The "decline and Fall" of Nontyphoidal Salmonella in the United Kingdom

Overview

Journal Clin Infect Dis

Publisher Oxford University Press

Specialty Infectious Diseases

Date 2012 Nov 21

PMID 23166188

Citations 54

Authors

Sarah J OBrien

Affiliations

Soon will be listed here.

Abstract

Remarkable changes in the epidemiology of human nontyphoidal salmonellosis have occurred in the United Kingdom over the last century. Between 1981 and 1991, the incidence of nontyphoidal salmonellosis in the United Kingdom rose by >170%, driven primarily by an epidemic of Salmonella enterica subspecies enterica serovar Enteritidis phage type (PT) 4, which peaked in 1993. Measures introduced to control this epidemic included legislation, food safety advice, and an industry-led vaccination program in broiler-breeder and laying poultry flocks. The incidence of Salmonella Enteritidis has been falling since 1997, and levels of Salmonella Enteritidis PT4 have fallen to preepidemic levels and have stayed low. The temporal relationship between vaccination programs and the reduction in human disease is compelling and suggests that these programs have made a major contribution to improving public health.

Citing Articles

Effect of vaccine diluents on the colonization of Typhimurium vaccine in chickens.

Jia S, McWhorter A, Khan S, Willson N, Andrews D, Underwood G Vet Anim Sci. 2024; 26:100409.

PMID: 39619868 PMC: 11607656. DOI: 10.1016/j.vas.2024.100409.

An Approach to Describe Salmonella Serotypes of Concern for Outbreaks: Using Burden and Trajectory of Outbreak-related Illnesses Associated with Meat and Poultry.

Marshall K, Cui Z, Gleason B, Hartley C, Wise M, Bruce B J Food Prot. 2024; 87(9):100331.

PMID: 39032785 PMC: 11366486. DOI: 10.1016/j.jfp.2024.100331.

Early vaccination of laying hens with the live bivalent vaccine AviPro™ Salmonella DUO results in successful vaccine uptake and increased gut colonization.

Cawthraw S, Goddard A, Huby T, Ring I, Chiverton L, Mueller-Doblies D Front Microbiol. 2024; 14:1327739.

PMID: 38293556 PMC: 10825957. DOI: 10.3389/fmicb.2023.1327739.

The Detection of Enteritidis on German Layer Farms after Cleaning and Disinfection.

Munster P, Poppel L, Antakli A, Muller-Doblies D, Radko D, Kemper N Animals (Basel). 2023; 13(16).

PMID: 37627379 PMC: 10451266. DOI: 10.3390/ani13162588.

Can foodborne illness estimates from different countries be legitimately compared?: case study of rates in the UK compared with Australia, Canada and USA.

Holland D, Clifford R, Mahmoudzadeh N, OBrien S, Poppy G, Meredith Z BMJ Open Gastroenterol. 2023; 10(1).

PMID: 36717154 PMC: 9887690. DOI: 10.1136/bmjgast-2022-001009.

References

Havelaar A, Ivarsson S, Lofdahl M, Nauta M . Estimating the true incidence of campylobacteriosis and salmonellosis in the European Union, 2009. Epidemiol Infect. 2012; 141(2):293-302. PMC: 9152072. DOI: 10.1017/S0950268812000568. View

Coyle E, Palmer S, Ribeiro C, Jones H, Howard A, Ward L . Salmonella enteritidis phage type 4 infection: association with hen's eggs. Lancet. 1988; 2(8623):1295-7. DOI: 10.1016/s0140-6736(88)92902-9. View

Tam C, Rodrigues L, Viviani L, Dodds J, Evans M, Hunter P . Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut. 2011; 61(1):69-77. PMC: 3230829. DOI: 10.1136/gut.2011.238386. View

Little C, Surman-Lee S, Greenwood M, Bolton F, Elson R, Mitchell R . Public health investigations of Salmonella Enteritidis in catering raw shell eggs, 2002-2004. Lett Appl Microbiol. 2007; 44(6):595-601. DOI: 10.1111/j.1472-765X.2007.02131.x. View

Cowden J, Chisholm D, OMahony M, Lynch D, Mawer S, Spain G . Two outbreaks of Salmonella enteritidis phage type 4 infection associated with the consumption of fresh shell-egg products. Epidemiol Infect. 1989; 103(1):47-52. PMC: 2249496. DOI: 10.1017/s095026880003034x. View

Kessel A, Gillespie I, OBrien S, Adak G, Humphrey T, Ward L . General outbreaks of infectious intestinal disease linked with poultry, England and Wales, 1992-1999. Commun Dis Public Health. 2001; 4(3):171-7. View

Pires S, Vigre H, Makela P, Hald T . Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe. Foodborne Pathog Dis. 2010; 7(11):1351-61. DOI: 10.1089/fpd.2010.0564. View

Ward L, Threlfall J, Smith H, OBrien S . Salmonella enteritidis epidemic. Science. 2001; 287(5459):1753-4; author reply 1755-6. DOI: 10.1126/science.287.5459.1753d. View

Noble D, Lane C, Little C, Davies R, de Pinna E, Larkin L . Revival of an old problem: an increase in Salmonella enterica serovar Typhimurium definitive phage type 8 infections in 2010 in England and Northern Ireland linked to duck eggs. Epidemiol Infect. 2011; 140(1):146-9. DOI: 10.1017/S0950268811000586. View

10.

Cogan T, Humphrey T . The rise and fall of Salmonella Enteritidis in the UK. J Appl Microbiol. 2003; 94 Suppl:114S-119S. DOI: 10.1046/j.1365-2672.94.s1.13.x. View

11.

Gormley F, Little C, Rawal N, Gillespie I, Lebaigue S, Adak G . A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992-2008). Epidemiol Infect. 2010; 139(5):688-99. DOI: 10.1017/S0950268810001858. View

12.

Adak G, Meakins S, Yip H, Lopman B, OBrien S . Disease risks from foods, England and Wales, 1996-2000. Emerg Infect Dis. 2005; 11(3):365-72. PMC: 3298246. DOI: 10.3201/eid1103.040191. View

13.

Cowden J, Lynch D, Joseph C, OMahony M, Mawer S, Rowe B . Case-control study of infections with Salmonella enteritidis phage type 4 in England. BMJ. 1989; 299(6702):771-3. PMC: 1837639. DOI: 10.1136/bmj.299.6702.771. View

14.

Gajraj R, Pooransingh S, Hawker J, Olowokure B . Multiple outbreaks of Salmonella braenderup associated with consumption of iceberg lettuce. Int J Environ Health Res. 2011; 22(2):150-5. DOI: 10.1080/09603123.2011.613114. View

15.

Barrow P . Salmonella control--past, present and future. Avian Pathol. 1993; 22(4):651-69. DOI: 10.1080/03079459308418954. View

16.

Humphrey T, Whitehead A, Gawler A, Henley A, Rowe B . Numbers of Salmonella enteritidis in the contents of naturally contaminated hens' eggs. Epidemiol Infect. 1991; 106(3):489-96. PMC: 2271858. DOI: 10.1017/s0950268800067546. View

17.

Gast R, Guraya R, Guard J, Holt P . The relationship between the numbers of Salmonella Enteritidis, Salmonella Heidelberg, or Salmonella Hadar colonizing reproductive tissues of experimentally infected laying hens and deposition inside eggs. Avian Dis. 2011; 55(2):243-7. DOI: 10.1637/9540-092810-Reg.1. View

18.

Gillespie I, OBrien S, Adak G, Ward L, Smith H . Foodborne general outbreaks of Salmonella Enteritidis phage type 4 infection, England and Wales, 1992-2002: where are the risks?. Epidemiol Infect. 2005; 133(5):795-801. PMC: 2870308. DOI: 10.1017/S0950268805004474. View

19.

Wahlstrom H, Andersson Y, Plym-Forshell L, Pires S . Source attribution of human Salmonella cases in Sweden. Epidemiol Infect. 2010; 139(8):1246-53. DOI: 10.1017/S0950268810002293. View

20.

Snow L, Davies R, Christiansen K, Carrique-Mas J, Wales A, OConnor J . Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Vet Rec. 2007; 161(14):471-6. DOI: 10.1136/vr.161.14.471. View