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Ham: Distributions of Bacillus cereus, Pseudomonas, Enterococcus, and coliforms Isolated from Agricultural Products
Original Article

J Bacteriol Virol 2017;47(3):139-147.

Published online: 9 February 2017

DOI: https://doi.org/10.4167/jbv.2017.47.3.139

Distributions of Bacillus cereus, Pseudomonas, Enterococcus, and coliforms Isolated from Agricultural Products

Heejin Ham∗

Anyang University, College of Liberal Arts, Anyang, Korea

∗Corresponding author: Heejin Ham. College of Liberal Arts, Anyang University, Anyang 14028, Korea. Phone: +82-10-4140-3823, Fax: +82-31-463-1386, e-mail: hhj3814@anyang.ac.kr

Received 3 July 20177 August 2017       Accepted 16 August 2017

Copyright © 2017 Journal of Bacteriology and Virology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

A survey was conducted on the bacterial contamination levels from 128 agricultural products, and identified 31 coliforms, 34 Bacillus spp., 35 Pseudomonas spp., and 3 Enterococcus spp. Antibiotic susceptibility testing of eight Escherichia coli (E. coli) isolates, thirteen Bacillus cereus (B. cereus) isolates and seven Pseudomonas aeruginosa (P. aeruginosa) reveled that none of the E. coli isolates shows multidrug resistance pattern. However, one B. cereus isolate was resistant to Amoxicillin/clavulanic acid + Ampicillin/sulbactam + Cephaloxin, and twelve B. cereus isolates were resistant to Amoxicillin/clavulanic acid + Ampicillin/sulbactam + Cephaloxin + Tetracycline. The data from the current study points out that many agricultural products contain multidrug resistant bacteria, and it can be suggested for the need of proper guidelines and special management on the use of antibiotics in agricultural products.

Keywords: B. cereus, Pseudomonas, Enterococcus, Drug resistance patterns, Agricultural products

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Table 1.
Prevalence of microbial contamination in the agricultural products from the market
Samplesa) No. of Sample Aerobic bacteria in 37℃ (CFU/g, SPC agar) Aerobic bacteria in 20℃ (CFU/g, R2 A agar)
Incidence rate (%) Average Bacteria No. Range Incidence rate (%) Average Bacteria No. Range
Leaf vegetable 41 97.6 2.8 × 105 0~9.6 × 108 87.8 8.5 × 104 0~1.1 × 108
Fruit vegetable 24 87.5 2.1 × 107 0~2.2 × 108 83.3 7.6 × 106 0~1.1 × 108
Leaf and stem vegetable 21 100.0 2.6 × 107 3.1 × 105 ~8.8 × 105 95.2 1.1 × 107 0~2.2 × 108
Fruits 19 36.8 1.6 × 108 0~1.6 × 106 26.3 8.7 × 107 0~4.5 × 105
Fungus 7 100.0 1.2 × 108 1.9 × 102 ~6.8 × 107 57.1 8.0 × 107 0~3.8 × 107
Root vegetable 7 85.7 6.2 × 107 0~1.8 × 108 71.4 1.3 × 107 0~7.6 × 107
Flow bean sprouts 7 85.7 1.3 × 108 0~1.8 × 108 71.4 4.7 × 107 0~7.6 × 107
Potatoes 2 100.0 9.5 × 107 1.4 × 107 ~1.1 × 108 100.0 4.8 × 107 3.7 × 106 ~2.3 × 107
Total or Average 128 85.9 7.7 × 107 0~9.6 × 108 75.8 3.7 × 107 0~1.1 × 108

a) Leaf vegetable, 엽채류; Fruit vegetable, 과채류; Leaf and stem vegetable, 엽경채류; Fruits, 과실류; Fungus, 버섯류; Root vegetable, 근채류; Flow bean sprouts, 두채류; Potatoes, 서류.

Table 2.
Bacterial distribution in the agricultural products from the market
Samples Bacterial species
Coliforms Bacillus spp. Pseudomonas spp. Enterococcus spp.
Leaf vegetable 14 13 18 3
Fruit vegetable 4 6 7 0
Leaf and stem vegetable 9 5 6 0
Fruits 1 3 0 0
Fungus 1 0 1 0
Root vegetable 0 3 1 0
Flow bean sprouts 2 3 2 0
Potatoes 0 1 0 0
Total 31 34 35 3
Table 3.
Prevalence of coliforms, Bacillus spp., Pseudomonas spp., and Enterococcus spp. in 128 agricultural products from the market
  Bacterial isolates Number of bacteria Isolation rate (%)
Coliforms E. coli 8  
  Serratia marcascenes 4  
  Serratia liquefaciens 4  
  Gemella haemolysans 4  
  Citrobacter freundii 3 24.2% (31/128)
  Roultella terrigena 1
  Pantoea spp. 1  
  Enterobacter sakazakii 1  
  Citrobacter braakii 1  
  Etc∗. 4  
Bacillus spp. B. mycoides 18  
  B. cereus 13 26.6% (34/128)
  Brevibacillus laterospororus 2
  B. firmus 1  
Pseudomonas spp. P. luteola 18  
  P. aeruginosa 7 27.3% (35/128)
  P. fluorescens 7
  Chromobacterium violaceum 3  
Enterococcus spp. Aerococcus viridans 3 2.3% (3/128)

Etc. = Aeromonas hydrophila/caviae/sobria

Table 4.
Antimicrobial susceptibility patterns of bacterial isolates from 128 agricultural products from the market
Antimicrobial drugs Concentration E. coli (n=8) B. cereus (n=13) P. aeruginosa (n=7)
Sa) (%) Ib) (%) Rc) (%) Sa) (%) Ib) (%) Rc) (%) Sa) (%) Ib) (%) Rc) (%)
Streptomycin (S) 10 mg 75.0 25.0   100     28.6 28.6 42.8
Kanamycin (K) 30 mg 87.5 12.5   100     57.1   42.9
Gentamycin (GM) 10 mg 100     100     100    
Amoxicillin/clavulanic acid (AMC) 30 μg 87.5 12.5       100     100
Chloramphenicol (C) 30 μg 100     100       14.3 85.7
Cephaloxin (CF) 30 μg 100         100     100
Ampicillin/sulbactam (SAM) 20 μg 87.5 12.5       100     100
Ciprofloxacin (CIP) 5 μg 100     100     100    
Tetracycline (Te) 30 mg 62.5   37.5 84.6 7.7 7.7   28.6 71.4
Amikacin (AN) 30 μg 100     100     100    
Nalidixic acid (NA) 30 μg 100     92.3   7.7 14.3   85.7
Norfloxacillin (NOR) 10 mg 100     100     100    
Levofloxacillin (LVX) 5 μg 100     100     100    
Vancomycin (VA) 30 μg 62.5 12.5 25.0 100         100

a) S: susceptible,

b) I, intermediate,

c) R, resistant

Table 5.
Multiple drug resistance patterns in B. cereus and P. aeruginosa isolates from 128 agricultural products
Multiple drug resistance pattern No. of isolate
B. cereus strains (n=13)  
  AMC+SAM+CF+TE 12
  AMC+SAM+CF 1
P. aeruginosa strains (n=7)  
  AMC+SAM+C+VA+NA+CF+S+TE 2
  AMC+SAM+VA+NA+CF+S+TE 1
  AMC+SAM+C+VA+NA+CF 2
  AMC+SAM+C+TE+CF 2
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