Fruit and Vegetables

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CHAPTER 50

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Fruit and Vegetables Michelle D. Danyluk, Marianne K. Fatica, Pardeepinder K. Brar, Rachel McEgan, Angela M. Valadez, Keith R. Schneider, and Valentina Trinetta Updated September 2013

50.1

wash water, rarely reduces microorganism populations on the surface of produce by more than about 2 log units.14,33,74,121,122 Chlorine is one of the most commonly used sanitizers, with many fruits and vegetables processed in flume tanks containing solutions of 150–200 ppm of available chlorine for a short time before packing.7 Unfortunately, chlorine agents are ineffective in entering the natural pockets or crevices of the hydrophobic, waxy cuticle of some produce; thus, they will not reduce microbial populations within the produce.13,75 Alternatives to chlorine-based sanitizers are other antimicrobial agents, such as peroxyacetic acid, ozone, or ultraviolet (UV) light, that may be used in produce-processing wash water; however, these alternatives are less common.

INTRODUCTION

This chapter will cover fresh, fresh-cut (minimally processed, MP), canned, frozen, and dehydrated fruits and vegetables. Some of these foods are intended to be consumed raw, some are available as ready-to-eat, some will be cooked before consumption, and others are used as ingredients in more complex foods.

50.2

GENERAL PROCESSES/CONTROL OF ORGANISMS FOR FRUITS AND VEGETABLES

50.2.1

Washing

Unless directly packed into consumer containers in the field, washing is among the first procedures to which many fruits and vegetables are exposed after harvest. Water sprays, usually containing a sanitizer, are often used to dislodge field soil and cool the product. By removing field soil, some soil-associated microorganisms are also removed. Generally, washing with water alone may remove about 1–2 log units of microorganisms. 33,122 However, if microbial populations are not controlled in soiled or recycled wash water, this can result in increases in the populations of microorganisms, some of which may be pathogenic. Temperature control of water used to wash fruits and vegetables can affect microorganism distributions. The contact between warm fruit and cool water may cause the plant cells to contract, resulting in the possible internalization of the water and pathogens, if present. This process has been shown to occur with both mangoes and tomatoes.7,99

50.2.2

50.2.3

Cutting and Chopping

Cutting, chopping, and slicing of produce can allow microorganisms to invade internal plant tissues and release nutrients that can be used for growth. Consequently, these practices can result in higher populations of microorganisms and more rapid spoilage.16 Improperly cleaned and sanitized cutting, chopping, and slicing equipment can be a source of cross-contamination of produce, resulting in increases in total populations or pathogen contamination.44 Other steps, such as peeling, coring, halving, and pitting of fruits, can occur prior to a heating or cooking step. For vegetables, these treatment steps often occur after blanching. For both fruits and vegetables, peeling can be performed either by a mechanical peeler, lye, or steam.66,120

50.2.4

Heat

Fruits and vegetables are subjected to heat during blanching and thermal processing (canning). Blanching is done primarily to inactivate plant enzymes that will reduce produce quality during storage, but as a secondary benefit, it also reduces surface vegetative microflora by 1-5 logs on many vegetables prior to freezing.50,103 It is recommended to avoid blanching some vegetables, such as peppers, leeks,

Sanitizers

Sanitizers or other antimicrobial agents are commonly used to control microorganism populations and prevent cross contamination in wash and processing waters. The use of most common sanitizers approved for use with foods, while very efficient at preventing cross-contamination in | 1 |

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Compendium of Methods for the Microbiological Examination of Foods |

and parsley, to preserve quality. One of the major differences in processing between fruits and vegetables is the blanching step. Most fruits do not undergo blanching, while many vegetables are blanched prior to filling in typical canning.66,120 In contrast to blanching, the canning process eliminates virtually all microorganisms, with the exception of some very thermophilic spores, resulting in ‘‘commercial sterility.’’

50.2.5

Freezing

Freezing produce does not normally kill microorganisms. Although many organisms are destroyed during freezing, some may survive. During prolonged storage under frozen conditions, bacterial numbers may decrease, but this is dependent on time, microorganism type, food matrix, and storage conditions including temperature.50 During the freezing of fruits, chemicals such as ascorbic acid or citric acid may be added to control oxidation or browning, respectively.50

50.2.6

Dehydration

During dehydration, the water activity (aw) of produce is reduced to ,0.6. Dehydration methods include: cross-flow hot-air drying, tunnel hot air drying, osmotic dehydration, spray drying, and freeze drying.36 Dehydration temperatures used can vary from 30–100uC.36 Some foods are treated with sulfur dioxide prior to drying to eliminate most microorganisms; those not treated are susceptible to fungal spoilage.36

50.2.7

Alternative Processing

Alternative nonthermal technologies are available for the fruit and vegetable industry. High-pressure processing (HPP) is broadly used to inactivate microorganisms and enzymes, extend product shelf-life, and maintain high quality and nutritional properties.85 This technology is suitable for ambient temperature processes, and it quickly inactivates microorganisms. In lemon juice samples that had been treated with 450 megapascals (MPa) for 2, 5, or 10 minutes, there was no fungal growth after 10 days of storage, whereas the corresponding controls were completely moldy.37 Pressure-treated fresh-cut pineapple pieces (340 MPa for 15 minutes) had an extended shelf-life compared to untreated pineapple and an overall reduction of inherent microflora.1 Gaseous treatments, such as ozone and chlorine dioxide, are also available, and their effects on quality and microbial safety of fruit and vegetables have been investigated. After a treatment with 10 mg/L chlorine dioxide gas for 3 minutes, nearly a 5 log CFU/g reduction of Salmonella enterica on Roma tomatoes was observed, and a 3-week extension in produce shelf-life was reported.110 A greater microbial inactivation rate was noted with the same ozone concentration (10 mg/L) for a 20-minute treatment of tomatoes, but the surface color changed from red to yellow.34 The use of ionizing radiation to control foodborne pathogens on fresh food (up to 1 kilogray [kGy]) on fresh iceberg lettuce and fresh spinach, with a maximum dose of 4 kGy, is permissible.114 The effect of irradiation differs depending on the type of microorganism. Gram-negative

bacteria are usually the most sensitive, whereas bacterial endospores and fungi are the most resistant.15

50.2.8

Packaging

Modified atmosphere packaging (MAP) is a hyperbaric process where carbon dioxide (CO2), nitrogen, and/or oxygen are flushed into the package. The main purpose of this storage/packaging technique is to reduce the produce’s metabolic rate, extend shelf-life; and maintain intact physiological, nutritional, and quality characteristics.92 In general, Gram-negative bacteria are more sensitive to CO2 inhibition compared to Gram-positive, and the antimicrobial effect of MAP is enhanced by low storage temperature.12 Despite the advantages of this technology, MAP for whole produce has only been applied to a few commodities. The need for packaging line system modifications and the necessity to maintain package integrity during storage and transportation have limited its use. Conversely, the application of MAP for MP fruit and vegetables is expanding rapidly. Because MP produce has a shorter exposure time to a modified atmosphere, its shelf life is shorter. New discoveries and improvements in film technology are advancing, and several researchers have demonstrated the interaction between MAP and inherent microflora inhibition.55,101 Another type of packaging that has recently received increasing interest is the use of active packaging: films and/ or coating that can serve as carriers for various antimicrobial agents (antimicrobials, antioxidants, and other preservatives). This type of packaging offers the advantages of protecting produce against foodborne pathogens, extending shelf-life, and improving appearance and nutritional value.6

50.3

FRESH FRUITS AND VEGETABLES

50.3.1

Introduction

Fruits and vegetables are susceptible to contamination with a variety of microbial pathogens, spoilage microbes, fungi, and parasites.46,79,80,90 According to the Code of Federal Regulations, fresh fruits and vegetables include all produce in fresh form generally considered as perishable, whether or not they are packed in ice or held in common/cold storage.42 This definition does not include those perishable fruits and vegetables that have been processed into food of a different kind. Operations such as coating, drying, gassing, heating, ripening, refrigerating, washing with or without chemicals, waxing, and packaging are not considered to change the commodity into a food with a different character. It is important to distinguish fresh-cut fruits and vegetables, which are considered a processed food, and will be covered later in the chapter (see Section 50.4, ‘‘Fresh-Cut Fruits and Vegetables’’).

50.3.2

Normal Flora

Numerous factors can influence the inherent microflora present on fresh fruits and vegetables, such as water, soil, animals, manure, worker hygiene, and packinghouse and processing plant conditions.9 Plants harbor bacterial and fungal microflora that utilize carbohydrates, protein, and inorganic salts provided by produce exudate or the plant epidermis.68,96 Bacterial microflora often isolated on plants

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include Pantoea spp., Bacillus spp., Cyanobacterium, Enterobacter, Pseudomonas, Erwinia spp., and Pectobacterium, which come from contact with the soil, water, and air.17,48,97 The intrinsic properties of the produce commodity and the environmental conditions often dictate the resident microflora.23,75 Aerobic plate counts (APCs) of microbial populations on plants can reach up to 9 log CFU/g, with more typical concentrations ranging from 4–6 log CFU/g.75,38,39,56 The relative proportions and concentrations of bacteria may also vary among plants and even leaves of the same plant.4,88 Fruit microflora differ from that of vegetables because their lower pH levels from the presence of organic acids can limit bacterial growth.15

50.3.3

Spoilage

Fungal species can also thrive in the plant environment and are often characterized as spoilage organisms rather than normal flora. Molds are usually responsible for spoilage, particularly on fruits due to their acidity, which limits bacterial growth and competition.109 The frequently encountered fungal spoilage microbes on plants include Aureobasidium, Fusarium, Alternaria, Botrytis, and Penicillium.8,109 Some of these molds are opportunistic plant pathogens, along with certain bacteria, and may act as either natural or spoilage microflora. Fungal agents are also an important cause of produce postharvest loss. In 2004 in the U.S., 5.1% of the total peaches harvested (of pound for fresh consumption) were successfully attacked and spoiled by Rhizopus, Botritis, and Penicillium, while 22.5% of lettuce heads (of pound for fresh consumption) were discarded due to Geotrichum, Botrytis, and Sclerotinia contamination.98 The common bacterial genera causing plant decay and soft-rot disease include Pectobacterium, Xanthomonas, and Pseudomonas spp. 63,118 Soil-associated bacteria (e.g., Pseudomonas, Bacillus, Paenibacillus, and Clostridium) can enter surface wounds and cause spoilage. Streptomyces spp. were found in potato scab lesions, and Xanthomonas campestris was isolated from citrus bacterial spot epidemics in central Florida nurseries.47,65

50.3.4

Pathogens

Contamination of produce with foodborne pathogens can occur during pre- and postharvest handling of the products.9 Major pathogens that have been associated in produce outbreaks include Escherichia coli O157:H7, Salmonella spp., Listeria monocytogenes, Shigella spp., Campylobacter spp., Yersinia entercolitica, Bacillus cereus, and parasites including Cyclospora and Giardia. 1 1 2 Foodborne viruses have also been associated with fresh produce.113 Pathogens are able to survive over time and at low temperatures in soil, manure, and water, and several studies have demonstrated the transmission of microorganisms from these contaminated sources to plants.17,20,53,117 Preharvest, produce can become contaminated with human pathogens through contaminated irrigation water, manure, fecal matter, or animal contact.9 Good Agricultural Practices (GAPs) should be in place; examples of GAPs are available from the Florida Tomato-Good Agricultural Practices and the Leafy Greens Marketing Agreement.43,62 In postharvest processing, the microbial quality of water and effective postharvest sanitation are critical for maintaining product safety. The use of contaminated water

Fruit and Vegetables

during processing introduces pathogens to the produce surface and may also cause pathogen internalization depending on the produce type and water temperature.7,99 Postharvest temperature abuse in storage and distribution can also facilitate pathogen growth on and in produce. Some human pathogens have shown a preference to the exposed plant tissues of tomatoes and lettuce leaves in comparison to the intact fruit surface, so precautions should be taken to minimize damage during processing and distribution.5,97 There is no complete microbial elimination step in typical fresh produce processing, so produce contamination in the pre- and postharvest environments must be minimized. Enteric pathogen survival in plant tissues is limited by nutrient acquisition. The degradation of plant tissue provides nutrients to pathogens and also produces an entry point into the internal plant tissues. The damage of plant tissues through either fungal or bacterial phytopathogens (organisms causing disease in plants) generally, but not always, promotes foodborne pathogen proliferation unless there is competition for a limiting nutrient. Unlike phytopathogens, Salmonella and E. coli do not produce compounds like pectinases that degrade plant tissue. A survey of supermarket produce revealed that Salmonella spp. incidence on produce was twice as likely in the presence of the soft-rot plant pathogen, Pectobacterium carotovora.118 There is growth of E. coli O157:H7 in apple tissue infected with the fungal phytopathogen Glomerella cingulate when held at room temperature.89 Furthermore, L. monocytogenes is inhibited by Pseudomonas fluorescens and Pseudomonas viridiflava but is unaffected by the presence of Xanthomonas campestris on potato slices. It is hypothesized that iron competition limits Listeria growth in the presence of Pseudomonas spp.63 While nutrient acquisition is an important factor in facilitating the proliferation or inhibition of foodborne pathogens, the overall effect of the relationship between phytopathogens and human pathogens is still not fully understood. Nonpathogenic plant microflora can act to support or inhibit the survival of human pathogens on the plant surface. Salmonella Thompson aggregates with plant-associated Pantoea agglomerans on the leaf surface of cilantro, while Salmonella Newport is outcompeted by Enterobacter asburiae on the surface of lettuce leaves.18,31 E. asburiae also outcompetes E. coli O157:H7 on lettuce, while Wausteria paucula supports its survival on lettuce leaves.31 The background microflora of endive leaves has also been shown to prevent L. monocytogenes growth.22 Interactions among human pathogens and plant microflora are diverse and vary depending on the specific pathogen, plant microbiota, plant type, and environmental conditions.17 Indicators and surrogate microorganisms are used to evaluate the microbiological quality and/or safety of raw or processed food products. This can help in validating and verifying the effectiveness of microbial control measures.116 The absence or low concentration of an indicator organism suggests that the food has not been exposed to conditions favorable for target pathogen growth. Choosing a satisfactory indicator for fresh produce is a challenging process because the microorganism needs to be significantly related to the target pathogen for the specific produce, source, | 3

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handling procedures, and distribution practices, but it cannot be part of the normal flora. For fresh fruits and vegetables, coliforms are a poor indicator organism as they are part of the normal flora.2,70,82,86,103 Generic E. coli and fecal coliforms have been used as indicators of compost and agricultural water quality.67,116

50.3.5

Sampling Requirements

The Investigations Operations Manual published by the U.S. Food and Drug Administration (FDA) suggests that a proper statistical sampling procedure can be designed based on commodity-specific characteristics.115 When investigating the presence of pathogens or indicators in fresh fruits and vegetables, several factors should be considered, including product origin, location source (field, processing plant, retail location), size and number of samples, portion to be tested, diluents to be used, the most appropriate microorganism extraction method (washing, stomaching, homogenizing, macerating, or blending), selective media and growth conditions, and the possible presence of injured cells.116 In general, if a sample has no visible lesions, microorganisms will be on the external surface; therefore, the objective will be to ‘‘wash’’ viable cells from the surface. Phosphate-buffered saline, Butterfield’s buffer, and 1% buffered peptone water are the most common diluents used.108 Samples can be stomached, blended, or shaken. Stomaching or blending can result in food sample disruption that can lead to a decrease in pH of the recovery solution and subsequently in cells’ inhibition, so pH adjustment or use of a buffering diluent may be needed. Throughout the sampling process, it is imperative to record sample conditions, such as temperature and handling conditions. The processing conditions of the produce before sampling should also be taken into account when designing a sampling procedure. Products washed with chlorine-based sanitizers may need to be treated with 0.1% sodium thiosulfate to neutralize any chlorine residuals on the produce so that pathogen counts are accurate. Thiosulfate treatment does not deleteriously affect the concentration of human pathogens, including E. coli O157:H7.58 Once sanitizer residuals have been neutralized, the pH of the suspension solution used to dilute the fruit or vegetable during sampling is also of concern. The pH of macerated strawberries in 0.1 M phosphate buffer is about 6.0, while that of strawberries in 0.1% peptone can be below 3.9, resulting in reduced bacterial recovery.60 The low pH of the peptone solution may cause acid injury to the pathogens, reducing the observed concentrations and possibly resulting in false-negative testing results. Ultimately, the sampling and testing plans should be carefully designed based on the produce commodity, pathogens of concern, and physical properties of the commodity.

50.4

FRESH-CUT FRUITS AND VEGETABLES

50.4.1

Introduction

Fresh-cut produce is defined as any fresh fruit and/or vegetable that has been altered from its original form but remains in a fresh state. All fresh-cut commodities are trimmed, peeled, washed, and cut into usable product, which is subsequently bagged or prepackaged.51 Minimally

processed fruits and vegetables (MPFVs) are a rapidly growing market with annual sales of $12 billion.52

50.4.2

Normal Flora

Many types of microorganisms can be found on fresh-cut fruits and vegetables, as raw materials and processing operations can contribute to contamination during production, harvesting, washing, cutting, packaging, and shipping.17 MPFVs usually have higher moisture levels and nutrient availability compared to whole produce. Gram-negative and -positive bacteria, yeast, and molds have been isolated from fresh-cut produce. Populations of aerobic microorganisms and coliforms reported in chopped lettuce, salad mix, and celery ranged from 5–7 log CFU/g. Spinach stored in refrigeration for 12 days presented a count of mesophilic bacteria around 7–10 log CFU/g, while the counts of Pseudomonas and enteric bacteria were between 7 and 10 log CFU/g.78 Lactic acid bacteria, yeast, and pectinolytic bacteria, such as Erwinia spp., Pseudomonas spp., Xanthomonas, and Flavobacterium have been isolated from carrots, while Klebsiella spp. and Pantoea spp. have been identified on mango cubes.64,84

50.4.3

Spoilage

Fresh-cut produce have different physical and chemical characteristics compared to whole produce. The epidermis that prevents microbial penetration in raw products is disrupted during MPFV preparation and handling procedures (e.g., chopping and packaging), which can pose a higher risk for cross-contamination. Psychotrophic and Gram-negative bacteria are often responsible for postharvest spoilage. They are able to survive and grow at refrigerated temperatures and in modified atmospheres.17 P. fluorescens is the most common spoilage microorganism of refrigerated MPFVs, and it has been isolated from celery, potato, chicory, lettuce, cabbage, and melons.17,19 Soft-rot plant pathogens, like P. carotovora, are also a common spoilage microorganism associated with fresh-cut fruits and vegetables.17 High levels of lactic acid bacteria (LAB) are frequently detected in fresh-cut honeydew, papaya, pineapple, cantaloupe, cabbage, chicory, celery, bell peppers, and salad mixes.3,54,77 LAB do not require oxygen for energy production and they grow well in anaerobic conditions. Yeast and molds can also cause fresh-cut produce quality loss. Genera like Saccharomyces, Candida, and Rhodotorula were identified in salad mixes, while Penicillium, Alternaria, Botrytis, Aspergillus, Rhizopus, and Colletotrichum are the common fungi that cause postharvest spoilage in fresh produce.10

50.4.4

Pathogens

MPFVs have been associated with cases of foodborne illness, including outbreaks from Campylobacter jejuni, pathogenic E. coli, Salmonella spp., L. monocytogenes, and norovirus.17,27,40 Clostridium botulinum is also a concern for MAP MPFVs. C. botulinum spores are commonly present in soil and on fruit and vegetable surfaces; these spores are able to survive many adverse conditions. In MAP, where oxygen is eliminated, C. botulinum growth and toxin production are possible. However, inoculated produce studies have demonstrated that spoilage is evident before


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significant toxin production is detected.116 Similar to fresh products, sources of contamination for MPFVs are located all along the production chain from growing to marketing. The added risk for MPFVs is postharvest microbial crosscontamination and the potential for pathogen growth on temperature-abused products.17 As previously mentioned in Section 50.3, indicators and surrogate microorganisms can be used to evaluate the microbiological quality and/or safety of raw or processed food products, while validating and verifying the effectiveness of microbial control measures.116 Other types of indicators, so called ‘‘freshness indicators’’ to indicate microbial contamination due to temperature abuse and package leaks, have recently been developed but are not yet commercialized. They are usually biosensors, such as microbial-specific metabolites or enzymes that are activated and change color if microbial growth is detected.81

50.4.5


The same observations made for fresh produce apply to fresh-cut fruits and vegetables (for details, see Section 50.3.5, ‘‘Sampling Requirements’’).

50.5.3

CANNED FRUITS AND VEGETABLES

50.5.1

Introduction

The goal of the canning process is to destroy any microorganisms in the food and prevent recontamination by microorganisms. Heat is the most common agent used to destroy microorganisms. Removal of oxygen can be used in conjunction with other methods to prevent the growth of oxygen-requiring microorganisms.100 In conventional canning, basic steps are similar for both fruits and vegetables. A typical commercial canning process consists of the following steps: washing, sorting/grading, preparation, container filling, exhausting, container sealing, heat treatment to achieve commercial sterilization, cooling, labeling/casing, and storage for shipment.100 Canned vegetables generally require harsher processing than fruits because vegetables have much lower acidity and contain more heat-resistant organisms. Also, most vegetables require more cooking than fruits to develop characteristic flavors and textures. Fruits may be canned in water, juice, or sweet syrup. The sweet syrup helps the fruit hold its shape, color, and flavor. Sugar present in the syrup lowers aw and may prevent microbial growth.87

50.5.2

Normal Flora

The normal flora for fruits and vegetables destined for canning are the same as those present on the raw fruits and vegetables used as ingredients, as described above (see Section 50.4.2, ‘‘Normal Flora’’). The primary concern for canned products is sporeformers, whose outgrowth under anaerobic conditions in the can may be harmful. To effectively control the hazard from sporeformers, canned foods need to be processed under more extreme conditions. Refer to chapters ‘‘Canned Foods—Tests for Commercial Sterility’’ and ‘‘Canned Foods—Tests for Cause of Spoilage’’ for further information.

Spoilage

Most vegetative cells are destroyed by heat and acidification during the canning process. Swollen cans often indicate spoilage by either microbial spoilage or hydrogen production due to the interaction of acids in the food product with the metals of the can. High summer temperatures and high altitudes may also increase the degree of swelling. Spoilage of high acid and other canned foods by yeast, molds, and bacteria has been reported in fruit and vegetable products. Leuconostoc mesenteroides has been found to cause gaseous spoilage of canned pineapple and ropiness in peaches. The mold Byssochlamys fulva causes spoilage of bottled and canned fruits. Bacillus thermoacidurans causes flat sour or fermentation without gas production after sealing of cans and is particularly prevalent in canned tomato juice.11 Butyric anaerobes cause swelling of canned foods like tomatoes and tomato juice. Cans may burst and produce a butyric odor. LAB can cause severe can swelling, possibly leading to bursting and acidic odor production. Sulfide spoilage causes blackening of cans without producing any visible signs of spoilage in canned foods like mushrooms and sweet potatoes.94

50.5.4 50.5


Pathogens

Commercially canned foods have an excellent safety record. However, both Staphylococcus aureus and C. botulinum in commercially canned foods have caused outbreaks. In 1989, canned mushrooms imported for use in foodservice establishments were implicated and later confirmed to be the carrier in several outbreaks in the U.S.24 In 2007, canned chili products and institutional-sized cans of vegetables were recalled due to potential contamination with C. botulinum. These were the first recalls of commercially canned foods in the U.S. linked to botulism in 33 years, and improper processing that allowed the survival of C. botulinum spores appears to have been the cause.26 From 1999 to 2008, 116 outbreaks of foodborne botulism were reported. Of the 48 outbreaks caused by home-prepared foods, 38% (18) were from home-canned vegetables.29,30 These home-canned outbreaks are believed to be due to incorrect preparation, pH, and thermal treatments/processing. The U.S. Department of Agriculture (USDA) provides a complete guide to home canning to ensure proper recipes, and specific techniques are used to prevent contamination.111 C. botulinum spores are naturally found in soils and may be present on fruits and vegetables prior to canning. If the thermal treatment used in the canning process is not adequate, C. botulinum spores can survive and outgrow in the anaerobic conditions in the can, causing botulism.95 Insufficient acidification can also result in the survival and outgrowth of pathogen spores. The germination of spores of botulism can be controlled at or below pH 4.6. Using the concept of pH, the FDA has divided foods into three different categories: 1) acid foods, having pH 4.6 or less; 2) acidified foods, in the case in which a definite amount of acid food or acid ingredients are added to low-acid foods that have aw greater than 0.85, reaching a finished equilibrium pH of 4.6 or less; and 3) low-acid food with pH greater than 4.6.35 In first two cases of acid foods or acidified foods, a heat treatment at 100uC or less for a sufficient time must be applied to kill the vegetative cells of | 5

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microorganisms. In those cases in which vegetables are low acid and cannot be acidified, such as peas, potatoes, lentils, and chickpeas, commercial sterilization becomes necessary.35 To kill C. botulinum spores, it is necessary to perform pressure canning, in which the cold spot reaches an internal temperature of at least 115.5uC.100

50.5.5


Some of the defects of canned foods can visibly be seen on the can surface, while others cannot. Swollen cans can spray out toxic content and should be chilled before opening.112 Please see chapters ‘‘Thermophilic Flat Sour Sporeformers,’’ ‘‘Thermophilic Anaerobic Sporeformers,’’ ‘‘Canned Foods—Tests for Commercial Sterility,’’ and ‘‘Canned Foods—Tests for Cause of Spoilage’’ for further details on can sample requirements.

50.6

FROZEN FRUITS AND VEGETABLES

50.6.1

Introduction

not survive blanching and cannot grow at frozen temperatures.50 Frozen vegetables are often cooked before consumption. This is not always the case with frozen fruit. In 1990 and 1997, hepatitis A was associated with consumption of frozen strawberries.25,49,76 Frozen mamey puree was implicated as the source of a foodborne outbreak with 19 cases of Salmonella Typhi in 1999 and nine cases in 2010.28,57 Foodborne outbreaks of norovirus infection associated with the consumption of frozen raspberries occurred in Denmark and France (2005) and Finland (2009); another norovirus outbreak associated with frozen strawberries was found in Germany (2012).21,32,61,93

50.6.5


If plant cells are damaged during the blanching and freezing processes, exudate may be present during thawing, necessitating a pH adjustment or use of a diluent with buffering capacity when sampling acidic fruits, such as strawberries.

Frozen fruits and vegetables often undergo a blanching process prior to preservation by freezing. The time lapse between processes should be minimal to avoid bacterial growth in or on the product. Blanching and the addition of chemicals to preserve quality are discussed in Sections 50.2.4 and 50.2.5, respectively. Microbial contamination of frozen produce can occur postblanching from slicers, cutters, choppers, conveyor belts, lifts, flumes, hoppers, and fillers.50,106 Cleaning and proper sanitation is critical to avoid postblanching microbial contamination. Freezing of produce is not a lethal process; further discussion is found in Section 50.2.5.

50.7

DEHYDRATED FRUITS AND VEGETABLES

50.7.1

Introduction

50.6.2

Due to the decreased aw, the normal flora of dehydrated fruits and vegetables consist predominately of yeasts and molds. Although many organisms are destroyed by dehydration, some, including vegetative cells, manage to survive. A further decrease in viable numbers occurs during the storage of dehydrated fruits and vegetables. The rate of decrease is influenced by many factors, such as storage conditions, food type, and the predominant microflora. Contamination can occur during preharvest, harvest, or processing.45 Botrytis, Alternaria, Cladosporium, Aspergillus, Eurotium, and Rhizopus make up the predominant microflora of dehydrated fruits and vegetables.91 Spore-forming bacteria are also often found in the spore state on dehydrated fruits and vegetables.59

Normal Flora

The total numbers of bacteria on frozen vegetables tend to be lower than on nonfrozen products. This is a result of the blanching process, the higher quality of produce used, and some natural reduction of microbial counts in the frozen state.41 Airborne microorganisms from the handling of raw produce can settle on postblanch surfaces.71,73 In frozen vegetables, the predominant microorganisms are LAB, followed by Leuconostoc mesenteroides, enterococci, micrococci, and coliforms.50,72,103,105 Chopped greens, chopped spinach, and chopped broccoli were shown to have mean APCs of 5.48–6.26 log CFU/g.104 The normal microflora of frozen fruits include fungi, such as yeast, that can proliferate on equipment used to prepare products for freezing.50 Maintenance of good hygienic practices can achieve aerobic colony population below 5 log CFU/g on a routine basis.50

50.6.3

Spoilage

Microbial growth and spoilage does not occur in frozen fruits and vegetables due to the reduced water activity and storage temperature.50 When frozen produce spoilage does occur, it is often nonmicrobial related. Occasionally, yeast spoilage leading to gas production may occur upon thawing.69,119

50.6.4

Pathogens

It is rare for frozen produce to be suspected sources of foodborne outbreaks. Nonspore-forming pathogens generally do

Dehydration is an effective means of extending the shelf life of fruits and vegetables. Many dehydrated vegetables, such as those included in dry soup mixes (e.g., carrot, red pepper, cabbage, and onion), will be consumed cooked; thus, a kill step will be applied. However, dehydrated fruits (e.g., raisins, prunes, figs, and apples) will either be consumed as ready-to-eat foods or included as ingredients in other items, such as breakfast cereals, biscuits, or cakes.

50.7.2

50.7.3

Normal Flora

Spoilage

Black aspergilli are the most common fungi responsible for spoilage.83

50.7.4

Pathogens

Due to the low water activity of these products, mold toxins, not bacterial pathogens, are the predominant concern. Ochratoxin A, produced by Aspergillus ochraceus and Penicillium verrucosum, is one of the most common food-contaminating mycotoxins; it is potentially carcinogenic to humans. Patulin, another mycotoxin produced by Aspergillus and Penicillium, is most commonly associated with apple products but can also be found in other fruits.


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Aflatoxins can be a problem in figs; dried figs should be screened for bright greenish-yellow fluorescence under long-wave UV light.107 Spore-forming bacterial pathogens may also be present in dehydrated fruits and vegetables. Bacillus cereus is a spore-forming bacteria that is widely established in the environment and can often be found associated with dehydrated fruits and vegetables, especially those grown at or in the ground.107 It can be a problem in rehydrated potato products. The potato dehydration process can select for spore-forming bacteria, and germination can be initiated in the subsequent rehydration and heating processes for preparation.107

50.7.5


Heat shocking of samples may be required to induce bacterial spore germination prior to enumeration. 107 Moisture content and water activity are the most important hurdles for microorganisms in dehydrated fruits and vegetables; they should be monitored and maintained at an aw below 0.6. Specific moisture content requirements are established for certain products; the required method of analysis is the AOAC Official Method 934.06—Moisture in Dried Fruits.

50.8

RECOMMENDED METHODS (SEE APPROPRIATE CHAPTERS)

Aerobic Plate Count Enterobacteriaceae, Coliforms, and Escherichia coli as Quality and Safety Indicators Yeasts and Molds Thermophilic Flat Sour Sporeformers Thermophilic Anaerobic Sporeformers Bacillus cereus Clostridium botulinum and its Toxins Pathogenic Escherichia coli Listeria monocytogenes Salmonella Shigella Waterborne and Foodborne Parasites Toxigenic Fungi and Fungal Toxins Foodborne Viruses Canned Foods—Tests for Commercial Sterility Canned Foods—Tests for Cause of Spoilage

50.9 RESULT INTERPRETATION The microbiology of fresh fruits and vegetables often has little relationship to their quality or safety. Sound vegetables, for example, may yield extremely high aerobic plate counts because of high resident populations or because of contamination from soil and other natural sources. The routine microbiological examination of most fresh fruits and vegetables for indicators, such as coliforms, E. coli, or total bacterial counts is not recommended. However, routine testing may be warranted if fruits or vegetables are intended for consumption by immunocompromised individuals. Environmental monitoring of facilities or production inputs (e.g., irrigation water) may be preferred to product testing. The likely source of most organisms on frozen and other processed fruits and vegetables is equipment surfaces or


production environments; aerobic plate counts may provide a means of assessing sanitation of the processing line or plant environment. Problems in controlling contamination may differ with the type of fruit or vegetable; tolerance limits should be determined for each specific produce type.104 Coliforms and enterococci are part of the normal flora of plant products, and populations of 2–3 log CFU/g on fruit and vegetable product are not uncommon. The presence of coliforms should not be interpreted as reflecting the sanitary quality or safety of fresh produce without further analysis for more specific indicators of fecal contamination. Coagulase-positive S. aureus may be present on vegetables but usually in low numbers, less than 1 CFU/g.102 Thus, the routine culturing of fruits and vegetables for Staphylococcus spp. is not justified.

50.10

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Robert E.