int J Food Microbiol. 2010;138:1–12.PubMed Vale F, Vítor J. Transmission pathway of helicobacter pylori: does food play a role in rural and urban areas? Int J Food Microbiol. 2010;138:1–12.PubMed
34.
go back to reference Angelidis AS, Tirodimos I, Bobos M, Kalamaki MS, Papageorgiou DK, Arvanitidou M. Detection of helicobacter pylori in raw bovine milk by fluorescence in situ hybridization (FISH). Int J Food Microbiol. 2011;151:252–6.PubMed Angelidis AS, Tirodimos I, Bobos M, Kalamaki MS, Papageorgiou DK, Arvanitidou M. Detection of helicobacter pylori in raw bovine milk by fluorescence in situ hybridization (FISH). Int J Food Microbiol. 2011;151:252–6.PubMed
35.
go back to reference Quaglia N, Dambrosio A, Normanno G, Parisi A, Patrono R, Ranieri G, et al. High occurrence of helicobacter pylori in raw goat, sheep and cow milk inferred by glmM gene: a risk of food-borne infection? Int J Food Microbiol. 2008;124:43–7.PubMed Quaglia N, Dambrosio A, Normanno G, Parisi A, Patrono R, Ranieri G, et al. High occurrence of helicobacter pylori in raw goat, sheep and cow milk inferred by glmM gene: a risk of food-borne infection? Int J Food Microbiol. 2008;124:43–7.PubMed
36.
go back to reference Talaei R, Souod N, Momtaz H, Dabiri H. Milk of livestock as a possible transmission route of helicobacter pylori infection. Gastroenterol Hepatol Bed Bench. 2015;8:S30.PubMedPubMedCentral Talaei R, Souod N, Momtaz H, Dabiri H. Milk of livestock as a possible transmission route of helicobacter pylori infection. Gastroenterol Hepatol Bed Bench. 2015;8:S30.PubMedPubMedCentral
37.
go back to reference Rahimi E, Kheirabadi EK. Detection of helicobacter pylori in bovine, buffalo, camel, ovine, and caprine milk in Iran. Foodborne Pathog Dis. 2012;9:453–6.PubMed Rahimi E, Kheirabadi EK. Detection of helicobacter pylori in bovine, buffalo, camel, ovine, and caprine milk in Iran. Foodborne Pathog Dis. 2012;9:453–6.PubMed
38.
go back to reference Osman EY, El-Eragi A, Musa AM, El-Magboul SB. Detection of helicobacter pylori glmM gene in bovine milk using nested polymerase chain reaction. Vet World. 2015;8:913.PubMedPubMedCentral Osman EY, El-Eragi A, Musa AM, El-Magboul SB. Detection of helicobacter pylori glmM gene in bovine milk using nested polymerase chain reaction. Vet World. 2015;8:913.PubMedPubMedCentral
39.
go back to reference Bianchini V, Recordati C, Borella L, Gualdi V, Scanziani E, Selvatico E, et al. Helicobacteraceae in bulk tank milk of dairy herds from northern Italy. Biomed Res Int. 2015;2015:1-4. Bianchini V, Recordati C, Borella L, Gualdi V, Scanziani E, Selvatico E, et al. Helicobacteraceae in bulk tank milk of dairy herds from northern Italy. Biomed Res Int. 2015;2015:1-4.
40.
go back to reference Safaei HG, Rahimi E, Zandi A, Rashidipour A. Helicobacter pylori as a zoonotic infection: the detection of H pylori antigens in the milk and faeces of cows. J Res Med Sci. 2011;16:184.PubMedPubMedCentral Safaei HG, Rahimi E, Zandi A, Rashidipour A. Helicobacter pylori as a zoonotic infection: the detection of H pylori antigens in the milk and faeces of cows. J Res Med Sci. 2011;16:184.PubMedPubMedCentral
41.
go back to reference Zamani M, Vahedi A, Maghdouri Z, Shokri-Shirvani J. Role of food in environmental transmission of helicobacter pylori. Caspian J Int Med. 2017;8:146. Zamani M, Vahedi A, Maghdouri Z, Shokri-Shirvani J. Role of food in environmental transmission of helicobacter pylori. Caspian J Int Med. 2017;8:146.
42.
go back to reference Talimkhani A, Mashak Z. Prevalence and genotyping of helicobacter pylori isolated from meat, Milk and vegetable in Iran. Jundishapur J Microbiol. 2017;10. Talimkhani A, Mashak Z. Prevalence and genotyping of helicobacter pylori isolated from meat, Milk and vegetable in Iran. Jundishapur J Microbiol. 2017;10.
43.
go back to reference Khaji L, Banisharif G, Alavi I. Genotyping of the helicobacter pylori isolates of raw milk and traditional dairy products. Microbiol Res. 2017;8:43–6. Khaji L, Banisharif G, Alavi I. Genotyping of the helicobacter pylori isolates of raw milk and traditional dairy products. Microbiol Res. 2017;8:43–6.
44.
go back to reference Esmaeiligoudarzi D, Tameshkel FS, Ajdarkosh H, Arsalani M, Sohani MH, Behnod V. Prevalence of helicobacter pyloriinIranian milk and dairy products using culture and ureC based-PCR techniques. Biomed Pharmacol J. 2015;8:179–83. Esmaeiligoudarzi D, Tameshkel FS, Ajdarkosh H, Arsalani M, Sohani MH, Behnod V. Prevalence of helicobacter pyloriinIranian milk and dairy products using culture and ureC based-PCR techniques. Biomed Pharmacol J. 2015;8:179–83.
45.
go back to reference Saeidi E, Sheikhshahrokh A. VacA genotype status of helicobacter pylori isolated from foods with animal origin. Biomed Res Int. 2016;2016:1-6. Saeidi E, Sheikhshahrokh A. VacA genotype status of helicobacter pylori isolated from foods with animal origin. Biomed Res Int. 2016;2016:1-6.
46.
go back to reference Hemmatinezhad B, Momtaz H, Rahimi E. VacA, cagA, iceA and oipA genotypes status and antimicrobial resistance properties of helicobacter pylori isolated from various types of ready to eat foods. Ann Clin Microbiol Antimicrob. 2016;15:2.PubMedPubMedCentral Hemmatinezhad B, Momtaz H, Rahimi E. VacA, cagA, iceA and oipA genotypes status and antimicrobial resistance properties of helicobacter pylori isolated from various types of ready to eat foods. Ann Clin Microbiol Antimicrob. 2016;15:2.PubMedPubMedCentral
47.
go back to reference Hunt R, Xiao S, Megraud F, Leon-Barua R, Bazzoli F, Van der Merwe S, et al. Helicobacter pylori in developing countries. J Gastrointestin Liver Dis. 2011;20:299–304.PubMed Hunt R, Xiao S, Megraud F, Leon-Barua R, Bazzoli F, Van der Merwe S, et al. Helicobacter pylori in developing countries. J Gastrointestin Liver Dis. 2011;20:299–304.PubMed
48.
go back to reference Torkan S, Shahreza MHS. VacA, CagA, IceA and OipA genotype status of helicobacter pylori isolated from biopsy samples from Iranian dogs. Trop J Pharmaceu Res. 2016;15:377–84. Torkan S, Shahreza MHS. VacA, CagA, IceA and OipA genotype status of helicobacter pylori isolated from biopsy samples from Iranian dogs. Trop J Pharmaceu Res. 2016;15:377–84.
49.
go back to reference Dabiri H, Jafari F, Baghaei K, Shokrzadeh L, Abdi S, Pourhoseingholi MA, et al. Prevalence of helicobacter pylori vacA, cagA, cagE, oipA, iceA, babA2 and babB genotypes in Iranian dyspeptic patients. Microb Pathog. 2017;105:226–30.PubMed Dabiri H, Jafari F, Baghaei K, Shokrzadeh L, Abdi S, Pourhoseingholi MA, et al. Prevalence of helicobacter pylori vacA, cagA, cagE, oipA, iceA, babA2 and babB genotypes in Iranian dyspeptic patients. Microb Pathog. 2017;105:226–30.PubMed
50.
go back to reference Podzorski RP, Podzorski DS, Wuerth A, Tolia V. Analysis of the vacA, cagA, cagE, iceA, and babA2 genes in helicobacter pylori from sixty-one pediatric patients from the Midwestern United States. Diagn Microbiol Infect Dis. 2003;46:83–8.PubMed Podzorski RP, Podzorski DS, Wuerth A, Tolia V. Analysis of the vacA, cagA, cagE, iceA, and babA2 genes in helicobacter pylori from sixty-one pediatric patients from the Midwestern United States. Diagn Microbiol Infect Dis. 2003;46:83–8.PubMed
51.
go back to reference Momtaz H, Dabiri H, Souod N, Gholami M. Study of helicobacter pylori genotype status in cows, sheep, goats and human beings. BMC Gastroenterol. 2014;14:61.PubMedPubMedCentral Momtaz H, Dabiri H, Souod N, Gholami M. Study of helicobacter pylori genotype status in cows, sheep, goats and human beings. BMC Gastroenterol. 2014;14:61.PubMedPubMedCentral
52.
go back to reference Gilani A, Razavilar V, Rokni N, Rahimi E. VacA and cagA genotypes status and antimicrobial resistance properties of helicobacter pylori strains isolated from meat products in Isfahan province. Iran Iran J Vet Res. 2017;18:97.PubMed Gilani A, Razavilar V, Rokni N, Rahimi E. VacA and cagA genotypes status and antimicrobial resistance properties of helicobacter pylori strains isolated from meat products in Isfahan province. Iran Iran J Vet Res. 2017;18:97.PubMed
53.
go back to reference Pakbaz Z, Shirazi MH, Ranjbar R. Frequency of sabA gene in helicobacter pylori strains isolated from patients in Tehran, Iran. Iran Red Crescent Med J. 2013;15:767.PubMedPubMedCentral Pakbaz Z, Shirazi MH, Ranjbar R. Frequency of sabA gene in helicobacter pylori strains isolated from patients in Tehran, Iran. Iran Red Crescent Med J. 2013;15:767.PubMedPubMedCentral
54.
go back to reference Souod N, Kargar M, Doosti A, Ranjbar R, Sarshar M. Genetic analysis of cagA and vacA genes in helicobacter pylori isolates and their relationship with gastroduodenal diseases in the west of Iran. Iran Red Crescent Med J. 2013;15:371.PubMedPubMedCentral Souod N, Kargar M, Doosti A, Ranjbar R, Sarshar M. Genetic analysis of cagA and vacA genes in helicobacter pylori isolates and their relationship with gastroduodenal diseases in the west of Iran. Iran Red Crescent Med J. 2013;15:371.PubMedPubMedCentral
55.
go back to reference Farshad S, Alborzi A, Japoni A, Ranjbar R, Asl KH, Badiee P, et al. Antimicrobial susceptibility of helicobacter pylori strains isolated from patients in shiraz, southern Iran. World J Gastroenterol. 2010;16:5746.PubMedPubMedCentral Farshad S, Alborzi A, Japoni A, Ranjbar R, Asl KH, Badiee P, et al. Antimicrobial susceptibility of helicobacter pylori strains isolated from patients in shiraz, southern Iran. World J Gastroenterol. 2010;16:5746.PubMedPubMedCentral
56.
go back to reference Ghasemi A, Shirazi M, Ranjbar R, Khorramizadeh M, Daryani N, Hosseini M. The prevalence of cagA and cagE genes in helicobacter pylori strains isolated from different patient groups by polymerase chain reaction. Pak J Biol Sci. 2008;11:2579–83.PubMed Ghasemi A, Shirazi M, Ranjbar R, Khorramizadeh M, Daryani N, Hosseini M. The prevalence of cagA and cagE genes in helicobacter pylori strains isolated from different patient groups by polymerase chain reaction. Pak J Biol Sci. 2008;11:2579–83.PubMed
57.
go back to reference Taneike I, Nami A, O'Connor A, Fitzgerald N, Murphy P, Qasim A, et al. Analysis of drug resistance and virulence-factor genotype of Irish helicobacter pylori strains: is there any relationship between resistance to metronidazole and cagA status? Aliment Pharmacol Ther. 2009;30:784–90.PubMed Taneike I, Nami A, O'Connor A, Fitzgerald N, Murphy P, Qasim A, et al. Analysis of drug resistance and virulence-factor genotype of Irish helicobacter pylori strains: is there any relationship between resistance to metronidazole and cagA status? Aliment Pharmacol Ther. 2009;30:784–90.PubMed
58.
go back to reference Boyanova L, Markovska R, Yordanov D, Gergova G, Mitov I. Clarithromycin resistance mutations in helicobacter pylori in association with virulence factors and antibiotic susceptibility of the strains. Microb Drug Resist. 2016;22:227–32.PubMed Boyanova L, Markovska R, Yordanov D, Gergova G, Mitov I. Clarithromycin resistance mutations in helicobacter pylori in association with virulence factors and antibiotic susceptibility of the strains. Microb Drug Resist. 2016;22:227–32.PubMed
59.
go back to reference Karabiber H, Selimoglu MA, Otlu B, Yildirim O, Ozer A. Virulence factors and antibiotic resistance in children with helicobacter pylori gastritis. J Pediatr Gastroenterol Nutr. 2014;58:608–12.PubMed Karabiber H, Selimoglu MA, Otlu B, Yildirim O, Ozer A. Virulence factors and antibiotic resistance in children with helicobacter pylori gastritis. J Pediatr Gastroenterol Nutr. 2014;58:608–12.PubMed
60.
go back to reference van Doorn LJ, Glupczynski Y, Kusters JG, Mégraud F, Midolo P, Maggi-Solcà N, et al. Accurate prediction of macrolide resistance in helicobacter pylori by a PCR line probe assay for detection of mutations in the 23S rRNA gene: multicenter validation study. Antimicrob Agents Chemother. 2001;45:1500–4.PubMedPubMedCentral van Doorn LJ, Glupczynski Y, Kusters JG, Mégraud F, Midolo P, Maggi-Solcà N, et al. Accurate prediction of macrolide resistance in helicobacter pylori by a PCR line probe assay for detection of mutations in the 23S rRNA gene: multicenter validation study. Antimicrob Agents Chemother. 2001;45:1500–4.PubMedPubMedCentral
61.
go back to reference Godoy AP, Ribeiro ML, Benvengo YH, Vitiello L, Miranda Mde C, Mendonça S, et al. Analysis of antimicrobial susceptibility and virulence factors in helicobacter pylori clinical isolates. BMC Gastroenterol. 2003;3:20.PubMedPubMedCentral Godoy AP, Ribeiro ML, Benvengo YH, Vitiello L, Miranda Mde C, Mendonça S, et al. Analysis of antimicrobial susceptibility and virulence factors in helicobacter pylori clinical isolates. BMC Gastroenterol. 2003;3:20.PubMedPubMedCentral
62.
go back to reference European Helicobacter pylori Study Group. Current European concepts in the management of helicobacter pylori infection. The Maastricht consensus report. Gut. 1997;41:8–13. European Helicobacter pylori Study Group. Current European concepts in the management of helicobacter pylori infection. The Maastricht consensus report. Gut. 1997;41:8–13.
63.
go back to reference Mégraud F, Lamouliatte H. The treatment of refractory helicobacter pylori infection. Aliment Pharmacol Ther. 2003;17:1333–43.PubMed Mégraud F, Lamouliatte H. The treatment of refractory helicobacter pylori infection. Aliment Pharmacol Ther. 2003;17:1333–43.PubMed
64.
go back to reference Mégraud F, Hazell S, Glupczynski Y. Antibiotic susceptibility and resistance. In: Mobley HLT, Mendz GL, Hazell SL, editors. Helicobacter pylori: physiology and genetics. Washington, DC: ASM Press; 2001. p. 511–30. Mégraud F, Hazell S, Glupczynski Y. Antibiotic susceptibility and resistance. In: Mobley HLT, Mendz GL, Hazell SL, editors. Helicobacter pylori: physiology and genetics. Washington, DC: ASM Press; 2001. p. 511–30.
Metadata
Title
Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk
Authors
Reza Ranjbar
Farid Yadollahi Farsani
Farhad Safarpoor Dehkordi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2018
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-018-0409-y

Other articles of this Issue 1/2018

Antimicrobial Resistance & Infection Control 1/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.