Producing Safe Eggs. Microbial Ecology of Salmonella

431 Pages·2016·5.073 MB·English

by  Steven C Ricke, Richard K Gast

Producing Safe Eggs
Microbial Ecology of Salmonella
Edited by
Steven C. Ricke
Richard K. Gast
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List of Contributors
Sandra Aehle
Elanco Animal Health, Inc., Pacific, MO, United States
Paul Barrow
University of Nottingham, Loughborough, Leicestershire, United Kingdom
Dante Javier Bueno
National Agricultural Technology Institute EAA Conception of Uruguay,
Conception of Uruguay, Entre Rios, Argentina
James A. Byrd
USDA-ARS, College Station, TX, United States
Todd R. Callaway
USDA/ARS, College Station, TX, United States
Kim L. Chiok
Washington State University, Pullman, WA, United States
Kapil K. Chousalkar
The University of Adelaide, Roseworthy, SA, Australia
Philip G. Crandall
University of Arkansas, Fayetteville, AR, United States
Roy Curtiss III
University of Florida, Gainesville, FL, United States
Rob Davies
Animal and Plant Health Agency (APHA), Addlestone, United Kingdom
Turki M. Dawoud
University of Arkansas, Fayetteville, AR, United States; King Saud University,
Riyadh, Saudi Arabia
Wolfgang De Cort
Ghent University, Gent, Belgium
Richard Ducatelle
Ghent University, Gent, Belgium
Tom S. Edrington
USDA/ARS, College Station, TX, United States
Jacob R. Elder
Washington State University, Pullman, WA, United States
Steven L. Foley
U.S. Food and Drug Administration, Jefferson, AR, United States
Richard K. Gast
US National Poultry Research Center, Athens, GA, United States
xvii
xviii List of Contributors
Eduardo Ignacio Godano
Tecnovo S.A., Industrial Park, Crespo, Entre Ríos, Argentina
Anup Kollanoor Johny
University of Minnesota, Saint Paul, MN, United States
Pravin R. Kaldhone
University of Arkansas, Fayetteville, AR, United States
Michael H. Kogut
USDA-ARS, College Station, TX, United States
Doug Korver
University of Alberta, Edmonton, AB, Canada
Young Min Kwon
University of Arkansas, Fayetteville, AR, United States
Soo-Kyoung Lee
Konkuk University, Seoul, South Korea; Animal and Plant Quarantine Agency,
Gimcheon, South Korea
Francesca Martelli
Animal and Plant Health Agency (APHA), Addlestone, United Kingdom
Lynn McMullen
University of Alberta, Edmonton, AB, Canada
Andrea McWhorter
The University of Adelaide, Roseworthy, SA, Australia
Meera Surendran Nair
University of Connecticut, Storrs, CT, United States
David J. Nisbet
USDA/ARS, College Station, TX, United States
Corliss A. O’Bryan
University of Arkansas, Fayetteville, AR, United States
Narayan C. Paul
Washington State University, Pullman, WA, United States
Francisco Procura
National Agricultural Technology Institute EAA Conception of Uruguay,
Conception of Uruguay, Entre Rios, Argentina; National Council of Scientific
and Technical Research (CONICET), Argentina
Steven C. Ricke
University of Arkansas, Fayetteville, AR, United States
Francisco Isabelino Rodriguez
National Agricultural Technology Institute EAA Conception of Uruguay,
Conception of Uruguay, Entre Rios, Argentina; National Council of Scientific
and Technical Research (CONICET), Argentina
List of Contributors xix
Kun-Ho Seo
Konkuk University, Seoul, South Korea
Devendra H. Shah
Washington State University, Pullman, WA, United States
Zhaohao Shi
University of Arkansas, Fayetteville, AR, United States
María Cecilia Soria
INIQUI-CONICET, National University of Salta, Salta, Argentina
Mario Alberto Soria
National Agricultural Technology Institute EAA Conception of Uruguay,
Conception of Uruguay, Entre Rios, Argentina
Indu Upadhyaya
University of Arkansas, Fayetteville, AR, United States
Filip Van Immerseel
Ghent University, Gent, Belgium
Kumar Venkitanarayanan
University of Connecticut, Storrs, CT, United States
Andrew Wales
Animal and Plant Health Agency (APHA), Addlestone, United Kingdom
Doug Waltman
Georgia Poultry Laboratory Network, Gainesville, GA, United States
Paul Wigley
University of Liverpool, Neston, Cheshire, United Kingdom
Hsin-Bai Yin
University of Connecticut, Storrs, CT, United States
About the Editors
Dr. Steven C. Ricke received his BS degree in Animal Science (1979) and MS
degree in Ruminant Nutrition (1982) from the University of Illinois and his PhD
degree (1989) from the University of Wisconsin with a co-major in Animal Science
and Bacteriology. From 1989 to 1992 Dr. Ricke was a US Department of Agriculture
(USDA)-Agricultural Research Service (ARS) postdoctorate in the Microbiology
Department at North Carolina State University. He was at Texas A&M University for
13 years and was a professor in the Poultry Science Department. In 2005 he joined
the Department of Food Science at the University of Arkansas and became the first
holder of the new Donald “Buddy” Wray Endowed Chair in Food Safety and Direc-
tor of the Center for Food Safety at the University of Arkansas. He received the
Poultry Science Association Research Award in 1999 and the American Egg Board
Award in 2006. He was also honored in 2002 by Texas A&M University as a Texas
Agricultural Experiment Station Faculty Fellow and in 2012 with the University of
Arkansas Division of Agriculture–John White Outstanding Research Award. Dr. Ricke’s
research program is primarily focused on virulence and pathogenic characteristics of
food-borne salmonellae. Dr. Ricke’s Salmonella research projects have emphasized
studies on the growth, survival, and pathogenesis of the organism under conditions
encountered during food animal production and processing.
Dr. Richard K. Gast is a Microbiologist and Research Leader for the Egg Safety
and Quality Research Unit at the US National Poultry Research Center in Athens,
Georgia, United States. The mission of this group is to develop improved technol-
ogies for egg production and processing that reduce or eliminate microorganisms
that can transmit disease to humans or cause spoilage. Richard’s personal research
program focuses on detecting and controlling Salmonella infections in poultry and
Salmonella contamination of eggs. He received MS and PhD degrees in Poultry
Science from The Ohio State University.
xxi
Preface
In his preface to the proceedings of an international conference in 1984, Dr. Glenn
Snoeyenbos noted that “raw foods of animal origin are frequently contaminated by
salmonellae and serve as a major source of human infection” (Snoeyenbos, 1984).
However, textbooks on poultry science or food microbiology that were published
before the 1980s typically contained only very brief considerations of eggs as poten-
tial sources of food-borne illness, as “the contents of normal fresh eggs are, as a
rule, sterile” (Nesheim et al., 1972). Although eggs were long known to be subject to
external bacterial contamination of shells, occurring as they pass through the same
exit portal of the chicken as voided feces, the edible contents were likely to become
contaminated only in cracked or dirty eggs. Elimination of these from table egg mar-
ket channels, along with the institution of consistently dependable pasteurization
standards for liquid egg products, reduced the association of eggs with disease to
negligible levels for many years.
The international emergence of Salmonella Enteritidis as a leading cause
of human illness in the mid-1980s represented a major turning point in the
history of egg safety. Within a few years, this serovar became a preeminent food-
borne disease agent in many countries, and eggs were consistently identified as
the principal source of these infections. Considerable investments of public and
private resources were directed toward this problem, in terms of government
regulatory programs, risk reduction practices for egg producers, and research to
develop improved tools for disease control. All of these efforts have achieved
tangible positive results, but the continuing occurrence of egg-transmitted illness
around the world calls for an ongoing commitment to finding better solutions to
this problem.
This volume explores several of the most important categories of issues that still
confront us regarding Salmonella contamination of eggs. The first section reviews
the nature of this problem as it is seen in a variety of individual nations or regions
around the world. This geographical presentation of the problem represents an effort
to define its scope and ongoing significance, and identifies important international
similarities and distinctions in both epidemiology and control practices. The sec-
ond section seeks to explore the mechanisms by which egg contamination occurs
as a consequence of infections of laying hens with salmonellae, and assesses cur-
rent efforts to harness this information for implementing effective control programs.
The third section presents a wide range of ideas and concepts being pursued by
researchers with the goal of improving our ability to prevent Salmonella infection
in egg-laying chickens, to prevent the production of contaminated eggs, or to elimi-
nate contaminants after they are deposited on or inside eggs. Although it is not yet
possible to identify a single treatment or practice that is likely to serve as a unilateral
or complete solution to disease transmission via contaminated eggs, the sustained
application of a coordinated and comprehensive control program with multiple risk
xxiii
xxiv Preface
reduction components offers much promise. We are grateful to the numerous authors
from around the world who have contributed their expertise to this book. We hope
that it will be the basis for a continuing dialogue and many further explorations about
this still evolving topic.
Steven C. Ricke
Richard K. Gast
May 2016
REFERENCES
Nesheim, M.C., Austic, R.E., Card, L.E., 1972. Poultry Production, twelfth ed. Lea and
Febiger, Philadelphia, PA.
Snoeyenbos, G.H., 1984. Proceedings of the International Symposium on Salmonella.
American Association of Avian Pathologists, Kennett Square, PA.
CHAPTER
1
Of Mice and Hens—
Tackling Salmonella in
Table Egg Production in
the United Kingdom and Europe
Francesca Martelli, Andrew Wales, Rob Davies
Animal and Plant Health Agency (APHA), Addlestone, United Kingdom
1. SALMONELLA CONTROL IN TABLE EGG
PRODUCTION IN EUROPE
In the European Union in 2014, 44% of the human cases of salmonellosis associ-
ated with a known food source were linked with eggs and egg products (EFSA,
2015). In Europe, the two Salmonella serovars that are specifically regulated in
laying flocks in all Member States are Enteritidis and Typhimurium (EC, 2003),
but in the Nordic Countries all serovars in poultry are subject to a slaughter
policy, and Salmonella Kentucky, which has been spreading rapidly in poultry
in some countries and is highly resistant to fluoroquinolones, has been added
to National Control Programmes (NCPs) in France. The European Union level
of prevalence of adult laying hen flocks that tested positive for Salmonella in
2014 was 2.54%. Salmonella Enteritidis was isolated from 0.7% of laying hen
flocks and Salmonella Typhimurium from 0.2% (EFSA, 2015). S. Enteritidis has
a special ability to colonize the ovary/oviduct of laying hens for long periods and
therefore to internally contaminate eggs, and has been the most frequent serovar
associated with egg-related foodborne outbreaks in Europe since the mid-1980s
(Thorns, 2000). S. Typhimurium is a common cause of foodborne outbreaks
in humans worldwide originating predominantly from cattle, pigs, and poultry
(EFSA, 2010). Foodborne outbreaks related to the consumption of S. Enteritidis-
contaminated eggs have been widely reported in Europe (Gormley et al., 2012;
Harker et al., 2014; Liu et al., 2012; Zenner et al., 2013; Zielicka-Hardy et al.,
2012), but have been decreasing since the introduction of harmonized monitoring
and control programs in laying hens across Europe in 2008.
The role of S. Typhimurium in egg-related foodborne infections appears to be
less significant than the one of S. Enteritidis (Martelli and Davies, 2011; Wales and
Davies, 2011), except in Australia, where S. Enteritidis never became established in
laying hens, since no infected primary breeding or parent stock was imported from
either Europe or the United States.
Producing Safe Eggs. http://dx.doi.org/10.1016/B978-0-12-802582-6.00001-X 3
Crown Copyright © 2017 Published by Elsevier Inc. All rights reserved.
4 CHAPTER 1 Tackling Salmonella in Table Egg Production
Other Salmonella serovars can be linked to poultry products, egg contamination,
and foodborne outbreaks (Okamura et al., 2001). For example, in the United States,
Salmonella Heidelberg and S. Kentucky are frequently associated with eggs, broilers,
turkeys, and poultry products and have resulted in large product recalls and outbreaks
of food poisoning in the human population (Foley et al., 2011; Reddy et al., 2016).
S. Enteritidis has been reported to have a greater ability to colonize avian
reproductive organs and contaminate eggs than other zoonotic serovars (e.g.,
S. Typhimurium, Salmonella Infantis, Salmonella Hadar, S. Heidelberg, Salmonella
Montevideo) in intravenously infected laying hens (Okamura et al., 2001). This abil-
ity to vertically transmit into the contents of forming eggs is shared with both biovars
of Salmonella Gallinarum, which are derived from a common S. Enteritidis ancestor
(Yao et al., 2016).
S. Enteritidis is often persistent in cage layer holdings where cleaning and dis-
infection procedures are not carried out appropriately and where there is a resident
infected rodent population (Snow et al., 2010). This can also happen in large non-
cage units, but is less common. Flocks infected with S. Enteritidis produce a variable
proportion of contaminated eggs, depending on the strain, level of contamination
of the flock, and time of the production period in which the eggs are laid (Braden,
2006). In a study conducted in France, S. Enteritidis was detected on up to 8.6% of
the shells of eggs produced by an infected flock (Chemaly et al., 2009). In a study
conducted in the United States, the estimated overall prevalence of egg contents
from flocks infected with S. Enteritidis was 2.64/10,000 eggs (varying from 0 to
62.5/10,000) (Henzler et al., 1998). In both studies, a positive correlation between
the level of environmental contamination and the proportion of positive eggs was
noted (Chemaly et al., 2009; Henzler et al., 1998).
Salmonella serovars differ in their ability to cause contamination on the eggshell
or the egg contents. In one study, a significant difference was found in the rate of egg
contamination between serovars, with S. Enteritidis causing a higher rate of contami-
nation of egg contents and a lower rate of contamination of eggshells per infected hen
(0.32% and 0.34%, respectively) compared with S. Typhimurium (0.23% and 0.94%,
respectively) and non–S. Enteritidis non–S. Typhimurium serovars (0.23% and 2.5%,
respectively) (Arnold et al., 2013).
NCPs for the control of Salmonella in commercial scale flocks have been imple-
mented in the European Union since 2008 (as detailed in regulations EC 2160/2003
and EC 517/2011). Flocks of layers on holdings with more than 1000 birds (National
Regulations specify smaller numbers in some countries, e.g., 350 birds in the United
Kingdom) are sampled at day old and 2 weeks before they are moved to the lay-
ing phase or laying unit and every 15 weeks during the laying phase. NCPs include
operator sampling by means of boot swabs (two pairs per flock) or naturally pooled
feces (300 g) during the period of egg production of each holding, supplemented by
official sampling of one flock per holding of more than 1000 birds per year, carried
out by agents of the competent authority, using the same method plus one additional
dust or fecal/boot swab sample. Official samples are collected by employees of the
competent authority or independent control bodies (in the United Kingdom only),