MICROBIOLOGICAL QUALITY OF
PRE-CUT FRUITS FOR SALE OR SERVING IN
RETAIL OUTLETS
December 2006
Centre for Food Safety
This is a publication of the Centre for Food Safety of the Food and Environmental Hygiene Department of the Government of the Hong Kong Special Administrative Region. Under no circumstances should the research data contained herein be reproduced, reviewed or abstracted in part or in whole, or in conjunction with other publications or research work unless a written permission is obtained from the Centre for Food Safety. Acknowledgement is required if other parts of this publication are used.
Correspondence:
Correspondence:
Risk Assessment Section
Centre for Food Safety
Food and Environmental Hygiene Department
43/F., Queensway Government Offices,
66 Queensway, Hong Kong
Email: enquiries@fehd.gov.hk
Fruit produce is known to carry natural non-pathogenic microflora; however, contamination with pathogens from human and/or animal sources can also occur sporadically at various stages along the production line. Globalisation of fresh fruits potentially increases human exposure to a wider variety of food-borne pathogens and has resulted in a potential increased risk of foodborne illness outbreaks associated with the consumption of these raw commodities. Overseas studies showed that Salmonella, Shigella, hepatitis A virus and Cyclospora might be present on the surface of cantaloupe, strawberries, raspberries, etc. These pathogens might invade the inner surface of the fruits during slicing or peeling. Studies have already confirmed that pre-cut fruits might be contaminated with Salmonella, Listeria monocytogenes and high counts of Staphylococcus aureus. The findings of this study showed that the microbiological quality of all pre-cut fruits taken from the retail outlets were satisfactory, suggesting that food hygiene controls are in place in sampled premises and the risk of pre-cut fruits for foodborne illness is low. However, due to the potential for contamination of fresh fruits occurring prior to their purchase by consumers and the outbreaks of food poisoning in other parts of the world, retailers and consumers are advised to wash fresh fruits before preparation (such as peeling and cutting) and consumption; handle and cut fruits using clean and sanitized utensils and surfaces; store cut fruits at 4oC or below until served or sold; and discard cut fruits kept at ambient temperature for more than 2 hours.
OBJECTIVES
The purpose of the study was to determine the microbiological quality of pre-cut fruits in various retail outlets. The results will be used to assess the risk of pre-cut fruits to public health and to provide scientific information to support the development of hygienic handling guidelines on pre-cut fruits for retail outlets.
INTRODUCTION
2. Over the last several years, the number of foodborne illness outbreaks linked to fresh produce has increased in some developed countries such as the United States1. Reasons for the increase, besides improved surveillance, include an increase in the consumption of fresh produce, changing global and domestic distribution systems, lack of a processing step to eliminate pathogens and lack of systematic controls to prevent the presence of pathogens in fruits and vegetables2.
3.
Fruit produce is known to carry a natural non-pathogenic microflora; however, contamination with pathogens from human and/or animal sources can occur at various stages along the food chain 3. Use of improperly treated manure, contaminated water and poor hygiene practices throughout the fresh produce chain have been reported to be the sources of contamination 4.
4. Outbreaks of salmonellosis have been associated with the consumption of cut watermelon and cantaloupe. Three outbreaks involving watermelons and Salmonella occurred in 1954, 1979 and 19912,5,6. In 1990, cantaloupes from either Mexico or Guatemala were linked to Salmonella enterica serotype Chester infection, causing 245 illnesses in 30 states of the US7. In 1991, pre-sliced cantaloupes originating from Texas were linked to Salmonella serotype Poona infections8. In 1998, another outbreak involving 22 cases of Salmonella serotype Oranienburg and cantaloupe was reported in Ontario of Canada9. During 2000 and 2002 three multistate outbreaks associated with eating cantaloupe imported from Mexico to the US were again linked to Salmonella serotype Poona infections10.
5. Outbreaks involving other types of pre-cut fresh fruits were also reported. In January, 2002, 15 persons in the Hennepia county of Minnesota, after attending a holiday party at a country club, developed gastrointestinal illness11. Pre-cut fruits (pineapple, strawberries, honeydew melon, cantaloupe, watermelon, and grapes) were suspected to be contaminated with norovirus. In December 2003, 22 individuals in Wellington, New Zealand sickened after eating fruits salad12. Investigation suggested that one of the fruit salad ingredients was contaminated with norovirus. Another outbreak, involving nine states and 429 cases of infections in 2004, was linked to the consumption of pre-sliced Roma tomatoes contaminated with Salmonella13.
6. For most of these outbreaks, it has been assumed that cutting, slicing and peeling remove the protective surfaces of the fruits and expose the edible surface to a range of conditions that may increase the potential for microbial contamination2, highlighting the need of applying good hygiene practices from farm to fork to prevent contamination and/or bacterial growth.
SCOPE OF STUDY
7. Pre-cut fruits intended for sale or serving in retail outlets were the target samples. For the purposes of this survey, “pre-cut fruits” refer to fruits that have been cut open, sliced into pieces, but remain in the fresh state, and stored/displayed for sale or for serving in retail outlets (e.g. fresh fruit packs in supermarkets, cut fruits in buffets, assorted fruits offered by Chinese restaurants, etc.)
METHODOLOGY
Sampling
8.
The sampling period was between April and August 2006.
9. A total of 136 pre-cut fruit samples was collected by Health Inspectors from various retail outlets:
Restaurants in hotels
General restaurants;
Light refreshment restaurants;
Supermarkets;
Retail outlets with permits to sell pre-cut fruits (i.e. fruit shops);
The sampling distribution among these categories is outlined in table 1.
Table 1. Sampling Distribution of Different Regions
Regions
No. of Samples to be taken *
RH
GR
LRR
SM
FS
Region Total
Hong Kong
4
26
5
5
5
45
Kowloon
5
25
5
5
5
45
New Territories
9
21
5
6
5
46
Total
18
72
15
16
15
136
* Samples, as far as possible, to be taken from different districts within the region .
RH = Restaurants in hotels
GR = General restaurants
LRR = Light refreshment restaurants
SM = Supermarkets
FS = Fruit shops
10. Health Inspectors were required to note down whether the samples taken were under refrigeration or not at the moment of sampling and were at liberty to pick premises for sampling; however, they should, as far as possible,
(i) take samples from different districts within their region; and
(ii) avoid sampling at different outlets belonging to the same retail chain;
Analyses of samples
11. All samples, being kept at 4°C or below during transport, were submitted to the Public Health Laboratory Centre for analysis within 4 hours of sampling.
12. Escherichia coli count, presence of salmonella and Staphylococcus aureus count were used to reflect the microbiological quality of the pre-cut fruits.
13. Data on the microbiological quality of pre-cut fruit samples were analysed by the Risk Assessment Section of the Centre for Food Safety. The microbiological quality of pre-cut fruits was assessed against the criteria listed in Table 2. This is part of the criteria for “Fruits and vegetables (fresh)” extracted from the Microbiological Guidelines for Ready-to-eat Food14 recommended by the Centre for Food Safety.
Table 2. Microbiological criteria to be used in this survey
14. The three microbiological parameters (i.e. E. coli count, presence of salmonella and S. aureus count) examined in this survey reflect different aspects of food hygiene and safety of pre-cut fruits in retail outlets.
15. E. coli is commonly found in the gastrointestinal tract and faeces of human beings 15. Its presence provides direct evidence of faecal contamination, probably resulting from poor personal hygiene (e.g. hands are not washed thoroughly after toileting) during processing and preparation.
16. Humans and animals are the primary reservoirs of S. aureus. Staphylococci are present in the nasal passages and throats and on the hair and skin of 50 percent or more of healthy individuals 16,17. The bacterium is transient and does not usually become part of the resident flora of the skin and numbers of S. aureus on normal, undamaged and disease-free skin generally are low. However, the bacterium may become established as part of the resident flora and multiply to high numbers on people who frequently immerse their hands in water resulting in soreness and damage to the skin. This condition has been known to occur on the hands of operatives in food-processing plants 16.
17. Foods that require considerable handling during preparation, particular with bare hands, and that are kept at elevated temperatures after preparation are often involved in staphylococcal food poisoning 17 . If fruits are cut and handled with bare hands, S. aureus may be present on the sliced fruits. Unsatisfactory levels of S. aureus indicate that time/temperature abuse of a food is likely to have occurred following improper handling of food with bare hands.
18. Salmonella were reported to be responsible for outbreaks involving fresh fruits or pre-cut fruits 1,2,3,4,5,6. Salmonella was found present on the rind, presumably contaminated in the field or during washing in a packinghouse, and that the edible surface became contaminated during cutting or slicing 2. The presence of this organism in food is hazardous to health and indicates poor food preparation and handling practices such as cross contamination.
Results
19. All the 136 samples taken from various retail outlets were considered satisfactory according to the criteria stated in the Microbiological Guidelines for Ready-to-eat Food (Table 3). All samples were reported having E. coli count < 10 cfu per gram and S. aureus count < 20 cfu per gram. No salmonella was detected in the samples.
Table 3. The microbiological quality of pre-cut fruits sampled from various retail outlets
Number of sample
Plate counts (cfu/g)
E. coli
Salmonella
S. aureus
136
< 10
Not detected in 25 g
< 20
20. As regards storing temperature of the pre-cut fruits at the retail outlets, all samples were reportedly kept under refrigeration.
DISCUSSION
Dietary Exposure
21. Consumption of fruit and vegetables increased significantly in many countries during the past decade. In the US , f rom 1982 to 1997, per capita consumption of fresh fruits and vegetables increased from 91.6 to 121.1 kg, an increase of 32%2 . In Australia , the annual consumption of fruit and vegetables also increased significantly from 1988/89 to 1998/99 when up to 135 kg per person per year of fruit and 162 kg of vegetables were consumed 18. However, the health of consumers can be adversely affected by consumption of microbiologically unsafe fruit and vegetables.
Contamination of pre-cut fruits
22. Fresh fruits can become contaminated at any point during their growth, harvesting, processing, distribution, retail sale and final preparation. Some fruits such as melons and strawberries grow in contact with or close to the ground and are often in contact with soil, insects and animals during growing and harvesting in the field. Soil, manure and irrigation water are potential sources of pathogenic micro-organisms such as E. coli O157:H7 and Salmonella19,20. Fruit harvested from trees, such as peaches and plums, can be contaminated with faecal pathogens by pickers and handlers in the fields including harvesting and packaging equipment 21.
23. Overseas studies showed that pathogenic microorganisms might be present on the surface of fresh fruits. In 1990, 11 of 1 440 (0.76%) cantaloupe imported to the US from Mexico were positive for eight different Salmonella serotypes. In 1991, 24 of 2 220 (1.08%) cantaloupe were positive with 12 different Salmonella serotypes isolated. In another study, Salmonella from eight (5.3%) and Shigella from three (2.0%) of 151 cantaloupe samples were detected on the surface of the fruit2. These results suggest that melons may be naturally contaminated with pathogenic bacteria. Other studies found that Salmonella and hepatitis A virus might be isolated from strawberries22 and Cyclospora from raspberries23.
24. Fruit possesses natural antimicrobial barriers in the form of skin, shell or rind. These barriers protect the fruit from infection and most pathogenic microorganisms are unable to grow on the surface of intact fruit, though they may survive. However, microbial invasion and growth in the underlying tissues of fresh fruit may occur if the antimicrobial barriers are damaged. Unhygienic handling and processing of fresh fruit especially during chopping, slicing or peeling will increase potential for the invasion or growth of pathogenic microorganisms and hence the risk of transmission of foodborne illness. Overseas studies have confirmed that pre-cut fruits might be contaminated with Salmonella, Listeria monocytogenes and high counts of Staphylococcusaureus24,25.
25. In this study, all the 136 samples taken from retail outlets were found satisfactory when comparing with the criteria in the Microbiological Guidelines for Ready-to-eat Food recommended by the Centre for Food Safety, implying that food hygiene controls are in place in sampled premises and the risk of pre-cut fruits for foodborne illness is low.
26. It must, however, be emphasised that transmission of pathogenic bacteria such as Salmonella, and others not examined for in this study such as E. coli O157, Shigella and Listeria, remains a risk because of the likelihood of surface contamination of fruits with pathogens. The food industry must not become complacent about the findings of the study as epidemiological data clearly show that food poisoning outbreaks occur if hygiene practices break down. In addition the infective dose of many of these pathogens is low.
Managing the risk
27. Although melon rind provides a natural biological barrier preventing contamination of the edible interior, unwashed rind may contaminate both the flesh and the cutting utensil during slicing, causing food poisoning outbreaks26. To manage the risk, the FDA recommends sanitation practices for preparation and serving of melons. The food industry and consumer are advised, inter alia, to w ash fruits under running wa ter thoroughly just before eating or cutting so as to remove dirt and bacteria27, 28,29. Firm-skin fruits such as melons may be rubbed with a clean produce brush while rinsing with running water. Soap and detergent are not reco mmended because f ruits are porous and can absorb the chemicals which may cause adverse effects on health.
28. Notwithstanding the recommendation from the FDA, a survey conducted in 2002 focussing on consumer handling of fresh fruits and vegetables in the US revealed that more than 35% of consumers did not wash melons before preparation30. Consumers thought that the rinds would not be consumed and therefore washing of melons was not necessary. In Hong Kong , although no similar survey was conducted, it is believed that some consumers would also not wash the skin or rind of fresh fruits (such as melons, oranges, longans or lychees) before eating due to the same belief. A s overseas epidemiological data clearly show that unwashed rind may contaminate the flesh during slicing and cause food poisoning outbreaks, local consumers should be advised to wash fresh fruits thoroughly before slicing and consumption.
29. Some studies reported that inclusion of a disinfecting agent such as hypochlorite in the water can improve the elimination of microorganisms associated with the produce during washing but this does not guarantee safety. This is because sanitising efficiencies depend on a number of factors such as water quality, cleaner/sanitizer used, contact time, type of scrubbing action and characteristics of the produce surface 31,32 (e.g. the surface of strawberry and cantaloupe has many small indentations where microorganisms may “hide”). These factors are difficult to control at the consumer level and hence, many food authorities advise consumers to w ash fruits under running wa ter only 28,33,34 . Some authorities such as the FDA state explicitly that w ashing fruits with soap or detergent or using commercial produce washes is not recommended 28.
Effects of chilling and shelf life
30. Decreasing the temperature can prevent or slow the growth of microorganisms depending on the temperature and the microorganisms concerned. Chill temperatures (< 4°C) will prevent the growth of mesophilic bacterial pathogens such as Salmonella, Shigella, E. coli and Clostridium perfringens and psychrotrophs such as Listeria monocytogenes will grow only relatively slowly 35.
31. Studies showed that Salmonella Montevideo grew on tomatoes stored at 20 and 30°C but not at 10°C 36 and E. coli O157:H7 grew on fresh-cut melon at 12-25 oC but not at 5°C 37. Hence, consumers are advised to keep pre-cut fruits at or below 4°C and consume the product as soon as possible, preferably within one to two days. Pre-cut fruits that are kept at ambient temperature for more than 2 hours should be discarded 27,33
CONCLUSION
32. Published studies showed that fresh fruits could become contaminated with microorganisms, including human pathogens during their growth, harvesting, processing, distribution, retail sale and final preparation . G lobalisation of fresh fruits potentially increases human exposure to a wider variety of food-borne pathogens and has resulted in a potential increased risk for foodborne illness outbreaks associated with the consumption of these raw commodities.
33. The findings of this study showed that the microbiological quality of all pre-cut fruits taken from the retail outlets was satisfactory and the risk of pre-cut fruits for foodborne illness was considered low. However, d ue to the potential for contamination of fresh fruits to occur prior to their purchase by retailers and consumers and the outbreaks of food poisoning in other parts of the world, retailers and consumers are advised to follow good hygienic practices when handling fresh fruits.
34. In particular, retailers and consumers are advised to wash fresh fruits before preparation (such as peeling and slicing) and consumption; handle and cut fruits using clean and sanitized utensils and surfaces; store cut fruits at 4°C or below until served or sold; and discard cut fruits kept at ambient temperature for more than 2 hours. The Centre for Food Safety has developed guidelines on the hygienic preparation and handling of pre-cut fruits for the retail food businesses and the consumer (Annex I and II) .
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Annex I
A Guide to Foodservice and Retails
Guidelines on hygienic preparation and handling of pre-cut fruits
This guidance is intended for retail businesses (i.e. foodservice and retail establishments) that prepare,
sell and/or serve pre-cut fruits on the premises. It helps the businesses implement food safety measures
in their operations in order to process and sell safe pre-cut fruits.
2. For the purposes of this guidance, "pre-cut fruits" refer to fruits that have been cut open, but remain in
the fresh state, and stored/displayed for sale or for serving in foodservice and retail stores.
3. The basic principles of control include:
I.
I. Avoid contamination of fresh fruits / pre-cut fruits with pathogens
during storage;
during preparation;
during display.
II.
II. Prevent growth of pathogens on pre-cut fruits
by keeping them at 4°C or below;
by limiting their shelf lives (e.g. limit the shelf lives of pre-cut fruits to one to two days).
Purchase
Obtained fresh fruits from an identifiable, reputable source.
Inspect fresh fruits on arrival and accept fresh fruits that are not bruised or damaged. Reject fresh
fruits that are grossly contaminated with dirt, soil, or other organic matter.
Storage of fresh fruits
Store fresh fruits away from raw foods (such as raw meat, poultry and seafood) to avoid
cross-contamination.
Refrigerate fresh fruits if they are not used immediately.
Preparation
Allocate a work area, together with facilities and utensils, to pre-cut fruit operations. If it is necessary
to share work space and facilities, there must be a schedule of operations, including personnel traffic,
product traffic, and cleaning and sanitising of food contact surfaces to reduce the potential for cross
contamination of the ready-to-eat pre-cut fruits.
Use different sets of cutting boards and knives to handle fresh ready-to-eat fruits and raw foods
(such as raw meat).
Wash and sanitise cutting boards, knives and counter tops thoroughly with soap before and after food
preparation.
Wash hands thoroughly before and after handling fresh fruits
No bare hand contact with the finished product, especially cut melons. Single use gloves or an appropriate
utensil should be used to prevent cross-contamination.
Cut away any bruised areas on fresh fruits before preparing. Discard any rotten fresh fruit.
Wash fresh fruits (including those with skins and rinds that are not eaten) thoroughly under running tap water
just before eating, peeling or cutting. Do not use soap or detergent.
Rub firm-skin fruits under running tap water or scrub with a clean produce brush while rinsing with water.
Prepare just enough pre-cut fruits for the day needed. It is a good practice to discard any leftover and prepare
fresh-cut fruits on the next day.
Storage of pre-cut fruits
Wrap fresh-cut or peeled fruits tightly in plastic wrap and refrigerate them immediately
(i.e. at a temperature of 4°C or below).
Refrigerate pre-cut fruits within two hours of peeling or cutting.
Serving
When serving melons, do not let the rind come in contact with the cut melon.
Leftover cut fruits should be discarded if left at room temperature for more than two hours.
Display
Clean all display areas on a daily basis. Remove and sanitise any spillages immediately occurring
throughout the day.
Inspect prepackaged cut fruits on a regular basis throughout the day for damage, breakdown and
spillages.
Remove any poor quality prepackaged precut-fruits from sale and be disposed of.
Annex II
A Guide to Consumers
Advice on hygienic preparation and handling of pre-cut fruits
Purchase
Buy fresh fruit that is not bruised or damaged.
If buying fresh-cut ready-to-eat fruit, choose only those items that are refrigerated.
Buy only quantities of fruits that you can use before they begin to spoil.
Separate fresh fruits from raw foods such as meat, poultry and seafood to avoid cross-contamination when taking fresh fruits home from the market.
Storage after returning from market
Pre-cut or peeled fruits should be refrigerated immediately to maintain both quality and safety.
Refrigerate perishable fresh fruits immediately.
Keep fresh fruits separate from raw meat, poultry or seafood in your refrigerator.
Preparation
Cut fresh fruits until you are ready to eat it.
Wash hands thoroughly before and after handling fresh fruits
Use different cutting boards and knives to handle fresh ready-to-eat fruits and raw foods (such as raw meat).
Wash cutting boards, knives and counter tops thoroughly with soap before and after food preparation.
For added protection, sanitise cutting boards, knives and counter tops periodically.
Cut away any bruised areas on fresh fruits before preparing. Discard any rotten fresh fruit.
Wash fresh fruits (including those with skins and rinds that are not eaten) thoroughly under running tap water just before eating, peeling or cutting. Do not use soap or detergent.
Rub firm-skin fruits under running tap water or scrub with a clean produce brush while rinsing with water.
Refrigerate pre-cut fruits within two hours of peeling or cutting.
When serving melons, do not let the rind come in contact with the cut melon.
When transporting cut and perishable fruits to a picnic or gathering, put them in a cooler with ice or gel packs
Leftover
If not consumed, w rap fresh- cut or peeled fruits tightly in plastic wrap and refrigerate immediately (i.e. at a temperature of 4°C or below).
Leftover cut fruits should be discarded if left at room temperature for more than two hours.
Last
revision date: 05-01-2007