Microbiological characterization of vegetables and their rhizosphere soil in Eastern Poland

Teresa Kłapeć 1  ,  
Department of Biological Health Hazards and Parasitology, Institute of Rural Health, Lublin, Poland
Ann Agric Environ Med 2016;23(4):559–565
The aim of this study was to investigate the bacteriological quality of 5 kinds of vegetables (lettuce, dill, radish, beetroot, carrot) and their rhizosphere soil, originating from conventional farms located in the Lublin Province of Eastern Poland. A total number of 35 samples of fresh vegetables (FV) taken immediately from soil, 35 samples of soil from rhizosphere of these vegetables (SR) and 35 samples of vegetables sold at retail in the markets in Lublin (VR) were examined. The samples were analysed for the content of: aerobic mesophilic bacteria (AMB) grown at 30°C and 37°C, Gram-negative bacteria of Enterobacteriaceae family, faecal coliform (FC) bacteria, Salmonella spp., and Clostridium perfringens. Median AMB values determined at 30°C for FV, SR and VR were 5.27, 5.00, and 5.00 log10CFU g-1, respectively, being significantly greater compared to those recorded at 37°C. The exceeding of the threshold value of 6.0 log10CFU g-1 proposed by Gelosa (1998) was noted only in 5 FV samples grown at 30°C (14.3%), and in 3 FV samples grown at 37°C (8.6%). The threshold value was never exceeded in SR and VR samples. Median concentrations of Enterobacteriaceae determined for FV, SR and VR were 4.03, 3.87, and 3.04 log10 CFU g-1, respectively. Eleven species of Enterobacteriaceae were identified in the FV, SR and VR samples. The percent of samples containing Escherichia coli was greatest for VR (22.9%), smaller for FV (17.1%) and smallest for SR (5.7%). The median concentrations of the faecal coliform bacteria (FC), determined by culture at 44°C, were low, amounting to 1.000 log10 CFU g-1 for FV and SR and 0.00 for VR. All examined vegetable and soil samples tested negative for the presence of Salmonella. The median concentrations of Clostridium perfringens were low, amounting to 0.00 log10 CFU g-1 for all categories of samples. This bacterium was relatively common in soil samples with the prevalence of 40.0%, but very rare in vegetable samples (occurring in 5.7% of FV and in none of VR samples). In conclusion, the results of the present study generally indicate that the microbiological quality of Polish vegetables grown on conventional farms is satisfactory and safe for consumers.
Teresa Kłapeć   
Department of Biological Health Hazards and Parasitology, Institute of Rural Health, Lublin, Poland
1. Aycicek H, Oguz U, Karci K. Determination of total aerobic and indicator bacteria on some raw eaten vegetables from wholesalers in Ankara, Turkey. Int J Hyg Environ Health. 2006; 209(2): 197–201.
2. Abadias M, Usall J, Anguera M, Solsona C, Viñas I. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol. 2008; 123(1–2): 121–129.
3. Ryu J H, Kim M, Kim E G, Beuchat L R, Kim H. Comparison of the microbiological quality of environmentally friendly and conventionally grown vegetables sold at retail markets in Korea. J Food Sci. 2014; 79(9): M1739–1744.
4. Cardamone C, Aleo A, Mammina C, Oliveri G, Di Noto A M. Assessment of the microbiological quality of fresh produce on sale in Sicily, Italy: preliminary results. J Biol Res. 2015; 22(3): 1–6.
5. Viswanathan P, Kaur R. Prevalence and growth of pathogens on salad vegetables, fruits and sprouts. Int J Hyg Environ Health. 2001; 203(3): 205–213.
6. Nguz K, Shindano J, Samapundo S, Huyghebaert A. Microbiological evaluation of fresh-cut organic vegetables produced in Zambia. Food Control. 2005; 15(5): 623–628.
7. Oliveira M, Usall J, Vinas I, Anguera M, Gatius F, Abadias M. Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol. 2010; 27: 679–684.
8. Seow J, Ágoston A, Phua L, Yuk H-G. Microbiological quality of fresh vegetables and fruits sold in Singapore. Food Control. 2012; 25(1): 39–44.
9. Sagoo S K, Little C L, Mitchell R T. The microbiological examination of ready-to-eat organic vegetables from retail establishments in the United Kingdom. Lett Appl Microbiol. 2001; 33(6): 434–439.
10. Johannessen G S, Loncarevic S, Kruse H. Bacteriological analysis of fresh produce in Norway. Int J Food Microbiol. 2002; 77(3): 199–204.
11. De Giusti M, Aurigemma C, Marinelli L, Tufi D, De Medici D, Di Pasquale S, el al. The evaluation of the microbial safety of fresh ready-to-eat vegetables produced by different technologies in Italy. J Appl Microbiol. 2010; 109(3): 996–1006.
12. Olaimat A N, Holey R A. Factors influencing the microbial safety of fresh produce: A review. Food Microbiol. 2012; 32: 1–19.
13. Da Silva Felicio M T, Hald T, Liebana E, Allende A, Hugas M, Nguyen-The C, Skoien Johannessen G, Niskanen T, Uyttendaele M, McLauchlin J. Risk ranking of pathogens in ready-to-eat unprocessed foods of non-animal origin (FoNAO) in the EU: Initial evaluation using outbreak data (2007–2011). Int J Food Microbiol. 2015; 195: 9–19.
14. Erickson M C, Webb C C, Diaz-Perez J C, Phatak S C, Silvoy J J, Davey L, et al. Infrequent internalization of Escherichia coli 0157:H7 into field-grown leafy greens. J Food Prot. 2010; 73: 500–506.
15. Lang N L, Smith S R. Influence of soil type, moisture content and biosolids application on the fate of Escherichia coli in agricultural soil under controlled laboratory conditions. J Appl Microbiol. 2007; 103: 2122–2131.
16. Nicholson F A, Groves S J, Chambers B J. Pathogen survival during livestock manure storage and following land application. Bioresour Technol. 2005; 96: 135–143.
17. Szejniuk B, Wasilewski P, Kubisz Ł, Szrajda P, Wroski G. Elimination of Salmonella senftenberg W 775 bacteria in the cultivation of some agricultural crops (in Polish). Acta Sci Pol Agricultura. 2007; 6(4): 73–81.
18. Holley R A, Arrus K M, Ominski K H, Tenuta M, Blank G. Salmonella survival in manure-treated soils during simulated seasonal temperature exposure. J Environ Qual. 2006; 35: 1170–1180.
19. Franz E, Diepeningen van A D, Vos de O J, Bruggen van A H C. Effects of cattle feed-ing regimen and soil management type on the fate of Escherichia coli O157:H7 and Salmonella enterica serovar typhimurium in manure, manure-amended soil and lettuce. Appl Environ Microbiol. 2005; 71: 6165–6174.
20. Stroczyńska-Sikorska M, Prażmo Z, Kłapeć T. The survival of Salmonella spp. and E. coli in a variety of soil types, and sanitary and epidemiological considerations. Materials Scientific Conference of the Medical Geography “Health and the Environment”, UMCS, Lublin 14–15.09.1993: 224–231 (in Polish).
21. Polish Standard PN-EN ISO 6222:2004. Water quality – Quantitative determination of microorganisms capable to grow. Determination the total number of colonies on nutrient agar culture (in Polish).
22. Polish Standards PN-77/C-04615/07. Water and sewage. Microbiological studies Determination of faecal coliform bacteria by tube fermentation technique (in Polish).
23. Polish Standards PN-Z-19000–1/2001. Soil quality-Assessment of the soil sanitary conditions-Detection of the Salmonella genus bacteria (in Polish).
24. Polish Standards PN-74/C-14615/2012. Water and sewage. Microbiological studies Determination of anaerobic sulfate reducing spore bacteria (Clostridium) farming method (in Polish).
25. Soriano J M, Rico H, Moltó J C, Mañes J. Assessment of the microbiological quality and wash treatments of lettuce served in University restaurants. Int J Food Microbiol. 2000; 58(1–2): 123–128.
26. Johnston L M, Jaykus L A, Moll D, Martinez M C, Anciso J, Mora B, et al. A field study of the microbiological quality of fresh produce. J Food Prot. 2005; 68(9): 1840–1847.
27. Johnston L M, Jaykus L A, Moll D, Anciso J, Mora B, Moe CL. A field study of the microbiological quality of fresh produce of domestic and Mexican origin. Int J Food Microbiol. 2006; 112(2): 83–95.
28. Wood J L, Chen J C, Friesen E, Delaquis P, Allen K J. Microbiological survey of locally grown lettuce sold at farmers‘markets in Vancouver, British Columbia. J Food Prot. 2015; 78(1): 203–208.
29. Ercolani G L. Bacteriological quality assessment of fresh marketed lettuce and fennel. Appl Environ Microbiol. 1976; 31(6): 847–852.
30. Hagenmaier R D, Baker RA. A survey of the microbial population and ethanol content of bagged salad. J Food Prot. 1998; 61(3): 357–359.
31. Valentin-Bon I, Jacobson A, Monday S R, Feng PC. Microbiological quality of bagged cut spinach and lettuce mixes. Appl Environ Microbiol. 2008; 74(4): 1240–1242.
32. Korir R C, Parveen S, Hashem F, Bowers J. Microbiological quality of fresh produce obtained from retail stores on the Eastern Shore of Maryland, United States of America. Food Microbiol. 2016; 56: 29–34.
33. Wójcik-Stopczyńska B. Microbiological quality of minimally processed vegetable salads (in Polish). Rocz Panstw Zakl Hig. 2004; 55(2): 139–45.
34. European Commission. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union 22.12.2005, L 338/2 EN.
35. McMahon M A, Wilson IG. The occurrence of enteric pathogens and Aeromonas species in organic vegetables. Int J Food Microbiol. 2001; 70(1–2): 155–162.
36. Loncarevic S, Johannessen G S, Rørvik L M. Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol. 2005; 41(2): 186–189.
37. Mukherjee A, Speh D, Dyck E, Diez-Gonzalez F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot. 2004; 67(5): 894–900.
38. Mukherjee A, Speh D, Jones A T, Buesing K M, Diez-Gonzalez F. Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. J Food Prot. 2006; 69(8): 1928–1936.
39. Tango C N, Choi N J, Chung M S, Oh D H. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot. 2014; 77(8): 1411–1417.