Journal of Applied Microbiology 1999, 86, 429–438
Effect of elevated oxygen and carbon dioxide on the surface
growth of vegetable-associated micro-organisms
A. Amanatidou, E.J. Smid and L.G.M. Gorris*
Agrotechnological Research Institute, Wageningen, The Netherlands
6790/07/98: received 1 July 1998, revised 12 October 1998 and accepted 14 October 1998
A. AMANATIDOU, E.J. SMID AND L.G.M. GORRIS. 1999. The impact of a novel type of
Modified Atmosphere (MA), referred to as high O
2
-MA, on micro-organisms associated with
the spoilage of minimally-processed vegetables was studied. Pure cultures of
Pseudomonas fluorescens, Enterobacter agglomerans, Aureobacterium strain 27,
Candida guilliermondii, C. sake, Salmonella typhimurium, Salm. enteritidis, Escherichia
coli, Listeria monocytogenes, Leuconostoc mesenteroides var. mesenteroides, Lactobacillus plantarum
and Lactococcus lactis were cultured on an agar-surface model system and incubated at
8 °C under an atmosphere composed of O
2
(80 or 90%, balanced with N
2
), CO
2
(10 or 20%,
balanced with N
2
), or a combination of both gases. In general, exposure to high O
2
alone did not inhibit microbial growth strongly, while CO
2
alone reduced growth
to some extent in most cases. Consistently strong inhibition was observed only when
the two gases were used in combination. With minimally-processed vegetables, where CO
2
levels of around 20% or above cannot be used because of physiological damage to the
produce, the combined treatment of high O
2
and 10–20% CO
2
may provide adequate
suppression of microbial growth, allowing a safe, prolonged shelf-life.
INTRODUCTION
Modified atmosphere packaging (MAP) is used to extend
shelf-life and maintain high quality of minimally-processed
fruits and vegetables. The rapid increase in the market share
of MAP of ‘ready-to-eat vegetables’ reflects the trends of
today’s consumers for fresh, additive-free foods.
Respiring products, like raw or processed vegetables and
ready-made salads, generate equilibrium gas conditions inside
the package that are typically very low in O
2
(2–3%) and
moderately high in CO
2
(5–20%). These conditions reduce
deterioration by limiting product respiration and maturation
(Kader 1986; Day 1992; Gorris and Peppelenbos 1992) as
well as by slowing down the proliferation of aerobic spoilage
micro-organisms (Hotchkiss 1988; Kader et al. 1989; Moleyar
and Narasimham 1994). The antimicrobial effect of CO
2
on
micro-organisms has been intensively documented (Molin
1983; Eklund 1984; Daniels et al. 1985; Dixon and Kell 1989).
Correspondence to: Dr Athina Amanatidou, Agrotechnological Research
Institute, PO Box 17, 6700 AA Wageningen, The Netherlands (e-mail:
A.AMANATIDOU@ATO.DLO.NL).
*Present address: Unilever Research Laboratorium, Olivier van Noortlaan
120, 3133 AT Vlaardingen, The Netherlands.
© 1999 The Society for Applied Microbiology
Although MA packaging of respiring produce has come
into substantial use in practice, some potential problems with
regard to product quality and safety remain to be solved. The
O
2
and CO
2
levels in an MA package are achieved mostly by
the active respiration of the produce and are often difficult to
predict and control (Ahvenainen 1996). All too frequently,
O
2
is completely depleted, resulting in the production of off-
odours and rapid deterioration of the product (Zagory and
Kader 1988). In addition, excessive levels of CO
2
(generally
over 20%) cause specific disorders such as the development
of brown stains (Lougheed 1987; Kader et al. 1995). Bennik
et al. (1995) showed that CO
2
levels from 20–50%, in com-
bination with low O
2
(1·5%), affect the growth rate of spoilage
bacteria relevant to minimally-processed vegetables but have
no effect on the maximum population densities or the lag
phase duration.
Concerning product safety, psychrotrophic pathogens such
as Listeria monocytogenes are not suppressed under MA con-
ditions that are optimal for respiring produce (Berrang et al.
1989; Brackett 1994; Bennik et al. 1995; Carlin et al. 1996;
Francis and O’Beirne 1997). On the contrary, growth may be
enhanced in certain cases because of suppression of the natu-