Importance of eggshell cuticle composition and maturity for avoiding
trans-shell Salmonella contamination in chicken eggs
Arantxa Mu
~
noz
a
, Nazaret Dominguez-Gasca
a
, Concepci
on Jimenez-Lopez
b
,
Alejandro B. Rodriguez-Navarro
a, *
a
Departmento de Mineralogia y Petrologia, Universidad de Granada, Campus Fuente Nueva s/n, 18071 Granada, Spain
b
Departmento de Microbiologia, Universidad de Granada, Campus Fuente Nueva s/n, 18071 Granada, Spain
article info
Article history:
Received 30 June 2014
Received in revised form
24 January 2015
Accepted 3 February 2015
Available online 28 February 2015
Keywords:
Cuticle
Eggshell
Food safety
Salmonella
ATR-FTIR
SEM
abstract
The cuticle coating the eggshell surface is the first line of defense of the egg against bacterial ingress.
However, the cuticle properties (i.e., thickness, degree of coverage, chemical composition) have a very
large natural variability and this work analyzed how this variability influence the risk of eggs being
contaminated by Salmonella. Microbial growth on the eggshell surface as well as the incidence of Sal-
monella penetration in eggs increases significantly with hen age for the groups (25, 35, and 52 weeks)
considered in this study. It shows also that the cuticle is most effective against bacterial penetration
between 6 and 72 h after eggs have being laid when this coating is fully mature and has not dried
excessively. In contrast, freshly laid eggs can be easily contaminated as they have an immature cuticle
which is not able to resist bacterial penetration. This study show also that the chemical composition of
the mature cuticle determines the risk of trans-shell contamination by Salmonella. In particular, it shows
that eggs with a cuticle rich in proteins have a decreased shell permeability and greater resistance
against Salmonella penetration. The novel analytical technique used here to quantify the cuticle quality
(based on infrared spectroscopy; ATR-FTIR) could be used in assisted selection programs aimed to
improve the quality and safety of eggs.
© 2015 Elsevier Ltd. All rights reserved.
1. Introduction
Hen eggs are a popular and inexpensive source of proteins
which are extensively consumed around the world (Nys, Bain, &
Van Immerseel, 2011). However, they are also commonly associ-
ated to food-poisoning outbreaks due to their contamination with
pathogenic bacteria (i.e., Salmonella enteritis). Only in the EU, there
is an estimated incidence of over 100.000 cases of salmonellosis per
year, that being a serious health problem with an important eco-
nomic impact (EFSA., 2009; Gastois et al., 2009; Messens,
Grijspeerdt, & Herman, 2005; Solomon et al., 1997). Thus, it is
important to take active actions to reduce the risk of such
contamination. Contamination of the egg can occur either prior to
the oviposition, due to infection of the reproductive organs, in
contaminated flocks, and/or during or after the oviposition, by
trans-shell penetration, which is considered the prevalent route for
bacterial contamination (Board & Tranter, 1995; Gantois et al.,
2009; Messens et al., 2005). Cracked eggs or eggs with a poor
eggshell quality (which can account for over 6% of total production)
can be more easily contaminated with bacteria and pose an
important risk to consumers as they need to be downgraded
causing important economic losses to producers (Dunn et al., 2010;
Hamilton, Hollands, Voisey, & Grunder, 1979; Washburn, 1982).
The egg is protected against bacterial contamination by the
eggshell and the shell membranes, which if intact, act together as
an effective physical barrier against bacterial penetration (Board &
Tranter,1995; De Reu et al., 2006; Jonchere et al., 2010). Even if the
eggshell integrity is good, the mineral shell is still perforated by
many pores that allow gas and water exchange necessary for the
developing chick embryo but also possibilities microbial ingress
and contamination of the egg content (Hincke, Nys, Gautron, Mann,
& Rodríguez-Navarro, 2012). The cuticle, a very thin (up to 12 um)
organic layer, coats the eggshell surface and plugs the eggshell pore
opening, thus limiting the movement of particles, water and
* Corresponding author. Departamento de Mineralogía y Petrología, Universidad
de Granada, 18002 Granada, Spain. Tel.: þ34 958240059; fax: þ34 958243368.
E-mail addresses: arantxa@ugr.es (A. Mu~ noz), nadoga@ugr.es (N. Dominguez-
Gasca), cjl@ugr.es (C. Jimenez-Lopez), anava@ugr.es (A.B. Rodriguez-Navarro).
Contents lists available at ScienceDirect
Food Control
journal homepage: www.elsevier.com/locate/foodcont
http://dx.doi.org/10.1016/j.foodcont.2015.02.028
0956-7135/© 2015 Elsevier Ltd. All rights reserved.
Food Control 55 (2015) 31e38