Approach to Epidemiological Mechanism of Infection or Colonization of Egg-Laying Chicken Farms by Salmonella enterica Serovar Enteritidis (SE) Becoming the Main Source of Contamination in Food Poisoning (Review)

Abstract



Salmonella enterica serovar Enteritidis (SE)-induced diarrhea in humans is the typical non-typhoid diarrhea. It develops acutely or subacutely and may be fatal. This SE infectious disease suddenly became a major public health issue worldwide in the 1980s. The main causative food material of SE food poisoning is chicken eggs, and many outbreaks of food poisoning caused by chicken eggs occurred throughout the world. SE epidemics occurred in layer farms, and this was the main cause of SE-induced food poisoning in humans. The major subject of our epidemiological study described in this report is why SE-contaminated eggs became the main causative food. In this study, we focused on difference of molecular expression for farm-isolated SEs. That is because recent studies have demonstrated that O-antigen enlargement may be related to pathogenicity in mice as well as 22-kDa polypeptide-expression (SEp22). We have discovered that many SE strains isolated from chicken farms do not express SEp22, and a deficiency or decreased level of cellular antigen 0-12 in SE strains isolated from chicken farms was clarified in a report. Additionally, SEp22 was deficient in SE strains passaged through chickens, whereas SEp22 was expressed at a high level in SE strains passaged through mice. These findings suggest that SE infection and retention more effectively occur in layer farms than in other animal maintenance environments, which may be a basis of the epidemiological hypothesis to explain the high-levelproduction of SE-contaminated eggs (the presence of mice may be the basis of the retention of SE infection in layer farms, and this may also be the mechanism causing the high-level production of SE-contaminated eggs).



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Toyota-Hanatani, Y. , Nakagawa, Y. , Hatabu, T. , Miyao, Y. and Ohta, H. (2014) Approach to Epidemiological Mechanism of Infection or Colonization of Egg-Laying Chicken Farms by Salmonella enterica Serovar Enteritidis (SE) Becoming the Main Source of Contamination in Food Poisoning (Review). International Journal of Clinical Medicine, 5, 376-392. doi: 10.4236/ijcm.2014.57053.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Koupal, L.R. and Deibel, R.H. (1975) Assay, Characterization, and Localization of an Enterotoxin Produced by Salmonella. Infection and Immunity, 11, 14-22.
[2] Tamura, A., Yamasaki, M., Okutani, A., Igimi, S., Saitoh, N., Ekawa, T., Ohta, H., Katayama, Y. and Amano, F. (2009) Dry-Resistance of Salmonella enterica Subsp. Enterica Serovar Enteritidis Is Regulated by Both SEp22, a Novel Pathogenicity-Related Factor of Salmonella, and Nutrients. Microbes and Environments, 24, 121-127.
http://dx.doi.org/10.1264/jsme2.ME09111
[3] Varga, C., Pearl, D.L., McEwen, S.A., Sargeant, J.M., Pollari, F. and Guerin, M.T. (2013) Incidence, Distribution, Seasonality, and Demographic Risk Factors of Salmonella Enteritidis Human Infections in Ontario, Canada, 2007-2009. BMC Infectious Diseases, 13, 212. http://dx.doi.org/10.1186/1471-2334-13-212
[4] Babu, U.S., Sommers, K., Harrison, L.M. and Balan, K.V. (2012) Effects of Fructooligosaccharide-Inulin on Salmonella-Killing and Inflammatory Gene Expression in Chicken Macrophages. Veterinary Immunology and Immunopathology, 149, 92-96. http://dx.doi.org/10.1016/j.vetimm.2012.05.003
[5] Johnston, C.E., Hartley, C., Salisbury, A.M. and Wigley, P. (2012) Immunological Changes at Point-of-Lay Increase Susceptibility to Salmonella enterica Serovar Enteritidis Infection in Vaccinated Chickens. PloS ONE, 7, e48195.
http://dx.doi.org/10.1371/journal.pone.0048195
[6] Kogut, M.H., Genovese, K.J., He, H., Swaggerty, C.L. and Jiang, Y. (2013) Modulation of Chicken Intestinal Immune Gene Expression by Small Cationic Peptides as Feed Additives during the First Week Posthatch. Clinical and Vaccine Immunology, 9, 1440-1448. http://dx.doi.org/10.1128/CVI.00322-13
[7] Matulova, M., Varmuzova, K., Sisak, F., Havlickova, H., Babak, V., Stejskal, K., Zdrahal, Z. and Rychlik, I. (2013) Chicken Innateimmune Response to Oral Infection with Salmonella enterica Serovar Enteritidis. Veterinary Research, 44, 37. http://dx.doi.org/10.1186/1297-9716-44-37
[8] Kogut, M.H., Rothwell, L. and Kaiser, P. (2003) Differential Regulation of Cytokine Gene Expression by Avian Heterophils during Receptor-Mediated Phagocytosis of Opsonized and Nonopsonized Salmonella Enteritidis. Journal of Interferon & Cytokine Research, 23, 319-327. http://dx.doi.org/10.1089/107999003766628160
[9] Sebkova, A., Karasova, D., Crhanova, M., Budinska, E. and Rychlik, I. (2008) Aro Mutations in Salmonella enterica Cause Defects in Cell Wall and Outer Membrane Integrity. Journal of Bacteriology, 9, 3155-3160.
http://dx.doi.org/10.1128/JB.00053-08
[10] He, G.Z., Tian, W.Y., Qian, N., Cheng, A.C. and Deng, S.X. (2010) Quantitative Studies of the Distribution Pattern for Salmonella Enteritidis in the Internal Organs of Chicken after Oral Challenge by a Real-Time PCR. Veterinary Research Communications, 34, 669-676. http://dx.doi.org/10.1007/s11259-010-9438-6
[11] Toyofuku, H. (2008) Epidemiological Data on Food Poisonings in Japan Focused on Salmonella, 1998-2004. Food Additives & Contaminants, Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment, 25, 1058-1066.
[12] Yoshida, I., Hayashi, Y., Katayama, K. and Yamada, S. (1998) Bacteriological and Virological Studies on the Cause of Sporadic Acute Gastroenteritis in Tama, Tokyo (1991-1996). Kansenshogaku Zasshi, 72, 599-608.
[13] Murase, M., Kurokawa, M., Nukina, M., Nakanishi, H. and Haruta, T. (2001) Surveillance of Various Enteropathogenic Bacteria from Diarrheal Cases during 1989-1999 in Kobe City. Kansenshogaku Zasshi, 75, 883-893.
[14] Esaki, H., Shimura, K., Yamazaki, Y., Eguchi, M. and Nakamura, M. (2013) National Surveillance of Salmonella Enteritidis in Commercial Eggs in Japan. Epidemiology and Infection, 141, 941-943.
http://dx.doi.org/10.1017/S0950268812001355
[15] Ekawa, T., Terai, S., Amano, F., Hanatani, Y. and Ohta, H. (2009) Diverse Pathogenicity of Salmonella Enteritidis Clones Isolated from Poultry Farms in Chicks and BALB/c Mice. Japanese Journal of Poultry Science, 46, 370-376.
http://dx.doi.org/10.2141/jpsa.46.370
[16] Chart, H., Rowe, B., Baskerville, A. and Humphrey, T.J. (1990) Serological Response of Chickens to Salmonella Enteritidis Infection. Epidemiology and Infection, 104, 63-71. http://dx.doi.org/10.1017/S0950268800054534
[17] Guard-Petter, J. (1998) Variants of Smooth Salmonella enterica Serovar Enteritidis That Grow to Higher Cell Density than the Wild Type Are More Virulent. Applied and Environmental Microbiology, 64, 2166-2172.
[18] Guard-Petter, J., Keller, L.H., Rahman, M.M., Carlson, R.W. and Silvers, S. (1996) A Novel Relationship between O-Antigen Variation, Matrix Formation, and Invasiveness of Salmonella Enteritidis. Epidemiology and Infection, 117, 219-231. http://dx.doi.org/10.1017/S0950268800001394
[19] Parker, C.T., Liebana, E., Henzler, D.J. and Guard-Petter, J. (2001) Lipopolysaccharide O-Chain Microheterogeneity of Salmonella Serotypes Enteritidis and Typhimurium. Environmental Microbiology, 3, 332-342.
http://dx.doi.org/10.1046/j.1462-2920.2001.00200.x
[20] Ross, I.L. and Heuzenroeder, M.W. (2009) A Comparison of Two PCR-Based Typing Methods with Pulsed-Field Gel Electrophoresis in Salmonella enterica Serovar Enteritidis. International Journal of Medical Microbiology, 299, 410-420. http://dx.doi.org/10.1016/j.ijmm.2008.12.002
[21] Arii, J., Tanabe, Y., Miyake, M., Mukai, T., Matsuzaki, M., Niinomi, N., Watanabe, H., Yokota, Y., Kohno, Y. and Noda, M. (2002) Clinical and Pathologic Characteristics of Nontyphoidal Salmonella Encephalopathy. Neurology, 58, 1641-1645. http://dx.doi.org/10.1212/WNL.58.11.1641
[22] Crhanova, M., Hradecka, H., Faldynova, M., Matulova, M., Havlickova, H., Sisak, F. and Rychlik, I. (2011) Immune Response of Chicken Gut to Natural Colonization by Gut Microflora and to Salmonella enterica Serovar Enteritidis Infection. Infection and Immunity, 79, 2755-2763. http://dx.doi.org/10.1128/IAI.01375-10
[23] Matiasovic, J., Stepanova, H., Volf, J., Kubala, L., Ovesna, P., Rychlik, I. and Faldyna, M. (2011) Influence of the Lipo-polysaccharide Structure of Salmonella enterica Serovar Enteritidis on Interactions with Pig Neutrophils. Veterinary Microbiology, 150, 167-172. http://dx.doi.org/10.1016/j.vetmic.2011.01.007
[24] Mitra, A., Loh, A., Gonzales, A., Laniewski, P., Willingham, C., Curtiss III, R. and Roland, K.L. (2013) Safety and Protective Efficacy of Live Attenuated Salmonella Gallinarum Mutants in Rhode Island Red Chickens. Vaccine, 31, 1094-1099. http://dx.doi.org/10.1016/j.vaccine.2012.12.021
[25] Ohta, H. and Toyota-Hanatani, Y. (2012) Salmonella enterica Serovar Enteritidis (SE) Infection in Chickens and Its Public-Health-Risk Control Using an SE Vaccine in Layer Flocks. In: Kumar, Y., Ed., Salmonella, Intech, 279-308.
http://dx.doi.org/10.5772/29068
[26] Burkholder, K.M., Thompson, K.L., Einstein, M.E., Applegate, T.J. and Patterson, J.A. (2008) Influence of Stressors on Normal Intestinal Microbiota, Intestinal Morphology, and Susceptibility to Salmonella enteritidis Colonization in Broilers. Poultry Science, 87, 1734-1741. http://dx.doi.org/10.3382/ps.2008-00107
[27] Coward, C., Sait, L., Williams, L., Humphrey, T.J., Cogan, T. and Maskell, D.J. (2012) Investigation into the Role of Five Salmonella enterica Serovar Enteritidis Genomic Islands in Colonization of the Chicken Reproductive Tract and Other Organs Following Oral Challenge. FEMS Microbiology Letters, 336, 73-78.
http://dx.doi.org/10.1111/j.1574-6968.2012.02652.x
[28] Allen-Vercoe, E., Dibb-Fuller, M., Thorns, C.J. and Woodward, M.J. (1997) SEF17 Fimbriae Are Essential for the Convoluted Colonial Morphology of Salmonella enteritidis. FEMS Microbiology Letters, 153, 33-42.
http://dx.doi.org/10.1111/j.1574-6968.1997.tb10460.x
[29] Altekruse, S., Koehler, J., Hickman-Brenner, F., Tauxe, R.V. and Ferris, K. (1993) A Comparison of Salmonella enteritidis Phage Types from Egg-Associated Outbreaks and Implicated Laying Flocks. Epidemiology and Infection, 110, 17-22. http://dx.doi.org/10.1017/S0950268800050639
[30] Bravo, D., Carter, J.A., Hoare, A., Alvarez, S.A., Blondel, C.J., Zaldiveno, M.A., Valvono, M.A. and Contreras, I. (2008) Growth-Phase Regulation of Lipopolysaccharide O-Antigen Chain Length Influences Serum Resistance in Serovars of Salmonella. Journal of Medical Microbiology, 57, 938-946. http://dx.doi.org/10.1099/jmm.0.47848-0
[31] Mizumoto, N., Toyota-Hanatani, Y., Sasai, K., Tani, H., Ekawa, T., Ohta, H. and Baba, E. (2004) Detection of Specific Antibodies against Deflagellated Salmonella Enteritidis and S. Enteritidis Fli C-Specific 9 kDa Polypeptide. Veterinary Microbiology, 99, 113-120. http://dx.doi.org/10.1016/j.vetmic.2003.11.009
[32] Piao, Z., Toyota-Hanatani, Y., Ohta, H., Sasai, K., Tani, H. and Baba, E. (2007) Effects of Salmonella enterica subsp. enterica Serovar Enteritidis Vaccination in Layer Hens Subjected to S. Enteritidis Challenge and Various Feed Withdrawal Regimens. Veterinary Microbiology, 125, 111-119. http://dx.doi.org/10.1016/j.vetmic.2007.05.008
[33] Okamura, M., Lillehoj, H.S., Raybourne, R.B., Babu, U. and Heckert, R. (2003) Antigen-Specific Lymphocyte Proliferation and Interleukin Production in Chickens Immunized with Killed Salmonella Enteritidis Vaccine or Experimental Subunit Vaccines. Avian Diseases, 47, 1331-1338. http://dx.doi.org/10.1637/6096
[34] Toyota-Hanatani, Y., Kyoumoto, Y., Baba, E., Ekawa, T., Ohta, H., Tani, H. and Sasai, K. (2009) Importance of Subunit Vaccine Antigen of Major Fli C Antigenic Site of Salmonella Enteritidis II: A Challenge Trial. Vaccine, 27, 1680-1684.
http://dx.doi.org/10.1016/j.vaccine.2009.01.024
[35] Miyamoto, T., Horie, T., Fukata, T., Sasai, K. and Baba, E. (1998) Changes in Microflora of the Cloaca and Oviduct of Hens after Intracloacal or Intravaginal Inoculation with Salmonella Enteritidis. Avian Diseases, 42, 536-544.
http://dx.doi.org/10.2307/1592680
[36] Coward, C., Sait, L., Cogan, T., Humphrey, T.J. and Maskell, D.J. (2013) O-Antigen Repeat Number in Salmonella enterica Serovar Enteritidis Is Important for Egg Contamination, Colonization of Chicken Reproductive Tract and Survival in Egg Albumen. FEMS Microbiology Letters, 343, 169-176. http://dx.doi.org/10.1111/1574-6968.12143
[37] Guard-Petter, J., Parker, C.T., Asokan, K. and Carlson, R.W. (1999) Clinical and Veterinary Isolates of Salmonella enterica Serovar Enteritidis Defective in Lipopolysaccharide O-Chain Polymerization. Applied and Environmental Microbiology, 65, 2195-2201.
[38] Kawahara, K., Hamaoka, T., Suzuki, S., Nakamura, M., Murayama, S.Y., Arai, T., Terakado, N. and Danbara, H. (1989) Lipopolysaccharide Alteration Mediated by the Virulence Plasmid of Salmonella. Microbial Pathogenesis, 7, 195-202.
http://dx.doi.org/10.1016/0882-4010(89)90055-7
[39] Ohta, H., Yoshikawa, Y., Kai, C., Yamanouchi, K. and Okada, H. (1984) Lysis of Horse Red Blood Cells Mediated by Antibody-Independent Activation of the Alternative Pathway of Chicken Complement. Immunology, 52, 437-444.
[40] Cogan, T.A. and Humphrey, T.J. (2003) The Rise and Fall of Salmonella Enteritidis in the UK. Journal of Applied Microbiology, 94, 114-119. http://dx.doi.org/10.1046/j.1365-2672.94.s1.13.x
[41] Cowden, J.M., Chisholm, D., O’Manhony, M., Lynch, D., Mawer, S.L., Spain, G.E., Ward, L. and Rowe, B. (1989) Two Outbreaks of Salmonella enteritidis Phage Type 4 Infection Associated with the Consumption of Fresh Shell-Egg Products. Epidemiology and Infection, 103, 47-52. http://dx.doi.org/10.1017/S095026880003034X
[42] Guard-Petter, J. (2001) The Chicken, the Egg and Salmonella enteritidis. Environmental Microbiology, 3, 421-430.
http://dx.doi.org/10.1046/j.1462-2920.2001.00213.x

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