| 
              
              
              Open Access  
Copyright: The authors. This article is an open access 
article licensed under the terms of the Creative Commons Attribution License 
 
 
(http://creativecommons.org/licenses/by/2.0) which permits unrestricted use, 
distribution and reproduction in any medium, provided the work is properly 
cited. 
 
              
              
              Research 
(Published 
online: 09-10-2014) 
              
              6. 
              Characterization of virulent Listeria 
              monocytogenes isolates recovered from ready-to-eat meat 
              products and consumers in Cairo, Egypt - 
              Maysa A. I. Awadallah 
              and Iman I. A. Suelam 
              
              Veterinary World, 7(10): 788-793   
              
   
                
                
doi: 
              10.14202/vetworld.2014.788-793 
                  Maysa 
              A. I. Awadallah: 
              
              Department of Zoonoses, Faculty of Veterinary Medicine, Zagazig 
              University, Zagazig, Egypt;
              
              
              maysavet@hotmail.com Iman I. 
              A. Suelam: Veterinary Hospital,Faculty of Veterinary Medicine, 
              Zagazig University, Zagazig, Egypt;
              
              Dakahlia2000@yahoo.com   Received: 
              30-06-2014, Revised: 01-09-2014, Accepted: 05-09-2014, Published 
              online: 08-10-2014   
              
              
              Corresponding author:
              
              Maysa A. I. Awadallah, e-mail: maysavet@hotmail.com 
 
              Abstract 
 Aim:
              This study aimed to investigate the occurrence of some 
              virulence genes distributed in Listeria monocytogenes 
              isolated from ready-to-eat (RTE) meat products and consumers in 
              Cairo province, Egypt.  
              Materials and Methods: A total of 120 beef luncheon, chicken 
              luncheon and frankfurter beef (40 samples, each) were collected 
              from 10 different local shops situated in Al-salam city, Cairo 
              province, Egypt. Stool samples were collected from 40 people who 
              had the habit of consuming RTE meat. The suspected L. 
              monocytogenes isolates were subjected to a multiplex 
              polymerase chain reaction (PCR) for rapid speciation and virulence 
              determination using primers specific for inIA, inIC, 
              and inIJ genes. 
              Results: Culture examination of all samples on Oxford media 
              revealed presence of colonies characteristic to L. 
              monocytogenes in 6 beef luncheon (15%), 4 chicken luncheon 
              (10%), 1 frankfurter beef (2.5%) and 1 human stool (2.5%) samples. 
              Species identity of L. monocytogenes was verified through 
              the amplification of a 800 bp fragment with inIA primers in 
              2 out of 6 culture isolates from beef luncheon (5%), and 1 out 4 
              culture isolates from chicken luncheon (2.5%) samples. Statistical 
              analysis revealed no significant difference between the occurrence 
              of L. monocytogenes in different food samples examined 
              (p>0.05). The virulence of these strains was ascertained by the 
              presence of 517 bp and 238 bp fragments of inIC and inIJ
              genes, respectively in the isolates that contained the 800 bp 
              fragment. The culture isolates obtained from one frankfurter beef 
              sample, and one human stool sample were found negative by 
              multiplex PCR for the presence of L. monocytogenes and its 
              virulence specific genes.  
              Conclusion: It could be concluded that L. monocytogenes 
              are circulating in beef and chicken luncheon sold in Cairo, Egypt. 
              Multiplex PCR is reliable for confirmation of L. monocytogenes. 
              This study suggests the implementation of hygienic measures at all 
              levels from production to consumption in order to improve food 
              safety. Furthermore, authors recommended consumption of beef 
              frankfurter or any RTE meat sold in their original intact packing 
              due to low level of contamination. 
              Keywords: Listeria monocytogenes,, consumers, 
              ready-to-eat meat, speciation and virulence determination. 
 
              References 
 
                
                  | 1. Dhama, K., Verma, A.K., Rajagunalan, S., Kumar, A., Tiwari, 
                  R., Chakraborty, S. and Kumar, R. (2013) Listeria 
                  monocytogenes infection in poultry and its public health 
                  importance with special reference to food borne zoonoses, Pak. 
                  J. Biol. Sci., 16: 301-8. http://dx.doi.org/10.3923/pjbs.2013.301.308
 PMid:24498796
 |  
                  |  |  
                  | 2. Jeyasekaran, G., Karunasagar, I. and Karunasagar, I. (1996) 
                  Incidence of Listeria spp. In tropical fish. Int. J. Food 
                  Microbiol., 31: 333-340. http://dx.doi.org/10.1016/0168-1605(96)00980-4
 |  
                  |  |  
                  | 3. Goulet, V., Hedberg, C., Le Monnier, A. and De Valk, H. 
                  (2008) Increasing incidence of listeriosis in France and other 
                  European countries. Emerg. Infect. Dis., 14: 734-740. http://dx.doi.org/10.3201/eid1405.071395
 PMid:18439354 PMCid:PMC2600261
 |  
                  |  |  
                  | 4. Wagner, M., Melzner, D., Bago, Z., Winter, P., Egerbacher, 
                  M., Schilcher, F., Zangana, A. and Schoder, D. (2005) Outbreak 
                  of listeriosis in sheep: Evaluation from possible 
                  contamination routes from feed to raw produce and humans. J. 
                  Vet. Med., 52: 278-283. http://dx.doi.org/10.1111/j.1439-0450.2005.00866.x
 PMid:16219091
 |  
                  |  |  
                  | 5. Lianou, A. and Sofos, J.N. (2007) A review of the incidence 
                  and transmission of Listeria monocytogenes in ready-to-eat 
                  products in retail and food service environment. J. Food 
                  Prot., 70: 2172-2198. PMid:17900099
 |  
                  |  |  
                  | 6. FAO/WHO. (2010) Risk assessment of Listeria monocytogenes 
                  in ready-to-eat food, 2004. Available from: http://www.fao.org/docrep/010/y5394e/y5394e00.htm. 
                  [Last accessed on 2010 May 31]. |  
                  |  |  
                  | 7. Blum-Menezes, D., Deliberalli, I., Bittencourt, N.C., do 
                  Couto, C.A.T., Barbosa, L.N., dos Santos, A.M. and Pinto, G.G. 
                  (2013) Listeriosis in the far South of Brazil: Neglected 
                  infection. Rev. Soc. Bras. Med. Trop., 46: 381-383. http://dx.doi.org/10.1590/0037-8682-0005-2013
 PMid:23856867
 |  
                  |  |  
                  | 8. Swaminathan, B. (2001) Listeria monocytogenes. In: Doyle, 
                  M.P., Beuchat, L.R. and Montville, TJ. editors. Food 
                  Microbiology. Food Fundamentals and Frontiers. American 
                  Society for Microbiology, Washington D.C., USA. p383-409. |  
                  |  |  
                  | 9. Gottlieb, S.L., Newbern, E.C., Griffin, P.M., Graves, L.M., 
                  Hoekstra, R.M., Baker, N.L., Hunter, S.B., Holt K.G., Ramsey, 
                  F., Head, M., Levine, P., Johnson, G., Schoonmaker-Bopp, D., 
                  Reddy, V., Kornstein, L., Gerwel, M., Nsubuga, J., Edwards, 
                  L., Stonecipher S., Hurd, S., Austin, D., Jefferson, M.A., 
                  Young, S.D., Hise, K., Chernak, E.D. and Sobel, J. (2006) 
                  Multistate outbreak of listeriosis linked to turkey deli meat 
                  and subsequent changes in US regulatory policy, Clin. Infect. 
                  Dis., 42: 29-36. http://dx.doi.org/10.1086/498113
 PMid:16323088
 |  
                  |  |  
                  | 10. Vazquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, 
                  T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., 
                  Wehlan, J. and Kreft, J. (2001) Listeria pathogenesis and 
                  molecular virulence determinants. Clin. Infect. Dis., 42: 
                  29-36. |  
                  |  |  
                  | 11. Peng, H. and Shelef, L.A. (2001) Automated simultaneous 
                  detection of low level of Listeria and salmonella in food. 
                  Int. J. Food Microbiol., 63: 225-233. http://dx.doi.org/10.1016/S0168-1605(00)00418-9
 |  
                  |  |  
                  | 12. Shalaby, M.A., Mohamed, M.S., Mansour, M.A. and 
                  Abd-El-Haffiz, A.S. (2011) Comparison of polymerase chain 
                  reaction and conventional methods for diagnosis of Listeria 
                  monocytogenes isolated from different clinical specimens and 
                  food stuffs. Clin. Lab., 57: 919-24. PMid:22239022
 |  
                  |  |  
                  | 13. Liu, D., Lawrence, M.L. Austin, F.W. and Ainsworth, A.J. 
                  (2007) A multiplex PCR for species and virulence-specific 
                  determination of Listeria monocytogenes. J. Microbiol. 
                  Methods., 71: 133-140. http://dx.doi.org/10.1016/j.mimet.2007.08.007
 PMid:17884210
 |  
                  |  |  
                  | 14. Arun, KB. (2008) Food-Borne Microbial Pathogen Mechanisms 
                  and Pathogenesis. 165-182. |  
                  |  |  
                  | 15. Farber, J.M., Pagotto, M. and Scherf, C. (2007) Incidence 
                  and behavior of L. monocytogenes in meat products. In: Ryser, 
                  E.T., Marth, E.H, editors. Listeria Listeriosis and Food 
                  Safety. CRC Press Taylor and Francis Group, New York. 
                  p503-570. |  
                  |  |  
                  | 16. Gelbicova, T. and Karpiskova, R. (2009) Occurrence and 
                  characteristics of L. monocytogenes in ready-to-eat food from 
                  retail market in the Czech Republic. Czech J. Food Sci., 
                  27(2): S2-3-S2-7. |  
                  |  |  
                  | 17. Lambertz, S.T., Nilsson, C., Bradenmark, A., Sylven, S., 
                  Johansson, A., Jansson, L.M. and Lindblad, M. (2012) 
                  Prevalence and level of L. monocytogenes in ready-to-eat food 
                  in Sweden. Int. J. Food Microbiol., 60: 24-31. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.09.010
 PMid:23141642
 |  
                  |  |  
                  | 18. Osaili, T.M., Al-Nabulsi, A.A., Shaker, R.R., Jaradat, Z.W., 
                  Taha, M., Al-Kherasha, M., Meherat, M. and Holley, R. (2014) 
                  Prevalence of Salmonella serovars, Listeria monocytogenes, and 
                  Escherichia coli O157:H7 in mediterranean ready-to-eat meat 
                  products in Jordan. J. Food Prot., 77:106-11. http://dx.doi.org/10.4315/0362-028X.JFP-13-049
 PMid:24406006
 |  
                  |  |  
                  | 19. El-shenawy, M.A., El-shenawy, M.A., Manes, J. and Soriano, 
                  J.M. (2011) Listeria species in street vended ready-to-eat 
                  food. Interdiscip. Perspect. Infect Dis, 968031: 6. |  
                  |  |  
                  | 20. Gombas, D.E., Chen, Y., Clavero, R.S. and Virginia, N. 
                  (2003) Survey of L. monocytogenes in ready-to-eat food. J. 
                  Food Prot., 66: 556-569. |  
                  |  |  
                  | 21. Johansson, T. (1998) Enhanced detection and enumeration of 
                  L. monocytogenes from foodstuffs and food processing 
                  environments. Int. J. Food Microbiol., 40: 77-85. http://dx.doi.org/10.1016/S0168-1605(98)00022-1
 |  
                  |  |  
                  | 22. Garrido, V., Vitas, A.I. and Garcia-Jalon, I. (2009) 
                  Survey of L. monocytogenes in ready-to-eat meat products: 
                  prevalence by brand and retail establishments for exposure 
                  assessment of listeriosis in Northern Spain. Food control., 
                  20: 986-991. http://dx.doi.org/10.1016/j.foodcont.2008.11.013
 |  
                  |  |  
                  | 23. Grif, K., Hein, I., Wagner, M., Brandl, E., Mpamuge, O., 
                  Mclauchlin, J., Dierich, M.P. and Allerberger, F. (2001) 
                  Prevalence and characterization of Listeria monocytogenes in 
                  faeces of healthy Austrians. Wien. Klin. Wochenschr., 113: 
                  737-742. PMid:11715752
 |  
                  |  |  
                  | 24. Grif, K., Patscheider, G., Dierich, M.P. and Allerberger, 
                  F. (2003) Incidence of fecal carriage of L. monocytogenes in 
                  three healthy volunteers: a one-year prospective stool survey. 
                  Europ. J. Clin. Microbiol. Infect. Dis., 22: 16-20. PMid:12582739
 |  
                  |  |  
                  | 25. Ahmed, H.A., Hussein, M.A. and El-Ashram, A.M.M. (2013) 
                  Seafood a potential source of some zoonotic bacteria in 
                  Zagazig, egypt, with the molecular detection of Listeria 
                  monocytogenes virulence genes. Vet. Italiana., 49: 299-308. PMid:24166481
 |  
                  |  |  
                  | 26. Cobb, C.A., Curtis, GD., Bansi, D.S., Slade, E., Mehal, 
                  W., Mitchell, R.G. and Chapman, R.W. (1996) Increased 
                  prevalence of L. monocytogenes in the faeces of patients 
                  receiving long-term H2 antagonistis. Eur. J. Gastroventrol. 
                  Hepatol., 8: 1071-1074. http://dx.doi.org/10.1097/00042737-199611000-00008
 PMid:8944368
 |  
                  |  |  
                  | 27. Amagliani, G., Giammarini, C., Omiccioli, E., Brandi, G. 
                  and Magani, M. (2007) Detection of L. monocytogenes using 
                  commercial PCR Kit and different DNA extraction methods. Food 
                  Control., 18: 1137-112. http://dx.doi.org/10.1016/j.foodcont.2006.06.012
 |  
                  |  |  
                  | 28. Germini, A., Masola, A., Carnevali, P. and Marchelli, R. 
                  (2009) Simultaneous detection of E. coli O157:H7, Salmonella 
                  species and L. monocytogenes by multiplex PCR. Food Control., 
                  20(8): 733-738. http://dx.doi.org/10.1016/j.foodcont.2008.09.010
 |  
                  |  |  
                  | 29. Kusar, D., Kavalic, M., Ocepek, M. and Zdovc, I. (2013) 
                  Report on overcoming the poor quality of ApaI pulsotypes with 
                  a short review on PFGE for Listeria monocytogenes. Polish. J. 
                  Microbiol., 62: 307-309. PMid:24459838
 |  
                  |  |  
                  | 30. Abdel-Malek, A.M., Sohaila, F.H.A., Hassanein, R., 
                  Abdel-Azeem, M., Mohamad and El-Sayh, K.I. (2010) Occurrence 
                  of Listeria species in meat chicken products and human stools 
                  in Assiut city, Egypt with PCR use for rapid identification of 
                  L. monocytogenes. Vet. World., 3(8): 335-359. |  
                  |  |  
                  | 31. Indrawattana, N., Nibaddhasobon, T., Sookrung, N., 
                  Chongsa-nguan, M., Tungtrongchitr, A., Makino, S., Tungyong, 
                  W. and Chaicumpa, W. (2011) Prevalence of Listeria 
                  monocytogenes in Raw Meats Marketed in Bangkok and 
                  Characterization of the Isolates by Phenotypic and Molecular 
                  Methods., J Health Popul Nutr. Feb 2011; 29(1): 26–38 http://dx.doi.org/10.3329/jhpn.v29i1.7565
 PMid:21528788 PMCid:PMC3075055
 |  |