Effect of Red Onion (Allium cepa var ascalonicum) Skin Ethanolic Extract on the Motility and the Adhesion Index of Pseudomonas aeruginosa and Macrophage Phagocytosis Index


Irma Prasety Ayu Nugraheni(1), Derana Widyastika(2), Sofia Maulida(3), Heni Susilowati(4), Alma Linggar Jonarta(5*)

(1) Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(2) Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(3) Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(4) Oral Biology Department, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(5) Oral Biology Department, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(*) Corresponding Author


Red onion skin (Allium cepa var ascalonicum) contains various ingredients that may function as antibacterial agents against microorganisms, as well as anti-inflammatory and immunomodulator agents for host cells, such as macrophages. Pseudomonas aeruginosa found in the oral cavity is commensal bacteria that may turn into opportunistic pathogen by utilizing its virulence factors such as motility and adhesion to the host cell. The purpose of this study was to investigate the effect of red-onion-skin ethanolic extract towards P. aeruginosa ATCC 9027 on the motility and adhesion ability, furthermore, to know its effect on the macrophage phagocytosis. The research was conducted into three parts of experiment using red-onion-skin ethanolic extract. Extract-induced bacterial motility test was carried out on semi-solid media, stained using 0.1% crystal violet, then the radial length of the bacterial movement was measured. The bacterial adhesion index to buccal cells was calculated after incubated for two hours and stained with Gram stain. Phagocytic activity of the host cells on P. aeruginosa was done by exposing the extract to the mouse peritoneal macrophages, then the phagocytosed bacteria were counted after Giemsa staining. Statistical test results from the three experiments showed significant differences between the test groups compared to the control groups (p <0.05). It was concluded that the red onion-skin ethanolic extract not only affects P. aeruginosa by reducing swarming motility and preventing bacterial adhesion to buccal epithelial cells, but also induces the host cells by increasing the ability of macrophage phagocytosis to these bacteria.


Red-onion-skin ethanolic extract; Pseudomonas aeruginosa ATCC 9027; swarming motility; Adhesion Index; Macrophage Phagocytosis Index

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Albrecht, M.T., Wang, W., Shamova, O., Lehrer, R.I., & Schiller, N.L., 2002, ‘Binding of protegrin-1 to Pseudomonas aeruginosa and Burkholderia cepacia’, Respir. Res., 3(1), 1–11.

Al-tahhan, R.A., Sandrin, T.R., Bodour, A.A., Maier, R.M., 2000, ‘Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates’, Appl. Environ. Microbiol., 66(8), 3262–3268.

Brooks, G. F., Jawetz, E., Melnick, J. L., & Adelberg, E. A. (2010). Jawetz, Melnick, & Adelberg's medical microbiology. New York: McGraw Hill Medical.

Burrows, L.L., 2012, ‘Twitching motility: type IV pili in action’, Annu. Rev. Microbiol, 66, 493–520.

Caldas, R.R., Gall, L., Revert, K., Rault, G., Virmaux, M., & Gouriou, S., 2015, ‘Pseudomonas aeruginosa and periodontal pathogens in the oral cavity and lungs of cystic fibrosis patients: a case-control study’, J. Clin. Microbiol., 53(6),1898–1907.

Campbell, N.A., Reece, J.B., & Mitchell, L.G., 2003, Biology, 5th ed., Benjamin/Cummings, Menlo Park, CA.

Colombo, A.V, Barbosa, G.M., Higashi, D., Micheli, G., Rodrigues, P.H., & Simionato, M.R.L., 2013, ‘Quantitative detection of Staphylococcus aureus, Enterococcus faecalis and Pseudomonas aeruginosa in human oral epithelial cells from subjects with periodontitis and periodontal health’, J. Med. Microbiol., 62, 1592–1600

Conrad, J.C., Gibiansky, M.L., Jin, F., Gordon, V.D., Motto, D., Mathewson, M.A., Stopka, W.G., Zelasko, D.C., Shrout, J.D., & Wong, G.C., 2011, ‘Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa’, Biophys. J, 100(7), 1608-1616

Deaziel, E., Comeau, Y., Villemur, R., 2001, ‘Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities’, J Bacteriol, 183(4), 1195-1204.

Dewanti, T., Sukardiman, Agus, D., & Darmanto, W., 2012, “The immunomodulatory effect of Mesona palustris BL extract on mice carcinogenesis’, J. Teknol. dan Industri Pangan, 23(1), 29-35.

Elberry, A. A., Mufti, S., Al- Maghrabi, J., Sattar, E. A., Ghareib, S. A., Mosli, H. A., & Gabr, S. A., 2014, ‘Immunomodulatory effect of red onion (Allium cepaLinn) scale extract on experimentally induced atypical prostatic hyperplasia in wistar rats’, Mediators Inflamm., 2014, 1-13. Article ID 640746, https://doi.org/10.1155/2014/640746

Evans, E. A., Kawli, T., & Tan, M. W., 2008, ‘Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans’, PLoS Pathog, 4(10), 1-18

Hancock, R.E.W., Overhage, J., Lewenza, S., & Marr, A.K., 2007, Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library, J. Bacteriol., 189(5), 2164-2169.

Harmsen, M., Yang, L., Pamp, J., Tolker-nielsen, T., & Tolker-nielsen, C.T., 2010, ‘An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal’, Immunol. Med. Microbiol., 59, 253–268.

Hidayat, R., 2015, Agonis Peroxisome Proliferator Activator Receptor (PPAR) γ reduced the level of anti-inflammatory cytokines TGF-β dan IL-10 on wistar rat vascular inflammation model’, Sains Medika, 2(3), 291-296.

Jensch-Junior, B.E., Pressinotil, N., Borges, J.C.S. & Cunha da Silva, J.R.M., 2006, ‘Characterization of macrophage phagocytosis of the tropical fish Prochilodus scrofa (Steindachner, 1881)’, Aquaculture, 251, 509-515

Johnson, M.D.L., Garrett, C.K., Bond, J.E., Coggan, K.A., Matthew, C., & Redinbo, M.R., 2011, ‘Pseudomonas aeruginosa PilY1 binds integrin in an RGD- and calcium-dependent manner’, PLos One, 6(12), 1–8.

Krachler, A.M., & Orth, K., 2013, ‘Targeting the bacteria-host interface: strategies in anti-adhesion therapy’, Virulence, 4(4), 284–94.

Lavoie, E. G., Wangdi, T., & Kazmierczak, B. I., 2011, ‘Innate immune responses to Pseudomonas aeruginosa infection’, Microbes Infect, 13(14), 1-21.

Limsuwan, S., Homlaead, S., Watcharakul, S., Chusri, S., Moosigapong, K., Saising, J., & Voravuthikunchai, S.P., 2014, ‘Inhibition of microbial adhesion to plastic surface and human buccal epithelial cells by Rhodomyrtus tomentosa leaf extract’. Arch Oral Biol, 59(12), 1256–1265.

Lister, P. D., Wolter, D. J., & Hanson, N. D., 2009, Antibacterial – resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms, Clin. Microbiol, Rev, 22(4), 582-610.

Mirzoeva, O.K., Grishanin, R.N., & Calder, P.C., 1997, ‘Antimicrobial action of propolis and some of its components: the effects on growth, membrane potential and motility of bacteria’, Microbial. Res., 152, 239-246

O’toole, G.A., & Kolter, R., 1998, ‘Initiation of biofilm formation in Pseudomonas aeruginosa WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis, Mol. Microbiol., 28(3), 449-461.

O’May, C., & Tufenkji, N., 2011, The swarming motility of Pseudomonas aeruginosa is blocked by Cranberry proanthocyanidins and other tannin-containing materials’, Appl. Environ. Microbiol. 77(9), 3061–3067.

Oura, H., Tashiro, Y., Toyofuku, M., et al., 2015, Inhibition of Pseudomonas aeruginosa swarming motility by 1-naphthol and other bicyclic compounds bearing hydroxyl groups. Appl. Environ. Microb., 81(8), 2808-2818.

Prayitno, A., Fitria, M. S., & Elmanda, A. Y., 2016, ‘Tumoricidal activation of macrophages using Jatropha curcas leaf extract: as a proxy for the treatment of cancer, Immunome Res, 12(1), 1-3.

Rashid, M. H., & Kornberg, A., 2000, ‘Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa’, Proc Natl Acad Sci, 97(9), 4885–4890.

Rauf, A., Haeria, & Anas, D. D., 2016, ‘ The immunostimulant effect of Katuk leaf fraction (Sauropus androgynus L. MERR.) on the phagocytosis activity and capacity of male mice (mus musculus) macrophage’, JF FIK UINAM, 4(1), 9-15.

Setyawan, A. B., 2015, ‘The effectivity of kejibeling leaves extract in increasing macrophage phagocytosis and the production of macrophage ROI – an experimental study on Staphylococcus aureus-infected Swiss mice’, JSK, 1(4), 195-201.

Skerget, M., Majhenie, L., & Bezjak, M., 2009, ‘Antioxidant, radical scavenging and antimicrobial activities of red onion (Allium cepa L) skin and edible part extract’s, Chem. Biochem. Eng. Q. 23(4), 435-444

Sotirova, A., Spasova, D., Vasileva-Tonkova, E., & Galabova, D., 2009, ‘Effects of rhamnolipid-biosurfactant on cell surface of Pseudomonas aeruginosa’, Microb. Res. 164(3), 297-303.

Sumarno. 2000. Molecular characterization of adhesion proteins Vibrio cholera 01 MO94 and its receptor protein in white rat small intestine epithelial cells (Wistar). A pathogenesis study of E. cholerae 01 MO94, Thesis, Program Pasca Sarjana, Universitas Airlangga Surabaya.

Sutasmi, Y. & Natsir, N., 2014, ‘Bacterial identification on chronic apical periodontitis tooth root canal’, Dentofasial, 13(3),182-185

Taweechaisupapong, S., Choopan, T., Singhara, S., Chatrchaiwiwatana, S., & Wongkham, S., 2005, ‘In vitro inhibitory effect of Streblus asper leaf-extract on adhesion of Candida albicans to human buccal epithelial cells’, J. Eth. Pharm., 96, 221–226.

Ulfah, M., Cahyani, V. S. N., & Kinasih, I., 2017, ‘The effect of Annona muricata L. infuse tea on the macrophage phagocytosis activity and lymphocyte proliferation of Hepatitis B vaccine-induced Balb/C mice’, Momentum, 13(2), 63-71.

Ulum, A. N., Ulfah, M., & Sasmito, E., 2016, ‘Immunomodulator activity test of fermented Kombucha yeast black tea on Balb Balb/c mice phagocytosis in vitro’, JSFK, 13(2): 24-31.

Wolska, K., Zabielska, K., & Jakubczak, A., 2006, ‘Effect of neuraminidase on adherence of Pseudomonas aeruginosa to human buccal epithelial cells. Inhibition of adhesion by monosaccharides’. Polish J. Microbiol, 55(1), 43-48.

Wu, H., Lee, B., Yang, L., Wang, H., Givskov, M., Molin, S., Hoiby, N., & Song, Z., 2011, ‘Effects of ginseng on Pseudomonas aeruginosa motility and biofilm formation, Immunol Med Microbial, 62, 49-5.

DOI: https://doi.org/10.22146/mot.45532

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