Pathogenesis and ToxinsOccurrence of microorganisms of public health and spoilage significance in fruit juices sold in retail markets in Greece
Introduction
Juices, like most acidic foods, frequently become spoiled as a result of contamination with aerobic acid-tolerant bacteria, together with yeasts and molds. Fruits and vegetables contain the nutrients necessary to support the rapid growth of foodborne pathogens, yet outbreaks of illness caused by consumption of fruits and vegetables are less frequent than outbreaks involving other foods. This higher level of protection is due in part to proper pasteurization and to the presence of external barriers such as the peels and rind of fruits, which prevent microorganisms from entering and subsequently growing in the interior of the fruit or vegetables [1], [4], [5]. However, in some cases, such as when fruits have become wounded or slices have been freshly cut, this external barrier is broken, creating an opportunity for bacterial colonization of the interior of the fruit. The occasional presence of foodborne pathogens has been recognized for many years. Thus, pathogens as well as spoilage microorganisms can contaminate fruits and vegetables via several different routes and at several points throughout the pre-harvest and post-harvest process [6].
In USA, Canada, New Zealand, and several EU countries, public health organizations have run campaigns recommending the daily consumption of at least five daily servings of fruit and vegetables. In Greece, freshly pasteurized juices are consumed throughout the year [2]. In the past these beverages were not regarded as potentially hazardous [3], [12]. However, in recent decades, juices have become frequent vehicle for transmitting pathogens, such as enterohaemorrhagic Escherichia coli O157:H7 [7], Salmonella [9] and Cryptosporidium [8]. Thus, the belief that high-acid foods are of minimal concern with regard to pathogenic bacteria has been challenged [11]. Nevertheless, only a few studies have reported the incidence of bacteria in juices, mainly in non-pasteurized ones [13], [14], [21]. Although they cannot grow at low pH, some strains of Enterobacteriaceae, including certain strains of E. coli, Shigella, and Salmonella, may survive for several days or even weeks in acidic foods [15]. Also, the actual pH range tolerance of E. coli O157:H7 has raised further doubts about the safety of acidic foods [29]. Some fruits, including oranges, are susceptible to attack by pathogenic fungi e.g., Aspergillus because of their low pH, higher moisture content, and nutrient composition [17]. Molds and yeasts tolerate conditions of high osmotic pressure and low pH and can grow at refrigerator temperatures (two factors that generally prohibit the growth of competitive bacteria) and can therefore cause spoilage in the processed product [25], [26]. Frequently isolated yeast species found in citrus juices are Candida parapsilosis, Candida stellata, Saccharomyces cerevisiae, Torulaspora delbrueckii, and Zygosaccharomyces rouxii, although species from the genera Rhodotorula, Pichia, Hanseniaspora, and Metschnikowia are also common [23]. Despite the economic importance of juices, there are only a few reports investigating the presence of yeasts in them [22], [23].
The objective of the present study was to evaluate the microbiological quality of domestic and imported pasteurized shelf-stable fruit juices sold in retail stores in Greece. The potential presence of Listeria monocytogenes, Salmonella spp., Staphylococcus aureus and epidermidis, Bacillus cereus, E. coli O157:H7, Clostridium perfrigens, Lactobacillus, E. coli, acidophilic bacteria, fecal streptococci, Blastomyces, fungi, and yeasts was evaluated. Also total microbial counts and total coliforms counts were investigated.
Section snippets
Materials and methods
All fruit juice samples were purchased in local retail shops in Greece by trained in sampling procedures laboratory personnel. The number of samples as well as the juice type tested is shown in Table 1. All tested juice samples had at least an extra 8 months expiration period. Fruit and vegetable juices containing dairy products (e.g., smoothies), freshly squeezed juices in sealed packages, and mixed juices with more than three ingredients were excluded from the sampling program.
In total, 120
Results
The pH of the tested juices ranged from 2.4 (lemon juice) to 4.8 (cocktail-type juice). The average pH of all the juices was 3.47 (Table 1). Sixty-three (52.5%) imported juices as well as fifty-seven (47.5%) domestic juices were analyzed. The total number of contaminated samples (bacterial and/or fungal) according to juice type is depicted in Fig. 1.
None of the tested samples was found to be positive for L. monocytogenes, Lactobacillus, Salmonella spp., St. aureus, B. cereus, C. perfrigens,
Discussion
The objective of the present study was to evaluate the microbiological quality of commercially sold juices in Greece. It is commonly accepted that products derived from fresh vegetables and fruits contain microorganisms, and some of these microorganisms are potentially hazardous to public health [11]. As was shown in the present study, some juices may contain bacteria or fungi that, if not treated properly, may cause serious illness in consumers or food spoilage. Although this is not the case
References (29)
Pathogenic microorganisms associated with fresh produce
J Food Prot
(1996)- et al.
Use of ion chromatography for monitoring microbial spoilage in the fruit juice industry
J Chromatogr
(1997) - et al.
Inactivation of Escherichia coli O157:H7 in single-strength lemon and lime juices
J Food Prot
(2009) - et al.
Effects of pH, dissolved oxygen, and ionic strength on the survival of Escherichia coli O157:H7 in organic acid solutions
J Food Prot
(2008) - et al.
Ochratoxin A production by Aspergillus westerdijkiae in orange fruit and juice
Int J Food Microbiol
(2009) - et al.
Heat resistance of Alicyclobacillus acidoterrestris spores as affected by various pH values and organic acids
J Food Prot
(1998) - et al.
Moulds and yeasts in fruit Salads and fruit juices
Food Microbiol
(2006) - et al.
Comparative survival of Salmonella typhimurium DT 104, Listeria monocytogenes, and Escherichia coli O157:H7 in preservative-free apple cider and simulated gastric fluid
Int J Food Microbiol
(1999 Feb 18) - et al.
Organic acids make Escherichia coli more resistant to pulsed electric fields at acid pH
Int J Food Microbiol
(2010) - et al.
Mould and yeast flora in fresh berries, grapes and citrus fruits
Int J Food Microbiol
(2005)
Internal contamination and spoilage of harvested apples by patulin-producing and other toxigenic fungi
Int J Food Microbiol
Human pathogens associated with raw produce and unpasteurized juices, and difficulties in decontamination
J Ind Microb Biotechnol
Microbiological quality of fresh minimally – processed fruit and vegetables and sprouts from retail establishments
Int J Food Microbiol
Survival and growth of Escherichia coli O157:H7 on salad and vegetables
Appl Environ Microbiol
Cited by (43)
Mentha piperita L. essential oil inactivates spoilage yeasts in fruit juices through the perturbation of different physiological functions in yeast cells
2019, Food MicrobiologyCitation Excerpt :However, fruit juices manufactured following this market trend are commonly spoiled by yeasts. Candida, Pichia, Rhodotorula and Saccharomyces are yeast genera involved in fruit juices contamination and spoilage (Tournas et al., 2006; Vantarakis et al., 2011; Aneja et al., 2014), causing alterations in taste and flavor in these products (Lawlor et al., 2009). Different emerging technologies (e.g., pulsed electric field, UV-C light and ultrasound) have been studied to preserve fruit juices (Carbonell-Capella et al., 2017; Carrillo et al., 2018), including the use of essential oils, which are generally recognized as safe (GRAS) and considered “green” antimicrobials to use in beverages (USFDA, 2015).
Microbial safety of nonalcoholic beverages
2019, Safety Issues in Beverage Production: Volume 18: The Science of Beverages