Ahead of Print -Salmonella enterica Serovar Enteritidis, England and Wales, 1945–2011 - Volume 20, Number 7—July 2014 - Emerging Infectious Disease journal - CDC

full-text ►

Ahead of Print -Salmonella enterica Serovar Enteritidis, England and Wales, 1945–2011 - Volume 20, Number 7—July 2014 - Emerging Infectious Disease journal - CDC

Volume 20, Number 7—July 2014

Synopsis

Salmonella enterica Serovar Enteritidis, England and Wales, 1945–2011

Article Contents

• Methods
• Results
• Discussion
• Acknowledgment
• References
• Figure 1
• Figure 2
• Figure 3
• Figure 4
• Figure 5
• Figure 6
• Table
• Suggested Citation

Christopher R. Lane, Susan LeBaigue, Oluwaseun B. Esan, Adedoyin A. Awofisyo, Natalie L. Adams, Ian S.T. Fisher, Kathie A. Grant, Tansy M. Peters, Lesley Larkin, Robert H. Davies, and Goutam K. Adak 

Author affiliations: Public Health England, London, UK (C.R. Lane, S. LeBaigue, O.B. Esan, A.A. Awofisayo, N.L. Adams, I.S.T. Fisher, K.A. Grant, T.M. Peters, G.K. Adak); Animal Health and Veterinary Laboratories Agency, London (L. Larkin, R.H. Davies)

Suggested citation for this article

Abstract

In England and Wales, the emergence of Salmonella enterica serovar Enteritidis resulted in the largest and most persistent epidemic of foodborne infection attributable to a single subtype of any pathogen since systematic national microbiological surveillance was established. We reviewed 67 years of surveillance data to examine the features, underlying causes, and overall effects of S. enterica ser. Enteritidis. The epidemic was associated with the consumption of contaminated chicken meat and eggs, and a decline in the number of infections began after the adoption of vaccination and other measures in production and distribution of chicken meat and eggs. We estimate that >525,000 persons became ill during the course of the epidemic, which caused a total of 6,750,000 days of illness, 27,000 hospitalizations, and 2,000 deaths. Measures undertaken to control the epidemic have resulted in a major reduction in foodborne disease in England and Wales.

A pandemic of Salmonella enterica serovar Enteritidis infection was recognized by epidemiologists in the United States in the late 1970s; a 6-fold rise in these infections was observed in northeastern United States during 1976–1986 (1). A review of outbreak investigations revealed that 27 (77%) of 35 outbreaks were associated with the consumption of foods containing grade A eggs (1). The most commonly reported phage types were SE8, SE13, and SE13a. In 1990, the World Health Organization reviewed Salmonella surveillance data for 1979–1987 and found that isolation rates for S. enterica ser. Enteritidis had increased in 24 of the 35 nations that provided data. Increases were recorded in countries from every continent except Asia (2). Evidence from outbreak investigations in Spain, Hungary, France, Norway, and the United States implicated eggs (3). Microbiologicical investigations conducted in the United Kingdom also showed the presence of phage type SE4 in chicken meat (4) and raw shell eggs (5,6). In 1988, the UK Public Health Laboratory Service Communicable Disease Surveillance Centre conducted a case–control study of primary sporadic SE4 infections in England. The investigators demonstrated associations between human infection and the consumption of chicken and raw egg dishes (7). We reviewed national surveillance and research data to examine the factors underlying the epidemic of S. enterica ser. Enteritidis and to estimate its overall impact on the population of England and Wales.

Methods

Surveillance of S. enterica Infections and Other Intestinal Diseases in England and Wales

Systematic national surveillance of laboratory-confirmed salmonellosis in humans in England and Wales has been in continuous operation since 1945. Diagnostic laboratories refer all Salmonellaisolates to the national reference laboratory for confirmation and characterization, and data on all first confirmations are entered into a national surveillance database (8).

We extracted data from this database to provide annual totals for human infection with S. enterica by serotype and phage type. Multipliers derived from previous studies (9–11) were applied to the number of laboratory reports received to produce estimates of the numbers of community cases, days of illness, hospitalizations, hospital bed-days occupied, and deaths for 1982–1987, 1988–1998, and 1999–2011 that were attributable to SE4. Multipliers published in 1996 (9) were used for the emergence and epidemic stages and those from 2008 (10) for the decline stage.

In addition, local health protection units return standardized data (i.e., etiology, outbreak location, morbidity/mortality rates, vehicles of infection, and evidence of association) on all detected general outbreaks of infectious intestinal diseases to national surveillance (12). These data are also stored in a dedicated database.

Surveillance of S. enterica in Poultry

Data on Salmonella spp. in poultry in Great Britain (England, Wales, and Scotland) are reported by the Animal Health and Veterinary Laboratory Agency (13). A Salmonella incident is defined as the first isolation of a given serovar from a particular animal, group of animals, or their environment on a single premises within a defined period (usually 30 days) (13).

Data Analyses

Data were abstracted from the national surveillance databases described above. Descriptive analyses were done in Microsoft Excel 2007 (Microsoft Corporation, Redmond, WA, USA); 95% CIs of the estimates of the burden of disease in the community were calculated from the upper and lower confidence limits reported in previous studies (9,10). All statistical analyses were performed by using Stata version 12 (StataCorp LP, College Station, TX, USA).

Mr Lane is an epidemiologist at Public Health England in London. He works in gastrointestinal disease surveillance, mainly focusing on the epidemiology of salmonellosis.

Acknowledgment

We thank the microbiologists, health protection, and environmental health specialists that have contributed data and reports to national surveillance systems and the epidemiologists and information officers who have worked on the national surveillance of intestinal infectious diseases for Centre for Infectious Disease Surveillance and Control and Health Protection Services Colindale.

References

1. St Louis ME, Morse DL, Potter ME, DeMelfi TM, Guzewich JJ, Taux RV, The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. JAMA. 1988;259:2103–7. DOIPubMed
2. Poppe C. Epidemiology of Salmonella enterica serovar Enteritidis. In: Saeed AM, Gast RK, Potter ME, Wall PG, editors. Salmonella enterica serovar Enteritidis in humans and animals: epidemiology, pathogenesis and control. Ames (IA): Iowa State University Press; 1999. p. 3–18.
3. Rodrigue DC, Tauxe RV, Rowe B. International increase in Salmonella enteritidis: a new pandemic? Epidemiol Infect. 1990;105:21–7. DOIPubMed
4. Humphrey TJ, Mead GC, Rowe B. Poultry meat as a source of human salmonellosis in England and Wales. Epidemiol Infect. 1988;100:175–84. DOIPubMed
5. Mawer SL, Spain GE, Rowe B. Salmonella Enteritidis phage type 4 and hens’ eggs.Lancet. 1989;333:280–1. DOIPubMed
6. Humphrey TJ, Baskerville A, Mawer S, Rowe B, Hopper S. Salmonella Enteritidis phage type 4 from the contents of intact eggs: a study involving naturally infected hens.Epidemiol Infect. 1989;103:415–23. DOIPubMed
7. Cowden JM, Lynch D, Joseph CA, O’Mahony M, Mawer SL, Rowe B, Case-control study of infections with Salmonella enteritidis phage type 4 in England. BMJ. 1989;299:771–3. DOIPubMed
8. Wall PG, de Louvois J, Gilbert RJ, Rowe B. Food poisoning: notifications, laboratory reports and outbreaks—where do the statistics come from and what do they mean?Commun Dis Rep CDR Rev. 1996;6:93–100. PMID: 8680502
9. Food Standards Agency. A report of the study of infectious intestinal disease in England. London: The Stationery Office; 2001.
10. Food Standards Agency. The second study of infectious intestinal disease in the community. London: The Food Standards Agency; 2012.
11. Adak GK, Long SM. O’Brien. Trends in indigenous foodborne disease and death, England and Wales: 1992–2000. Gut. 2002;51:832–41. DOIPubMed
12. Gormley FJ, Little CL, Rawal N, Gillespie IA, LeBaigue S, Adak GK. A 17 year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992–2008). Epidemiol Infect. 2011;139:688–99. DOIPubMed
13. Veterinary Laboratories Agency. Salmonella in livestock production in GB—2011 report [cited 2012 Oct 10].http://vla.defra.gov.uk/reports/rep_salm_rep11.htm
14. Committee on the Microbiological Safety of Food. The microbiological safety of food. Part1. London: The Stationery Office; 1990.
15. McCoy JH. Trends in salmonella food poisoning in England and Wales 1941–72. J Hyg (Lond). 1975;74:271–82. DOIPubMed
16. Advisory Committee on the Microbiological Safety of Food. Report on microbial antibiotic resistance in relation to food safety. London: The Stationery Office; 1999.
17. Evans SJ, Davies RH, Wray C. Epidemiology of Salmonella enterica serovar Enteritidis infection in British poultry flocks. In: Saeed AM, Gast RK, Potter ME, Wall PG, editors.Salmonella enterica serovar Enteritidis in humans and animals: epidemiology, pathogenesis and control. Ames (IA): Iowa State University Press; 1999. p. 313–324.
18. Bullis KL. The history of avian medicine in the US. II. Pullorum disease and fowl typhoid.Avian Dis. 1977;21:422–9. DOIPubMed
19. Bäumler AJ, Hargis BM, Tsolis RM. Tracing the origins of Salmonella outbreaks. Science.2000;287:50–2. DOIPubMed
20. Little CL, Rhoades JR, Hucklesby L, Greenwood M, Surman-Lee S, Bolton FJ, Survey ofSalmonella contamination of raw shell eggs used in food service premises in the United Kingdom, 2005 through 2006. J Food Prot. 2008;71:19–26.PubMed
21. Department of Environment, Food and Rural Affairs. UK national control programme for salmonella in breeding flocks (Gallus gallus). 2005 [cited 2012 Oct 10].http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/zoonoses/documents/salmonella-breeders.pdf 
22. Department of Environment. Food and Rural Affairs. UK national control programme for salmonella in layers (Gallus gallus). 2007 [cited 2012 Oct 10].http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/zoonoses/documents/salmonella-layers.pdf 
23. The British Lion code of practice [cited 2012 Oct 10].http://www.egginfo.co.uk/british-lion-code-practice
24. Patrick ME, Adcock PM, Gomez TM, Altecruse SF, Holland BH, Tauxe RV, SalmonellaEnteritidis infections, United States, 1985–1999. Emerg Infect Dis. 2004;10:1–7. DOIPubMed
25. Wegener HC, Hald T, Lo Fo Wong D, Madsen M, Korsgaard H, Bager F, Salmonella control programs in Denmark. Emerg Infect Dis. 2003;9:774–80. DOIPubMed
26. European Food Safety Authority Panel on Biological Hazards. Scientific opinion on quantitative estimation of the public health impact of setting a new target for the reduction of the Salmonella in laying hens [cited 2012 Oct 10].http://www.efsa.europa.eu/en/efsajournal/doc/1546.pdf 
27. European Food Safety Authority and European Centre for Disease Control and Prevention. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. [cited 2012 Oct 10].http://www.efsa.europa.eu/en/efsajournal/doc/2597.pdf 
28. Centers for Disease Control and Prevention. Investigation update: multistate outbreak of human Salmonella Enteritidis infections associated with shell eggs [cited 2012 Oct10].http://www.cdc.gov/salmonella/enteritidis
29. Fisher IST; Enter-net participants. 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. Euro Surveill. 2004;9:43–5.PubMed
30. Health Protection Agency. S. Enteritidis infections in England in 2009: national case–control study report [cited 2012 Oct10].http://www.hpa.org.uk/hpr/archives/2010/hpr0610.pdf 
31. Gormley FJ, Rawal N, Little CL. Choose your menu wisely: cuisine-associated food-poisoning risks in restaurants in England and Wales. Epidemiol Infect.2012;140:997–1007. DOIPubMed

Figures

• Figure 1. Laboratory reporting of Salmonella enterica infections in England and Wales, 1945–2011Emergence stage, 1982–1987; epidemic stage, 1988–1998; decline stage, 1999–2011Ser., serovar.
• Figure 2. Laboratory reporting of indigenously acquired Salmonella enterica serovar Enteritidis infections in England and Wales, 1982–2011Emergence stage, 1982–1987; epidemic stage, 1988–1998; decline stage, 1999–2011SE4, S. enterica serEnteritidis phage type 4....
• Figure 3. Trends in the pathogens associated with general outbreaks of foodborne infection in England and Wales, 1992–2011SE4, Salmonella enterica serovar Enteritidis phage type 4.
• Figure 4. Trends in the reporting of general outbreaks of salmonellosis associated with the consumption of eggs in England and Wales 1992–2011SE4, Salmonella enterica serovar Enteritidis phage type 4.
• Figure 5. Trends in the reporting of incidents of Salmonella enterica in chickens in Great Britain versus laboratory reporting of human S. enterica serovar Enteritidis infection, England and Wales, 1985–2011SE4, S....
• Figure 6. Trends in reporting of Salmonella enterica serovar Enteritidis phage type 4 (SE4), extrapolated burden of disease, and estimated number of cases prevented by SE4 elimination programs, England and Wales,...

Table

• Table. Estimated rates of disease attributable to Salmonella enterica serovar Enteritidis phage type 4 during 3 periods, England and Wales, 1982–2011

Suggested citation for this article: Lane CR, LeBaigue S, Esan OB, Awofisyo AA, Adams NL, Fisher, IST. Salmonella enterica serovar Enteritidis, England and Wales, 1945–2011. Emerg Infect Dis [Internet]. 2014 Jul [date cited]. http://dx.doi.org/10.3201/eid2007.121850

DOI: 10.3201/eid2007.121850