Antimicrobial Effects of Medicinal Plants on Helicobacter pylori
-
Leila Shafiee
,
Sajedeh Yousefinodeh
,
Dorna Asadi
,
Nafiseh Salehi Kakhki
,
Ali Alnaqeeb
,
Yalda Malekzadegan
,
Faezeh Ariamanesh
,
Atefeh Kamali
,
Mehrab Oldin Hajarzadeh
,
Zohreh Sadeghi
,
Afsane Mirshekari
Abstract
This review thoroughly investigates the antimicrobial properties of medicinal plants against Helicobacter pylori (H. pylori) and highlights their potential to address the issue of drug resistance. The review highlights the significance of exploring compounds derived from plants that can efficiently suppress bacterial growth through distinct mechanisms, and it also examines the combined effects of using multiple compounds from plant extracts. The rising antibiotic resistance of H. pylori has sparked increased interest in alternative treatments, including medicinal plants, which may offer effective and safer methods for preventing and managing diseases caused by this bacterium. Currently, there is heightened interest in medicinal plants due to their lower side effects, ease of use, availability, and generally lower cost. In summary, in light of the escalating antibiotic resistance of H. pylori, this study explores the inhibitory effects of medicinal plants on this pathogen. The study underscores the vital importance of herbal medicines in tackling resistant strains of H. pylori and emphasizes the need for additional research to create new treatment strategies.
1. Bashir SK, Khan MB. Overview of Helicobacter pylori infection, prevalence, risk factors, and its prevention. Adv Gut Microbiome Res 2023; 2023(1):9747027.
2. Mozaffarian D, Blanck HM, Garfield KM, Wassung A, Petersen R. A Food is Medicine approach to achieve nutrition security and improve health. Nature Med 2022; 28(11):2238-40.
3. Li XH, Xu JY, Wang X, Liao LJ, Huang L, Huang Y-Q, et al. BanXiaXieXin decoction treating gastritis mice with drug-resistant Helicobacter pylori and its mechanism. World J Gastroenterol 2023; 29(18):2818.
4. Zhao LY, Mei JX, Yu G, et al. Role of the gut microbiota in anticancer therapy: from molecular mechanisms to clinical applications. Signal Trans Tar Ther 2023; 8(1):201.
5. Khoder G, Muhammad JS, Mahmoud I, Soliman SS, Burucoa C. Prevalence of Helicobacter pylori and its associated factors among healthy asymptomatic residents in the United Arab Emirates. Pathogens 2019; 8(2):44.
6. Sathianarayanan S, Ammanath AV, Biswas R, et al. A new approach against Helicobacter pylori using plants and its constituents: A review study. Microb Path 2022; 168:105594.
7. Hooi JK, Lai WY, Ng WK, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterol 2017;153(2):420-9.
8. Kao CY, Sheu BS, Wu JJ. Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis. Biomed J 2016; 39(1):14-23.
9. Li RJ, Xu JY, Wang X, et al. Therapeutic effect of demethylated hydroxylated phillygenin derivative on Helicobacter pylori infection. Front Microbiol 2023; 14:1071603.
10. FitzGerald R, Smith SM. An overview of Helicobacter pylori infection. Helicobacter pylori 2021:1-14.
11. Losurdo G, Cubisino R, Barone M, et al. Probiotic monotherapy and Helicobacter pylori eradication: A systematic review with pooled-data analysis. World J Gastroenterol 2018; 24(1):139.
12. Ji J, Yang H. Using probiotics as supplementation for Helicobacter pylori antibiotic therapy. Int J Mol Sci 2020; 21(3):1136.
13. Thuy TTD, Kuo PY, Lin SM, et al. Anti-Helicobacter pylori activity of potential probiotic Lactiplantibacillus pentosus SLC13. BMC Microbiol 2022; 22(1):277.
14. Wu S, Xu Y, Chen Z, et al. Lactiplantibacillus plantarum ZJ316 reduces Helicobacter pylori adhesion and inflammation by inhibiting the expression of adhesin and urease genes. Mol Nut Food Res 2023; 67(18):2300241.
15. Liu M, Gao H, Miao J, et al. Helicobacter pylori infection in humans and phytotherapy, probiotics, and emerging therapeutic interventions: a review. Front Microbiol 2024; 14:1330029.
16. Sun L, Zhao H, Liu L, et al. Effects of Lactobacillus on the inhibition of Helicobacter pylori growth. Biotech Biotechnol Equipment 2018; 32(6):1533-40.
17. Namkin K, Zardast M, Basirinejad F. Saccharomyces boulardii in Helicobacter pylori eradication in children: a randomized trial from Iran. Iran J Pediatrics 2016; 26(1).
18. Sulakvelidze A. Phage therapy: an attractive option for dealing with antibiotic-resistant bacterial infections. Drug Discovery Today 2005; 12(10):807-9.
19. Viertel TM, Ritter K, Horz H-P. Viruses versus bacteria—novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J Antimicrobial Chemother 2014; 69(9):2326-36.
20. Abedon ST. Use of phage therapy to treat long-standing, persistent, or chronic bacterial infections. Adv Drug Delivery Rev 2019; 145:18-39.
21. Abdel-Haliem ME, Askora A. Isolation and characterization of bacteriophages of Helicobacter pylori isolated from Egypt. Future Virol 2013; 8(8):821-6.
22. Nobrega FL, Costa AR, Santos JF, et al. Genetically manipulated phages with improved pH resistance for oral administration in veterinary medicine. Sci Rep 2016; 6(1):39235.
23. Vinner GK, Rezaie-Yazdi Z, Leppanen M, et al. Microencapsulation of Salmonella-specific bacteriophage Felix O1 using spray-drying in a pH-responsive formulation and direct compression tableting of powders into a solid oral dosage form. Pharmaceuticals 2019; 12(1):43.
24. Muñoz AB, Stepanian J, Trespalacios AA, et al. Bacteriophages of Helicobacter pylori. Front Microbiol 2020; 11:549084.
25. Marshall BJ, Armstrong J, Francis GJ, et al. Antibacterial action of bismuth in relation to Campylobacter pyloridis colonization and gastritis. Digestion 1987; 37(Suppl 2):16-30.
26. Goodwin C, Armstrong J, Marshall B. Campylobacter pyloridis, gastritis, and peptic ulceration. J Clin Pathol 1986; 39(4):353-65.
27. Al-Mutairi R, Tovmasyan A, Batinic-Haberle I, et al. Sublethal photodynamic treatment does not lead to development of resistance. Front Microbiol 2018; 9:1699.
28. Battisti A, Morici P, Signore G, et al. Compositional analysis of endogenous porphyrins from Helicobacter pylori. Biophysical Chem 2017; 229:25-30.
29. Battisti A, Morici P, Ghetti F, et al. Spectroscopic characterization and fluorescence imaging of Helicobacter pylori endogenous porphyrins. Biophysical Chem 2017; 229:19-24.
30. Gueutin C, Frebourg G, Burucoa C, et al. Erythromycin encapsulation in nanoemulsion-based delivery systems for treatment of Helicobacter pylori infection. PSBBRC 2017; 493(1):146-51.
31. Hennart PF, Brasseur DJ, Delogne-Desnoeck JB, et al. Lysozyme, lactoferrin, and secretory immunoglobulin A content in breast milk: influence of duration of lactation, nutrition status, prolactin status, and parity of mother. Am J Clin Nut 1991; 53(1):32-9.
32. Sorensen M, Sorensen S. Compte rendu des Travaux du Laboratoire de Carlsberg. Proteins Whey 1939; 83(432):3-9.
33. Masson P, Heremans J. Lactoferrin in milk from different species. 1971.
34. Luqmani Y, Campbell T, Bennet C, et al. Expression of lactoferrin in human stomach. Int J Cancer 1991; 49(5):684-7.
35. Nakao K, Imoto I, Gabazza E, et al. Gastric juice levels of lactoferrin and Helicobacter pylori infection. Scand J Gastroenterol 1997; 32(6):530-4.
36. Nakao K, Imoto I, Ikemura N, et al. Relation of lactoferrin levels in gastric mucosa with Helicobacter pylori infection and with the degree of gastric inflammation. Am J Gastroenterol (Springer Nature) 1997; 92(6).
37. Aisen P, Leibman A. Lactoferrin and transferrin: a comparative study. Biochimica et Biophysica Acta (BBA)-Protein Structure 1972; 257(2):314-23.
38. Yamazaki N, Yamauchi K, Kawase K, et al. Antibacterial effects of lactoferrin and a pepsin-generated lactoferrin peptide against Helicobacter pylori in vitro. J Infect Chemother 1997; 3(2):85-9.
39. Hosseini H, Abbasi A, Sabahi S, et al. Assessing the potential biological activities of postbiotics derived from Saccharomyces cerevisiae: an in vitro study. Probiotics Antimicrob Proteins 2023; 1-17.
40. Ma L, Tu H, Chen T. Postbiotics in human health: a narrative review. Nutrients 2023; 15(2):291.
41. Canducci F, Armuzzi A, Cremonini F, et al. A lyophilized and inactivated culture of Lactobacillus acidophilus increases Helicobacter pylori eradication rates. Aliment Pharmacol Ther 2000; 14(12):1625-9.
42. Neshani A, Zare H, Akbari Eidgahi MR, et al. Review of antimicrobial peptides with anti-Helicobacter pylori activity. Helicobacter 2019; 24(1):e12555.
43. Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nature Rev Microbiol 2005; 3(3):238-50.
44. Mahlapuu M, Håkansson J, Ringstad L, et al. Antimicrobial peptides: an emerging category of therapeutic agents. Front Cell Infec Microbiol 2016; 6:235805.
45. Mba IE, Nweze EI. Focus: antimicrobial resistance: antimicrobial peptides therapy: an emerging alternative for treating drug-resistant bacteria. Yale J Bio Med 2022; 95(4):445.
46. Nuding S, Gersemann M, Hosaka Y, et al. Gastric antimicrobial peptides fail to eradicate Helicobacter pylori infection due to selective induction and resistance. PLoS One 2013; 8(9):e73867.
47. Pero R, Coretti L, Nigro E, et al. β-Defensins in the Fight against Helicobacter pylori. Molecules 2017; 22(3):424.
48. Pero R, Brancaccio M, Laneri S, et al. A novel view of human Helicobacter pylori infections: Interplay between microbiota and beta-defensins. Biomolecules 2019; 9(6):237.
49. Zhang X, Jiang A, Qi B, et al. Secretion expression of human neutrophil peptide 1 (HNP1) in Pichia pastoris and its functional analysis against antibiotic-resistant Helicobacter pylori. Applied Microbiol Biotechnol 2018; 102:4817-27.
50. Jiang M, Ma L, Huang Y, et al. Antimicrobial activities of peptide Cbf-K16 against drug-resistant Helicobacter pylori infection in vitro and in vivo. Microbial Path 2020; 138:103847.
51. Narayana JL, Huang HN, Wu CJ, et al. Efficacy of the antimicrobial peptide TP4 against Helicobacter pylori infection: in vitro membrane perturbation via micellization and in vivo suppression of host immune responses in a mouse model. Oncotarget 2015; 6(15):12936.
52. Téné N, Roche-Chatain V, Rifflet A, et al. Potent bactericidal effects of bicarinalin against strains of the Enterobacter and Cronobacter genera. Food Control 2014; 42:202-6.
53. Ekor M. The growing use of herbal medicines: issues relating to adverse reactions and challenges in monitoring safety. Front Pharmacol 2014; 10;4:177.
54. Rath G, Suryakanta, Kumar D. Importance of herbal medicine in the treatment of various ailments. Int J Herbal Med 2017; 5(4):98-102.
55. Newman DJ, Cragg GM. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J Nat Products 2020; 83(3):770-803.
56. Petrovska BB. Historical review of medicinal plants’ usage. Pharmacog Rev 2012; 6(11):1.
57. Nabavi SF, Di Lorenzo A, Izadi M, et al. Antibacterial effects of cinnamon: From farm to food, cosmetic and pharmaceutical industries. Nutrients 2015; 7(9):7729-48.
58. Cowan MM. Plant products as antimicrobial agents. Clin Microbiol Rev 1999; 12(4):564-82.
59. Ríos JL, Recio MC. Medicinal plants and antimicrobial activity. J Ethnopharmacol 2005; 100(1-2):80-4.
60. Vasquez A, Olofsson TC, Sammataro D. Streptococcus. In: Encyclopedia of Food and Health. 2015:572-7.
61. Lorenzi V, Muselli A, Bernardini AF, et al. Geraniol restores antibiotic activities against multidrug-resistant isolates from gram-negative species. Antimicrob Agents Chemother 2009; 53(5):2209-11.
62. Nostro A, Blanco AR, Cannatelli MA, et al. Susceptibility of methicillin-resistant staphylococci to oregano essential oil, carvacrol and thymol. FEMS Microbiol Lett 2004; 230(2):191-5.
63. Tong SY, Davis JS, Eichenberger E, et al. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28(3):603-61.
64. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 2019; 17(4):203-218.
65. Yuan G, Wahlqvist ML, He G, et al. Natural products and anti-inflammatory activity. Asia Pac J Clin Nutr 2006; 15(2):143-52.
66. Jafri H, Ansari SA, Alvi IA. Antimicrobial activity of plant extracts against Staphylococcus aureus biofilm. J Herbal Med 2021; 27:100430.
67. Palaniappan K, Holley RA. Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. Int J Food Microbiol 2010; 140(2-3):164-8.
68. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2(2):123-40.
69. Croxen MA, Law RJ, Scholz R, et al. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 2013; 26(4):822-80.
70. Elshafie HS, Camele I. An overview of the biological effects of some mediterranean essential oils on human health. Biomed Res Int 2017; 2017:9268468.
71. Burt SA, Reinders RD. Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett Appl Microbiol 2003; 36(3):162-7.
72. Lopez-Romero JC, González-Ríos H, Borges A, et al. Antibacterial effects and mode of action of selected essential oils components against Escherichia coli and Staphylococcus aureus. Evid Based Complement Alternat Med 2015; 2015:795435.
73. Gellatly SL, Hancock RE. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 2013; 67(3):159-73.
74. Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 2012; 36(4):893-916.
75. Manner S, Fallarero A. Screening of natural products for biofilm inhibition. Curr Biotechnol 2018; 7(3):268-90.
76. Nazzaro F, Fratianni F, De Martino L, et al. Effect of essential oils on pathogenic bacteria. Pharmaceuticals (Basel) 2013; 6(12):1451-74.
77. Koo H, Allan RN, Howlin RP, et al. Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 2017; 15(12):740-755.
78. Kwee TC, Koo H. Ginkgo biloba extract and its biofilm inhibiting effect against Pseudomonas aeruginosa. J Med Plant Res 2017; 11(9):171-8.
79. Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 2016; 14(9):576-88.
80. Cavaliere F, Romanelli A, Di Franco S, et al. Rosemary extract reduces quorum sensing and biofilm formation in Pseudomonas aeruginosa. Nat Prod Res 2019; 35(24):1-8.
81. Borges A, Abreu AC, Ferreira C, et al. Antibacterial activity and mode of action of selected phytochemicals against Listeria innocua. Nat Prod Res 2016; 30(10):1171-6.
82. Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol 2010; 2(5):a000414.
83. Livermore DM. British society for antimicrobial chemotherapy working party on the urgent need: Regenerating antibacterial drug discovery and development. discovery research: the scientific challenge of finding new antibiotics. J Antimicrob Chemother 2011; 66(9):1941-4.
84. Burt S. Essential oils: their antibacterial properties and potential applications in foods--a review. Int J Food Microbiol 2004; 94(3):223-53.
85. Zhang L, Lee CH. Mechanisms of Helicobacter pylori resistance to antibiotics and their inhibition strategies. Biomed Pharmacother 2020; 129:110387.
86. Koo H, Hay ID. Biofilm formation in Helicobacter pylori and the impact of antimicrobial treatments. Clin Microbiol Rev 2017; 30(2):347–70.
87. Mann CM, Markham JL. Anti-bacterial and anti-biofilm activity of plant extracts against Helicobacter pylori. J Appl Microbiol 2017; 123(1):55-64.
88. Lee JH, Park KH. Efficacy of plant-derived compounds in the inhibition of Helicobacter pylori and their potential as therapeutic agents. Molecules 2019; 24(7):1256.
89. Kusters JG, van Vliet AH, Kuipers EJ. Helicobacter pylori in gastritis and ulcer disease. Nat Rev Microbiol 2019; 17(6):349–61.
90. Ghosh S, Mondal S. Antibacterial activity of Zingiber officinale against Helicobacter pylori. J Med Plants Res 2018; 12(22):425–31.
91. Siddiqui AA, Khan MN. Antimicrobial effects of Allium sativum against Helicobacter pylori. J Ethnopharmacol 2020; 248:112320.
92. Khan MS, Saeed S. Potential of garlic (Allium sativum) as an adjunct therapy for Helicobacter pylori eradication. Phytother Res 2020; 34(6):1245-53.
93. Ali M, Awais M. Efficacy of Punica granatum extracts against Helicobacter pylori in vitro. J Agric Food Chem 2021; 69(15):4320-7.
94. Mishra S, Choudhary D. Antibacterial activity of Azadirachta indica (neem) against Helicobacter pylori. Clin Microbiol Infect 2022; 28(3):380-6.
95. Burt SA. Essential oils and their antibacterial activity. Int J Food Microbiol 2021; 360:109211.
96. Pérez-Gutierrez RM, Vargas AA. Urease inhibition in Helicobacter pylori by plant-derived compounds. Molecules 2019; 24(6):1234.
97. Koo H, Hay ID. Effect of plant extracts on Helicobacter pylori biofilm formation. J Appl Microbiol 2021; 130(2):589-98.
98. Singh R, Gupta A. Antibacterial properties of plant extracts against Helicobacter pylori: A review. J Med Plants Stud 2021; 9(3):42-50.
99. Hussain SZ, Khan MN. Plant-based therapies for Helicobacter pylori infections: A review. Phytother Res 2022; 36(5):1746-60.
100. Kusters JG, van Vliet AH, Kuipers EJ. Helicobacter pylori in gastritis and ulcer disease. Nat Rev Microbiol 2019; 17(6):349-61.
101. Mou X, Shi Y. Antibacterial activity of tea tree oil against Helicobacter pylori. J Appl Microbiol 2020; 129(1):198-205.
102. Oghbaei M, Moghadam BM. Antibacterial effects of Origanum vulgare essential oil on Helicobacter pylori. J Med Plants Res 2021; 15(4):59-67.
103. Yuan C, Zhang X. Eugenol as an effective agent against Helicobacter pylori. Phytother Res 2019; 33(6):1635-42.
104. Khalil M, Khan S. Antibacterial effects of lavender oil against Helicobacter pylori. J Essent Oil Res 2022; 34(2):142-50.
105. Hematizad I, Khanjari A. In vitro antibacterial activity of gelatin-nanochitosan films incorporated with Zataria multiflora Boiss essential oil and its influence on microbial, chemical, and sensorial properties of chicken breast meat during refrigerated storage. Food Pack Shelf Life 2021; 28:100751.
106. Sharaf M, Arif M. Preparation, urease inhibition mechanisms, and anti-Helicobacter pylori activities of hesperetin-7-rhamnoglucoside. Curr Res Microb 2021; 100103.
107. Elbestawy KM, El-Sherbiny GM, Moghannem SA. Antibacterial, antibiofilm and anti-inflammatory activities of eugenol clove essential oil against resistant Helicobacter pylori. Molecules 2023; 28(6):2448.
108. Dinat S, Orchard A, Van Vuuren S. Antimicrobial activity of Southern African medicinal plants on Helicobacter pylori and Lactobacillus species. J Ethnopharmacol 2024; 118238.
109. Liu M, Gao H. Helicobacter pylori infection in humans and phytotherapy, probiotics, and emerging therapeutic interventions: a review. Front Microbiol 2023; 14:1330029.
110. Ghosh S, Mondal S. Antibacterial activity of Zingiber officinale against Helicobacter pylori. J Medicinal Plants Res 2019; 13(1):50-7.
111. Siddiqui A A, Khan M N. Antimicrobial effects of Allium sativum against Helicobacter pylori. J Ethnopharmacol 2020; 248:112320.
112. Ali M, Awais M. Efficacy of Punica granatum extracts against Helicobacter pylori and Streptococcus mutans. J Agricultural Food Chem 2021; 69(15):4320-7.
113. Mishra S, Choudhary D. Antibacterial activity of Azadirachta indica (neem) against Helicobacter pylori and Escherichia coli. Clin Microbiol Infect 2022; 28(3):380-6.
114. Corona-Gómez L, Hernández-Andrade L. In vitro antimicrobial effect of essential tea tree oil (Melaleuca alternifolia), thymol, and carvacrol on microorganisms isolated from cases of bovine clinical mastitis. J Adv Vet Anim Res 2022; 9(1):72-79.
115. Nikolić I, Chua EG. Savory, oregano and thyme essential oil mixture counteracts Helicobacter pylori. Molecules 2023; 28(5):2138.
116. Hung TT, Ngan LTM, Le BV. Effects of plant essential oils and their constituents on Helicobacter pylori: A review. Plant Science Today 2023; 10(2):407-16.
117. Karaca TD, Aru B, Çağlar K. Evaluation of Antimicrobial activities of various herbal oils against Helicobacter pylori and their cytotoxic effects on HUVEC cell line. H J Basic Clin Sci 2023; 51(1):103-13.
2. Mozaffarian D, Blanck HM, Garfield KM, Wassung A, Petersen R. A Food is Medicine approach to achieve nutrition security and improve health. Nature Med 2022; 28(11):2238-40.
3. Li XH, Xu JY, Wang X, Liao LJ, Huang L, Huang Y-Q, et al. BanXiaXieXin decoction treating gastritis mice with drug-resistant Helicobacter pylori and its mechanism. World J Gastroenterol 2023; 29(18):2818.
4. Zhao LY, Mei JX, Yu G, et al. Role of the gut microbiota in anticancer therapy: from molecular mechanisms to clinical applications. Signal Trans Tar Ther 2023; 8(1):201.
5. Khoder G, Muhammad JS, Mahmoud I, Soliman SS, Burucoa C. Prevalence of Helicobacter pylori and its associated factors among healthy asymptomatic residents in the United Arab Emirates. Pathogens 2019; 8(2):44.
6. Sathianarayanan S, Ammanath AV, Biswas R, et al. A new approach against Helicobacter pylori using plants and its constituents: A review study. Microb Path 2022; 168:105594.
7. Hooi JK, Lai WY, Ng WK, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterol 2017;153(2):420-9.
8. Kao CY, Sheu BS, Wu JJ. Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis. Biomed J 2016; 39(1):14-23.
9. Li RJ, Xu JY, Wang X, et al. Therapeutic effect of demethylated hydroxylated phillygenin derivative on Helicobacter pylori infection. Front Microbiol 2023; 14:1071603.
10. FitzGerald R, Smith SM. An overview of Helicobacter pylori infection. Helicobacter pylori 2021:1-14.
11. Losurdo G, Cubisino R, Barone M, et al. Probiotic monotherapy and Helicobacter pylori eradication: A systematic review with pooled-data analysis. World J Gastroenterol 2018; 24(1):139.
12. Ji J, Yang H. Using probiotics as supplementation for Helicobacter pylori antibiotic therapy. Int J Mol Sci 2020; 21(3):1136.
13. Thuy TTD, Kuo PY, Lin SM, et al. Anti-Helicobacter pylori activity of potential probiotic Lactiplantibacillus pentosus SLC13. BMC Microbiol 2022; 22(1):277.
14. Wu S, Xu Y, Chen Z, et al. Lactiplantibacillus plantarum ZJ316 reduces Helicobacter pylori adhesion and inflammation by inhibiting the expression of adhesin and urease genes. Mol Nut Food Res 2023; 67(18):2300241.
15. Liu M, Gao H, Miao J, et al. Helicobacter pylori infection in humans and phytotherapy, probiotics, and emerging therapeutic interventions: a review. Front Microbiol 2024; 14:1330029.
16. Sun L, Zhao H, Liu L, et al. Effects of Lactobacillus on the inhibition of Helicobacter pylori growth. Biotech Biotechnol Equipment 2018; 32(6):1533-40.
17. Namkin K, Zardast M, Basirinejad F. Saccharomyces boulardii in Helicobacter pylori eradication in children: a randomized trial from Iran. Iran J Pediatrics 2016; 26(1).
18. Sulakvelidze A. Phage therapy: an attractive option for dealing with antibiotic-resistant bacterial infections. Drug Discovery Today 2005; 12(10):807-9.
19. Viertel TM, Ritter K, Horz H-P. Viruses versus bacteria—novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J Antimicrobial Chemother 2014; 69(9):2326-36.
20. Abedon ST. Use of phage therapy to treat long-standing, persistent, or chronic bacterial infections. Adv Drug Delivery Rev 2019; 145:18-39.
21. Abdel-Haliem ME, Askora A. Isolation and characterization of bacteriophages of Helicobacter pylori isolated from Egypt. Future Virol 2013; 8(8):821-6.
22. Nobrega FL, Costa AR, Santos JF, et al. Genetically manipulated phages with improved pH resistance for oral administration in veterinary medicine. Sci Rep 2016; 6(1):39235.
23. Vinner GK, Rezaie-Yazdi Z, Leppanen M, et al. Microencapsulation of Salmonella-specific bacteriophage Felix O1 using spray-drying in a pH-responsive formulation and direct compression tableting of powders into a solid oral dosage form. Pharmaceuticals 2019; 12(1):43.
24. Muñoz AB, Stepanian J, Trespalacios AA, et al. Bacteriophages of Helicobacter pylori. Front Microbiol 2020; 11:549084.
25. Marshall BJ, Armstrong J, Francis GJ, et al. Antibacterial action of bismuth in relation to Campylobacter pyloridis colonization and gastritis. Digestion 1987; 37(Suppl 2):16-30.
26. Goodwin C, Armstrong J, Marshall B. Campylobacter pyloridis, gastritis, and peptic ulceration. J Clin Pathol 1986; 39(4):353-65.
27. Al-Mutairi R, Tovmasyan A, Batinic-Haberle I, et al. Sublethal photodynamic treatment does not lead to development of resistance. Front Microbiol 2018; 9:1699.
28. Battisti A, Morici P, Signore G, et al. Compositional analysis of endogenous porphyrins from Helicobacter pylori. Biophysical Chem 2017; 229:25-30.
29. Battisti A, Morici P, Ghetti F, et al. Spectroscopic characterization and fluorescence imaging of Helicobacter pylori endogenous porphyrins. Biophysical Chem 2017; 229:19-24.
30. Gueutin C, Frebourg G, Burucoa C, et al. Erythromycin encapsulation in nanoemulsion-based delivery systems for treatment of Helicobacter pylori infection. PSBBRC 2017; 493(1):146-51.
31. Hennart PF, Brasseur DJ, Delogne-Desnoeck JB, et al. Lysozyme, lactoferrin, and secretory immunoglobulin A content in breast milk: influence of duration of lactation, nutrition status, prolactin status, and parity of mother. Am J Clin Nut 1991; 53(1):32-9.
32. Sorensen M, Sorensen S. Compte rendu des Travaux du Laboratoire de Carlsberg. Proteins Whey 1939; 83(432):3-9.
33. Masson P, Heremans J. Lactoferrin in milk from different species. 1971.
34. Luqmani Y, Campbell T, Bennet C, et al. Expression of lactoferrin in human stomach. Int J Cancer 1991; 49(5):684-7.
35. Nakao K, Imoto I, Gabazza E, et al. Gastric juice levels of lactoferrin and Helicobacter pylori infection. Scand J Gastroenterol 1997; 32(6):530-4.
36. Nakao K, Imoto I, Ikemura N, et al. Relation of lactoferrin levels in gastric mucosa with Helicobacter pylori infection and with the degree of gastric inflammation. Am J Gastroenterol (Springer Nature) 1997; 92(6).
37. Aisen P, Leibman A. Lactoferrin and transferrin: a comparative study. Biochimica et Biophysica Acta (BBA)-Protein Structure 1972; 257(2):314-23.
38. Yamazaki N, Yamauchi K, Kawase K, et al. Antibacterial effects of lactoferrin and a pepsin-generated lactoferrin peptide against Helicobacter pylori in vitro. J Infect Chemother 1997; 3(2):85-9.
39. Hosseini H, Abbasi A, Sabahi S, et al. Assessing the potential biological activities of postbiotics derived from Saccharomyces cerevisiae: an in vitro study. Probiotics Antimicrob Proteins 2023; 1-17.
40. Ma L, Tu H, Chen T. Postbiotics in human health: a narrative review. Nutrients 2023; 15(2):291.
41. Canducci F, Armuzzi A, Cremonini F, et al. A lyophilized and inactivated culture of Lactobacillus acidophilus increases Helicobacter pylori eradication rates. Aliment Pharmacol Ther 2000; 14(12):1625-9.
42. Neshani A, Zare H, Akbari Eidgahi MR, et al. Review of antimicrobial peptides with anti-Helicobacter pylori activity. Helicobacter 2019; 24(1):e12555.
43. Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nature Rev Microbiol 2005; 3(3):238-50.
44. Mahlapuu M, Håkansson J, Ringstad L, et al. Antimicrobial peptides: an emerging category of therapeutic agents. Front Cell Infec Microbiol 2016; 6:235805.
45. Mba IE, Nweze EI. Focus: antimicrobial resistance: antimicrobial peptides therapy: an emerging alternative for treating drug-resistant bacteria. Yale J Bio Med 2022; 95(4):445.
46. Nuding S, Gersemann M, Hosaka Y, et al. Gastric antimicrobial peptides fail to eradicate Helicobacter pylori infection due to selective induction and resistance. PLoS One 2013; 8(9):e73867.
47. Pero R, Coretti L, Nigro E, et al. β-Defensins in the Fight against Helicobacter pylori. Molecules 2017; 22(3):424.
48. Pero R, Brancaccio M, Laneri S, et al. A novel view of human Helicobacter pylori infections: Interplay between microbiota and beta-defensins. Biomolecules 2019; 9(6):237.
49. Zhang X, Jiang A, Qi B, et al. Secretion expression of human neutrophil peptide 1 (HNP1) in Pichia pastoris and its functional analysis against antibiotic-resistant Helicobacter pylori. Applied Microbiol Biotechnol 2018; 102:4817-27.
50. Jiang M, Ma L, Huang Y, et al. Antimicrobial activities of peptide Cbf-K16 against drug-resistant Helicobacter pylori infection in vitro and in vivo. Microbial Path 2020; 138:103847.
51. Narayana JL, Huang HN, Wu CJ, et al. Efficacy of the antimicrobial peptide TP4 against Helicobacter pylori infection: in vitro membrane perturbation via micellization and in vivo suppression of host immune responses in a mouse model. Oncotarget 2015; 6(15):12936.
52. Téné N, Roche-Chatain V, Rifflet A, et al. Potent bactericidal effects of bicarinalin against strains of the Enterobacter and Cronobacter genera. Food Control 2014; 42:202-6.
53. Ekor M. The growing use of herbal medicines: issues relating to adverse reactions and challenges in monitoring safety. Front Pharmacol 2014; 10;4:177.
54. Rath G, Suryakanta, Kumar D. Importance of herbal medicine in the treatment of various ailments. Int J Herbal Med 2017; 5(4):98-102.
55. Newman DJ, Cragg GM. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J Nat Products 2020; 83(3):770-803.
56. Petrovska BB. Historical review of medicinal plants’ usage. Pharmacog Rev 2012; 6(11):1.
57. Nabavi SF, Di Lorenzo A, Izadi M, et al. Antibacterial effects of cinnamon: From farm to food, cosmetic and pharmaceutical industries. Nutrients 2015; 7(9):7729-48.
58. Cowan MM. Plant products as antimicrobial agents. Clin Microbiol Rev 1999; 12(4):564-82.
59. Ríos JL, Recio MC. Medicinal plants and antimicrobial activity. J Ethnopharmacol 2005; 100(1-2):80-4.
60. Vasquez A, Olofsson TC, Sammataro D. Streptococcus. In: Encyclopedia of Food and Health. 2015:572-7.
61. Lorenzi V, Muselli A, Bernardini AF, et al. Geraniol restores antibiotic activities against multidrug-resistant isolates from gram-negative species. Antimicrob Agents Chemother 2009; 53(5):2209-11.
62. Nostro A, Blanco AR, Cannatelli MA, et al. Susceptibility of methicillin-resistant staphylococci to oregano essential oil, carvacrol and thymol. FEMS Microbiol Lett 2004; 230(2):191-5.
63. Tong SY, Davis JS, Eichenberger E, et al. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28(3):603-61.
64. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 2019; 17(4):203-218.
65. Yuan G, Wahlqvist ML, He G, et al. Natural products and anti-inflammatory activity. Asia Pac J Clin Nutr 2006; 15(2):143-52.
66. Jafri H, Ansari SA, Alvi IA. Antimicrobial activity of plant extracts against Staphylococcus aureus biofilm. J Herbal Med 2021; 27:100430.
67. Palaniappan K, Holley RA. Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. Int J Food Microbiol 2010; 140(2-3):164-8.
68. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2(2):123-40.
69. Croxen MA, Law RJ, Scholz R, et al. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 2013; 26(4):822-80.
70. Elshafie HS, Camele I. An overview of the biological effects of some mediterranean essential oils on human health. Biomed Res Int 2017; 2017:9268468.
71. Burt SA, Reinders RD. Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett Appl Microbiol 2003; 36(3):162-7.
72. Lopez-Romero JC, González-Ríos H, Borges A, et al. Antibacterial effects and mode of action of selected essential oils components against Escherichia coli and Staphylococcus aureus. Evid Based Complement Alternat Med 2015; 2015:795435.
73. Gellatly SL, Hancock RE. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 2013; 67(3):159-73.
74. Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 2012; 36(4):893-916.
75. Manner S, Fallarero A. Screening of natural products for biofilm inhibition. Curr Biotechnol 2018; 7(3):268-90.
76. Nazzaro F, Fratianni F, De Martino L, et al. Effect of essential oils on pathogenic bacteria. Pharmaceuticals (Basel) 2013; 6(12):1451-74.
77. Koo H, Allan RN, Howlin RP, et al. Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 2017; 15(12):740-755.
78. Kwee TC, Koo H. Ginkgo biloba extract and its biofilm inhibiting effect against Pseudomonas aeruginosa. J Med Plant Res 2017; 11(9):171-8.
79. Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 2016; 14(9):576-88.
80. Cavaliere F, Romanelli A, Di Franco S, et al. Rosemary extract reduces quorum sensing and biofilm formation in Pseudomonas aeruginosa. Nat Prod Res 2019; 35(24):1-8.
81. Borges A, Abreu AC, Ferreira C, et al. Antibacterial activity and mode of action of selected phytochemicals against Listeria innocua. Nat Prod Res 2016; 30(10):1171-6.
82. Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol 2010; 2(5):a000414.
83. Livermore DM. British society for antimicrobial chemotherapy working party on the urgent need: Regenerating antibacterial drug discovery and development. discovery research: the scientific challenge of finding new antibiotics. J Antimicrob Chemother 2011; 66(9):1941-4.
84. Burt S. Essential oils: their antibacterial properties and potential applications in foods--a review. Int J Food Microbiol 2004; 94(3):223-53.
85. Zhang L, Lee CH. Mechanisms of Helicobacter pylori resistance to antibiotics and their inhibition strategies. Biomed Pharmacother 2020; 129:110387.
86. Koo H, Hay ID. Biofilm formation in Helicobacter pylori and the impact of antimicrobial treatments. Clin Microbiol Rev 2017; 30(2):347–70.
87. Mann CM, Markham JL. Anti-bacterial and anti-biofilm activity of plant extracts against Helicobacter pylori. J Appl Microbiol 2017; 123(1):55-64.
88. Lee JH, Park KH. Efficacy of plant-derived compounds in the inhibition of Helicobacter pylori and their potential as therapeutic agents. Molecules 2019; 24(7):1256.
89. Kusters JG, van Vliet AH, Kuipers EJ. Helicobacter pylori in gastritis and ulcer disease. Nat Rev Microbiol 2019; 17(6):349–61.
90. Ghosh S, Mondal S. Antibacterial activity of Zingiber officinale against Helicobacter pylori. J Med Plants Res 2018; 12(22):425–31.
91. Siddiqui AA, Khan MN. Antimicrobial effects of Allium sativum against Helicobacter pylori. J Ethnopharmacol 2020; 248:112320.
92. Khan MS, Saeed S. Potential of garlic (Allium sativum) as an adjunct therapy for Helicobacter pylori eradication. Phytother Res 2020; 34(6):1245-53.
93. Ali M, Awais M. Efficacy of Punica granatum extracts against Helicobacter pylori in vitro. J Agric Food Chem 2021; 69(15):4320-7.
94. Mishra S, Choudhary D. Antibacterial activity of Azadirachta indica (neem) against Helicobacter pylori. Clin Microbiol Infect 2022; 28(3):380-6.
95. Burt SA. Essential oils and their antibacterial activity. Int J Food Microbiol 2021; 360:109211.
96. Pérez-Gutierrez RM, Vargas AA. Urease inhibition in Helicobacter pylori by plant-derived compounds. Molecules 2019; 24(6):1234.
97. Koo H, Hay ID. Effect of plant extracts on Helicobacter pylori biofilm formation. J Appl Microbiol 2021; 130(2):589-98.
98. Singh R, Gupta A. Antibacterial properties of plant extracts against Helicobacter pylori: A review. J Med Plants Stud 2021; 9(3):42-50.
99. Hussain SZ, Khan MN. Plant-based therapies for Helicobacter pylori infections: A review. Phytother Res 2022; 36(5):1746-60.
100. Kusters JG, van Vliet AH, Kuipers EJ. Helicobacter pylori in gastritis and ulcer disease. Nat Rev Microbiol 2019; 17(6):349-61.
101. Mou X, Shi Y. Antibacterial activity of tea tree oil against Helicobacter pylori. J Appl Microbiol 2020; 129(1):198-205.
102. Oghbaei M, Moghadam BM. Antibacterial effects of Origanum vulgare essential oil on Helicobacter pylori. J Med Plants Res 2021; 15(4):59-67.
103. Yuan C, Zhang X. Eugenol as an effective agent against Helicobacter pylori. Phytother Res 2019; 33(6):1635-42.
104. Khalil M, Khan S. Antibacterial effects of lavender oil against Helicobacter pylori. J Essent Oil Res 2022; 34(2):142-50.
105. Hematizad I, Khanjari A. In vitro antibacterial activity of gelatin-nanochitosan films incorporated with Zataria multiflora Boiss essential oil and its influence on microbial, chemical, and sensorial properties of chicken breast meat during refrigerated storage. Food Pack Shelf Life 2021; 28:100751.
106. Sharaf M, Arif M. Preparation, urease inhibition mechanisms, and anti-Helicobacter pylori activities of hesperetin-7-rhamnoglucoside. Curr Res Microb 2021; 100103.
107. Elbestawy KM, El-Sherbiny GM, Moghannem SA. Antibacterial, antibiofilm and anti-inflammatory activities of eugenol clove essential oil against resistant Helicobacter pylori. Molecules 2023; 28(6):2448.
108. Dinat S, Orchard A, Van Vuuren S. Antimicrobial activity of Southern African medicinal plants on Helicobacter pylori and Lactobacillus species. J Ethnopharmacol 2024; 118238.
109. Liu M, Gao H. Helicobacter pylori infection in humans and phytotherapy, probiotics, and emerging therapeutic interventions: a review. Front Microbiol 2023; 14:1330029.
110. Ghosh S, Mondal S. Antibacterial activity of Zingiber officinale against Helicobacter pylori. J Medicinal Plants Res 2019; 13(1):50-7.
111. Siddiqui A A, Khan M N. Antimicrobial effects of Allium sativum against Helicobacter pylori. J Ethnopharmacol 2020; 248:112320.
112. Ali M, Awais M. Efficacy of Punica granatum extracts against Helicobacter pylori and Streptococcus mutans. J Agricultural Food Chem 2021; 69(15):4320-7.
113. Mishra S, Choudhary D. Antibacterial activity of Azadirachta indica (neem) against Helicobacter pylori and Escherichia coli. Clin Microbiol Infect 2022; 28(3):380-6.
114. Corona-Gómez L, Hernández-Andrade L. In vitro antimicrobial effect of essential tea tree oil (Melaleuca alternifolia), thymol, and carvacrol on microorganisms isolated from cases of bovine clinical mastitis. J Adv Vet Anim Res 2022; 9(1):72-79.
115. Nikolić I, Chua EG. Savory, oregano and thyme essential oil mixture counteracts Helicobacter pylori. Molecules 2023; 28(5):2138.
116. Hung TT, Ngan LTM, Le BV. Effects of plant essential oils and their constituents on Helicobacter pylori: A review. Plant Science Today 2023; 10(2):407-16.
117. Karaca TD, Aru B, Çağlar K. Evaluation of Antimicrobial activities of various herbal oils against Helicobacter pylori and their cytotoxic effects on HUVEC cell line. H J Basic Clin Sci 2023; 51(1):103-13.
| Files | ||
| Issue | Vol 13 No 1 (2025) | |
| Section | Review Articles | |
| DOI | https://doi.org/10.18502/jmb.v13i1.18051 | |
| Keywords | ||
| Alternative treatments Antimicrobial effects Drug resistance Helicobacter pylori Medicinal plants. | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Shafiee L, Yousefinodeh S, Asadi D, Salehi Kakhki N, Alnaqeeb A, Malekzadegan Y, Ariamanesh F, Kamali A, Hajarzadeh MO, Sadeghi Z, Mirshekari A. Antimicrobial Effects of Medicinal Plants on Helicobacter pylori. J Med Bacteriol. 2025;13(1):69-83.
