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YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI

Year 2023, Volume: 48 Issue: 3, 575 - 586, 16.06.2023
https://doi.org/10.15237/gida.GD22112

Abstract

Çanakkale semt pazarlarında satılan 96 adet yeşil sebze örneğinde “beta laktam” dirençli Enterobacterales suşlarının varlığı araştırılmıştır. Gövde, yaprak kısımlarından alınan örneklerden Violet Red Bile Glucose (VRBG) Agara ekilmiştir. Enterobacterales yükleri <1 log KOB/g ile 6.11 log KOB/g arasında tespit edilmiştir. Kromojenik GSBL Agar ve 2 mg/ml meropenem içeren EMB Agarda üreyen 129 adet izolat MALDI-TOF MS yöntemine göre Serratia liquefaciens (n=35), Serratia plymuthica (n=31), Klebsiella oxytoca (n=25), Klebsiella pneumonia (n=6), Raoultella ornithinolytica (n=14), Raoultella terrigena (n=3), Enterobacter cloacae (n=11), Enterobacter ludwigii (n=4), Enterobacter asburiae (n=1), Lelliottia amnigena (n=16), Escherichia coli (n=2), Escherichia hermannii (n=1), Leclercia adecarboxylata (n=3), Pantoea agglomerans (n=3), Kluyvera intermedia (n=2), Kosakonia cowanii (n=1) ve Hafnia alvei (n=1) olarak tanımlanmıştır. Disk difüzyon yöntemine göre izolatların %11.62’sinin (n=15) Genişlemiş Spektrumlu “Beta Laktamaz” (GSBL), %4.65’inin (n=6) karbapenemaz pozitif olduğu belirlenmiştir. Yeşil sebzelerde GSBL ve karbapenem dirençli izolatların varlığı ısıl işlem görmeden tüketilen bu gıdalardaki halk sağlığı riskini ortaya koymaktadır.

Supporting Institution

Çanakkale Onsekiz Mart Üniversitesi

Project Number

FYL-2019-2808

References

  • Anonim, (2011). Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği, 29 Aralık 2011/ Resmî Gazete Sayı : 28157.
  • Alves, M. S., Pereira, A., Araújo, S. M., Castro, B. B., Correia, A., & Henriques, I. (2014). Seawater is a reservoir of multi-resistant Escherichia coli, including strains hosting plasmid-mediated quinolones resistance and extended-spectrum beta-lactamases genes. Frontiers in microbiology, 5, 426.
  • Ayçiçek, H., Oguz, U., ve Karci, K. (2006). Determination of total aerobic and indicator bacteria on some raw eaten vegetables from wholesalers in Ankara, Turkey. International Journal of Hygiene and Environmental Health, 209(2), 197- 201.
  • Bain, R., Cronk, R., Hossain, R., Bonjour, S., Onda, K., Wright, J., Yang, H., Slaymaker, T., Hunter, P., Prüss-Ustün, A., and Bartram, J. (2014). Global assessment of exposure to faecal contamination through drinking water based on a systematic review. Tropical Medicine & International Health, 19(8), 917-927.
  • Ben Sallem, R., Ben Slama, K., Sáenz, Y., Rojo-Bezares, B., Estepa, V., Jouini, A., ... & Torres, C. (2012). Prevalence and characterization of extended-spectrum beta-lactamase (ESBL)–and CMY-2–producing Escherichia coli isolates from healthy food-producing animals in Tunisia. Foodborne pathogens and disease, 9(12), 1137-1142.
  • Blaak, H., van Hoek, A. H., Veenman, C., van Leeuwen, A. E. D., Lynch, G., van Overbeek, W. M., & de Roda Husman, A. M. (2014). Extended spectrum ß-lactamase-and constitutively AmpC-producing Enterobacteriaceae on fresh produce and in the agricultural environment. International journal of food microbiology, 168, 8-16.
  • Cordeiro-Araújo, M. K., Chia, M. A., Hereman, T. C., Sasaki, F. F., & do Carmo Bittencourt-Oliveira, M. (2015). Selective membrane permeability and peroxidase activity response of lettuce and arugula irrigated with cyanobacterial-contaminated water. Environmental Earth Sciences, 74(2), 1547-1553.
  • Boehme, S., Werner, G., Klare, I., Reissbrodt, R., & Witte, W. (2004). Occurrence of antibiotic‐resistant enterobacteria in agricultural foodstuffs. Molecular nutrition & food research, 48(7), 522-531.
  • Budak, S., Aktaş, Z., & Erdem, H. (2012). Enterik Gram-negatif bakterilerde laboratuvardan kliniğe karbapenemazlar. Mediterranean Journal of Infection Microbes and Antimicrobials, 1, 1-11.
  • Coudron, P. E. (2005). Inhibitor-based methods for detection of plasmid-mediated AmpC β-lactamases in Klebsiella spp., Escherichia coli, and Proteus mirabilis. Journal of clinical microbiology, 43(8), 4163-4167.
  • Demirer, B. ve Özdemir M. 2021. "Gıdalardaki Antibiyotik Kalıntıları." Academic Platform Journal of Halal Lifestyle 3.1: 17-25.
  • Edelstein, M., Sundborger, C., Hergens, M. P., Ivarsson, S., Dryselius, R., Insulander, M., . & Wallensten, A. (2014). Barriers to trace-back in a salad-associated EHEC outbreak, Sweden, June 2013. PLoS currents, 6.
  • EUCAST. 2022. European Committee on Antimicrobial Susceptibility Testing breakpoint tables for interpretation of MICs and zone diameters, version 7.1. https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_12.0_Breakpoint_Tables.pdf
  • Giske, CG., Gezelius, L., Samuelsen, O., Warner, M., Sundsfjord, A., Woodford, N., 2011. A sensitive and specific phenotypic assay for detection of metallo-βlactamases and KPC in Klebsiella pneumoniae with the use of meropenem disks supplemented with aminophenylboronic acid, dipicolinic acid and cloxacillin. Clin Microbiol Infect. 17(4):552-6.
  • O'Flaherty, E., Solimini, A. G., Pantanella, F., De Giusti, M., & Cummins, E. (2019). Human exposure to antibiotic resistant-Escherichia coli through irrigated lettuce. Environment international, 122, 270-280.
  • Hamilton-Miller, J. M. T., & Shah, S. (2001). Identity and antibiotic susceptibility of enterobacterial flora of salad vegetables. International journal of antimicrobial agents, 18(1), 81-83.
  • Hudson, J. A., Frewer, L. J., Jones, G., Brereton, P. A., Whittingham, M. J., & Stewart, G. (2017). The agri-food chain and antimicrobial resistance: A review. Trends in Food Science & Technology, 69, 131-147.
  • Franz, E., Semenov, A. V., & van Bruggen, A. H. C. (2009). Modelling the contamination of lettuce with Escherichia coli O157: H7 from manure-amended soil and the effect of intervention strategies (vol 105, pg 1569, 2008). Journal of Applied Microbiology, 106(5), 1761-1761.
  • Gupta, G., Tak, V., & Mathur, P. (2014). Detection of AmpC β lactamases in gram-negative bacteria. Journal of laboratory physicians, 6, 1-6. Jiang, X., & Shepherd, M. (2009). The role of manure and compost in produce safety. Microbial safety of fresh produce, 143. Sagoo, S. K., C. L. Little, and R. T. Mitchell. 2003. Microbiological quality of open ready-to-eat salad vegetables: effectiveness of food hygiene training of management. J. Food Prot. 66:1581–1586.
  • Smalla K., Blau K., Bettermann A., Jechalke S., Fornefeld E., Vanrobaeys Y., Stalder T., Top Em., 2018. Joint press release of the Julius Kühn Institute (JKI) and the BfR on a study of antimicrobial-resistant bacteria with multiple transferable resistance genes on fresh produce The transferable resistome of produce, mBio 9:e01300-18.
  • Liu, B. T., and Song, F. J. (2019). Emergence of two Escherichia coli strains co-harboring mcr-1 and blaNDM in fresh vegetables from China. Infection and Drug Resistance, 12, 2627.
  • McManus, P. S. (2014). Does a drop in the bucket make a splash? Assessing the impact of antibiotic use on plants. Current opinion in microbiology, 19, 76-82.
  • Njage, P. M., & Buys, E. M. (2015). Pathogenic and commensal E scherichia coli from irrigation water show potential in transmission of extended spectrum and AmpC β‐lactamases determinants to isolates from lettuce. Microbial biotechnology, 8(3), 462-473.
  • Nordmann, P., & Poirel, L. (2002). Emerging carbapenemases in Gram-negative aerobes. Clinical Microbiology and Infection, 8(6), 321-331.
  • Nousiainen, L. L., Joutsen, S., Lunden, J., Hänninen, M. L., & Fredriksson-Ahomaa, M. (2016). Bacterial quality and safety of packaged fresh leafy vegetables at the retail level in Finland. International journal of food microbiology, 232, 73-79.
  • Poeta, P., Radhouani, H., Pinto, L., Martinho, A., Rego, V., Rodrigues, R., ... & Igrejas, G. (2009). Wild boars as reservoirs of extended‐spectrum beta‐lactamase (ESBL) producing Escherichia coli of different phylogenetic groups. Journal of basic microbiology, 49(6), 584-588.
  • Poirel, L., Naas, T., Guibert, M., Chaibi, E. B., Labia, R., & Nordmann, P. (1999). Molecular and biochemical characterization of VEB-1, a novel class A extended-spectrum β-lactamase encoded by an Escherichia coli integron gene. Antimicrobial agents and chemotherapy, 43(3), 573-581.
  • Rico, H., Gozalbo, D., Sebastiá, C., & Falomir, M. P. (2003). Enterobacter cloacae in fresh vegetables: A potential carrier of antibiotic resistances to consumers. Food Studies: Interdiscipl J 2: 1–8.
  • Said, L. B., Jouini, A., Klibi, N., Dziri, R., Alonso, C. A., Boudabous, A., ... & Torres, C. (2015). Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia. International journal of food microbiology, 203, 86-92.
  • Szczech, M., Kowalska, B., Smolińska, U., Maciorowski, R., Oskiera, M., & Michalska, A. (2018). Microbial quality of organic and conventional vegetables from Polish farms. International journal of food microbiology, 286, 155-161.
  • Taormina, P. J., & Beuchat, L. R. (1999). Comparison of chemical treatments to eliminate enterohemorrhagic Escherichia coli O157: H7 on alfalfa seeds. Journal of food protection, 62(4), 318-324.
  • Tan, T. Y., Ng, L. S. Y., He, J., Koh, T. H., & Hsu, L. Y. (2009). Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. Antimicrobial agents and chemotherapy, 53(1), 146-149.
  • Thanner, S., Drissner, D., and Walsh, F. (2016). Antimicrobial resistance in agriculture. MBio 7 (2): e02227–e02215.
  • Tien, Y. C., Li, B., Zhang, T., Scott, A., Murray, R., Sabourin, L., ... & Topp, E. (2017). Impact of dairy manure pre-application treatment on manure composition, soil dynamics of antibiotic resistance genes, and abundance of antibiotic-resistance genes on vegetables at harvest. Science of the Total Environment, 581, 32-39.
  • Van Hoek, A. H., Veenman, C., van Overbeek, W. M., Lynch, G., de Roda Husman, A. M., & Blaak, H. (2015). Prevalence and characterization of ESBL-and AmpC-producing Enterobacteriaceae on retail vegetables. International journal of food microbiology, 204, 1-8.
  • Xylia, P., Botsaris, G., Chrysargyris, A., Skandamis, P., & Tzortzakis, N. (2019). Variation of microbial load and biochemical activity of ready-to-eat salads in Cyprus as affected by vegetable type, season, and producer. Food microbiology, 83, 200-210.

INVESTIGATION OF EXTENDED SPECTRUM BETA-LACTAMASE AND CARBAPENEMASE PRODUCING ENTEROBACTERALES STRAINS IN GREEN VEGETABLES

Year 2023, Volume: 48 Issue: 3, 575 - 586, 16.06.2023
https://doi.org/10.15237/gida.GD22112

Abstract

The presence of beta-lactam resistant Enterobacterales strains was investigated in 96 green vegetable samples sold in Çanakkale neighborhood markets. Samples taken from stem and leaf parts were inoculated in Violet Red Bile Glucose (VRBG) Agar. Enterobacterales loads were determined between <1 log CFU/g and 6.11 log CFU/g. One hundred twenty-nine isolates grown on EMB Agar containing 2 mg/ml meropenem and chromogenic ESBL Agar were identified as, Serratia liquefaciens (n=35), Serratia plymuthica (n=31), Klebsiella oxytoca (n=25), Klebsiella pneumonia (n=6), Raoultella ornithinolytica (n=14), Raoultella terrigena (n=3), Enterobacter cloacae (n=11), Enterobacter ludwigii (n=4), Enterobacter asburiae (n=1), Lelliottia amnigena (n=16), Escherichia coli (n=2), Escherichia hermannii (n=1), Leclercia adecarboxylata (n=3), Pantoea agglomerans (n=3), Kluyvera intermedia (n=2), Kosakonia cowanii (n=1) and Hafnia alvei (n=1) with MALDI-TOF MS method. According to the disk diffusion method, 11.62% (n=15) of the isolates were found to be Extended Spectrum Beta Lactamase (ESBL) and 4.65% (n=6) carbapenemase positive. ESBL and carbapenem-resistant isolates in green vegetables reveal the public health risk in these foods consumed without heat treatment.

Project Number

FYL-2019-2808

References

  • Anonim, (2011). Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği, 29 Aralık 2011/ Resmî Gazete Sayı : 28157.
  • Alves, M. S., Pereira, A., Araújo, S. M., Castro, B. B., Correia, A., & Henriques, I. (2014). Seawater is a reservoir of multi-resistant Escherichia coli, including strains hosting plasmid-mediated quinolones resistance and extended-spectrum beta-lactamases genes. Frontiers in microbiology, 5, 426.
  • Ayçiçek, H., Oguz, U., ve Karci, K. (2006). Determination of total aerobic and indicator bacteria on some raw eaten vegetables from wholesalers in Ankara, Turkey. International Journal of Hygiene and Environmental Health, 209(2), 197- 201.
  • Bain, R., Cronk, R., Hossain, R., Bonjour, S., Onda, K., Wright, J., Yang, H., Slaymaker, T., Hunter, P., Prüss-Ustün, A., and Bartram, J. (2014). Global assessment of exposure to faecal contamination through drinking water based on a systematic review. Tropical Medicine & International Health, 19(8), 917-927.
  • Ben Sallem, R., Ben Slama, K., Sáenz, Y., Rojo-Bezares, B., Estepa, V., Jouini, A., ... & Torres, C. (2012). Prevalence and characterization of extended-spectrum beta-lactamase (ESBL)–and CMY-2–producing Escherichia coli isolates from healthy food-producing animals in Tunisia. Foodborne pathogens and disease, 9(12), 1137-1142.
  • Blaak, H., van Hoek, A. H., Veenman, C., van Leeuwen, A. E. D., Lynch, G., van Overbeek, W. M., & de Roda Husman, A. M. (2014). Extended spectrum ß-lactamase-and constitutively AmpC-producing Enterobacteriaceae on fresh produce and in the agricultural environment. International journal of food microbiology, 168, 8-16.
  • Cordeiro-Araújo, M. K., Chia, M. A., Hereman, T. C., Sasaki, F. F., & do Carmo Bittencourt-Oliveira, M. (2015). Selective membrane permeability and peroxidase activity response of lettuce and arugula irrigated with cyanobacterial-contaminated water. Environmental Earth Sciences, 74(2), 1547-1553.
  • Boehme, S., Werner, G., Klare, I., Reissbrodt, R., & Witte, W. (2004). Occurrence of antibiotic‐resistant enterobacteria in agricultural foodstuffs. Molecular nutrition & food research, 48(7), 522-531.
  • Budak, S., Aktaş, Z., & Erdem, H. (2012). Enterik Gram-negatif bakterilerde laboratuvardan kliniğe karbapenemazlar. Mediterranean Journal of Infection Microbes and Antimicrobials, 1, 1-11.
  • Coudron, P. E. (2005). Inhibitor-based methods for detection of plasmid-mediated AmpC β-lactamases in Klebsiella spp., Escherichia coli, and Proteus mirabilis. Journal of clinical microbiology, 43(8), 4163-4167.
  • Demirer, B. ve Özdemir M. 2021. "Gıdalardaki Antibiyotik Kalıntıları." Academic Platform Journal of Halal Lifestyle 3.1: 17-25.
  • Edelstein, M., Sundborger, C., Hergens, M. P., Ivarsson, S., Dryselius, R., Insulander, M., . & Wallensten, A. (2014). Barriers to trace-back in a salad-associated EHEC outbreak, Sweden, June 2013. PLoS currents, 6.
  • EUCAST. 2022. European Committee on Antimicrobial Susceptibility Testing breakpoint tables for interpretation of MICs and zone diameters, version 7.1. https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_12.0_Breakpoint_Tables.pdf
  • Giske, CG., Gezelius, L., Samuelsen, O., Warner, M., Sundsfjord, A., Woodford, N., 2011. A sensitive and specific phenotypic assay for detection of metallo-βlactamases and KPC in Klebsiella pneumoniae with the use of meropenem disks supplemented with aminophenylboronic acid, dipicolinic acid and cloxacillin. Clin Microbiol Infect. 17(4):552-6.
  • O'Flaherty, E., Solimini, A. G., Pantanella, F., De Giusti, M., & Cummins, E. (2019). Human exposure to antibiotic resistant-Escherichia coli through irrigated lettuce. Environment international, 122, 270-280.
  • Hamilton-Miller, J. M. T., & Shah, S. (2001). Identity and antibiotic susceptibility of enterobacterial flora of salad vegetables. International journal of antimicrobial agents, 18(1), 81-83.
  • Hudson, J. A., Frewer, L. J., Jones, G., Brereton, P. A., Whittingham, M. J., & Stewart, G. (2017). The agri-food chain and antimicrobial resistance: A review. Trends in Food Science & Technology, 69, 131-147.
  • Franz, E., Semenov, A. V., & van Bruggen, A. H. C. (2009). Modelling the contamination of lettuce with Escherichia coli O157: H7 from manure-amended soil and the effect of intervention strategies (vol 105, pg 1569, 2008). Journal of Applied Microbiology, 106(5), 1761-1761.
  • Gupta, G., Tak, V., & Mathur, P. (2014). Detection of AmpC β lactamases in gram-negative bacteria. Journal of laboratory physicians, 6, 1-6. Jiang, X., & Shepherd, M. (2009). The role of manure and compost in produce safety. Microbial safety of fresh produce, 143. Sagoo, S. K., C. L. Little, and R. T. Mitchell. 2003. Microbiological quality of open ready-to-eat salad vegetables: effectiveness of food hygiene training of management. J. Food Prot. 66:1581–1586.
  • Smalla K., Blau K., Bettermann A., Jechalke S., Fornefeld E., Vanrobaeys Y., Stalder T., Top Em., 2018. Joint press release of the Julius Kühn Institute (JKI) and the BfR on a study of antimicrobial-resistant bacteria with multiple transferable resistance genes on fresh produce The transferable resistome of produce, mBio 9:e01300-18.
  • Liu, B. T., and Song, F. J. (2019). Emergence of two Escherichia coli strains co-harboring mcr-1 and blaNDM in fresh vegetables from China. Infection and Drug Resistance, 12, 2627.
  • McManus, P. S. (2014). Does a drop in the bucket make a splash? Assessing the impact of antibiotic use on plants. Current opinion in microbiology, 19, 76-82.
  • Njage, P. M., & Buys, E. M. (2015). Pathogenic and commensal E scherichia coli from irrigation water show potential in transmission of extended spectrum and AmpC β‐lactamases determinants to isolates from lettuce. Microbial biotechnology, 8(3), 462-473.
  • Nordmann, P., & Poirel, L. (2002). Emerging carbapenemases in Gram-negative aerobes. Clinical Microbiology and Infection, 8(6), 321-331.
  • Nousiainen, L. L., Joutsen, S., Lunden, J., Hänninen, M. L., & Fredriksson-Ahomaa, M. (2016). Bacterial quality and safety of packaged fresh leafy vegetables at the retail level in Finland. International journal of food microbiology, 232, 73-79.
  • Poeta, P., Radhouani, H., Pinto, L., Martinho, A., Rego, V., Rodrigues, R., ... & Igrejas, G. (2009). Wild boars as reservoirs of extended‐spectrum beta‐lactamase (ESBL) producing Escherichia coli of different phylogenetic groups. Journal of basic microbiology, 49(6), 584-588.
  • Poirel, L., Naas, T., Guibert, M., Chaibi, E. B., Labia, R., & Nordmann, P. (1999). Molecular and biochemical characterization of VEB-1, a novel class A extended-spectrum β-lactamase encoded by an Escherichia coli integron gene. Antimicrobial agents and chemotherapy, 43(3), 573-581.
  • Rico, H., Gozalbo, D., Sebastiá, C., & Falomir, M. P. (2003). Enterobacter cloacae in fresh vegetables: A potential carrier of antibiotic resistances to consumers. Food Studies: Interdiscipl J 2: 1–8.
  • Said, L. B., Jouini, A., Klibi, N., Dziri, R., Alonso, C. A., Boudabous, A., ... & Torres, C. (2015). Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia. International journal of food microbiology, 203, 86-92.
  • Szczech, M., Kowalska, B., Smolińska, U., Maciorowski, R., Oskiera, M., & Michalska, A. (2018). Microbial quality of organic and conventional vegetables from Polish farms. International journal of food microbiology, 286, 155-161.
  • Taormina, P. J., & Beuchat, L. R. (1999). Comparison of chemical treatments to eliminate enterohemorrhagic Escherichia coli O157: H7 on alfalfa seeds. Journal of food protection, 62(4), 318-324.
  • Tan, T. Y., Ng, L. S. Y., He, J., Koh, T. H., & Hsu, L. Y. (2009). Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. Antimicrobial agents and chemotherapy, 53(1), 146-149.
  • Thanner, S., Drissner, D., and Walsh, F. (2016). Antimicrobial resistance in agriculture. MBio 7 (2): e02227–e02215.
  • Tien, Y. C., Li, B., Zhang, T., Scott, A., Murray, R., Sabourin, L., ... & Topp, E. (2017). Impact of dairy manure pre-application treatment on manure composition, soil dynamics of antibiotic resistance genes, and abundance of antibiotic-resistance genes on vegetables at harvest. Science of the Total Environment, 581, 32-39.
  • Van Hoek, A. H., Veenman, C., van Overbeek, W. M., Lynch, G., de Roda Husman, A. M., & Blaak, H. (2015). Prevalence and characterization of ESBL-and AmpC-producing Enterobacteriaceae on retail vegetables. International journal of food microbiology, 204, 1-8.
  • Xylia, P., Botsaris, G., Chrysargyris, A., Skandamis, P., & Tzortzakis, N. (2019). Variation of microbial load and biochemical activity of ready-to-eat salads in Cyprus as affected by vegetable type, season, and producer. Food microbiology, 83, 200-210.
There are 36 citations in total.

Details

Primary Language Turkish
Subjects Food Engineering
Journal Section Articles
Authors

Vasfi Mehmet Balki 0000-0002-3196-3016

Nükhet Nilüfer Demirel Zorba 0000-0001-6851-6474

Nesrin Çakıcı 0000-0001-8662-7215

Project Number FYL-2019-2808
Early Pub Date April 4, 2023
Publication Date June 16, 2023
Published in Issue Year 2023 Volume: 48 Issue: 3

Cite

APA Balki, V. M., Demirel Zorba, N. N., & Çakıcı, N. (2023). YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI. Gıda, 48(3), 575-586. https://doi.org/10.15237/gida.GD22112
AMA Balki VM, Demirel Zorba NN, Çakıcı N. YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI. The Journal of Food. June 2023;48(3):575-586. doi:10.15237/gida.GD22112
Chicago Balki, Vasfi Mehmet, Nükhet Nilüfer Demirel Zorba, and Nesrin Çakıcı. “YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI”. Gıda 48, no. 3 (June 2023): 575-86. https://doi.org/10.15237/gida.GD22112.
EndNote Balki VM, Demirel Zorba NN, Çakıcı N (June 1, 2023) YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI. Gıda 48 3 575–586.
IEEE V. M. Balki, N. N. Demirel Zorba, and N. Çakıcı, “YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI”, The Journal of Food, vol. 48, no. 3, pp. 575–586, 2023, doi: 10.15237/gida.GD22112.
ISNAD Balki, Vasfi Mehmet et al. “YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI”. Gıda 48/3 (June 2023), 575-586. https://doi.org/10.15237/gida.GD22112.
JAMA Balki VM, Demirel Zorba NN, Çakıcı N. YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI. The Journal of Food. 2023;48:575–586.
MLA Balki, Vasfi Mehmet et al. “YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI”. Gıda, vol. 48, no. 3, 2023, pp. 575-86, doi:10.15237/gida.GD22112.
Vancouver Balki VM, Demirel Zorba NN, Çakıcı N. YEŞİL SEBZELERDE GENİŞLEMİŞ SPEKTRUMLU BETA LAKTAMAZ VE KARBAPENEMAZ ÜRETEN ENTEROBACTERALES SUŞLARININ ARAŞTIRILMASI. The Journal of Food. 2023;48(3):575-86.

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