Research Article
BibTex RIS Cite

Helianthus annuus Yapraklarının İnfüzyon veya Dekoksiyon Özütleri: Pseudomonas aeruginosa’nın QS Sistemi ve Biyofilm Oluşumu Üzerine Potansiyel İnhibitörler

Year 2020, Volume: 32 Issue: 4, 499 - 506, 01.11.2020

Arhun Ali Balkan , Ayla Yıldız , Didem Berber , Barış Gökalsın , Cenk Sesal

https://doi.org/10.7240/jeps.741137

Abstract

Pseudomonas aeruginosa is one of the drug-resistant opportunistic pathogens with the ability to form biofilm and to produce a number of virulence factors via Quorum Sensing (QS) regulation. Most researchers have focused on QS inhibition to overcome the drug resistance problem. QS inhibitor molecules are investigated from natural resources. In the present study, anti-QS activities of ethyl acetate extracts of decoction and infusion samples from Helianthus annuus leaves were tested on biosensor strains of P. aeruginosa (lasB-gfp, rhlA-gfp and pqsA-gfp), as well as anti-biofilm activities on PAO1 wild type. H. annuus leaf samples were firstly infused or decocted and then extracted with ethyl acetate. The efficacies of infusion or decoction extracts were examined at the concentrations of 240, 120, and 60 μg/ml in 96-well microplates and evaluated in Citation 3 multimode microplate reader (Biotek). The inhibition rates of decoction extracts were recorded as 70.61% for las, 44.09% for rhl and 83.77% pqs system at 240 μg/ml. The biofilm inhibition percentages of the extracts were determined to be 50.82% (±1.36). Moreover, inhibition rates for infusion extracts were detected as 62.08% for las, 45.15% for rhl and 77.79% for pqs, and 53.88% (±3.94) for biofilm formation. In conclusion, the potential efficacies of the extracts of decocted or infused H.annuus leaves were demonstrated on QS system and biofilm formation of P. aeruginosa. However, there is a need for more detailed investigations and determination of the active substances that have QSI and anti-biofilm effect.

Keywords

Helianthus annuus las system rhl system pqs system quorum sensing inhibitor anti-biofilm

References

  • [1] Butler, M.S., Blaskovich, M.A. and Cooper, M.A. (2013). Antibiotics in the clinical pipeline in 2013. The Journal of Antibiotics, 66(10), 571-591.
  • [2] Wright, G.D. (2017). Opportunities for natural products in 21 st century antibiotic discovery. Natural Product Reports, 34(7), 694-701.
  • [3] Centres for Disease Control and Prevention (US). (2013). Antibiotic resistance threats in the United States.
  • [4] Pandhare, A. (2015). Bacterial resistance in India: Studying plasma antibiotic levels. Indian Journal of Critical Care Medicine, 19(10), 574.
  • [5] World Health Organization. (2017). Antibacterial agents in clinical development. World Health Organization: Geneva, Switzerland.
  • [6] Rasko, D.A. and Sperandio, V. (2010). Anti-virulence strategies to combat bacteria-mediated disease. Nature Reviews Drug Discovery, 9(2), 117-128.
  • [7] Dickey, S.W., Cheung, G.Y. and Otto, M. (2017). Different drugs for bad bugs: antivirulence strategies in the age of antibiotic resistance. Nature Reviews Drug Discovery, 16(7), 457.
  • [8] Miller, M.B. and Bassler, B.L. (2001). Quorum sensing in bacteria. Annual Reviews in Microbiology, 55(1), 165-199.
  • [9] Smith, R.S. and Iglewski, B.H. (2003). Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. The Journal of Clinical Investigation, 112(10), 1460-1465.
  • [10] Williams, P. and Cámara, M. (2009). Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Current Opinion in Microbiology, 12(2), 182-191.
  • [11] Antunes, L.C.M., Ferreira, R.B., Buckner, M.M. and Finlay, B.B. (2010). Quorum sensing in bacterial virulence. Microbiology, 156(8), 2271-2282.
  • [12] Rutherford, S.T. and Bassler, B.L. (2012). Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspectives in Medicine, 2(11), a012427.
  • [13] Olson, M.E., Ceri, H., Morck, D.W., Buret, A.G. and Read, R.R. (2002). Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can. J. Vet. Res., 66(2): 86.
  • [14] Driscoll, J.A., Brody, S.L. and Kollef, M.H. (2007). The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs, 67(3), 351-368.
  • [15] Lee, J., Wu, J., Deng, Y., Wang, J., Wang, C., Wang, J., Chang, C., Dong, Y., Williams, P. and Zhang, L.H. (2013). A cell-cell communication signal integrates quorum sensing and stress response. Nature Chemical Biology, 9(5), 339.
  • [16] Lee, J. And Zhang, L. (2015). The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein & Cell, 6(1), 26-41.
  • [17] Erickson, D.L., Endersby, R., Kirkham, A., Stuber, K., Vollman, D.D., Rabin, H.R., Mitchell, I. and Storey, D.G. (2002). Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infection and Immunity, 70(4), 1783-1790.
  • [18] Kalia, VC. (2015). Quorum sensing vs quorum quenching: a battle with no end in sight. Springer, New Delhi, India.
  • [19] Yesilyurt, E.B., Simsek, I., Tuncel, T., Akaydın, G. And Yesilada, E. (2017). Marmara Bölgesi’nin bazı yerleşim merkezlerinde halk ilacı olarak kullanılan bitkiler. Marmara Pharmaceutical Journal, 21: 132-148.
  • [20] Bashir, T., Zahara, K., Haider, S. And Tabassum, S. (2015). Chemistry, pharmacology and ethnomedicinal uses of Helianthus annuus (sunflower): a review. Pure and Applied Biology, 4(2), 226.
  • [21] Fowler, M.W. (2006). Plants, medicines and man. Journal of the Science of Food and Agriculture, 86(12), 1797-1804.
  • [22] Karunamoorthi, K., Jegajeevanram, K., Vijayalakshmi, J. and Mengistie, E. (2013). Traditional medicinal plants: a source of phytotherapeutic modality in resource-constrained health care settings. Journal of Evidence-Based Complementary & Alternative Medicine, 18(1), 67-74.
  • [23] Kocabas, A. (2017). Ease of phytochemical extraction and analysis from plants? Anatolian Journal of Botany, 1(2):6-31.
  • [24] Jarić, S., Popović, Z., Mačukanović-Jocić, M., Djurdjević, L., Mijatović, M., Karadžić, B., Mitrovic´, M. and Pavlović, P. (2007). An ethnobotanical study on the usage of wild medicinal herbs from Kopaonik Mountain (Central Serbia). Journal of Ethnopharmacology, 111(1), 160-175.
  • [25] Cepni, E. and Gurel, F. (2011). Bitkilerden elde edilen anti quorum sensing bileşikleri ve yeni ilaç geliştirmedeki potansiyelleri. Turkish Journal of Microbiology, 41 (4):131-138. [26] Al-douri, N.A. (2000). A survey of medicinal plants and their traditional uses in Iraq. Pharmaceutical Biology, 38(1), 74-79.
  • [27] Gaur, R.K., Petrov, N.M., Patil, B.L. and Stoyanova, M.I. (Eds.). (2016). Plant Viruses: Evolution and Management. Springer.
  • [28] Sharma, D., Lavania, A.A. and Sharma, A. (2009). In vitro comparative screening of antibacterial and antifungal activities of some common plants and weeds extracts. Asian J. Exp. Sci, 23(1), 169-172.
  • [29] Subashini, R. and Rakshitha, S.U. (2012). Phytochemical screening, antimicrobial activity and in vitro antioxidant investigation of methanolic extract of seeds from Helianthus annuus L. Chem. Sci. Rev. Lett., 1(1), 30-34.
  • [30] Bnouham, M., Mekhfi, H., Legssyer, A. and Ziyyat, A. (2002). Ethnopharmacology forum medicinal plants used in the treatment of diabetes in Morocco. Int J Diabetes & Metabolism, 10, 33-50.
  • [31] Visscher, M.O. (2009). Update on the use of topical agents in neonates. Newborn and Infant Nursing Reviews, 9(1), 31-47.
  • [32] Stoia, M. and Oancea, S. (2015). Selected evidence-based health benefits of topically applied sunflower oil. App. Sci. Rep., 10, 45-49.
  • [33] Guo, S., Ge, Y. and Jom, K.N. (2017). A review of phytochemistry, metabolite changes, and medicinal uses of the common sunflower seed and sprouts (Helianthus annuus L.). Chemistry Central Journal, 11(1), 95.
  • [34] Hentzer, M., Riedel, K., Rasmussen, T.B., Heydorn, A., Andersen, J.B., Parsek, M.R., Rice, S.A., Eberl, L., Molin, S., Høiby, M., Kjelleberg, S. and Givskov, M. (2002). Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology, 148(1), 87-102.
  • [35] Yang, L., Barken, K.B., Skindersoe, M.E., Christensen, A.B., Givskov, M. and Tolker-Nielsen, T. (2007). Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology, 153(5), 1318-1328.
  • [36] Yang, L., Rybtke, M. T., Jakobsen, T.H., Hentzer, M., Bjarnsholt, T., Givskov, M. and Tolker-Nielsen, T. (2009). Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrobial Agents and Chemotherapy, 53(6), 2432-2443.
  • [37] Bjarnsholt, T., Jensen, P. Ø., Rasmussen, T. B., Christophersen, L., Calum, H., Hentzer, M., Hougen, H.P., Rygaard, J., Moser, C., Eberl, L., Høiby, N. and Givskov, M. (2005). Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology, 151(12), 3873-3880.
  • [38] Walsh, C. (2003). Antibiotics: actions, origins, resistance. American Society for Microbiology Press, Washington DC, USA.
  • [39] Werner, G., Strommenger, B. and Witte W. (2008). Acquired vancomycin resistance in clinically relevant pathogens. Future Microbiol., 3(5), 547–562.
  • [40] Ventola, C.L. (2015). The antibiotic resistance crisis: part 1: causes and threats. Pharmacy and Therapeutics, 40(4), 277.
  • [41] LaSarre, B., and Federle, M.J. (2013). Exploiting quorum sensing to confuse bacterial pathogens. Microbiol. Mol. Biol. Rev., 77(1), 73-111.
  • [42] Alibe, I.M. and Inuwa, B. (2012). Physicochemical and anti-microbial properties of sunflower (Helianthus annuus L.) seed oil. International Journal of Science and Technology, 2(4), 151-154.
  • [43] Pérez-López, M., Garcia-Contreras, R., Soto-Hernández, M., Rodríguez-Zavala, J.S., Martínez-Vázquez, M., Prado-Galbarro, F.J. and Castillo-Juárez, I. (2018). Antiquorum sensing activity of seed oils from oleaginous plants and protective effect during challenge with Chromobacterium violaceum. Journal of Medicinal Food, 21(4), 356-363.
  • [44] Bone K, Mills, S. (2012). Principles and practice of phytotherapy modern herbal medicine: Dosage and dosage forms in herbal medicine. Churchill Livingstone Elsevier. 2nd ed. 121-133.

Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa

Year 2020, Volume: 32 Issue: 4, 499 - 506, 01.11.2020

Arhun Ali Balkan , Ayla Yıldız , Didem Berber , Barış Gökalsın , Cenk Sesal

https://doi.org/10.7240/jeps.741137

Abstract

Pseudomonas aeruginosa is one of the drug-resistant opportunistic pathogens with the ability to form biofilm and to produce a number of virulence factors via Quorum Sensing (QS) regulation. Most researchers have focused on QS inhibition to overcome the drug resistance problem. QS inhibitor molecules are investigated from natural resources. In the present study, anti-QS activities of ethyl acetate extracts of decoction and infusion samples from Helianthus annuus leaves were tested on biosensor strains of P. aeruginosa (lasB-gfp, rhlA-gfp and pqsA-gfp), as well as anti-biofilm activities on PAO1 wild type. H. annuus leaf samples were firstly infused or decocted and then extracted with ethyl acetate. The efficacies of infusion or decoction extracts were examined at the concentrations of 240, 120, and 60 μg/ml in 96-well microplates and evaluated in Citation 3 multimode microplate reader (Biotek). The inhibition rates of decoction extracts were recorded as 70.61% for las, 44.09% for rhl and 83.77% pqs system at 240 μg/ml. The biofilm inhibition percentages of the extracts were determined to be 50.82% (±1.36). Moreover, inhibition rates for infusion extracts were detected as 62.08% for las, 45.15% for rhl and 77.79% for pqs, and 53.88% (±3.94) for biofilm formation. In conclusion, the potential efficacies of the extracts of decocted or infused H.annuus leaves were demonstrated on QS system and biofilm formation of P. aeruginosa. However, there is a need for more detailed investigations and determination of the active substances that have QSI and anti-biofilm effect.

Keywords

Helianthus annuus las system rhl system pqs system quorum sensing inhibitor anti-biofilm

References

  • [1] Butler, M.S., Blaskovich, M.A. and Cooper, M.A. (2013). Antibiotics in the clinical pipeline in 2013. The Journal of Antibiotics, 66(10), 571-591.
  • [2] Wright, G.D. (2017). Opportunities for natural products in 21 st century antibiotic discovery. Natural Product Reports, 34(7), 694-701.
  • [3] Centres for Disease Control and Prevention (US). (2013). Antibiotic resistance threats in the United States.
  • [4] Pandhare, A. (2015). Bacterial resistance in India: Studying plasma antibiotic levels. Indian Journal of Critical Care Medicine, 19(10), 574.
  • [5] World Health Organization. (2017). Antibacterial agents in clinical development. World Health Organization: Geneva, Switzerland.
  • [6] Rasko, D.A. and Sperandio, V. (2010). Anti-virulence strategies to combat bacteria-mediated disease. Nature Reviews Drug Discovery, 9(2), 117-128.
  • [7] Dickey, S.W., Cheung, G.Y. and Otto, M. (2017). Different drugs for bad bugs: antivirulence strategies in the age of antibiotic resistance. Nature Reviews Drug Discovery, 16(7), 457.
  • [8] Miller, M.B. and Bassler, B.L. (2001). Quorum sensing in bacteria. Annual Reviews in Microbiology, 55(1), 165-199.
  • [9] Smith, R.S. and Iglewski, B.H. (2003). Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. The Journal of Clinical Investigation, 112(10), 1460-1465.
  • [10] Williams, P. and Cámara, M. (2009). Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Current Opinion in Microbiology, 12(2), 182-191.
  • [11] Antunes, L.C.M., Ferreira, R.B., Buckner, M.M. and Finlay, B.B. (2010). Quorum sensing in bacterial virulence. Microbiology, 156(8), 2271-2282.
  • [12] Rutherford, S.T. and Bassler, B.L. (2012). Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspectives in Medicine, 2(11), a012427.
  • [13] Olson, M.E., Ceri, H., Morck, D.W., Buret, A.G. and Read, R.R. (2002). Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can. J. Vet. Res., 66(2): 86.
  • [14] Driscoll, J.A., Brody, S.L. and Kollef, M.H. (2007). The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs, 67(3), 351-368.
  • [15] Lee, J., Wu, J., Deng, Y., Wang, J., Wang, C., Wang, J., Chang, C., Dong, Y., Williams, P. and Zhang, L.H. (2013). A cell-cell communication signal integrates quorum sensing and stress response. Nature Chemical Biology, 9(5), 339.
  • [16] Lee, J. And Zhang, L. (2015). The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein & Cell, 6(1), 26-41.
  • [17] Erickson, D.L., Endersby, R., Kirkham, A., Stuber, K., Vollman, D.D., Rabin, H.R., Mitchell, I. and Storey, D.G. (2002). Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infection and Immunity, 70(4), 1783-1790.
  • [18] Kalia, VC. (2015). Quorum sensing vs quorum quenching: a battle with no end in sight. Springer, New Delhi, India.
  • [19] Yesilyurt, E.B., Simsek, I., Tuncel, T., Akaydın, G. And Yesilada, E. (2017). Marmara Bölgesi’nin bazı yerleşim merkezlerinde halk ilacı olarak kullanılan bitkiler. Marmara Pharmaceutical Journal, 21: 132-148.
  • [20] Bashir, T., Zahara, K., Haider, S. And Tabassum, S. (2015). Chemistry, pharmacology and ethnomedicinal uses of Helianthus annuus (sunflower): a review. Pure and Applied Biology, 4(2), 226.
  • [21] Fowler, M.W. (2006). Plants, medicines and man. Journal of the Science of Food and Agriculture, 86(12), 1797-1804.
  • [22] Karunamoorthi, K., Jegajeevanram, K., Vijayalakshmi, J. and Mengistie, E. (2013). Traditional medicinal plants: a source of phytotherapeutic modality in resource-constrained health care settings. Journal of Evidence-Based Complementary & Alternative Medicine, 18(1), 67-74.
  • [23] Kocabas, A. (2017). Ease of phytochemical extraction and analysis from plants? Anatolian Journal of Botany, 1(2):6-31.
  • [24] Jarić, S., Popović, Z., Mačukanović-Jocić, M., Djurdjević, L., Mijatović, M., Karadžić, B., Mitrovic´, M. and Pavlović, P. (2007). An ethnobotanical study on the usage of wild medicinal herbs from Kopaonik Mountain (Central Serbia). Journal of Ethnopharmacology, 111(1), 160-175.
  • [25] Cepni, E. and Gurel, F. (2011). Bitkilerden elde edilen anti quorum sensing bileşikleri ve yeni ilaç geliştirmedeki potansiyelleri. Turkish Journal of Microbiology, 41 (4):131-138. [26] Al-douri, N.A. (2000). A survey of medicinal plants and their traditional uses in Iraq. Pharmaceutical Biology, 38(1), 74-79.
  • [27] Gaur, R.K., Petrov, N.M., Patil, B.L. and Stoyanova, M.I. (Eds.). (2016). Plant Viruses: Evolution and Management. Springer.
  • [28] Sharma, D., Lavania, A.A. and Sharma, A. (2009). In vitro comparative screening of antibacterial and antifungal activities of some common plants and weeds extracts. Asian J. Exp. Sci, 23(1), 169-172.
  • [29] Subashini, R. and Rakshitha, S.U. (2012). Phytochemical screening, antimicrobial activity and in vitro antioxidant investigation of methanolic extract of seeds from Helianthus annuus L. Chem. Sci. Rev. Lett., 1(1), 30-34.
  • [30] Bnouham, M., Mekhfi, H., Legssyer, A. and Ziyyat, A. (2002). Ethnopharmacology forum medicinal plants used in the treatment of diabetes in Morocco. Int J Diabetes & Metabolism, 10, 33-50.
  • [31] Visscher, M.O. (2009). Update on the use of topical agents in neonates. Newborn and Infant Nursing Reviews, 9(1), 31-47.
  • [32] Stoia, M. and Oancea, S. (2015). Selected evidence-based health benefits of topically applied sunflower oil. App. Sci. Rep., 10, 45-49.
  • [33] Guo, S., Ge, Y. and Jom, K.N. (2017). A review of phytochemistry, metabolite changes, and medicinal uses of the common sunflower seed and sprouts (Helianthus annuus L.). Chemistry Central Journal, 11(1), 95.
  • [34] Hentzer, M., Riedel, K., Rasmussen, T.B., Heydorn, A., Andersen, J.B., Parsek, M.R., Rice, S.A., Eberl, L., Molin, S., Høiby, M., Kjelleberg, S. and Givskov, M. (2002). Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology, 148(1), 87-102.
  • [35] Yang, L., Barken, K.B., Skindersoe, M.E., Christensen, A.B., Givskov, M. and Tolker-Nielsen, T. (2007). Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology, 153(5), 1318-1328.
  • [36] Yang, L., Rybtke, M. T., Jakobsen, T.H., Hentzer, M., Bjarnsholt, T., Givskov, M. and Tolker-Nielsen, T. (2009). Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrobial Agents and Chemotherapy, 53(6), 2432-2443.
  • [37] Bjarnsholt, T., Jensen, P. Ø., Rasmussen, T. B., Christophersen, L., Calum, H., Hentzer, M., Hougen, H.P., Rygaard, J., Moser, C., Eberl, L., Høiby, N. and Givskov, M. (2005). Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology, 151(12), 3873-3880.
  • [38] Walsh, C. (2003). Antibiotics: actions, origins, resistance. American Society for Microbiology Press, Washington DC, USA.
  • [39] Werner, G., Strommenger, B. and Witte W. (2008). Acquired vancomycin resistance in clinically relevant pathogens. Future Microbiol., 3(5), 547–562.
  • [40] Ventola, C.L. (2015). The antibiotic resistance crisis: part 1: causes and threats. Pharmacy and Therapeutics, 40(4), 277.
  • [41] LaSarre, B., and Federle, M.J. (2013). Exploiting quorum sensing to confuse bacterial pathogens. Microbiol. Mol. Biol. Rev., 77(1), 73-111.
  • [42] Alibe, I.M. and Inuwa, B. (2012). Physicochemical and anti-microbial properties of sunflower (Helianthus annuus L.) seed oil. International Journal of Science and Technology, 2(4), 151-154.
  • [43] Pérez-López, M., Garcia-Contreras, R., Soto-Hernández, M., Rodríguez-Zavala, J.S., Martínez-Vázquez, M., Prado-Galbarro, F.J. and Castillo-Juárez, I. (2018). Antiquorum sensing activity of seed oils from oleaginous plants and protective effect during challenge with Chromobacterium violaceum. Journal of Medicinal Food, 21(4), 356-363.
  • [44] Bone K, Mills, S. (2012). Principles and practice of phytotherapy modern herbal medicine: Dosage and dosage forms in herbal medicine. Churchill Livingstone Elsevier. 2nd ed. 121-133.
There are 43 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Arhun Ali Balkan 0000-0002-8836-7469

Ayla Yıldız 0000-0002-8017-4080

Didem Berber 0000-0001-5813-160X

Barış Gökalsın 0000-0001-5060-6834

Cenk Sesal 0000-0002-0737-0122

Publication Date November 1, 2020
Published in Issue Year 2020 Volume: 32 Issue: 4

Cite

APA Balkan, A. A., Yıldız, A., Berber, D., Gökalsın, B., et al. (2020). Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa. International Journal of Advances in Engineering and Pure Sciences, 32(4), 499-506. https://doi.org/10.7240/jeps.741137
AMA Balkan AA, Yıldız A, Berber D, Gökalsın B, Sesal C. Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa. JEPS. November 2020;32(4):499-506. doi:10.7240/jeps.741137
Chicago Balkan, Arhun Ali, Ayla Yıldız, Didem Berber, Barış Gökalsın, and Cenk Sesal. “Infusion or Decoction Extracts of Helianthus Annuus Leaves: Potential Inhibitors for QS System and Biofilm Formation in Pseudomonas Aeruginosa”. International Journal of Advances in Engineering and Pure Sciences 32, no. 4 (November 2020): 499-506. https://doi.org/10.7240/jeps.741137.
EndNote Balkan AA, Yıldız A, Berber D, Gökalsın B, Sesal C (November 1, 2020) Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa. International Journal of Advances in Engineering and Pure Sciences 32 4 499–506.
IEEE A. A. Balkan, A. Yıldız, D. Berber, B. Gökalsın, and C. Sesal, “Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa”, JEPS, vol. 32, no. 4, pp. 499–506, 2020, doi: 10.7240/jeps.741137.
ISNAD Balkan, Arhun Ali et al. “Infusion or Decoction Extracts of Helianthus Annuus Leaves: Potential Inhibitors for QS System and Biofilm Formation in Pseudomonas Aeruginosa”. International Journal of Advances in Engineering and Pure Sciences 32/4 (November 2020), 499-506. https://doi.org/10.7240/jeps.741137.
JAMA Balkan AA, Yıldız A, Berber D, Gökalsın B, Sesal C. Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa. JEPS. 2020;32:499–506.
MLA Balkan, Arhun Ali et al. “Infusion or Decoction Extracts of Helianthus Annuus Leaves: Potential Inhibitors for QS System and Biofilm Formation in Pseudomonas Aeruginosa”. International Journal of Advances in Engineering and Pure Sciences, vol. 32, no. 4, 2020, pp. 499-06, doi:10.7240/jeps.741137.
Vancouver Balkan AA, Yıldız A, Berber D, Gökalsın B, Sesal C. Infusion or Decoction Extracts of Helianthus annuus Leaves: Potential Inhibitors for QS system and Biofilm Formation in Pseudomonas aeruginosa. JEPS. 2020;32(4):499-506.