D CONTROL (fresh fruits)

Summary Signiﬁcant hazards a r Bacteria: E. coli O157:H7, salmonellae

r Protozoa, parasites, viruses: Cryptosporidium parvum, Cyclospora

cayetanensis, hepatitis A virus, Noroviruses. r Mycotoxins: Patulin in apples (Pen. expansum), aﬂatoxin in ﬁgs

(Asp. ﬂavus), ochratoxin A in grapes (Asp. carbonarius).

Control measures

Initial level (H 0 ) r Avoid hazardous agricultural practices. r Avoid applying untreated or improperly treated manure in fruit orchards:

treat manure to kill bacteria before it is used as fertilizer. r Keep contaminated irrigation water away from fruits.

r Use potable or treated water for washing and processing fruits.; r Avoid using dropped or windfall fruits.; r Discard badly bruised or rotten fruits immediately.; r Assure microbiological safety and quality of fresh fruit by good agricultural

practices and proper handling on the farm, and effective processing and handling at packinghouses and during shipment and subsequent marketing.

Reduction (ΣR) r Few measures are available other than sorting and washing to reduce hazards. Increase (ΣI)

r Minimise increase by appropriate storage. r Train workers to wash their hands properly and make sure they have access

to toilets. r Keep packing facilities clean and free of pests.

Testing

r Routine microbiological testing of fruit is not recommended. r Aerobic colony counts may be useful to monitor effectiveness of processing

on the microbial populations.

E. coli may be used as an indicator of faecal contamination. r Equipment hygiene may be monitored using rapid tests such as ATP.

Spoilage

r Spoilage of most fruits is caused by fungal growth. Most of the practices preventing food safety hazards will also prevent spoilage.

a In particular circumstances, other hazards may need to be considered.

337 Control measures.

FRUITS AND FRUIT PRODUCTS

A correctly constructed HACCP plan for production of fruit can signiﬁcantly reduce the risk that fruit would be a source of foodborne disease (Rushing et al., 1996). The HACCP should take account of the possibility that fruit may carry pathogenic microorganisms. Fruits and fruit products are frequently consumed raw without having been exposed to a process that can reliably eliminate pathogens. Therefore, it is essential that measures to prevent contamination of fruit with pathogens of faecal origin, are in place at all points in the growing, processing, storage, distribution, and preparation chain (Brackett, 1992). These measures include avoiding hazardous agricultural practices, for example inappropriate use of organic fertilisers or the harvesting of fallen apples that may have been exposed to animal faeces. Good sanitation must be practised during picking, packing, and grading. Washing of fruit in water, brings about a small reduction in the microbial load if done correctly. The addition of chlorine to the wash water or dipping in chlorine solutions, can signiﬁcantly reduce the concentration of pathogens on the surface of fruit, and therefore reduce hazards to the consumer, but cannot be relied upon to eliminate pathogens (Beuchat, 1996). Inadequate sanitation of processing environments and poor hygiene among workers are particularly hazardous when fruit is being peeled and sliced or otherwise prepared for consumption.

Many of the same practices that improve the microbiological safety of fresh fruits, are the ones that help prevent spoilage. Care must be exercised to minimize damage to the fruit, maintain appropriate storage temperatures and conditions, wash and cool fruit in a manner that minimizes inﬁltration of microorganisms, and maintain adequate sanitation. Segregation of contaminated fruit at the earliest, will help prevent the spread of contamination to adjacent pieces.

Fungi. Before harvest, fungicides and insecticides are effective in reducing the incidence of fungal invasion of fruit. Control depends on adequate conditions for handling, transport, and storage. However, implementing control measures is made difﬁcult by (i) the variety of spoilage fungi which may occur; (ii) limitations due to the physiology of the fruit; and (iii) conditions favourable to senescence and ripening of fruit are also favourable for fungal growth (Smith, 1962).

Control of temperature, relative humidity, atmospheric composition, and the use of chemical in- hibitors are all important in preservation of fresh fruit. Again, avoidance of physical damage to the fruit and the prevention of internalization of mold spores are important. Some details are given below.

Citrus fruit. Control of fungal spoilage in citrus fruit relies primarily on careful handling. Post- harvest treatments are based on washes heated to 40–50 ◦

C and containing detergents, weak alkali, and/or fungicides such as thiabendazole or sodium o-phenylphenate (SOPP). After dipping, fruits may

be individually wrapped in waxed paper containing biphenyl or packed in trays that ensure separation of individual fruits (Ryall and Pentzer, 1982). Control of Geo. candidum relies on storage at temperatures below 5 ◦ C.

Pome fruits. Control measures include careful handling and the use of fungicides such as benomyl, dichloran or SOPP. Because rots spread by contact from fruit to fruit, it is also common practice to individually wrap fruits in waxed papers containing a fungicide such as biphenyl. Properly controlled atmospheric storage can effectively maintain unspoiled fruit, particularly apples, for extended periods of time.

Stone fruits. Infection by Monilia fructicola commences in the orchard. Rigorous pre-harvest spray programs with benomyl or similar benzimidazole fungicides are necessary. Storage temperatures below

C assist in control (Snowdon, 1990). Dichloran is an effective fungicide against Rhizopus. A combined benomyl and dichloran pre-harvest spray program for the control of both Monilia and Rhizopus, has been used extensively for peaches, apricots, and nectarines (Hall and Scott, 1977; Ryall and Pentzer, 1982).

MICROORGANISMS IN FOODS 6

Grapes. Fungal control involves the use of pre-harvest sprays with benomyl and rapid transfer of fruits to cold storage, after picking. Post-harvest treatments with sulphur dioxide or benomyl, are also effective (Hall and Scott, 1977).

Berry fruits. Pre-harvest spray programs with benomyl, are important for control, as is refrigerated storage. For most soft fruits, avoidance of wetting is critical for extending shelf-life. Post- harvest antifungal treatments are of little beneﬁt (Ryall and Pentzer, 1982), however, low dose irradiation has proven highly effective for delaying mold spoilage (Thayer and Rajkowski, 1999).

Tomatoes and melons. Alternaria alternata can be transmitted through seeds, so fungicide treatment before planting can be beneﬁcial for both tomatoes and melons. Alternaria alternata grows at all acceptable handling temperatures, so post-harvest invasion can be avoided only by rapid marketing. Careful irrigation and handling to avoid cracking and post-harvest fungicidal dips will reduce losses (Snowdon, 1991).

Rhizopus rot in tomatoes can be effectively reduced by improved hygienic practice in the ﬁeld: removal of fallen or culled fruit to reduce spore dispersal, disinfection of ﬁeld boxes by heating, and careful harvesting (Snowdon, 1991). Post-harvest hot water or fungicide dips, irradiation, waxing, and wrapping are all of value.

Sour (Geotrichum) rot control requires control of insects, that puncture fruit, reduction in mechanical damage, and culling of cracked fruit (Snowdon, 1991). Anthracnose of melons must be controlled by strict hygienic conditions, by the removal of all crop debris and cleaning of containers. Planting on plastic sheets, also decreases contact with soil. Inoculating young plants with the fungus will reduce disease severity and fungicide sprays can be of value (Snowdon, 1991). The use of resistant cultivars can reduce or overcome Cladosporium rot.

Fusarium rots are difﬁcult to control, sometimes requiring soil disinfection, seed dressing, systemic fungicides, and careful inspection in the packing house (Snowdon, 1991).

Tropical fruits. Benomyl and thiabendazole, chlorine, and hot water have all been quite successfully used for the control of banana rot (Eckert et al., 1975). Control of anthracnoses relies on benomyl or

a variety of other fungicides. Colletotrichum conidia appears to be especially heat sensitive, and hot water dips for 5 min at about 55 ◦

C have been beneﬁcial for preservation of mangoes (Smoot and Segall, 1963) and other fruits. However, after such heat treatments, care must be taken that only appropriately treated water is subsequently used to cool the fruit. Contaminated cooling water has been linked to mango-associated cases of salmonellosis. For further information on the control of diseases of tropical fruits, see Eckert et al. (1975) and Champ et al. (1994).

IV Pre-cut (minimally processed) fruit

A Effects of processing on microorganisms Pre-cut (P-C) fruits include ready-to-use/eat, pre-cut, lightly processed, and fresh-cut fresh fruits. These

are sold under refrigerated storage in supermarkets, retail food stores and restaurants or chilled on ice by roadside fruit stalls in many developing countries. P-C fruits are products that contain live tissues or those that have been only slightly modiﬁed from the fresh condition and are like fresh in character and quality (Wiley, 1994). Such minimally processed refrigerated fruits meet consumer demands, for e.g., “like-fresh” fruit products with extended shelf-life, that ensure food safety and maintain nutritional and sensory quality. Typical production of P-C fruits often includes preservation methods in which some,

339 but not all species of microorganisms are reduced in count and speciﬁc enzyme systems may be partially

FRUITS AND FRUIT PRODUCTS

or fully inactivated in the package or prior to packaging (Wiley, 1994). In processing P-C fruits, operations such as peeling remove important natural barriers to contamination. Likewise, the cutting of the fruit exposes new surface to microbial contamination and generally releases nutrients that enhance the growth of microorganisms. The process of cutting/slicing can transfer microorganisms from the exterior surfaces onto the newly exposed cut surfaces (Lin and Wei, 1997). For a number of fruits, the newly exposed interior surfaces can support the growth of a variety of microorganisms including enteric bacteria that are pathogenic for humans (Escartin et al., 1989; Liao and Sapers, 2000; Larson and Johnson, 1999; Riordan et al., 2000; Weissinger et al., 2000). Thus, an important step in the successful preparation of P-C fruits are effective cleaning and sanitization of the fruit surfaces, prior to cutting and the maintenance of a high level of sanitation throughout processing and packaging. Typically, the fruits undergo extensive washing and disinfection with 200 ppm chlorine or other sanitizing agents (see below).

B Spoilage The type and importance of P-C fruit spoilage reﬂects the intended use of the product and the adequacy

of the cold chain. For street vendors, where the shelf-life of the product is a few hours and the product is generally not refrigerated or packaged for extended storage, spoilage is generally not an issue. As the shelf-life of the product becomes increasingly extended, it becomes more important to adequately re- frigerate. With a product that has a 7–14 day shelf-life, the microorganisms of concern are psychrotrophs that are capable of growing at 2–4 ◦

C, and typically have an optimal growth at temperatures between 20–30 ◦

C (Brackett, 1994). Properly processed P-C fruits contain low microbial loads as shown for durian and dragon fruits (Anonymous, 1999a,b). For P-C jack fruit, the microbial counts (TPC, yeast, mould, and coliforms) (see a) need to be reduced by 1–3 log cycles (Faridah et al., 1999). Microbial contamination of P-C durian sampled from wet markets and supermarkets was reported to be low and no pathogens were detected.

Samples from the wet market were reported to have TPC and yeasts ranging from 10 2 to 10 4 cfu/g, mold too few to count, coliforms from <3 to 23 MPN/g and E. coli of <3 MPN/g. Those obtained from supermarkets yielded the following results: TPC from not detected to 10 3 cfu/g, yeasts from not detected to

10 2 cfu/g, mold too few to count, coliforms from <3 to 9 MPN/g and E. coli at <3 MPN/g (Chudhangkura et al., 1999). An evaluation of 30 samples of street-vended sliced papaya observed TPC between

10 3 –10 7 cfu/g, coliforms were detectable in 70% of the samples at a range of <3–160 cfu/g, and E. coli was veriﬁed in approximately half of the samples containing coliforms (Mukhopadhyay et al., 2002).

C Pathogens Pathogens can be introduced into fruits from soil, water, animal waste, insects, and fruit-handlers.

Fruits can serve as vehicles for almost any foodborne pathogenic microorganisms that can result in disease under favorable conditions. However, only a relatively few pathogenic microorganisms would normally be considered a serious threat to refrigerated fruits (Brackett, 1994). A number of outbreaks have occured with precut fruits, such as salmonellosis associated with pre-cut watermelons (Gayler et al., 1955; Lawson et al., 1979; CDC, 1979) and pre-cut cantaloupes (CDC, 1991). There have been several outbreaks of salmonellosis associated with pre-cut tomato products (O’Mahoney et al., 1990; Cummings et al., 2001), and at least one report of Campylobacter infections associated with pre-sliced cucumbers and tomatoes (Kirk et al., 1997).

More recently, concerns have been raised about growth of Listeria monocytogenes in fruits such as melons where pH is between 5.5 and 6.5 (Ukuku and Fett 2002; Leverentz et al. 2003), and some studies

MICROORGANISMS IN FOODS 6

(Leverentz et al., 2003) have demonstrated that rapid growth of the organism can occur during storage at 10 ◦ C.

An outbreak caused by E. coli O157 was recently traced in cucumbers in a cucumber salad (Duffell et al. 2003) and fresh fruits may need to be considered as a vehicle of this organism.

D CONTROL (fresh fruits)