Table of Contents Author Guidelines Submit a Manuscript
International Journal of Microbiology
Volume 2016, Article ID 4292417, 14 pages
http://dx.doi.org/10.1155/2016/4292417
Research Article

Hiding in Fresh Fruits and Vegetables: Opportunistic Pathogens May Cross Geographical Barriers

1Department of Food Science & Nutrition, College of Agricultural and Marine Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khod, 123 Muscat, Oman
2Department of Crop Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khod, 123 Muscat, Oman
3Department of Soils, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khod, 123 Muscat, Oman

Received 30 September 2015; Accepted 24 January 2016

Academic Editor: Susana Merino

Copyright © 2016 Zahra S. Al-Kharousi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. Prasanna, T. N. Prabha, and R. N. Tharanathan, “Fruit ripening phenomena—an overview,” Critical Reviews in Food Science and Nutrition, vol. 47, no. 1, pp. 1–19, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. Y.-L. Lee, T. Cesario, Y. Wang, E. Shanbrom, and L. Thrupp, “Antibacterial activity of vegetables and juices,” Nutrition, vol. 19, no. 11-12, pp. 994–996, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Berg, A. Erlacher, K. Smalla, and R. Krause, “Vegetable microbiomes: is there a connection among opportunistic infections, human health and our 'gut feeling'?” Microbial Biotechnology, vol. 7, no. 6, pp. 487–495, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. C. A. Lozupone, J. I. Stombaugh, J. I. Gordon, J. K. Jansson, and R. Knight, “Diversity, stability and resilience of the human gut microbiota,” Nature, vol. 489, no. 7415, pp. 220–230, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. A. N. Olaimat and R. A. Holley, “Factors influencing the microbial safety of fresh produce: a review,” Food Microbiology, vol. 32, no. 1, pp. 1–19, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. L. R. Beuchat, “Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables,” Microbes and Infection, vol. 4, no. 4, pp. 413–423, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. S. A. Hassan, A. D. Altalhi, Y. A. Gherbawy, and B. A. El-Deeb, “Bacterial load of fresh vegetables and their resistance to the currently used antibiotics in Saudi Arabia,” Foodborne Pathogens and Disease, vol. 8, no. 9, pp. 1011–1018, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. S. S. Al-Abri, A. K. Al-Jardani, M. S. Al-Hosni, P. J. Kurup, S. Al-Busaidi, and N. J. Beeching, “A hospital acquired outbreak of Bacillus cereus gastroenteritis, Oman,” Journal of Infection and Public Health, vol. 4, no. 4, pp. 180–186, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Hauswaldt, M. Nitschke, F. Sayk, W. Solbach, and J. K.-M. Knobloch, “Lessons learned from outbreaks of Shiga toxin producing Escherichia coli,” Current Infectious Disease Reports, vol. 15, no. 1, pp. 4–9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. Centers for Disease Control and Prevention (CDC), 2014, http://www.cdc.gov/outbreaks/.
  11. J. W. Leff and N. Fierer, “Bacterial communities associated with the surfaces of fresh fruits and vegetables,” PLoS ONE, vol. 8, no. 3, Article ID e59310, pp. 1–9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. L. U. Opara, F. A. Al-Said, and A. Al-Abri, “Assessment of what the consumer values in fresh fruit quality: case study of Oman,” New Zealand Journal of Crop and Horticultural Science, vol. 35, no. 2, pp. 235–243, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Hammer, J. Gebauer, S. Al Khanjari, and A. Buerkert, “Oman at the cross-roads of inter-regional exchange of cultivated plants,” Genetic Resources and Crop Evolution, vol. 56, no. 4, pp. 547–560, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Nguz, J. Shindano, S. Samapundo, and A. Huyghebaert, “Microbiological evaluation of fresh-cut organic vegetables produced in Zambia,” Food Control, vol. 16, no. 7, pp. 623–628, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Abriouel, N. B. Omar, A. C. Molinos et al., “Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water and soil, and clinical samples,” International Journal of Food Microbiology, vol. 123, no. 1-2, pp. 38–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. S. N. Al-Bahry, M. A. Al-Zadjali, I. Y. Mahmoud, and A. E. Elshafie, “Biomonitoring marine habitats in reference to antibiotic resistant bacteria and ampicillin resistance determinants from oviductal fluid of the nesting green sea turtle, Chelonia mydas,” Chemosphere, vol. 87, no. 11, pp. 1308–1315, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. D. J. Reasoner and E. E. Geldreich, “A new medium for the enumeration and subculture of bacteria from potable water,” Applied and Environmental Microbiology, vol. 49, no. 1, pp. 1–7, 1985. View at Google Scholar · View at Scopus
  19. M. J. Allen, S. C. Edberg, and D. J. Reasoner, “Heterotrophic plate count bacteria—what is their significance in drinking water?” International Journal of Food Microbiology, vol. 92, no. 3, pp. 265–274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. G. R. Siragusa, W. J. Dorsa, C. N. Cutter, G. L. Bennett, J. E. Keen, and M. Koohmaraie, “The incidence of Escherichia coli on beef carcasses and its association with aerobic mesophilic plate count categories during the slaughter process,” Journal of Food Protection, vol. 61, no. 10, pp. 1269–1274, 1998. View at Google Scholar · View at Scopus
  21. R. Ruimy, A. Brisabois, C. Bernede et al., “Organic and conventional fruits and vegetables contain equivalent counts of Gram-negative bacteria expressing resistance to antibacterial agents,” Environmental Microbiology, vol. 12, no. 3, pp. 608–615, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. N. S. Al-Zoreky, “Antimicrobial activity of pomegranate (Punica granatum L.) fruit peels,” International Journal of Food Microbiology, vol. 134, no. 3, pp. 244–248, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. S. M. S. Menezes, L. N. Cordeiro, and G. S. B. Viana, “Punica granatum (pomegranate) extract is active against dental plaque,” Journal of Herbal Pharmacotherapy, vol. 6, no. 2, pp. 79–92, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. S. A. Al-Maiman and D. Ahmad, “Changes in physical and chemical properties during pomegranate (Punica granatum L.) fruit maturation,” Food Chemistry, vol. 76, no. 4, pp. 437–441, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. P. H. Nhung, K. Ohkusu, N. Mishima et al., “Phylogeny and species identification of the family Enterobacteriaceae based on dnaJ sequences,” Diagnostic Microbiology & Infectious Disease, vol. 58, no. 2, pp. 153–161, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Mathur and R. Singh, “Antibiotic resistance in food lactic acid bacteria—a review,” International Journal of Food Microbiology, vol. 105, no. 3, pp. 281–295, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Forslund, S. Sunagawa, J. R. Kultima et al., “Country-specific antibiotic use practices impact the human gut resistome,” Genome Research, vol. 23, no. 7, pp. 1163–1169, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Abadias, J. Usall, M. Anguera, C. Solsona, and I. Viñas, “Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments,” International Journal of Food Microbiology, vol. 123, no. 1-2, pp. 121–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Jonas, B. Spitzmüller, F. D. Daschner, J. Verhoef, and S. Brisse, “Discrimination of Klebsiella pneumoniae and Klebsiella oxytoca phylogenetic groups and other Klebsiella species by use of amplified fragment length polymorphism,” Research in Microbiology, vol. 155, no. 1, pp. 17–23, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. T. Hamilton-Miller and S. Shah, “Identity and antibiotic susceptibility of enterobacterial flora of salad vegetables,” International Journal of Antimicrobial Agents, vol. 18, no. 1, pp. 81–83, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Brady, I. Cleenwerck, S. Venter, T. Coutinho, and P. De Vos, “Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): Proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter,” Systematic and Applied Microbiology, vol. 36, no. 5, pp. 309–319, 2013. View at Publisher · View at Google Scholar
  32. P. Kämpfer, S. P. Glaeser, M. W. Raza, S. A. Abbasi, and J. D. Perry, “Pseudocitrobacter gen. nov., a novel genus of the Enterobacteriaceae with two new species Pseudocitrobacter faecalis sp. nov., and Pseudocitrobacter anthropi sp. nov, isolated from fecal samples from hospitalized patients in Pakistan,” Systematic and Applied Microbiology, vol. 37, no. 1, pp. 17–22, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Harada, H. Oyaizu, Y. Kosako, and H. Ishikawa, “Erwinia aphidicola, a new species isolated from pea aphid, Acyrthosiphon pisum,” Journal of General and Applied Microbiology, vol. 43, no. 6, pp. 349–354, 1997. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Marín, M. Santos, F. Carretero, J. A. Yau, and F. Diánez, “Erwinia aphidicola isolated from commercial bean seeds (Phaseolus vulgaris),” Phytoparasitica, vol. 39, no. 5, pp. 483–489, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Tash, “Rahnella aquatilis bacteremia from a suspected urinary source,” Journal of Clinical Microbiology, vol. 43, no. 5, pp. 2526–2528, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Hejazi and F. R. Falkiner, “Serratia marcescens,” Journal of Medical Microbiology, vol. 46, no. 11, pp. 903–912, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. L. A. Grohskopf, V. R. Roth, D. R. Feikin et al., “Serratia liquefaciens bloodstream infections from contamination of epoetin alfa at a hemodialysis center,” The New England Journal of Medicine, vol. 344, no. 20, pp. 1491–1497, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. V. Drelichman and J. D. Band, “Bacteremias due to Citrobacter diversus and Citrobacter freundii: incidence, risk factors, and clinical outcome,” Archives of Internal Medicine, vol. 145, no. 10, pp. 1808–1810, 1985. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Nada and M. Areej, “Raoultella planticola, a central venous line exit site infection,” Journal of Taibah University Medical Sciences, vol. 9, no. 2, pp. 158–160, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Österblad, O. Pensala, M. Peterzéns, H. Heleniusc, and P. Huovinen, “Antimicrobial susceptibility of Enterobacteriaceae isolated from vegetables,” Journal of Antimicrobial Chemotherapy, vol. 43, no. 4, pp. 503–509, 1999. View at Google Scholar
  41. R. J. Gilbert, J. de Louvois, T. Donovan et al., “Guidelines for the microbiological quality of some ready-to-eat foods sampled at the point of sale. PHLS Advisory Committee for Food and Dairy Products,” Communicable Disease and Public Health, vol. 3, no. 3, pp. 163–167, 2000. View at Google Scholar
  42. S. Kuramoto, H. Kodama, K. Yamada et al., “Food poisoning attributable to Staphylococcus aureus deficient in all of the staphylococcal enterotxoin gene so far reported,” Japanese Journal of Infectious Diseases, vol. 59, no. 5, p. 347, 2006. View at Google Scholar
  43. L. L. McGowan, C. R. Jackson, J. B. Barrett, L. M. Hiott, and P. J. Fedorkacray, “Prevalence and antimicrobial resistance of enterococci isolated from retail fruits, vegetables, and meats,” Journal of Food Protection, vol. 69, no. 12, pp. 2976–2982, 2006. View at Google Scholar
  44. A. B. Boehm and L. M. Sassoubre, “Enterococci as indicators of environmental fecal contamination,” in Enterococci: From Commensals to Leading Causes of Drug Resistant Infections, M. S. Gilmore, D. B. Clewell, Y. Ike et al., Eds., Massachusetts Eye and Ear Infirmary, Boston, Mass, USA, 2014. View at Google Scholar
  45. T. J. Eaton and M. J. Gasson, “Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates,” Applied and Environmental Microbiology, vol. 67, no. 4, pp. 1628–1635, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. T. G. Emori and R. P. Gaynes, “An overview of nosocomial infections, including the role of the microbiology laboratory,” Clinical Microbiology Reviews, vol. 6, no. 4, pp. 428–442, 1993. View at Google Scholar · View at Scopus
  47. K. Gqunta, J. van Wyk, P. Ekermans, C. Bamford, C. Moodley, and S. Govender, “First report of an IMI-2 carbapenemase-producing Enterobacter asburiae clinical isolate in South Africa,” Southern African Journal of Infectious Diseases, vol. 30, no. 1, pp. 34–35, 2015. View at Publisher · View at Google Scholar
  48. C. Westerfeld, G. N. Papaliodis, I. Behlau, M. L. Durand, and L. Sobrin, “Enterobacter amnigenus endophthalmitis,” Retinal Cases & Brief Reports, vol. 3, no. 4, pp. 409–411, 2009. View at Publisher · View at Google Scholar
  49. A. W. Paton and J. C. Paton, “Enterobacter cloacae producing a Shiga-like toxin II-related cytotoxin associated with a case of hemolytic-uremic syndrome,” Journal of Clinical Microbiology, vol. 34, no. 2, pp. 463–465, 1996. View at Google Scholar · View at Scopus
  50. P. N. Wenger, J. I. Tokars, P. Brennan et al., “An outbreak of Enterobacter hormaechei infection and colonization in an intensive care nursery,” Clinical Infectious Diseases, vol. 24, no. 6, pp. 1243–1244, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Khajuria, A. K. Praharaj, N. Grover, and M. Kumar, “First report of an Enterobacter ludwigii isolate coharboring NDM-1 and OXA-48 carbapenemases,” Antimicrobial Agents and Chemotherapy, vol. 57, no. 10, pp. 5189–5190, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Iaria, G. Stassi, G. B. Costa, R. di Leo, A. Toscano, and A. Cascio, “Enterococcal meningitis caused by Enterococcus casseliflavus. First case report,” BMC Infectious Diseases, vol. 5, article 3, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Zeana, C. J. Kubin, P. Della-Latta, and S. M. Hammer, “Vancomycin-resistant Enterococcus faecium meningitis successfully managed with linezolid: Case report and review of the literature,” Clinical Infectious Diseases, vol. 33, no. 4, pp. 477–482, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Poyart, T. Lambert, P. Morand et al., “Native valve endocarditis due to Enterococcus hirae,” Journal of Clinical Microbiology, vol. 40, no. 7, pp. 2689–2690, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. B. S. Freyaldenhoven, G. Schlieper, R. Lütticken, and R. R. Reinert, “Enterococcus raffinosus infection in an immunosuppressed patient: case report and review of the literature,” Journal of Infection, vol. 51, no. 3, pp. e121–e124, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Högenauer, C. Langner, E. Beubler et al., “Klebsiella oxytoca as a causative organism of antibiotic-associated hemorrhagic colitis,” The New England Journal of Medicine, vol. 355, no. 23, pp. 2418–2426, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Elemam, J. Rahimian, and W. Mandell, “Infection with panresistant Klebsiella pneumoniae: a report of 2 cases and a brief review of the literature,” Clinical Infectious Diseases, vol. 49, no. 2, pp. 271–274, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. M. C. Liberto, G. Matera, R. Puccio, T. Lo Russo, E. Colosimo, and E. Focà, “Six cases of sepsis caused by Pantoea agglomerans in a teaching hospital,” New Microbiologica, vol. 32, no. 1, pp. 119–123, 2009. View at Google Scholar · View at Scopus
  59. M. S. Alves, L. W. Riley, and B. M. Moreira, “A case of severe pancreatitis complicated by Raoultella planticola infection,” Journal of Medical Microbiology, vol. 56, no. 5, pp. 696–698, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. K. O' Connell, J. Kelly, and U. NiRiain, “A rare case of soft-tissue infection caused by Raoultella planticola,” Case Reports in Medicine, vol. 2010, Article ID 134086, 2 pages, 2010. View at Publisher · View at Google Scholar
  61. R. A. Equi and W. R. Green, “Endogenous Serratia marcescens endophthalmitis with dark hypopyon: a case report and review,” Survey of Ophthalmology, vol. 46, no. 3, pp. 259–268, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Tascini, A. Di Paolo, M. Polillo et al., “Case report of a successful treatment of methicillin-resistant Staphylococcus aureus (MRSA) bacteremia and MRSA/vancomycin-resistant Enterococcus faecium cholecystitis by daptomycin,” Antimicrobial Agents and Chemotherapy, vol. 55, no. 5, pp. 2458–2459, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. P. H. Nhung, K. Ohkusu, N. Mishima et al., “Phylogeny and species identification of the family Enterobacteriaceae based on dnaJ sequences,” Diagnostic Microbiology and Infectious Disease, vol. 58, no. 2, pp. 153–161, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. F. Rezzonico, T. H. Smits, E. Montesinos, J. E. Frey, and B. Duffy, “Genotypic comparison of Pantoea agglomerans plant and clinical strains,” BMC Microbiology, vol. 9, article 204, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Spröer, U. Mendrock, J. Swiderski, E. Lang, and E. Stackebrandt, “The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae,” International Journal of Systematic Bacteriology, vol. 49, no. 4, pp. 1433–1438, 1999. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Takahashi, I. Satoh, and N. Kikuchi, “Phylogenetic relationships of 38 taxa of the genus Staphylococcus based on 16S rRNA gene sequence analysis,” International Journal of Systematic Bacteriology, vol. 49, no. 2, pp. 725–728, 1999. View at Publisher · View at Google Scholar · View at Scopus
  67. S. M. Naser, F. L. Thompson, B. Hoste et al., “Application of multilocus sequence analysis (MLSA) for rapid identification of Enterococcus species based on rpoA and pheS genes,” Microbiology, vol. 151, no. 7, pp. 2141–2150, 2005. View at Publisher · View at Google Scholar · View at Scopus