The effects of active and passive modified atmosphere packaging on the survival of
Salmonella enterica serotype Typhimurium on washed romaine lettuce leaves
Batia Horev, Shlomo Sela, Yakov Vinokur, Elena Gorbatsevich, Riky Pinto, Victor Rodov ⁎
Institute of Postharvest and Food Sciences, Agricultural Research Organization, The Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel
abstract article info
Article history:
Received 26 February 2011
Accepted 31 May 2011
Keywords:
Lettuce
Ready-to-eat
Modified atmosphere
Active MAP
Food safety
Salmonella
Modified atmosphere packaging (MAP) is commonly used to preserve the quality of ready-to-eat lettuce by
inhibiting oxidative browning and growth of microbial populations. The efficacy of MAP is improved by the
initial displacement of air with a gas mixture of a desirable composition (active MAP). The present work
focused on the effects of MAP on indigenous microbial populations and the survival of Salmonella enterica on
the surface of the lettuce. Chlorine-washed leaves of romaine lettuce were inoculated with S. enterica serotype
Typhimurium or not inoculated and packaged in one of the three systems: (a) passive MAP in polyethylene
bags; (b) active MAP in the same bags with a gas mixture of 10% O
2
, 10% CO
2
, and 80% N
2
; and (c) control
without MAP. Active MAP ensured the more rapid establishment of a steady-state atmosphere and favorable
conditions during the transitional period preceding the steady state. The active MAP had an antimicrobial
effect on indigenous lettuce microflora, but not on Salmonella and even favored the survival of the pathogen,
possibly due to the elimination of its natural antagonists. The effects of the passive MAP were less pronounced.
The results obtained draw attention to potential safety risks of ready-to-eat fresh produce kept in active MAP
and require further investigation.
© 2011 Elsevier Ltd. All rights reserved.
1. Introduction
Ready-to-eat (RTE) packaged lettuce salads were implicated in
several salmonellosis outbreaks (Little & Gillespie, 2008). Large-scale
industrial processing and distribution of RTE products exacerbate the
risk of cross-contamination and can lead to geographically widespread
outbreaks. Therefore, the study of the food-safety implications of
technologies used in the production and handling of RTE lettuce is of
great importance.
Modified atmosphere packaging (MAP) is commonly used to
preserve the quality of minimally processed lettuce by inhibiting the
oxidative browning and the growth of microbial populations. The
antimicrobial effect of MAP is mainly related to the enhanced
concentration of carbon dioxide (Bennik, Smid, Rombouts, & Gorris,
1995), whereas the inhibition of browning is due to reduced oxygen
level (Smyth, Song, & Cameron, 1998). In passive MAP, generation of
modified atmosphere by produce respiration typically takes one to
several days. During this transitional period, the produce continues to
deteriorate. Initial displacement of air with a gas mixture of desired
composition (active MAP) allows the avoidance of the transitional
period, thereby improving the quality of the product (Ares, Lareo,
& Lema, 2008).
However, a concern exists that under MAP conditions foodborne
pathogens like Salmonella that are relatively tolerant to high CO
2
(Hintlian & Hotchkiss, 1987) and low oxygen (Ryan, 1972) may outgrow
spoilage microorganisms, resulting in more visually appealing, but
unsafe products (Farber et al., 2003). Indeed, certain enhancement of
Salmonella growth parallel to inhibition of mesophilic and psychro-
trophic microorganisms was observed on shredded romaine lettuce
kept in passive MAP (Oliveira et al., 2010). To the best of our knowledge,
no data are available concerning the effect of active MAP on the survival
of Salmonella on RTE lettuce.
The purpose of this work was to study the effects of active and
passive MAP on indigenous microflora on washed RTE lettuce leaves
and on the survival of Salmonella enterica serotype Typhimurium on
the surface of these leaves.
2. Material and methods
2.1. Product preparation and storage
The heads of romaine lettuce were taken from the farm on the day of
harvest. The aseptically separated medium-size leaves were soaked for
2 min in sodium hypochlorite solution (Sterosept; Johnson Diversey,
Yavne, Israel) containing 200 ppm free chlorine (test kit HI3831F;
Hanna Instruments, Padova, Italy), rinsed with tap water and dried in a
basket centrifuge K50-7ECO (Kronen GmbH, Kehl am Rhein, Germany).
The leaves intended for Salmonella inoculation were treated as
described in Section 2.2.
Food Research International 45 (2012) 1129–1132
⁎ Corresponding author: Tel.: + 972 3 9683609; fax: + 972 3 9683622.
E-mail address: vrodov@agri.gov.il (V. Rodov).
0963-9969/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2011.05.037
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