PREVALENCE OF GRAM-NEGATIVE BACTERIA ISOLATED FROM FRUIT AND VEGETABLES RETAILED IN ADANA PROVINCE

Mevhibe Terkuran; Zerrin Erginkaya; Fatih Köksal

doi:10.17780/ksujes.1180743

EN TR

PREVALENCE OF GRAM-NEGATIVE BACTERIA ISOLATED FROM FRUIT AND VEGETABLES RETAILED IN ADANA PROVINCE

Abstract

In this study, 65 samples of fresh products (leafy vegetables, ready-to-eat mixed salads, and fruits) retailed in Adana province of Turkiye were investigated for presence of Gram-negative bacteria. Salmonella spp. was undetected in any samples. However, Klebsiella pneumoniae (22%), Stenotrophomonas maltophilia (15%), Citrobacter freundii (11%), E. coli (11%), Klebsiella oxytoca (11%), Acinetobacter spp. [A. baumannii, A. pittii, (7%)], Pseudomonas putida (7%), were the predominant microorganisms and were detected in (19/65) 29.2% of samples by MALDI-TOF system. Their bacterial counts were between 3.6 and 8.3 log CFU/g. Strains of Enterobacter ludwigii (4%), Delftia lacustris (4%), Burkholderia cenocepacia (4%), and Burkholderia vietnamiensis (4%) were less detected. Our results revealed the fruits and vegetables produced in Adana province generally comply with microbiological criteria of the Turkish Food Codex interms of Salmonella spp., but higher bacterial counst of E. coli (between 5.8 and 6.3 log CFU/g) was found. Besides, Escherichia coli, Acinetobacter spp., Klebsiella pneumoniae, Citrobacter freundii, and Stenotrophomonas maltophilia species could be risky to human health.

Keywords

ADANA İLİNDE PERAKENDE SATILAN MEYVE VE SEBZELERDEN İZOLE EDİLEN GRAM-NEGATİF BAKTERİLERİN YAYGINLIĞI

Öz

Bu çalışmada, Türkiye’nin Adana ilinde perakende satışı yapılan 65 adet taze ürün örneğinde (yapraklı sebzeler, hazır karışık salatalar ve meyveler), Gram- negatif bakteri varlığı araştırılmıştır. Salmonella spp. hiç bir örnekte bulunmamıştır. Ancak, Klebsiella pneumoniae (%22), Stenotrophomonas maltophilia (%15), Citrobacter freundii (%11), E. coli (%11), Klebsiella oxytoca (%11), Acinetobacter spp. [A. baumannii, A. pittii, (%7)], Pseudomonas putida (%7) baskın mikroorganizmalar olup, örneklerin (19/65) %29.2’sinde MALDI-TOF sistemi ile tespit edilmiştir. Bakteri sayıları 3.6 ile 8.3 log CFU/g arasında bulunmuştur. Enterobacter ludwigii (%4), Delftia lacustris (%4), Burkholderia cenocepacia (%4) ve Burkholderia vietnamiensis (%4) suşları ise daha az oranda tespit edilmiştir. Sonuçlarımız Adana ilinde üretilen meyve ve sebzelerin, Salmonella spp. açısından Türk Gıda Kodeksi mikrobiyolojik kriterlerine genel olarak uygun olduğunu, ancak E. coli sayısının daha yüksek olduğunu (5.8 ile 6.3 log CFU/g arasında) ortaya koymuştur. Ayrıca, Escherichia coli, Acinetobacter spp., Klebsiella pneumoniae, Citrobacter freundii ve Stenotrophomonas maltophilia türleri, insan sağlığı için riskli olabilir.

Anahtar Kelimeler

Destekleyen Kurum

Scientific Research Project Unit of Osmaniye Korkut Ata University

Proje Numarası

grant number; OKUBAP-2020-PT 2-001

Teşekkür

All authors thanks to Osmaniye Korkut Ata University [This work was supported by Scientific Research Project Unit of Osmaniye Korkut Ata University (grant number; OKUBAP-2020-PT 2-001)].

Kaynakça

Abebe, E., Gugsa, G., & Ahmed, M. (2020). Review on major food-borne zoonotic bacterial pathogens. Journal of Tropical Medicine, 2020.https://doi.org/10.1155/2020/4674235
Alam, M.S., Feroz, F., Rahman, H., Das, K.K., Noor, R. (2015). Microbiological Contamination Sources of Freshly Cultivated Vegetables. Nutrition & Food Science, 45(4), 646-658.https://doi.org/10.1108/NFS-04-2015-0032
Ayçiçek, H., Sarimehmetoğlu, B., & Çakiroğlu, S. (2004). Assessment of the microbiological quality of meals sampled at the meal serving units of a military hospital in Ankara, Turkey. Food Control, 15, 379-384.https://doi.org/10.1016/S0956-7135(03)00101-4
Bekele, F.,Shumbej, T., Dendir, A., Mesfin, D., Solomon, A., Jemal, A., & Alemayheu, M. (2020). Contamination rate of commonly consumed fresh vegetables and fruits with parasites of medically importance in Wolkite and Butajira Towns of Gurage Zone, Southern Ethiopia. International Journal of Public Health Science (IJPHS), 9(3), 211.https://doi.org/10.11591/ijphs.v9i3.20395
Bolton, E. (2009). Guidelines for assessing the microbiological safety of ready-to-eat, foods placed on the market; Health Protection Agency: London UK, p, 33.
Carvalheira, A., Silva, J., & Teixeira, P. (2017). Lettuce and fruits as a source of multidrug resistant Acinetobacter spp. Food Microbiology, 64,119-125.https://doi.org/10.1016/j.fm.2016.12.005
Colosi, I. A.,Baciu, A. M., Opriș, R. V., Peca, L., Gudat, T., Simon, L. M.,& Costache, C. (2020). Prevalence of ESBL, AmpC and carbapenemase-producing Enterobacterales isolated from raw vegetables retailed in Romania. Foods, 9(12), 1726. https://doi.org/10.3390/foods9121726
De Oliveira, M. A., De Souza, V. M., Bergamini, A., M. M., & De Martinis, E., C. P. (2011). Microbiological quality of ready-to-eat minimally processed vegetables consumed in Brazil. Food Control, 22(8),1400-1403.https://doi.org/10.1016/j.foodcont.2011.02.020

Dunn, S. J., Connor, C., & McNally, A. (2019). The evolution and transmission of multi-drug resistant Escherichia coli and Klebsiella pneumoniae: the complexity of clones and plasmids. Current Opinion in Microbiology, 51, 51-56.https://doi.org/10.1016/j.mib.2019.06.004
Ehuwa, O., Jaiswal, A. K., & Jaiswal, S. (2021). Salmonella, food safety, and food handling practices. Foods, 10(5), 907.https://doi.org/10.3390/foods10050907
Espinal, P., Seifert, H., Dijkshoorn, L., Vila, J., & Roca, I. (2012). Rapid and accurate identification of genomic species from the Acinetobacter baumannii (Ab) group by MALDI-TOF MS. Clinical Microbiology and Infection, 18(11), 1097-1103.https://doi.org/10.1111/j.1469-0691.2011.03696.x
European Food Safety Authority (EFSA) (2018). European Centre for Disease Prevention and Control multi-country outbreak of Listeria monocytogenes serogroup IVb, multi-locus sequence type 6, infections linked to frozen corn and possibly to other frozen vegetables. First update, EFSA Supporting Publ, 15.
Falomir, M.P., Gozalbo, D., Sebastia C., & Rico, H. (2010a). Detection and antibiotic susceptibility of coliform bacteria in fresh vegetables. In: Microorganisms in industry and environment, from scientific and industrial research to consumer products. Mendez-Vilas A (ed,), Hackensack, NJ: World Scientific Publishing Co, 372–376.https://doi.org/10.1142/9789814322119_0080
Falomir, M. P., Gozalbo, D., & Rico, H. (2010b). Coliform bacteria in fresh vegetables: from cultivated lands to consumers. Current Research, Technology and Education TopicsIn Applied Microbiology and Microbial Biotechnology, 2,1175-1181.
Gülmez, M., Sezer, Ç., Duman, B., Vatansever, L., Oral, N., & Baz, E. (2005). Lokantalarda tüketime sunulan bazı gıdaların ve içme sularının mikrobiyolojik kaliteleri. Kafkas Üniversitesi Veterinerlik Fakültesi Dergisi, 11(1),5-10.
Heaton, J. C.,& Jones, K. (2008). Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. Journal of AppliedMicrobiology, 104(3), 613-626.https://doi.org/10.1111/j.1365-2672.2007.03587.x
Holt, J.G., Krieg, N.R., Sneath, P.H.A., Stanley, J.T. & William, S.T. (1994). Bergey’s Manual of Determinative Bacteriology. Williams and Wilikins, Baltimore, 587-685.
Igiehon, O. O.,Adekoya, A. E., Idowu, A. T. (2020). A review on the consumption of vended fruits: microbial assessment, risk, and its control. Food Quality and Safety, 4(2), 77-81.https://doi.org/10.1093/fqsafe/fyaa014
Kirzinger, M. W., Nadarasah, G., & Stavrinides, J. (2011). Insights into cross-kingdom plant pathogenic bacteria. Genes, 2(4), 980-997.https://doi.org/10.3390/genes2040980
Luna-Guevara, J. J., Arenas-Hernandez, M. M., Martínez de la Peña, C., Silva, J. L., Luna-Guevara, M. L. (2019). The role of pathogenic E. coli in fresh vegetables: behavior, contamination factors, and preventive measures. International Journal of Microbiology, 2019. https://doi.org/10.1155/2019/2894328
Lupo, A., Vogt., D., Seiffert, S.N., Endimiani, A., & Perreten, V. (2014). Antibiotic resistance and phylogenetic characterization of Acinetobacter baumannii strains isolated from commercial raw meat in Switzerland. Journal of Food Protection, 77, 1976-1981.https://doi.org/10.4315/0362-028X.JFP-14-073
Lynch, M. F., Tauxe, R. V., & Hedberg, C. W. (2009). The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiology & Infection, 137(3), 307-315.https://doi.org/10.1017/S0950268808001969
Meldrum R.J., Little C.L., Sagoo, S., Mithani, V., Mc Lauchlin J., & De Pinna E. (2009). Assessment of the microbiological safety of salad vegetables and sauces from kebab take-away restaurants in the United Kingdom. Food Microbiology, 26(6), 573-7.https://doi.org/10.1016/j.fm.2009.03.013
MesbahZekar, F., Granier, S. A., Marault, M., Yaici, L., Gassilloud, B., Manceau, C., & Millemann, Y. (2017). From farms to markets: Gram-negative bacteria resistant to third-generation cephalosporins in fruits and vegetables in a region of North Africa. Frontiers in Microbiology, 8, 1569.https://doi.org/10.3389/fmicb.2017.01569
Özdamar, K. (1999). Paket Programlar ile İstatistiksel Veri Analizi. Kaan Kitabevi, Eskişehir, Türkiye, 535s. Papadopoulou, E., Haug, L. S., Sakhi, A. K., Andrusaityte, S., Basagaña, X., Brantsaeter, A. L., & Chatzi, L. (2019).
Diet as a source of exposure to environmental contaminants for pregnant women and children from six European countries. Environmental Health Perspectives, 127(10),107005.https://doi.org/10.1289/EHP5324
Ruimy, R., Brisabois, A., Bernede, C., Skurnik, D., Barnat, S., Arlet, G., & Andremont, A. (2010). Organic and conventional fruits and vegetables contain equivalent counts of Gram‐negative bacteria expressing resistance to antibacterial agents. Environmental Microbiology, 12(3), 608-615.https://doi.org/10.1111/j.1462-2920.2009.02100.x
Schwaiger, K., Helmke, K., Hölzel, C. S., & Bauer, J. (2011a). Antibiotic resistance in bacteria isolated from vegetables with regards to the marketing stage (farm vs, supermarket). International Journal of Food Microbiology, 148(3), 191-196.https://doi.org/10.1016/j.ijfoodmicro.2011.06.001
Schwaiger, K., Helmke, K., Hölzel, C. S., & Bauer, J. (2011b). Comparative analysis of the bacterial flora of vegetables collected directly from farms and from supermarkets in Germany. International Journal of Environmental Health Research, 21(3), 161-172.https://doi.org/10.1080/09603123.2010.515672
Sivapalasingam, S, Friedman, C, R, Cohen, L, & Tauxe, R., V. (2004). Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997.Journal of Food Protection, 67(10), 2342-2353.https://doi.org/10.4315/0362-028X-67.10.2342
Sun, L., Zhang, H., Chen, J., Chen, L., Qi, X., & Zhang, R. (2021). Epidemiology of foodborne disease outbreaks caused by Nontyphoidal Salmonella in Zhejiang Province, China, 2010–2019. Foodborne Pathogens and Disease, 18(12), 880-886.http://doi.org/10.1089/fpd.2021.0006
Turkish Food Codex (2011). Official newspaper. Turkish Food Codex Regulation on Microbiological Criteria. (29 December 2011) Official Gazette. 2011:28157.
Uhlig, E, Olsson, C, He, J, Stark, T, Sadowska, Z, Molin, G., & Håkansson, Å., (2017). Effects of household washing on bacterial load and removal of Escherichia coli from lettuce and “ready‐to‐eat” salads. Food Science &Nutrition, 5(6), 1215-1220.https://doi.org/10.1002/fsn3.514
Usui, M, Ozeki K, Komatsu, T, &Fukuda, A, (2019), Tamura, Y, Prevalence of extended-spectrum b-lactamase–producing bacteria on fresh vegetables in Japan. Journal of Food Protection, 82, 1663–1666.https://doi.org/10.4315/0362-028X.JFP-19-138
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.https://doi.org/10.1016/j.fm.2019.05.013
Younus, M.I., Sabuj, A.A.M., Haque, Z.F., Sayem, S. M., Majumder, S., Parvin, M. S., & Saha, S. (2020). Microbial risk assessment of ready-to-eat mixed vegetable salads from different restaurants of Bangladesh Agricultural University campus. Journal of Advanced Veterinary Animal Research, 7(1), 34-41. https://doi.org/10.5455/javar.2020.g390

Ayrıntılar

Birincil Dil

İngilizce

Konular

Gıda Mühendisliği

Bölüm

Araştırma Makalesi

Yazarlar

Mevhibe Terkuran ^*
0000-0002-3150-459X
Türkiye

Zerrin Erginkaya
0000-0001-6208-2927
Türkiye

Fatih Köksal
0000-0003-0790-1525
Türkiye

Yayımlanma Tarihi

3 Eylül 2023

Gönderilme Tarihi

27 Eylül 2022

Kabul Tarihi

28 Temmuz 2023

Yayımlandığı Sayı

Yıl 2023 Cilt: 26 Sayı: 3

DOI

https://doi.org/10.17780/ksujes.1180743

IZ

https://izlik.org/JA67BB32DD

Kaynak Göster

RIS / Bibtex

APA

Terkuran, M., Erginkaya, Z., & Köksal, F. (2023). PREVALENCE OF GRAM-NEGATIVE BACTERIA ISOLATED FROM FRUIT AND VEGETABLES RETAILED IN ADANA PROVINCE. Kahramanmaraş Sütçü İmam Üniversitesi Mühendislik Bilimleri Dergisi, 26(3), 580-588. https://doi.org/10.17780/ksujes.1180743

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