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Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae'ye karşı sinerjik potansiyeli

Year 2020, Volume: 13 Issue: 3, 371 - 381, 05.12.2020
https://doi.org/10.26559/mersinsbd.718890

Abstract

Amaç: Pelargonium endlicherianum uçucu yağının enfeksiyon tedavilerinde sıklıkla kullanılan benzilpenisilin ile kombine edilerek in vitro deney modeli içerisinde Streptoccus pneumoniae’ye karşı antimikrobiyal etkisinin ortaya çıkarılması ve insan lökosit hücreleri üzerindeki fonksiyonun tespit edilmesi amaçlandı. Yöntem: P. endlicherianum uçucu yağının benzilpenisilin ile kombine kullanımının Streptococcus pneumoniae’ye karşı antimikrobiyal etkisi agar difüzyon tekniği kullanılarak ve lökosit hücreleri üzerindeki fagositik fonksiyonları in vitro hücre deney modeli içinde insan lökosit hücresi WBC 264-9C ATCC HB-8902 kullanılarak ortaya çıkarılmıştır. P. endlicherianum uçucu yağ ve benzilpenisilinin bakterisidal etkisi zamana bağlı öldürme yöntemi ile zamana ve antibiyotik yoğunluğuna bağlı olarak dinamik olarak ortaya konuldu. Uçucu yağın tek başına ve antibiyotik ile kombine kullanıldığında bakteriyel dış membrandaki geçirgenliği U.V. spektrofotometre ve morfolojik görüntüsü taramalı elektron mikroskobu ile analiz edildi. Bulgular: Tedavi sonrası 24. saatte, ilaç kombinasyonu sadece uçucu yağ tedavisi ile karşılaştırıldığında, yaşayabilir hücre sayısında azalma olduğu gözlendi. Uçucu yağ+antibiyotik kombinasyonlarında uçucu yağ ve antibiyotik arasında sinerjizm gözlenmiş olup, lökosit hücrelerinin fagositik aktivitesi artarak canlı bakteri sayısında belirgin bir düşüş belirlendi. Sonuç: Çalışmanın sonuçlarına göre S. pneumoniae’ye karşı kullanılan benzilpenisilinin P. endlicherianum uçucu yağı ile kombine kullanımı sonucu antibiyotik etkinliğinin arttığı ve böylece bakterilerin antibiyotiklere karşı direnç geliştirmesi engellenerek etkin bir tedavi sağlanabileceği gösterilmiştir.

Supporting Institution

Türkiye Bilimsel ve Teknolojik Araştırma Kurumu (TUBİTAK)

Project Number

216S666

Thanks

Bu çalışmada, 216S666 projesine mali destek sağladığı için Türkiye Bilimsel ve Teknolojik Araştırma Kurumu'na (TÜBİTAK) teşekkür ederiz. Çalışmamıza istatiksel olarak destek sağlayan Eda Merve Kurtuluş’a teşekkür ederiz.

References

  • 1. Ayaz C. Antibiyotik Kombinasyonları. Klimik Dergisi. 2001; 14(3): 140-143.
  • 2. Moellering RC Jr. Principles of antiinfective therapy. In: Mandell GL, Douglas RG, Bennett JE, Eds., Principles and Practice of Infectious Diseases, 4th Ed., New York: Churchill Livingstone, 1995: 199-212.
  • 3. Uzun Ö. Birden fazla antibiyotikle tedavi ilkeleri. Medikal Magazin. 1993; 91 (1993): 74-76.
  • 4. Çolak H. Ampirik antibiyotik tedavisi: genel ilkeler. In: Tümbay E, Ünci R, Hilmioğlu S, Eds., Antimikrobik Kemoterapi Günleri: Klinik-Laboratuvar Uygulamaları ve Yenilikler 3rd. Ed., İstanbul: Türk Mikrobiyoloji Cemiyeti Yayınları. 1997; 31: 26-29.
  • 5. Adrar N, Oukil N, Bedjou F. Antioxidant and antibacterial activities of Thymus numidicus and Salvia officinalis essential oils alone or in combination. Ind Crops Prod. 88 (2016):112-119. https://doi.org/10.1016/j.indcrop.2015.12.007
  • 6. Yap PSX, Lim SHE, Hu CP, Yiap BC. Combination of essential oils and antibiotics reduce antibiotic resistance in plasmid-conferred multidrug resistant bacteria. Phytomedicine. 2013;20(8-9):710-713. doi: 10.1016/j.phymed.2013.02.013
  • 7. Kwiatkowski P, Mnichowska-Polanowska M, Pruss A, Masiuk H. The effect of fennel essential oil in combination with antibiotics on Staphylococcus aureus strains isolated from carriers. Burns. 2017;43(7):1544-1551. https://doi.org/10.1016/j.burns.2017.04.014
  • 8. Williams CA, Harborne JB. Phytochemistry of the genus Pelargonium. In: Lis-BalchinMEd., Geranium and Pelargonium, 1st Ed., London: Taylor and Francis; 2002: 5-7.
  • 9. Lis-Balchin M. A Guide for Healthcare.Professionals Aromatherapy Science, 1st Ed., London: Pharmaceutical Press; 2006: 196-199.
  • 10. Bozan B, Ozek T, Kürkcüoğlu M, Kırımer N, Başer KHC. The analysis of essential oil and headspace volatiles of the flowers of Pelargonium endlicherianum used as an anthelminthic in folk medicine. Planta Med. 1999;65(8):781-782. doi: 10.1055/s-2006-960872
  • 11. Şeker Karatoprak G, Göger F, Yerer MB, Koşar M. Chemical composition and biological investigation of Pelargonium endlicherianum root extracts. Pharm Biol. 2017;55(1):1608-1618. https://doi.org/10.1080/13880209.2017.1314511
  • 12. Dumlupinar B, Karatoprak G., Celik DD, Gürer ÜS, Demirci B, Gürbüz B, Rayaman P, Kurtulus EM. Synergic potential of Pelargonium endlicherianum Fenzl. Essential oil and antibiotic combinations against Klebsiella pneumoniae. S Afr J Bot. 2020;135:117-126.
  • 13. Kirbağ S, Zengin F, Kursat M. Antimicrobial activities of extracts of some plants. Pak J Bot. 2009;41(4):2067-2070.
  • 14. CLSI, M100-S17; Antibiyotik Duyarlılık testleri için Uygulama Standartları; On yedinci Bilgi Eki. Ankara: Bilimsel Tıp Kitabevi;2007.
  • 15. EUCAST Version 8.0. The European Committee on Antimicrobial Susceptibility Testing. Routine and extended internal quality control for MIC determination and disk diffusion as recommended by http://www.eucast.org. 2018.
  • 16. Yin X, Knecht DA, Lynes MA. Metallothionein mediates leukocyte chemotaxis. BMC Immunol. 2005; 15:6-21. doi: 10.1186/1471-2172-6-21
  • 17. Novelli A, Fallani S, Cassetta MI, Contı S, Mazzei T. Postantibiotic Leukocyte Enhancement of Meropenem against Gram-Positive and Gram-Negative Strains. Antimicrob Agents Chemother. 2000;44(11):3174–3176. doi: 10.1128/AAC.44.11.3174-3176.2000
  • 18. Pruul H, McDonald PJ. Enhancement of Leukocyte Activity Against Escherichia coli After Brief Exposure to Chloramphenicol. Antimicrob Agents Chemother. 1979;16(6):695-700. doi: 10.1128/aac.16.6.695
  • 19. Davis PH, Hedge IC. Pelargonium L’Hérit In: Flora of Turkey and the East Aegean Islands. University Press, Edinburgh. 1967;2:487-489.
  • 20. Pereira V, Dias C, Vasconcelos MC, Rosa E, Saavedraa MJ. Antibacterial activity and synergistic effects between Eucalyptus globulus leaf residues (essential oils and extracts) and antibiotics against several isolates of respiratory tractinfections (Pseudomonas aeruginosa). Ind Crops Prod. 2014;52:1-7. https://doi.org/10.1016/j.indcrop.2013.09.032
  • 21. Alma MH, Nitz S, Kollmannsberger H, Digrak M, Efe FT, Yilmaz N. Chemical Composition and Antimicrobial Activity of the Essential Oils from the Gum of Turkish Pistachio (Pistacia veraL.). J Agric Food Chem. 2004;52(12): 3911–3914. doi: 10.1021/jf040014e
  • 22. Brehm-Stecher BF and Johnson EA. Sensitization of Staphylococcus aureus and Escherichia coli to Antibiotics by the Sesquiterpenoids Nerolidol, Farnesol, Bisabolol, and Apritone. Antimicrob Agents Chemother. 2003;47(10):3357–3360. doi: 10.1128/AAC.47.10.3357-3360.2003
  • 23. Pepeljnjak S, Kosalec I, Kaloera Z, Blazevıc N. Antimicrobial activity of juniper berry essential oil (Juniperus communis L., Cupressaceae). Acta Pharm. 2005;55 (4):417-422.
  • 24. Al Maqtari MAA, Alghalibi SM, Alhamzy EH. Chemical composition and antimicrobial activity of essential oil of Thymus vulgaris from Yemen. Turk Biyokim Derg. 2011;36 (4):342–349.
  • 25. Borges A, Ferreira C, Saavedra MJ. Simoes M. Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb Drug Resist. 2013;19(4):256-265. https://doi.org/10.1089/mdr.2012.0244
  • 26. Gerber AU, Bruddger UHP, Feller C, Stritzko T, Stalder B. Antibiotic therapy of infections due to Pseudomonas aeruginosa in normal and granulocytopenic mice: comparison of murine and human pharmacokinetics. International of Infectious Disease. 1986;153(1):90–97. doi:10.1093/infdis/153.1.90
  • 27. Macheboeuf P, Contreras-Martel C, Job V, Dideberg O, Dessen A. Penicillin binding proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol Rev. 2006;30(5):673-691. https://doi.org/10.1111/j.1574-6976.2006.00024.x
  • 28. Gilbert P, Evans DJ, Evans E, Duguid IG, Brown MR. Surface characteristics and adhesion of Escherichia coli and Staphylococcus epidermidis. J Appl Bacteriol. 1991;71:72-77. https://doi.org/10.1111/j.1365-2672.1991.tb04665.x
  • 29. Bryan LE, Godfrey AJ. β-Lactam antibiotics: mode of action and bacterial resistance. In Antibiotics in Laboratory Medicine. 3rd edn (Lorian, V. Ed.), 1991; 599-664. Williams & Wilkins, Baltimore, MD.
  • 30. Carson CF, Mee BJ, Riley TV. Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob Agents Chemother. 2002;46(6):1914-1920. doi: 10.1128/AAC.46.6.1914-1920.2 002
  • 31. Hemaiswarya S, Doble M. Synergistic interaction of eugenol with antibiotics against Gram negative bacteria. Phytomedicine. 2009;16(11):997-1005. https://doi.org/10.1016/j.phymed.2009.04.006
  • 32. Luqman S, Dwivedi GR, Darokar MP, Kalra A, Khanuja SP. Potential of rosemary oil to be used in drug-resistant infections. Altern Ther Health Med. 2007;13(5):54-59.
  • 33. Su JY, Zhu L, Tian YJ. Chemical composition and antimicrobial activities of essential oil of Matricaria songarica. Int J Agric Biol. 2012;14(1):107-110.
  • 34. Sikkema J, de Bont JAM, Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev. 1995;59(2):201–222.
  • 35. Hammer KA, Carson CF, Riley TV. Antifungal effects of Melaleuca alternifolia (tea tree) oil and its components on Candida albicans, Candida glabrata and Saccharomyces cerevisiae. J Antimicrob Chemother. 2004;53(6):1081–1085. DOI: 10.1093/jac/dkh243

Synergic potential of pelargonium endlicherianum fenzl. essential oil and penicillin combination against streptoccus pneumoniae

Year 2020, Volume: 13 Issue: 3, 371 - 381, 05.12.2020
https://doi.org/10.26559/mersinsbd.718890

Abstract

Aim: The main aim of the study is to combine Pelargonium endlicherianum essential oil with benzylpenicillin used in the treatment of infection, revealing the antimicrobial effect against S. pneumoniae in human in vitro experimental model and its functions on human leukocyte cells. Method: The antimicrobial effect of the use of P. endlicherianum essential oil combined with benzylpenicillin against Streptococcus pneumoniae was demonstrated using agar diffusion technique and its phagocytic functions on leukocyte cells in an in vitro cell assay model using the human leukocyte cell WBC 264-9C ATCC HB-8902. Bactericidal effect of essential oil and antibiotic combination was dynamically detected by the method of Time Kill assay, was analyzed by U.V spectrophotometer and morphologic images was analysed by scanning electron microscopy. Results: A reduction in the number of viable cells was observed at 24 hours after treatment, when the drug combination was compared only with essential oil treatment. In essential oil + antibiotic combination, synergism was observed between essential oil and antibiotic, and the phagocytic activity of leukocyte cells increased, and a significant decrease in the number of live bacteria was determined. Conclusion: According to the results, the use of benzylpenicillin, which are used in infection treatments, together with a phytochemical P. endlicherianum essential oil, increases the effectiveness of antibiotic and thus, it has been shown that an effective treatment can be achieved by preventing bacteria from developing resistance to antibiotics.

Project Number

216S666

References

  • 1. Ayaz C. Antibiyotik Kombinasyonları. Klimik Dergisi. 2001; 14(3): 140-143.
  • 2. Moellering RC Jr. Principles of antiinfective therapy. In: Mandell GL, Douglas RG, Bennett JE, Eds., Principles and Practice of Infectious Diseases, 4th Ed., New York: Churchill Livingstone, 1995: 199-212.
  • 3. Uzun Ö. Birden fazla antibiyotikle tedavi ilkeleri. Medikal Magazin. 1993; 91 (1993): 74-76.
  • 4. Çolak H. Ampirik antibiyotik tedavisi: genel ilkeler. In: Tümbay E, Ünci R, Hilmioğlu S, Eds., Antimikrobik Kemoterapi Günleri: Klinik-Laboratuvar Uygulamaları ve Yenilikler 3rd. Ed., İstanbul: Türk Mikrobiyoloji Cemiyeti Yayınları. 1997; 31: 26-29.
  • 5. Adrar N, Oukil N, Bedjou F. Antioxidant and antibacterial activities of Thymus numidicus and Salvia officinalis essential oils alone or in combination. Ind Crops Prod. 88 (2016):112-119. https://doi.org/10.1016/j.indcrop.2015.12.007
  • 6. Yap PSX, Lim SHE, Hu CP, Yiap BC. Combination of essential oils and antibiotics reduce antibiotic resistance in plasmid-conferred multidrug resistant bacteria. Phytomedicine. 2013;20(8-9):710-713. doi: 10.1016/j.phymed.2013.02.013
  • 7. Kwiatkowski P, Mnichowska-Polanowska M, Pruss A, Masiuk H. The effect of fennel essential oil in combination with antibiotics on Staphylococcus aureus strains isolated from carriers. Burns. 2017;43(7):1544-1551. https://doi.org/10.1016/j.burns.2017.04.014
  • 8. Williams CA, Harborne JB. Phytochemistry of the genus Pelargonium. In: Lis-BalchinMEd., Geranium and Pelargonium, 1st Ed., London: Taylor and Francis; 2002: 5-7.
  • 9. Lis-Balchin M. A Guide for Healthcare.Professionals Aromatherapy Science, 1st Ed., London: Pharmaceutical Press; 2006: 196-199.
  • 10. Bozan B, Ozek T, Kürkcüoğlu M, Kırımer N, Başer KHC. The analysis of essential oil and headspace volatiles of the flowers of Pelargonium endlicherianum used as an anthelminthic in folk medicine. Planta Med. 1999;65(8):781-782. doi: 10.1055/s-2006-960872
  • 11. Şeker Karatoprak G, Göger F, Yerer MB, Koşar M. Chemical composition and biological investigation of Pelargonium endlicherianum root extracts. Pharm Biol. 2017;55(1):1608-1618. https://doi.org/10.1080/13880209.2017.1314511
  • 12. Dumlupinar B, Karatoprak G., Celik DD, Gürer ÜS, Demirci B, Gürbüz B, Rayaman P, Kurtulus EM. Synergic potential of Pelargonium endlicherianum Fenzl. Essential oil and antibiotic combinations against Klebsiella pneumoniae. S Afr J Bot. 2020;135:117-126.
  • 13. Kirbağ S, Zengin F, Kursat M. Antimicrobial activities of extracts of some plants. Pak J Bot. 2009;41(4):2067-2070.
  • 14. CLSI, M100-S17; Antibiyotik Duyarlılık testleri için Uygulama Standartları; On yedinci Bilgi Eki. Ankara: Bilimsel Tıp Kitabevi;2007.
  • 15. EUCAST Version 8.0. The European Committee on Antimicrobial Susceptibility Testing. Routine and extended internal quality control for MIC determination and disk diffusion as recommended by http://www.eucast.org. 2018.
  • 16. Yin X, Knecht DA, Lynes MA. Metallothionein mediates leukocyte chemotaxis. BMC Immunol. 2005; 15:6-21. doi: 10.1186/1471-2172-6-21
  • 17. Novelli A, Fallani S, Cassetta MI, Contı S, Mazzei T. Postantibiotic Leukocyte Enhancement of Meropenem against Gram-Positive and Gram-Negative Strains. Antimicrob Agents Chemother. 2000;44(11):3174–3176. doi: 10.1128/AAC.44.11.3174-3176.2000
  • 18. Pruul H, McDonald PJ. Enhancement of Leukocyte Activity Against Escherichia coli After Brief Exposure to Chloramphenicol. Antimicrob Agents Chemother. 1979;16(6):695-700. doi: 10.1128/aac.16.6.695
  • 19. Davis PH, Hedge IC. Pelargonium L’Hérit In: Flora of Turkey and the East Aegean Islands. University Press, Edinburgh. 1967;2:487-489.
  • 20. Pereira V, Dias C, Vasconcelos MC, Rosa E, Saavedraa MJ. Antibacterial activity and synergistic effects between Eucalyptus globulus leaf residues (essential oils and extracts) and antibiotics against several isolates of respiratory tractinfections (Pseudomonas aeruginosa). Ind Crops Prod. 2014;52:1-7. https://doi.org/10.1016/j.indcrop.2013.09.032
  • 21. Alma MH, Nitz S, Kollmannsberger H, Digrak M, Efe FT, Yilmaz N. Chemical Composition and Antimicrobial Activity of the Essential Oils from the Gum of Turkish Pistachio (Pistacia veraL.). J Agric Food Chem. 2004;52(12): 3911–3914. doi: 10.1021/jf040014e
  • 22. Brehm-Stecher BF and Johnson EA. Sensitization of Staphylococcus aureus and Escherichia coli to Antibiotics by the Sesquiterpenoids Nerolidol, Farnesol, Bisabolol, and Apritone. Antimicrob Agents Chemother. 2003;47(10):3357–3360. doi: 10.1128/AAC.47.10.3357-3360.2003
  • 23. Pepeljnjak S, Kosalec I, Kaloera Z, Blazevıc N. Antimicrobial activity of juniper berry essential oil (Juniperus communis L., Cupressaceae). Acta Pharm. 2005;55 (4):417-422.
  • 24. Al Maqtari MAA, Alghalibi SM, Alhamzy EH. Chemical composition and antimicrobial activity of essential oil of Thymus vulgaris from Yemen. Turk Biyokim Derg. 2011;36 (4):342–349.
  • 25. Borges A, Ferreira C, Saavedra MJ. Simoes M. Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb Drug Resist. 2013;19(4):256-265. https://doi.org/10.1089/mdr.2012.0244
  • 26. Gerber AU, Bruddger UHP, Feller C, Stritzko T, Stalder B. Antibiotic therapy of infections due to Pseudomonas aeruginosa in normal and granulocytopenic mice: comparison of murine and human pharmacokinetics. International of Infectious Disease. 1986;153(1):90–97. doi:10.1093/infdis/153.1.90
  • 27. Macheboeuf P, Contreras-Martel C, Job V, Dideberg O, Dessen A. Penicillin binding proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol Rev. 2006;30(5):673-691. https://doi.org/10.1111/j.1574-6976.2006.00024.x
  • 28. Gilbert P, Evans DJ, Evans E, Duguid IG, Brown MR. Surface characteristics and adhesion of Escherichia coli and Staphylococcus epidermidis. J Appl Bacteriol. 1991;71:72-77. https://doi.org/10.1111/j.1365-2672.1991.tb04665.x
  • 29. Bryan LE, Godfrey AJ. β-Lactam antibiotics: mode of action and bacterial resistance. In Antibiotics in Laboratory Medicine. 3rd edn (Lorian, V. Ed.), 1991; 599-664. Williams & Wilkins, Baltimore, MD.
  • 30. Carson CF, Mee BJ, Riley TV. Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob Agents Chemother. 2002;46(6):1914-1920. doi: 10.1128/AAC.46.6.1914-1920.2 002
  • 31. Hemaiswarya S, Doble M. Synergistic interaction of eugenol with antibiotics against Gram negative bacteria. Phytomedicine. 2009;16(11):997-1005. https://doi.org/10.1016/j.phymed.2009.04.006
  • 32. Luqman S, Dwivedi GR, Darokar MP, Kalra A, Khanuja SP. Potential of rosemary oil to be used in drug-resistant infections. Altern Ther Health Med. 2007;13(5):54-59.
  • 33. Su JY, Zhu L, Tian YJ. Chemical composition and antimicrobial activities of essential oil of Matricaria songarica. Int J Agric Biol. 2012;14(1):107-110.
  • 34. Sikkema J, de Bont JAM, Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev. 1995;59(2):201–222.
  • 35. Hammer KA, Carson CF, Riley TV. Antifungal effects of Melaleuca alternifolia (tea tree) oil and its components on Candida albicans, Candida glabrata and Saccharomyces cerevisiae. J Antimicrob Chemother. 2004;53(6):1081–1085. DOI: 10.1093/jac/dkh243
There are 35 citations in total.

Details

Primary Language Turkish
Subjects Health Care Administration
Journal Section Articles
Authors

Berrak Dumlupınar 0000-0002-0898-3043

Gökçe Şeker Karatoprak 0000-0001-5829-6914

Project Number 216S666
Publication Date December 5, 2020
Submission Date April 12, 2020
Acceptance Date October 10, 2020
Published in Issue Year 2020 Volume: 13 Issue: 3

Cite

APA Dumlupınar, B., & Şeker Karatoprak, G. (2020). Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae’ye karşı sinerjik potansiyeli. Mersin Üniversitesi Sağlık Bilimleri Dergisi, 13(3), 371-381. https://doi.org/10.26559/mersinsbd.718890
AMA Dumlupınar B, Şeker Karatoprak G. Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae’ye karşı sinerjik potansiyeli. Mersin Univ Saglık Bilim derg. December 2020;13(3):371-381. doi:10.26559/mersinsbd.718890
Chicago Dumlupınar, Berrak, and Gökçe Şeker Karatoprak. “Pelargonium Endlicherianum Fenzl. Uçucu yağı Ve Penisilin kombinasyonlarının Streptoccus pneumoniae’ye karşı Sinerjik Potansiyeli”. Mersin Üniversitesi Sağlık Bilimleri Dergisi 13, no. 3 (December 2020): 371-81. https://doi.org/10.26559/mersinsbd.718890.
EndNote Dumlupınar B, Şeker Karatoprak G (December 1, 2020) Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae’ye karşı sinerjik potansiyeli. Mersin Üniversitesi Sağlık Bilimleri Dergisi 13 3 371–381.
IEEE B. Dumlupınar and G. Şeker Karatoprak, “Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae’ye karşı sinerjik potansiyeli”, Mersin Univ Saglık Bilim derg, vol. 13, no. 3, pp. 371–381, 2020, doi: 10.26559/mersinsbd.718890.
ISNAD Dumlupınar, Berrak - Şeker Karatoprak, Gökçe. “Pelargonium Endlicherianum Fenzl. Uçucu yağı Ve Penisilin kombinasyonlarının Streptoccus pneumoniae’ye karşı Sinerjik Potansiyeli”. Mersin Üniversitesi Sağlık Bilimleri Dergisi 13/3 (December 2020), 371-381. https://doi.org/10.26559/mersinsbd.718890.
JAMA Dumlupınar B, Şeker Karatoprak G. Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae’ye karşı sinerjik potansiyeli. Mersin Univ Saglık Bilim derg. 2020;13:371–381.
MLA Dumlupınar, Berrak and Gökçe Şeker Karatoprak. “Pelargonium Endlicherianum Fenzl. Uçucu yağı Ve Penisilin kombinasyonlarının Streptoccus pneumoniae’ye karşı Sinerjik Potansiyeli”. Mersin Üniversitesi Sağlık Bilimleri Dergisi, vol. 13, no. 3, 2020, pp. 371-8, doi:10.26559/mersinsbd.718890.
Vancouver Dumlupınar B, Şeker Karatoprak G. Pelargonium endlicherianum fenzl. uçucu yağı ve penisilin kombinasyonlarının streptoccus pneumoniae’ye karşı sinerjik potansiyeli. Mersin Univ Saglık Bilim derg. 2020;13(3):371-8.

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