Drastic decrease of Salmonella Enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks

SUMMARY In Belgium, non-typhoidal salmonellosis and campylobacteriosis are the two most frequently reported foodborne illnesses. During 2005, a 71% decrease of Salmonella Enteritidis infections compared with the average annual number cases in the period 2000–2004 was recorded by the Belgian National Reference Centre for Salmonella and Shigella. After the peak of 1999, the total number of salmonellosis cases decreased gradually, with the exception of 2003 when an increase was again recorded due to the rise of isolates belonging to the serotype Enteritidis. PT4, the predominant phage type of serotype Enteriditis over recent years (except in 2003), became the second most prevalent phage type in 2005 after PT21. We present in this paper the epidemiology (incidence and trends) of human salmonellosis in Belgium and assess the role of the vaccination programme in layer flocks on the decline of the incidence of human salmonellosis and foodborne outbreaks due to S. Enteritidis.

[1]  F. Boyen,et al.  Oral immunisation of laying hens with the live vaccine strains of TAD Salmonella vac E and TAD Salmonella vac T reduces internal egg contamination with Salmonella Enteritidis. , 2006, Vaccine.

[2]  K. Ekdahl,et al.  The comparative burden of salmonellosis in the European Union member states, associated and candidate countries , 2006, BMC public health.

[3]  Y. V. van Duynhoven,et al.  Risk factors for Salmonella Enteritidis and Typhimurium (DT104 and non-DT104) infections in The Netherlands: predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections , 2005, Epidemiology and Infection.

[4]  Yasmine Ghafir,et al.  Belgian surveillance plans to assess changes in Salmonella prevalence in meat at different production stages. , 2005, Journal of food protection.

[5]  M. Drake,et al.  A simple method for the direct detection of Salmonella and Escherichia coli O157:H7 from raw alfalfa sprouts and spent irrigation water using PCR. , 2005, Journal of food protection.

[6]  R. Ducatelle,et al.  Vaccination and early protection against non-host-specific Salmonella serotypes in poultry: exploitation of innate immunity and microbial activity , 2005, Epidemiology and Infection.

[7]  V. Bremer,et al.  Syphilis surveillance and trends of the syphilis epidemic in Germany since the mid-90s. , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[8]  N. Dupin,et al.  Syphilis surveillance in France, 2000-2003. , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[9]  I. Fisher.  Dramatic shift in the epidemiology of Salmonella enterica serotype Enteritidis phage types in western Europe, 1998-2003 - results from the Enter-net international salmonella database. , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[10]  I. Fisher.  International trends in salmonella serotypes 1998-2003 - a surveillance report from the Enter-net international surveillance network. , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[11]  S. Kovats,et al.  A large increase of Salmonella infections in 2003 in the Netherlands: hot summer or side effect of the avian influenza outbreak? , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[12]  P. Cieslak,et al.  Hospitalizations and deaths due to Salmonella infections, FoodNet, 1996-1999. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[13]  P. Cieslak,et al.  FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[14]  S. Salmaso,et al.  Rubella control in Italy. , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[15]  T. Humphrey,et al.  The rise and fall of Salmonella Enteritidis in the UK , 2003, Journal of applied microbiology.

[16]  A. Kyriakides,et al.  Salmonella: A Practical Approach to the Organism and its Control in Foods , 2001 .

[17]  C. Kemp,et al.  Four linked outbreaks of Salmonella enteritidis phage type 4 infection--the continuing egg threat. , 2000, Communicable disease and public health.

[18]  J. Prescott,et al.  Salmonella enterica serovar enteritidis in humans and animals : epidemiology, pathogenesis, and control , 1999 .

[19]  I. Fisher.  The Enter-net international surveillance network - how it works. , 1999, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[20]  J. Desenclos,et al.  Risk factors for the occurrence of sporadic Salmonella enterica serotype enteritidis infections in children in France: a national case-control study , 1998, Epidemiology and Infection.

[21]  A. A. Fadl,et al.  Genotypic evaluation of Salmonella enteritidis isolates of known phage types by arbitrarily primed polymerase chain reaction. , 1997, Avian diseases.

[22]  R. Tauxe,et al.  Outbreaks of Salmonella enteritidis infections in the United States, 1985-1991. , 1994, The Journal of infectious diseases.

[23]  A. Rampling.  Salmonella enteritidis five years on , 1993, The Lancet.

[24]  S. Altekruse,et al.  A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks , 1993, Epidemiology and Infection.

[25]  L. Budnick,et al.  A nosocomial outbreak of Salmonella enteritidis infection due to the consumption of raw eggs. , 1990, The New England journal of medicine.

[26]  R. Tauxe,et al.  International increase in Salmonella enteritidis: A new pandemic? , 1990, Epidemiology and Infection.

[27]  J. Cowden,et al.  Case-control study of infections with Salmonella enteritidis phage type 4 in England. , 1989, BMJ.

[28]  R. Tauxe,et al.  The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. , 1988, JAMA.

[29]  S. Schroeder,et al.  Salmonellosis in the United States--a five-year review. , 1970, American journal of epidemiology.

[30]  Moez Sanaa,et al.  Review of the Community Summary Report on Trends and Sources of Zoonoses, Zoonotic agents and Antimicrobial Resistance in the European Union in 2005 Scientific Opinion of the Scientific Panel on Biological Hazards (BIOHAZ) and Animal Health and Welfare (AHAW) , 2007 .

[31]  Large variation in prevalence of salmonella in laying hen flocks in EU: EFSA preliminary report. , 2006, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[32]  I. Fisher.  Dramatic shift in the epidemiology of Salmonella enterica serotype Enteritidis phage types in western Europe, 1998-2003--results from the Enter-net international salmonella database. , 2004, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[33]  S. Ladely,et al.  Salmonella enterica Serotype enteritidis in Table Egg Layer House Environments and in Mice in U.S. Layer Houses and Associated Risk Factors , 2003, Avian diseases.

[34]  J. D. de Wit,et al.  Vaccination against Salmonella enteritidis in Dutch commercial layer flocks with a vaccine based on a live Salmonella gallinarum 9R strain: evaluation of efficacy, safety, and performance of serologic Salmonella tests. , 2001, Avian diseases.

[35]  S. Palmer,et al.  Undercooked hens eggs remain a risk factor for sporadic Salmonella enteritidis infection. , 1999, Communicable disease and public health.

[36]  It Istituto Superiore di Sanit,et al.  Epidemiology of Salmonella enterica serovar enteritidis infections in Italy , 1999 .

[37]  M. Popoff.  Antigenic formulas of the Salmonella serovars , 1997 .

[38]  E. Threlfall,et al.  The identification, typing and fingerprinting of Salmonella: laboratory aspects and epidemiological applications. , 1990, The Journal of applied bacteriology.