The antibiofilm effects of some Cistus spp. against pathogenic microorganisms

Sevim Feyza Erdoğmuş; Cihat Bilecen; Özlem Erdal Altıntaş; Sevgi Ulukütük; Mustafa Kargıoğlu

doi:10.29228/ijpbp.7

Authors

Sevim Feyza Erdoğmuş Afyonkarahisar Health Sciences University, Faculty of Pharmacy, Department of Basic Pharmaceutical Sciences, Afyonkarahisar, Turkey https://orcid.org/0000-0002-4319-7558
Cihat Bilecen Afyon Kocatepe University, Faculty of Veterinary Medicine, Department of Medical Biology and Genetics, Afyonkarahisar, Turkey https://orcid.org/0000-0002-0499-7317
Özlem Erdal Altıntaş Afyonkarahisar Health Sciences University, Şuhut Vocational School of Health Services, Department of Medical Services and Techniques, Afyonkarahisar, Turkey https://orcid.org/0000-0003-4680-1738
Sevgi Ulukütük Afyon Kocatepe University, Şuhut Vocational School, Department of Food Processing, Afyonkarahisar, Turkey https://orcid.org/0000-0002-5760-8493
Mustafa Kargıoğlu Afyon Kocatepe University, Faculty of Arts and Sciences, Department of Molecular Biology and Genetics, Turkey https://orcid.org/0000-0003-0386-9716

DOI:

https://doi.org/10.29228/ijpbp.7

Keywords:

Antibiofilm, Cistus creticus L., Cistus laurifolius L., Cistus salviifolius L., Pathogen microorganism

Abstract

Recently, the potential antibacterial or antibiofilm effects of some plant species belonging to the Cistus sp. have motivated investigation of their use as herbal remedies. In this study, antibiofilm activities of aqueous (dH₂O) leaf extracts of Cistus laurifolius L., C. creticus L. and C. salviifolius L. on some pathogenic microorganisms with biofilm forming ability were investigated. Biofilm forming ability of pathogen test microorganisms were evaluated by congo red agar method and microtiter plate method and all tested microorganisms were confirmed as biofilm producers. Staphylococcus aureus ATCC 25923, Pseudomonas aeruginosa ATCC 11778, S. aureus ATCC 6538, P. aeruginosa ATCC 27853 and S. aureus ATCC 12600 were evaluated as strong biofilm producers. The highest concentration of examined extracts both showed biofilm inhibition and biofilm eradication against the tested pathogen microorganisms. In particular, studied plant extracts showed good antibiofilm effect, and biofilm eradication against S. aureus ATCC 6538 and S. aureus ATCC 12600. MBIC₅₀ values of S. aureus ATCC 6538 were found as 6.25 µg/ml of C. laurifolius, and 50 µg/ml of C. creticus extracts. Also, 50 µg/ml of C. creticus extract showed ≥ 90% inhibition of biofilm growth (MBIC₉₀ = 50 µg/ml). MBEC₅₀ values of S. aureus ATCC 12600 were determined as 6.25 µg/ml in all tested plant extracts and 50 µg/ml of C. creticus extract was required to induce ≥ 90% eradication (MBEC₉₀) of biofilm growth of S. aureus ATCC 12600. Our study revealed that aqueous leaf extracts of C. laurifolius, C. creticus and C. salviifolius could be potential candidates for drug discovery to treat pathogen test microorganisms capable to induce infectious diseases especially by their biofilm forming ability.

References

Álvarez-Martínez, F.J., Rodríguez, J.C., Borrás-Rocher, F., Barrajón-Catalán, E., Micol, V., 2021. The antimicrobial capacity of Cistus salviifolius and Punica granatum plant extracts against clinical pathogens is related to their polyphenolic composition. Scientific Reports, 11(1), 1-12.

Aslam, B., Wang, W., Arshad, M.I., Khurshid, M., Muzammil, S., Rasool, M.H., Baloch, Z., 2018. Antibiotic resistance: a rundown of a global crisis. Infection and Drug Resistance, 11, 1645-1658.

Attaguile, G., Russo, A., Campisi, A., Savoca, F., Acquaviva, R., Ragusa, N., Vanella, A., 2000. Antioxidant activity and protective effect on DNA cleavage of extracts from Cistus incanus L. and Cistus monspeliensis L. Cell Biology and Toxicology, 16(2), 83-90.

Barrajón‐Catalán, E., Fernández‐Arroyo, S., Roldán, C., Guillén, E., Saura, D., Segura‐Carretero, A., Micol, V., 2011. A systematic study of the polyphenolic composition of aqueous extracts deriving from several Cistus genus species: evolutionary relationship. Phytochemical Analysis, 22(4), 303-312.

Barros, L., Dueñas, M., Alves, C.T., Silva, S., Henriques, M., Santos-Buelga, C., Ferreira, I.C., 2013. Antifungal activity and detailed chemical characterization of Cistus ladanifer phenolic extracts. Industrial Crops and Products, 41, 41-45.

Ben Bakrim, W., Aghraz, A., Hriouch, F., Larhsini, M., Markouk, M., Bekkouche, K., Dugo, G., 2022. Phytochemical study and antioxidant activity of the most used medicinal and aromatic plants in Morocco. Journal of Essential Oil Research, 34(2), 131-142.

Benali, T., Bouyahya, A., Habbadi, K., Zengin, G., Khabbach, A., Hammani, K., 2020. Chemical composition and antibacterial activity of the essential oil and extracts of Cistus ladaniferus subsp. ladanifer and Mentha suaveolens against phytopathogenic bacteria and their ecofriendly management of phytopathogenic bacteria. Biocatalysis and Agricultural Biotechnology, 28, 101696.

Bowler, P., Murphy, C., Wolcott, R., 2020. Biofilm exacerbates antibiotic resistance: Is this a current oversight in antimicrobial stewardship?. Antimicrobial Resistance & Infection Control, 9(1), 1-5.

Catoni, R., Gratani, L., Varone, L., 2012. Physiological, morphological and anatomical trait variations between winter and summer leaves of Cistus species. Flora-Morphology, Distribution, Functional Ecology of Plants, 207(6), 442-449.

Cetin, H., Yanikoglu, A., 2006. A study of the larvicidal activity of Origanum (Labiatae) species from southwest Turkey. Journal of Vector Ecology, 31(1), 118-122.

Comandini, O., Contu, M., Rinaldi, A.C., 2006. An overview of Cistus ectomycorrhizal fungi. Mycorrhiza, 16(6), 381-395.

Costa, O.Y., Raaijmakers, J.M., Kuramae, E.E., 2018. Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Frontiers in Microbiology, 9, 1636.

Croes, S., Deurenberg, R.H., Boumans, M.L.L., Beisser, P.S., Neef, C., Stobberingh, E.E., 2009. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiology, 9(1), 1-9.

Darwish, S.F., Asfour, H.A., 2013. Investigation of biofilm forming ability in Staphylococci causing bovine mastitis using phenotypic and genotypic assays. The Scientific World Journal, 2013, 378492.

Davies, D., 2003. Understanding biofilm resistance to antibacterial agents. Nature Reviews Drug Discovery, 2(2), 114-122.

Davis, P.H., 1988: Flora of Turkey and the East Aegean Islands. Vol. 10. Edinburgh University Press, p. 61–62.

Demetzos, C., Dimas, K., Hatziantoniou, S., Anastasaki, T., Angelopoulou, D., 2001. Cytotoxic and anti-inflammatory activity of labdane and cis-clerodane type diterpenes. Planta Medica, 67(07), 614-618.

Dimas, K., Demetzos, C., Angelopoulou, D., Kolokouris, A., Mavromoustakos, T., 2000. Biological activity of myricetin and its derivatives against human leukemic cell lines in vitro. Pharmacological Research, 42(5), 475-478.

Donlan, R.M., Costerton, J.W., 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15(2), 167-193.

Ehrhardt, C., Hrincius, E.R., Korte, V., Mazur, I., Droebner, K., Poetter, A., Ludwig, S., 2007. A polyphenol rich plant extract, CYSTUS052, exerts anti influenza virus activity in cell culture without toxic side effects or the tendency to induce viral resistance. Antiviral Research, 76(1), 38-47.

Fernandes, J.B.C., Zanardo, L.G., Galvão, N.N., Carvalho, I.A., Nero, L.A., Moreira, M.A.S., 2011. Escherichia coli from clinical mastitis: serotypes and virulence factors. Journal of Veterinary Diagnostic Investigation, 23(6), 1146-1152.

Fierascu, R.C., Fierascu, I., Baroi, A.M., Ortan, A., 2021. Selected aspects related to medicinal and aromatic plants as alternative sources of bioactive compounds. International Journal of Molecular Sciences, 22(4), 1521.

Flemming, H.C., Wingender, J., Szewwzyk, U., Steinberg, P., Rice, S.A., Kjelleberg, S., 2016. Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology, 14,563-575.

Freeman, D.J., Falkiner, F.R., Keane, C.T., 1989. New method for detecting slime production by coagulase negative staphylococci. Journal of Clinical Pathology, 42(8), 872-874.

Ganaie, H.A., 2021. Review of the active principles of medicinal and aromatic plants and their disease fighting properties. In Medicinal and aromatic plants (pp. 1-36). Academic Press.

Ghorbanpour, M., Hadian, J., Nikabadi, S., Varma, A., 2017. Importance of medicinal and aromatic plants in human life. In Medicinal Plants and Environmental Challenges (pp. 1-23). Springer, Cham.

Gomes, F., Martins, N., Ferreira, I.C., Henriques, M., 2019. Anti-biofilm activity of hydromethanolic plant extracts against Staphylococcus aureus isolates from bovine mastitis. Heliyon, 5(5), e01728.

Güvenç, A., Yıldız, S., Özkan, A.M., Erdurak, C.S., Coşkun, M., Yılmaz, G., Okada, Y., 2005. Antimicrobiological studies on turkish Cistus species. Pharmaceutical Biology, 43(2), 178-183.

Hall-Stoodley, L., Costerton, J.W., Stoodley, P., 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nature Reviews Microbiology, 2(2), 95-108.

Hannig, C., Spitzmüller, B., Al-Ahmad, A., Hannig, M., 2008. Effects of Cistus-tea on bacterial colonization and enzyme activities of the in situ pellicle. Journal of Dentistry, 36(7), 540-545.

Heidari H.M., Ebrahim-Saraie H.S., Mirzaei A., Taji, A., Hosseini S.R., Motamedifar, M., 2018. Characterization of virulence factors, antimicrobial resistance patterns and biofilm formation of Pseudomonas aeruginosa and Staphylococcus spp. strains isolated from corneal infection. Journal Français d'Ophtalmologie, 41, 9823-829.

Jain, A., Agarwal, A., 2009. Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. Journal of Microbiological Methods, 76(1), 88-92.

Jamal, M., Andleeb, S., Jalil, F., Imran, M., Nawaz, M.A., Hussain, T., Das, C.R., 2019. Isolation, characterization and efficacy of phage MJ2 against biofilm forming multi-drug resistant Enterobacter cloacae. Folia Microbiologica, 64(1), 101-111.

Jasovský, D., Littmann, J., Zorzet, A., Cars, O., 2016. Antimicrobial resistance—a threat to the world’s sustainable development. Upsala Journal of Medical Sciences, 121(3), 159-164.

Kairo, S.K., Bedwell, J., Tyler, P.C., Carter, A., Corbel, M.J., 1999. Development of a tetrazolium salt assay for rapid determination of viability of BCG vaccines. Vaccine, 17(19), 2423-2428.

Kenar, B., Erik, M., Erdoğmuş, S.F., Korcan, S.E., Köse, Z., Durmaz, G., 2020. The determination of antimicrobial and antibiofilm activities of foodborne lactic acid bacteria against Enterobacter cloacae isolates. Turkish Journal of Veterinary & Animal Sciences, 44(1), 59-68.

Küpeli, E., Yesilada, E., 2007. Flavonoids with anti-inflammatory and antinociceptive activity from Cistus laurifolius L. leaves through bioassay-guided procedures. Journal of Ethnopharmacology, 112(3), 524-530.

Latiff, N.A., Ong, P.Y., Abd Rashid, S.N.A., Abdullah, L.C., Mohd Amin, N.A., Fauzi, N.A.M., 2021. Enhancing recovery of bioactive compounds from Cosmos caudatus leaves via ultrasonic extraction. Scientific Reports, 11(1), 17297.

Lekbach, Y., Xu, D., El Abed, S., Dong, Y., Liu, D., Khan, M.S., Yang, K., 2018. Mitigation of microbiologically influenced corrosion of 304L stainless steel in the presence of Pseudomonas aeruginosa by Cistus ladanifer leaves extract. International Biodeterioration & Biodegradation, 133, 159-169.

Leone, S., Molinaro, A., Alfieri, F., Cafaro, V., Lanzetta, R., Di Donato, A., Parrilli, M., 2006. The biofilm matrix of Pseudomonas sp. OX1 grown on phenol is mainly constituted by alginate oligosaccharides. Carbohydrate Research, 341(14), 2456-2461.

Marshall, V.M., Rawson, H.L., 1999. Effects of exopolysaccharide‐producing strains of thermophilic lactic acid bacteria on the texture of stirred yoghurt. International Journal of Food Science & Technology, 34(2), 137-143.

Monzón, M., Oteiza, C., Leiva, J., Lamata, M., Amorena, B., 2002. Biofilm testing of Staphylococcus epidermidis clinical isolates: low performance of vancomycin in relation to other antibiotics. Diagnostic Microbiology and Infectious Disease, 44(4), 319-324.

Olsen, I., 2015. Biofilm-specific antibiotic tolerance and resistance. European Journal of Clinical Microbiology & Infectious Diseases, 34(5), 877-886.

Rasmussen, T.B., Givskov, M., 2006. Quorum sensing inhibitors: a bargain of effects. Microbiology, 152(4), 895-904.

Raza, A., Muhammad, G., Sharif, S., Atta, A., 2013. Biofilm producing Staphylococcus aureus and bovine mastitis: a review. Molecular Microbiology Research, 3(1), 1-18.

Richardson, L.A., 2017. Understanding and overcoming antibiotic resistance. PLoS Biology, 15(8), e2003775.

Roy, R., Tiwari, M., Donelli, G., Tiwari, V., 2019. Strategies for Combating Bacterial Biofilms: A Focus on Anti-Biofilm Agents and Their Mechanisms of Action. Virulence, 9(1), 522–554.

Sabir, N., Ikram, A., Zaman, G., Satti, L., Gardezi, A., Ahmed, A., Ahmed, P., 2017. Bacterial biofilm-based catheter-associated urinary tract infections: Causative pathogens and antibiotic resistance. American Journal of Infection Control, 45(10), 1101-1105.

Saxena, N., Maheshwari, D., Dadhich, D., Singh, S., 2014. Evaluation of Congo red agar for detection of biofilm production by various clinical Candida isolates. Journal of Evolution of Medical and Dental Sciences, 3(59), 13234-13239.

Sayah, K., Chemlal, L., Marmouzi, I., El Jemli, M., Cherrah, Y., Faouzi, M.E.A., 2017. In vivo anti-inflammatory and analgesic activities of Cistus salviifolius (L.) and Cistus monspeliensis (L.) aqueous extracts. South African Journal of Botany, 113, 160-163.

Silva, V.O., Soares, L.O., Silva Júnior, A., Mantovani, H.C., Chang, Y.F., Moreira, M.A.S., 2014. Biofilm formation on biotic and abiotic surfaces in the presence of antimicrobials by Escherichia coli isolates from cases of bovine mastitis. Applied and Environmental Microbiology, 80(19), 6136-6145.

Soares, G.G., Costa, J.F., Melo, F., Mola, R., Balbino, T.C.L., 2016. Biofilm production and resistance profile of Enterobacter sp. strains isolated from pressure ulcers in Petrolina, Pernambuco, Brazil. Jornal Brasileiro de Patologia e Medicina Laboratorial, 52, 293-298.

Stepien, A., Aebisher, D., Bartusik-Aebisher, D., 2018. Biological properties of Cistus species. European Journal of Clinical and Experimental Medicine, 16, 127-132.

Szczuka, E., Kaznowski, A., 2014. Antimicrobial activity of tigecycline alone or in combination with rifampin against Staphylococcus epidermidis in biofilm. Folia Microbiologica, 59(4), 283-288.

Teanpaisan, R., Senapong, S., Puripattanavong, J., 2014. In vitro antimicrobial and antibiofilm activity of Artocarpus lakoocha (Moraceae) extract against some oral pathogens. Tropical Journal of Pharmaceutical Research, 13(7), 1149-1155.

Ustun, O., Baykal, T., 2016. Bioactivities of ethanolic extract and its fractions of Cistus laurifolius L. (Cistaceae) and Salvia wiedemannii Boiss. (Lamiaceae) species. Pharmacognosy Magazine, 12(Suppl 1), S82-S85.

Van Houdt, R., Michiels, C.W., 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology, 109(4), 1117-1131.

Walencka, E., Sadowska, B., Ro´zalska, S., Hryniewicz, W., Rozalska, B., 2005. Lysostaphin as a potential therapeutic agent for staphylococcal biofilm eradication. Polish Journal of Microbiology, 54, 191-200.

Wu, X., Al Farraj, D.A., Rajaselvam, J., Alkufeidy, R.M., Vijayaraghavan, P., Alkubaisi, N.A., Alshammari, M.K., 2020. Characterization of biofilm formed by multidrug resistant Pseudomonas aeruginosa DC-17 isolated from dental caries. Saudi Journal of Biological Sciences, 27(11), 2955-2960.

Yan, J., Bassler, B.L., 2019. Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host & Microbe, 26(1), 15-21.

Zalegh, I., Akssira, M., Bourhia, M., Mellouki, F., Rhallabi, N., Salamatullah, A.M., Mhand, R.A., 2021. A review on Cistus sp.: Phytochemical and antimicrobial activities. Plants, 10(6), 1214.