Sains
Malaysiana 49(2)(2020): 411-420
http://dx.doi.org/10.17576/jsm-2020-4902-20
In vitro Study
of Anti-Helicobacter pylori Activity
of Honey: A Systematic Review
(Kajian In vitro ke atas Aktiviti
Anti-Helicobacter pylori oleh Madu: Ulasan Sistematik)
ADAM QURAISIAH1, ANNUAR FAZALDA1,
HANAFIAH ALFIZAH2 & MOHD FAHAMI NUR AZLINA1*
1Department of Pharmacology, Faculty of Medicine, Universiti
Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300, Kuala Lumpur, Federal
Territory, Malaysia
2Department of Medical Microbiology & Immunology, Faculty
of Medicine, Jalan Raja Muda Abdul Aziz, 50300, Kuala Lumpur, Federal Territory,
Malaysia
Received: 6 May 2019/Accepted: 4 November 2019
ABSTRACT
This review explores the
beneficial effects of honey on Helicobacter pylori-induced gastric ulcer and duodenal ulcer. The research of the effectiveness
of honey on H.
pylori infection
using electronic databases was done, these include Medline via Ovid Medline, Scopus and ScienceDirect published from the year 2000 to
2018. The articles were evaluated and selected based on the criteria
which report on the effects of honey on gastric ulcer and duodenum
ulcer caused by H. pylori infection. There are 53
articles were identified, which stated to the studies that relate
to the criteria. Afterwards, nine articles on honey and its extracts
were selected and assessed accordingly in this review. All studies
reported positive effects of honey on H. pylori-induced gastric ulser
and duodenal ulcer. Most of the studies showed at minimum 10% of
honey concentration were effective as anti-H.
pylori activity. This systematic
review emphasized the potential of honey used to inhibit the H.
pylori infection in-vitro. Future extensive studies are required to find the active component and
molecular mechanism of honey before animal and human observational
studies could be conducted to deliver valid evidence.
Keywords: Duodenal
ulcer; gastric cancer; gastric ulcer; gastritis; Helicobacter pylori; honey
ABSTRAK
Ulasan
ini adalah untuk mengkaji kesan manfaat madu pada Helicobacter
pylori teraruh ulser gaster
dan ulser duodenal. Satu kajian terhadap
keberkesanan madu pada jangkitan H. pylori menggunakan pangkalan data elektronik telah
dilakukan, ini termasuklah Medline melalui Ovid Medline, Scopus
dan ScienceDirect yang telah diterbitkan dari tahun 2000-2018. Artikel
telah dinilai dan dipilih berdasarkan kriteria yang melaporkan mekanisme dan kesan madu pada
ulser gaster dan ulser duodenal yang disebabkan oleh jangkitan H.
pylori. Terdapat 53
artikel telah dikenal pasti yang merujuk kepada kajian yang sepadan dengan
kriteria. Seterusnya, sembilan artikel mengenai madu dan ekstrak
madu telah dipilih dan dinilai sewajarnya dalam kajian ini. Semua
kajian melaporkan kesan positif pada madu terhadap H.
pylori yang berpunca daripada
ulser gastrik dan ulser duodenal. Kebanyakan kajian menunjukkan
sekurang-kurangnya kepekatan madu sebanyak 10% berkesan sebagai
aktiviti anti-H. pylori. Kajian sistematik ini menekankan potensi
madu yang digunakan untuk merencatkan jangkitan H. pylori secara in-vitro. Kajian menyeluruh pada masa akan datang adalah perlu untuk mencari komponen
aktif dan mekanisme molekul yang ada pada madu sebelum kajian pengamatan
terhadap haiwan dan manusia dijalankan untuk memberi bukti yang
sah.
Kata kunci: Gastritis; Helicobacter pylori; kanser gaster; madu; ulser duodenal; ulser
gaster
REFERENCES
Abdel-Latif,
M.M.M. & Abouzied, M.M. 2016. Molecular mechanisms of natural
honey against H. pylori
infection via suppression of NF-κB and AP-1
activation in gastric epithelial cells. Archives of Medical Research
47(5): 340-348.
Abhishek Chauhan, Vimlendu Pandey, K.M. Chacko. & R.K. Khandal. 2010.
Antibacterial activity of raw and processed honey. Electronic Journal of
Biology 5(3): 58-66.
Alfizah, H.,
Rizal, A.M., Isa, M.R., Aminuddin, A., Jasmi, A.Y. & Ramelah, M. 2010. Four year analysis of Helicobacter pylori infection among patients with dyspepsia at
Universiti Kebangsaan Malaysia Medical Centre. Med. & Health 5(1): 13-21.
Alfizah, H., Norazah, A., Hamizah, R. & Ramelah, M. 2014. Resistotype
of Helicobacter pylori isolates: The
impact on eradication outcome. Journal of Medical Microbiology 63(5):
703-709.
Ali, A.T., Chowdhury, M.N. & al Humayyd, M.S. 1991. Inhibitory effect
of natural honey on Helicobacter pylori. Tropical gastroenterology: Official Journal of the Digestive Diseases
Foundation 12(3): 139-143.
Allsop, K.A. & Miller, J. 1996. Honey revisited: A reappraisal of
honey in pre-industrial diets. British
Journal of Nutrition 75: 513-520.
Alnaqdy, A., Al-Jabri, A., Al Mahrooqi, Z., Nzeako, B.
& Nsanze, H. 2005. Inhibition effect of honey on the adherence of Salmonella to intestinal epithelial
cells in vitro. International Journal of Food Microbiology 103: 347-351.
Altman, E., Fernández, H., Chandan, V., Harrison, B.A., Schuster, M.W.,
Rademacher, L.O. & Toledo, C. 2008. Analysis of Helicobacter pylori isolates from Chile: Occurrence of selective
type 1 Lewis b antigen expression in lipopolysaccharide. Journal of Medical
Microbiology 57(5): 585-591.
Al Somal, N., Coley, K.E., Molan, P.C. & Hancock, B.M. 1994.
Susceptibility of Helicobacter pylori to the antibacterial activity of manuka honey. Journal of the Royal Society
of Medicine 87(1): 9-12.
Basson, N.J. & Grobler, S.R. 2008. Antimicrobial activity of two South
African honeys produced from indigenous Leucospermum
cordifolium and Erica species on
selected micro-organisms. BMC Complementary and Alternative Medicine 8:
41. doi:10.1186/1472-6882-8-41.
Boyanova, L., Ilieva, J., Gergova, G., Vladimirov, B., Nikolov, R. &
Mitov, I. 2015. Honey and green/black tea consumption may reduce the risk of Helicobacter pylori infection. Diagnostic
Microbiology and Infectious Disease 82(1): 85-86.
Cui, Y.M., Dong, X.W., Chen, W., Wang, W.J., Li, Y.G. & Zhu, H.L.
2012. Synthesis, inhibitory activity and molecular docking studies of two
Cu(II) complexes against Helicobacter
pylori urease. J. Enzyme Inhib. Med. Chem. 27(4): 528-532.
Dastouri, M.R., Fakhimzadeh, K., Shayeg, J., Dolgari-Sharaf, J., Valilou,
M.R. & Maheri-Sis, N. 2008. Evaluating antibacterial activity of the
Iranian honey through MIC method on some dermal and intestinal pathogenic
bacteria. Journal of Animal and Veterinary Advances 7(4): 409-412.
De Monte, C., Bizzarri, B., Gidaro, M.C., Carradori, S., Mollica, A.,
Luisi, G., Granese, A., Alcaro, S., Costa, G., Basilico, N., Parapini, S.,
Scaltrito, M.M. & Sisto, F. 2015. Bioactive compounds of Crocus sativus L. and their
semi-synthetic derivatives as promising anti-Helicobacter pylori, anti-malarial and anti-leishmanial agents. Journal
of Enzyme Inhibition and Medicinal Chemistry 30(6): 1027-1033.
Erejuwa, O.O., Sulaiman, S.A., Suhaimi, M. & Wahab, A. 2010.
Antioxidant protective effect of glibenclamide and metformin in combination
with honey in pancreas of streptozotocin- induced diabetic rats. Int. J. Mol. Sci. 11(5): 2056-2066.
Erejuwa, O.O., Sulaiman, S.A., Suhaimi, M. & Wahab, A. 2011.
Glibenclamide or metformin combined with honey improves glycemic control in
streptozotocin-induced diabetic rats. Int.
J. Biol. Sci. 7(2): 244-252.
Estevinho, L., Pereira, A.P., Moreira, L., Dias, L.G.
& Pereira, E. 2008. Antioxidant and antimicrobial effects of phenolic compounds
extracts of Northeast Portugal honey. Food and Chemical Toxicology 46(12): 3774-3779.
Eusebi, L.H. & Zagari, R.M.B.F. 2014. Epidemiology of Helicobacter pylori infection. Helicobacter 19(1): 1-5. doi:10.1017/CBO9781107415324.004.
Ghazali, F.C. 2009. Morphological characterization study of Malaysian
honey - A VPSEM, EDX randomised attempt. Annal. Microsco. 9: 93-102.
Gisbert, J.P. & Calvet, X. 2012. Alimentary pharmacology and
therapeutics review article: Rifabutin in the treatment of refractory Helicobacter pylori infection. Aliment. Pharmacol. Ther. 35: 209-221.
Hussein, S.Z., Mohd Yusoff, K., Makpol, S. & Mohd Yusof, Y.A. 2013.
Gelam honey attenuates carrageenan-induced rat paw inflammation via NF-κB Pathway. PLoS ONE 8(8): e72365. doi:10.1371/journal.pone.0072365.
Hussein, S.Z., Mohd Yusoff, K., Makpol, S. & Mohd Yusof, Y.A. 2012.
Gelam honey inhibits the production of proinflammatory, mediators NO, PGE 2,
TNF-α, and IL-6 in carrageenan-induced acute paw edema in rats. Evidence-based
Complementary and Alternative Medicine 2012: 109636.
doi:10.1155/2012/109636.
Jerković, I., Marijanović, Z., Kezić, J. & Gugić,
M. 2009. Headspace, volatile and semi-volatile organic compounds diversity and
radical scavenging activity of ultrasonic solvent extracts from Amorpha fruticosa honey samples. Molecules 14(8): 2717-2728.
Johnson, R.J., Segal, M.S., Sautin, Y., Nakagawa, T., Feig, D.I., Kang,
D., Gersch, M.S., Benner, S. & Sánchez-Lozada, L.G. 2007.
Potential role of sugar (fructose) in the epidemic of hypertension, obesity and
the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am. J. Clin. Nutr. 86(4): 899-906.
Kanizaj, T.F. & Kunac, N. 2014. Helicobacter
pylori: Future perspectives in therapy reflecting three decades of
experience. World Journal of Gastroenterology 20(3): 699-705.
Kim, S.G., Han, S.M., Jang, H.R., Hong, I.P. & Woo, S.O. 2015.
Composition and anti- Helicobacter pylori activity of the different floral honeys from Korea. Journal of Apiculture 30(3): 217-223.
Kim, S., Hong, I., Woo, S., Jang, H., Pak, S. & Han, S. 2017.
Isolation of abscisic acid from Korean acacia honey with anti-Helicobacter pylori activity. Pharmacognosy
Magazine 13(2): S170-S173.
Lamb, A. & Chen, L.F. 2010. The many roads traveled by Helicobacter pylori to NFκB
activation. Gut. Microbes 1(2): 109-113.
Malfertheiner, P., Mégraud, F., O'Morain, C., Hungin, P.S., Jones,
R., Axon, A., Graham,
D. & Tytgat, G. 2002. Current concepts in the management of
Helicobacter pylori infection-The
Maastricht 2-2000 Consensus Report. Alimentary Pharmacology &
Therapeutics 16(2): 167-180.
Malnick, S.D., Melzer, E., Attali, M., Duek, G. & Yahav, J. 2014. Helicobacter pylori: Friend or foe? World
J. Gastroenterol. 20(27): 8979-8985.
Mannina, L., Sobolev, A.P., Di Lorenzo, A., Vista, S., Tenore,
G.C. & Daglia, M. 2015. Chemical composition of different botanical origin honeys
produced by Sicilian black honeybees (Apis
mellifera ssp. sicula). Journal of Agricultural and Food Chemistry 63(25): 5864-5874.
Manyi-Loh, C.E., Clarke, A.M., Green, E. & Ndip, R.N. 2013. Inhibitory
and bactericidal activity of selected South African honeys and their solvent
extracts against clinical isolates of Helicobacter
pylori. Pakistan Journal of Pharmaceutical Sciences 26(5): 897-906.
Manyi-Loh, C.E., Clarke, A.M. & Ndip, R.N. 2012. Detection of
phytoconstituents in column fractions of n-hexane extract of goldcrest honey
exhibiting anti-Helicobacter pylori activity. Archives of Medical Research 43(3): 197-204.
Manyi-Loh, C.E., Clarke, A.M., Munzhelele, T., Green, E., Mkwetshana, N.F.
& Ndip, R.N. 2010. Selected South African honeys and their extracts possess in vitro anti-Helicobacter pylori activity. Archives of Medical Research 41(5): 324-331.
Matongo, F. & Nwodo, U.U. 2014. In
vitro assessment of Helicobacter
pylori ureases inhibition by honey fractions. Archives of Medical
Research 45(7): 540-546.
McGovern, D.P., Abbas, S.Z., Vivian, G. & Dalton, H.R. 1999. Manuka
honey against Helicobacter pylori. Journal
of the Royal Society of Medicine 92(8): 439. doi: 10.1177/014107689909200832.
Molan, P. 2001. Why honey is effective as a medicine: 2. The scientific
explanation of its effects. Bee World 82(1): 22-40.
Molan, P.C. 1996. Authenticity of honey. In Food Authentication, edited by Ashurst, P.R. & Dennis, M.J.
Boston: Springer. pp. 259-303.
Molan, P.C. & Russell, K.M. 1988. Non-peroxide antibacterial activity
in some New Zealand honeys. Journal of Apicultural Research
27(1): 62-67.
Nasir, N.M., Halim, A.S., Singh, K.B. & Dorai, A.A. 2010.
Antibacterial properties of tualang honey and its effect in burn wound
management: A comparative study. BMC
Complement. Altern. Med. 10: 31. doi:10.1186/1472-6882-10-31.
Ndip, R.N., Takang, A.E.M., Echakachi, C.M., Malongue, A., Akoachere,
J.F.T.K., Ndip, L.M. & Luma, H.N. 2007. In
vitro antimicrobial activity of selected honeys on clinical isolates of Helicobacter pylori. African Health
Sciences 7(74): 228-231.
Nzeako, B.C. & Al-Namaani, F. 2006. The antibacterial activity of
honey on Helicobacter pylori. Sultan Qaboos Univ. Med. J. 6(2): 71-76.
Osato, M.S., Reddy, S.G. & Graham, D.Y. 1999. Osmotic effect of honey
on growth and viability of Helicobacter
pylori. Dig. Dis. Sci. 44(3): 462-464.
Othman, N.H. 2012. Honey and cancer: Sustainable inverse relationship particularly
for developing nations-A review. Evidence-Based Complementary
and Alternative Medicine 2012: 410406. doi:10.1155/2012/410406.
Rückriemen, J., Klemm, O. & Henle, T. 2017. Manuka honey (Leptospermum scoparium) inhibits jack
bean urease activity due to methylglyoxal and dihydroxyacetone. Food
Chemistry 230: 540-546.
Samie, A., Obi, C.L., Barrett, L.J., Powell, S.M. & Guerrant, R.L.
2007. Prevalence of Campylobacter species, Helicobacter pylori and Arcobacter species in stool samples from
the Venda region, Limpopo, South Africa: Studies using molecular diagnostic
methods. Journal of Infection 54(6): 558-566.
Seo, J.H., Lim, J.W., Kim, H. & Kim, K.H. 2004. Helicobacter pylori in a Korean isolate activates
mitogen-activated protein kinases, AP-1, and NF-κB and induces chemokine
expression in gastric epithelial AGS cells. Laboratory Investigation 84(1): 49-62.
Sherlock, O., Dolan, A., Athman, R., Power, A., Gethin, G., Cowman, S.
& Humphreys, H. 2010. Comparison of the antimicrobial activity of Ulmo
honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC Complement. Altern. Med. 10: 47.
Tan, H.T., Rahman, R.A., Gan, S.H., Halim, A.S., Hassan, S.A., Sulaiman,
S.A. & Kirnaur-Kaur, B.S. 2009. The antibacterial properties of Malaysian
Tualang honey against wound and enteric microorganisms in comparison to Manuka
honey. BMC Complement. Altern. Med. 9: 34. doi:10.1186/1472-6882-9-34.
Tanih, N.F., Okeleye, B.I., Naidoo, N., Clarke, A.M., Mkwetshana, N.,
Green, E., Ndip, L.M. & Ndip, R.N. 2010. Marked susceptibility of South
African Helicobacter pylori strains
to ciprofloxacin and amoxicillin: Clinical implications. South African
Medical Journal 100(1): 49-52.
Vallianou, N. 2014. Honey and its anti-inflammatory, anti-bacterial and
anti-oxidant properties. General Medicine: Open Access 2(2): 132.
doi:10.4172/2327-5146.1000132.
Yao, L., Datta, N., Tomás-Barberán, F.A., Ferreres, F., Martos, I. &
Singanusong, R. 2003. Flavonoids, phenolic acids and abscisic acid in
Australian and New Zealand Leptospermum honeys. Food Chemistry 81(2):
159-168.
Yaoa, L., Jiang, Y., Singanusong, R., Datta, N. & Raymont, K. 2005.
Phenolic acids in Australian Melaleuca, Guioa, Lophostemon, Banksia and
Helianthus honeys and their potential for floral authentication. Food
Research International 38(6): 651-658.
Zaghloul, A.A., El-Shattawy, H.H., Kassem, A.A., Ibrahim, E.A., Reddy,
I.K. & Khan, M.A. 2001. Honey, a prospective antibiotic: Extraction,
formulation, and stability. Pharmazie 56(8): 643-647.
*Corresponding
author; email: nurazlinamf@ukm.edu.my
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