Impact of the prevalence of different pathogens on the performance of sampling plans
in lettuce products
Fernando Pérez-Rodríguez
a,
⁎, Patricia González-García
b
, Antonio Valero
a
,
Marta Hernández
b
, David Rodríguez-Lázaro
b,c,
⁎⁎
a
Department of Food Science and Technology, International Campus of Excellence in the AgriFood Sector ceiA3, University of Córdoba, Córdoba, Spain
b
Subdirección de Investigación y Tecnología. Instituto Tecnológico Agrario de Castilla y León, Carretera de Burgos Km, 119, Valladolid, Spain
c
Microbiology Section, Faculty of Science, University of Burgos, Burgos, Spain
abstract article info
Available online xxxx
Keywords:
Food-borne pathogens
Leafy green
Predictive microbiology
Virus
Microbial testing
Prevalence and concentration of Listeria monocytogenes, Salmonella spp. and enteric pathogenic viruses (namely
Hepatitis A—HAV, and noroviruses genogroup I—NoVGI and genogroup II—NoVGII) were determined in raw and
RTE lettuce from a Spanish processing premise. Fifteen samplings were made from September 2010 to February
2012 (n = 600 samples). Sampling strategies for pathogen detection were suggested by the characterization of
the uncertainty in prevalence associated with the performance of two-class attributes sampling plans (c = 0). A
probabilistic model was run (1000 iterations) using a Bayesian approach with a conjugate beta distribution con-
sidering the impact of taking different number of samples on the proportion of positive samples and lots (within-
and between-lot prevalence). No enumeration results were obtained for the pathogens tested. Presence of
L. monocytogenes and NoVGII in RTE lettuce (10%) and NoVGI and NoVGII in unprocessed lettuce (10%) was ob-
tained in the tested lots during cold season. Results evidenced that, as the number of samples increased, the prob-
ability of rejecting a contaminated lot became higher, yielding right-skewed distributions with values close to 1.
According to our results, 25 samples would result in 80% of rejected lots, while 95% confidence level would be
reached with n N 100. However, although those levels would imply a unrealistic high number of samples making
the application of the sampling plan unfeasible, these results might be useful for food operators and risk man-
agers to know the underlying distributions of microbial contamination together with potential control measures
to be applied to assure a safer production of minimally processed vegetables.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Consumption of fresh produce is becoming more popular in devel-
oped countries due to their convenience, ease of preparation and
healthy and nutritional benefits (Alegre et al., 2010). Among the main
fresh products, ready-to-eat (RTE) iceberg lettuce is one of the most
consumed increasing in salad bar patronage and meals eaten outside
the home (Buck et al., 2003; USDA, 2002). Severe foodborne disease
outbreaks can be caused by pathogenic microorganisms associated
with fresh produce (Delaquis et al., 2007). In the EU in 2009 and 2010,
respectively 4.4% and 10% of the foodborne verified outbreaks were
linked with the consumption of vegetables, fruits, berries, juices (and
products thereof) (EFSA/ECDC, 2014). Contamination sources may
come from the field by direct contact with animal waste, irrigated
water, and inadequately treated manure (Johannessen et al., 2005). Fur-
ther, fresh cut products are prone to contamination because the current
industrial sanitizing treatments do not guarantee the total elimination
of the pathogen when present (Beuchat, 1996; Parish et al., 2003;
Abadias et al., 2008, Pérez-Rodríguez et al., 2011; Posada-Izquierdo
et al., 2014).
Enteric pathogens such as Salmonella spp. appear to be particularly
prone to lettuce contamination. Franz et al. (2007) reported that 18%
of all lettuce-associated outbreaks were caused by Salmonella and 10%
of all Salmonella outbreaks with fresh produce were related to lettuce.
The presence of Listeria monocytogenes in leafy greens has been studied
extensively through risk assessment (Franz et al., 2010; Oliveira et al.,
2010) since this commodity may support the growth of L. monocytogenes
(Carrasco et al., 2008; Francis and O'Beirne, 2005; Szabo et al., 2000).
Other causal agents such as foodborne viruses, mainly noroviruses, are
linked to the consumption of leafy greens. Until recently, no data was
available about the prevalence of NoV on fresh produce. Nevertheless,
NoV outbreaks have been reported linked to leafy greens (Ethelberg
et al., 2010; Gallimore et al., 2005).
International Journal of Food Microbiology xxx (2014) xxx–xxx
⁎ Corresponding author. Tel.: +34 957218516.
⁎⁎ Correspondence to: D. Rodríguez-Lázaro, Subdirección de Investigación y Tecnología.
Instituto Tecnológico Agrario de Castilla y León, Carretera de Burgos Km 119, Valladolid,
Spain. Tel.: +34 637451100.
E-mail addresses: b42perof@uco.es (F. Pérez-Rodríguez), rodlazda@gmail.com
(D. Rodríguez-Lázaro).
FOOD-06516; No of Pages 5
http://dx.doi.org/10.1016/j.ijfoodmicro.2014.04.019
0168-1605/© 2014 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
International Journal of Food Microbiology
journal homepage: www.elsevier.com/locate/ijfoodmicro
Please cite this article as: Pérez-Rodríguez, F., et al., Impact of the prevalence of different pathogens on the performance of sampling plans in
lettuce products, Int. J. Food Microbiol. (2014), http://dx.doi.org/10.1016/j.ijfoodmicro.2014.04.019