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The Microbiological Examination of Ready-to Eat Organic Vegetables from Retail Establishments

LACOTS/PHIS Coordinated Food Liaison Group Studies 15jun01

[ Press Release ]

SK Sagoo, CL Little and RT Mitchell.
LACOTS/PHIS Coordinated Food Liaison Group Studies
PHLS Environmental Surveillance Unit, 61 Colindale Avenue, London NW9 5EQ.

On behalf of the Local Authorities Coordinated Body on Food and Trading Standards and the Public Health Laboratory Service.

Summary

There has been a significant expansion of the UK organic market since 1998/99. Of the various commodity sectors making up the organic market, fruit and vegetables is the largest sector and this has been reflected in an increased interest in their microbiological safety. During May and June 2000 a microbiological study of uncooked ready-to-eat organic vegetables was undertaken to determine the microbiological quality of these organic vegetables on retail sale, and is the first study to provide such information. Examination of organic vegetables from supermarkets, health food shops, farmers' shops or markets, greengrocers, market stalls, and box schemes revealed that the vast majority (3185 of 3200; 99.5%) were of satisfactory/acceptable quality whilst only 15 (0.5%) were of unsatisfactory quality. Unsatisfactory results were due to Escherichia coli and Listeria spp. (not L. monocytogenes) levels in excess of 102 cfu/g. L. monocytogenes, Salmonella spp., Campylobacter spp. and Escherichia coli 0157 were not detected in any of the samples examined, indicating that overall agricultural, hygiene, harvesting and production practices were good.

Introduction

Organic food is grown using those principles and techniques that predated the introduction of modern agrochemical and intensive farming techniques. On-going food concerns, specifically about Bovine Spongiform Encephalopathy (BSE) and Genetically Modified (GM) foods are without doubt generating a significantly increased interest in organic foods, s. The word 'organic' may only be applied to crop products that have been grown, processed and packaged in accordance with the requirements of the European Community (EC) Regulation 2092/912 (implemented in the UK as the Organic Products Regulations 1992, as amended)21. All food sold as organic must come from growers, processors or importers who are registered and subject to regular inspection. In the UK, the United Kingdom Register of Organic Food Standards (UKROFS) ensures that the various UK certification bodies, such as the Soil Association, properly apply the Regulation. EC legislation for organic produce also require labels to indicate, by a unique code number the organic certification body (e.g. in the UK, 1 to 7) with which the producer or packer is registered.

Organic food is a small but growing part of the food industry in the European Union, and its existence provides an element of consumer choice, for which there is growing demand18. From 1993 to 1998/99 the sale of organic food in the UK has risen markedly from 100 million to 390 million19. The largest sector is fruit and vegetables, and in 1998/99 this commodity area accounted for 175m (45% of the total), of which 82% was imported. Overall, 70% of organic food was sold in supermarkets during 1998/9919. With an annual market growth of 50%, it is estimated that by 2005 organic food in the UK will account for 20% of the total food market with a potential value of over l billion by early 20015,17.

Manure and other animal wastes are widely used in agriculture, both organic and conventional. The use of manure as fertiliser, whether in organic or conventional agriculture, gives rise to concern about the possible contamination of produce with microbial pathogens, especially Escherichia coli 01577. However, the Soil Association recommendations for manure storage and treatment on organic farms may lead to enhanced reductions to the levels of pathogens in stored manures that are to be spread to land19. The UK Food Standards Agency (FSA) view is that there is currently no firm evidence to support the assertion that organic produce is more or less microbiologically safe than conventionally farmed produce 4. A recent review by the Ministry of Agriculture, Fisheries and Food also concludes that at present there is insufficient information to state categorically whether the risk of pathogen transfer to produce on organic farms differs significantly from the risk associated with conventional farming practices.8

As a consequence of the lack of information concerning the microbiological quality of organic vegetables, despite their increased consumption, the Local Authorities Coordinating Body on Food and Trading Standards (LACOTS) / and the Public Health Laboratory Service (PHLS) Coordinated Food Liaison Group programme undertook a study on the microbiological quality of uncooked ready-to-eat organic vegetables on retail sale in the UK. The study was specifically not a comparative study of organic and conventionally produced vegetables.

Materials and Methods

Sample Collection

Ready-to-eat organic vegetables collected from retail outlets and doorstep delivery schemes were examined in PHLS and non-PHLS laboratories in the UK between 1st May and 30th June 2000 according to a standardised protocol and reporting system. Vegetables included in the study were those that could be consumed without any cooking or further preparation by the consumer other than portioning as necessary and light washing and/or scraping. Vegetables sampled (-150g) were those that were grown in close proximity or in contact with soil (e.g. broccoli, cabbage, carrot, cauliflower, celeriac, celery, cress, lettuce, mushrooms, radish, spring onions, watercress), and other salad vegetables, such as cucumber, pepper, and tomato. Samples were collected from supermarkets, health food stores, greengrocers, farmshops/markets, market stalls, doorstep box-scheme deliveries, and warehouse/storage area box-schemes by staff from local Environmental Health Departments and were transported to the laboratory in accordance with the Food Safety Act 1990, Code of Practice No 710.

Information on the organic vegetable samples and outlets was obtained by observation and enquiry and recorded on a standard proforma. This included the country of origin, organic certification body number, packaging, and details concerning the retail display of the product.

Sample Examination

Four representative (-25g) samples from the organic vegetables were required for microbiological examination (Table 1). Samples were collected and examined within their `best before date' or `display date'. Gram-negative pathogenic organisms if detected would be sent to the Laboratory of Enteric Pathogens (LEP), Central Public Health Laboratory (CPHL). Listeria monocytogenes at levels at 103 cfu/g or more and other species of Listeria at levels of 104 or more were sent to the Food Safety Microbiology Laboratory (FSML), CPHL for further characterisation.

Table 1. Methods for the microbiological examination of ready-to-eat organic vegetables

Microorganism   Microbiological Method
Escherichia coli Enumeration PHLS Standard Methods for Food Products F20
Listeria spp. Enumeration Based on BS EN ISO 11290-2: Part 2 19982, using Oxford Listeria Agar incubated at 30C in place of PALCAM agar incubated at 37C
Listeria monocytogenes Enumeration Based on BS EN ISO 11290-2: Part 2 19982, using Oxford Listeria Agar incubated at 30C in place of PALCAM agar incubated at 37C
Campylobacter spp. Detection PHLS Standard Methods for Food Products F21'
Salmonella spp. Detection PHLS Standard Methods for Food Products F1315
Escherichia coli 0157 Detection PHLS Standard Methods for Food Products F17'6

Results

A total of 3200 uncooked ready-to-eat organic vegetable samples were examined by 43 laboratories (30 Public Health Laboratories (PHLS) from all 8 PHLS Groups; 13 non-PHLS) in England, Wales, Scotland and Northern Ireland. Fifty-two Local Authority Food Liaison Groups participated in this study (Annex 1) and samples were submitted by 350 Local Authorities. A further 352 samples did not fit the criteria described in the study protocol and were not included in the analysis as they were either not ready-to-eat vegetables or were fruit.

Microbiological Results

E. coli was detected in 1.5% (48/3200) of ready-to-eat organic vegetable samples, and was present at 102 cfu/g or more in 0.3% (11) samples (Table 2). Listeria spp. (not including L. monocytogenes) were detected in 0.2% (6/3200) samples, and were present at 102 cfu/g or more in 0.1% (4) samples. Further characterisation of the two Listeria spp. found in excess of 103 cfu/g revealed the organisms to be L. innocua (from a sample of watercress) and L.seeligeri (from a sample of radish). L. monocytogenes, Salmonella spp., Campylobacter spp. and E. coli 0157 were not detected in any of the samples examined.

Table 2. Microbiological results of 3200 uncooked ready-to-eat organic vegetables

  NDa
in
25g
Db in
25g
<20c 20-
<102
102 -
<102
103 -
<104
104 -
<105
105 -
<106
106 -
<107
>107 NEd

Escherichia coli

 

 

3150f

37

9

2

 

 

 

 

2

Listeria spp.

 

 

3192f

2

2

2

 

 

 

 

2

L. monocytogenes

 

 

3198f

 

 

 

 

 

 

 

2

Campylobacter spp.

2883

 

 

 

 

 

 

 

 

 

317e

Salmonella spp.

3196

 

 

 

 

 

 

 

 

 

4

Escherichia coli 0157

3193

 

 

 

 

 

 

 

 

 

7

a   ND, Not Detected
b   D, Detected
c   cfu/g
d   NE, Not examined (full set of microbiological parameters not performed on sample due to insufficient sample collected)
e   These were not examined due to unavailability of the selected supplement cycloheximide during May - June 2000
f    lower limit of detection 20 cfu/g

Microbiological Quality of Uncooked Ready-to-eat Organic Vegetables

Based on the PHLS Microbiological Guidelines for some ready-to-eat foods sampled at the point of sale,12 3146 (98.5%) of 3200 ready-to-eat organic vegetables were satisfactory, 39 (1%) acceptable, and 15 (0.5%) were of unsatisfactory microbiological quality. E. coli and Listeria spp. (not L. monocytogenes) were the microbiological parameters associated with unsatisfactory results. None of the samples examined were of unacceptable microbiological quality (Figure 1 and Table 3).

Figure 1 Microbiological quality of ready-to-eat organic vegetables based on the 2000 PHLS Microbiological Guidelines

Table 3. Key to classification 12

Criterion Microbiological quality (cfu per gram unless stated)
Satisfactory Acceptable Unsatisfactory Unacceptable/
potentially hazardous
Escherichia coli <20 20-<10 >10, N/A*
Listeria spp. <20 20-<10' z10, N/A
Listeria monocytogenes <20 20 -<10' N/A 210,
Campylobacter spp. Not detected in 25g     Detected in 25g
Salmonella spp. Not detected in 25g     Detected in 25g
Escherichia coli 0157 Not detected in 25g     Detected in 25g

A major feature of the data is that of the microorganisms tested (Table 2), none were found in 3146 of the 3200 (98.5%) samples examined. As this forms the vast majority of the data, information collected on the organic vegetable samples and outlets (presented below) had no significant effect on the microbiological quality of the vegetables with regard to samples of unsatisfactory quality (data not shown), i.e. no correlation was found between samples of unsatisfactory quality and product information.

Product Information

Types of Ready-to-eat Organic Vegetables

A total of 21 different vegetable types were examined (Table 4). The majority of the vegetables examined were grown in close proximity or in contact with the soil (74%; 2349/2300) with the remainder being non-soil contact vegetables (26%; 851).

Table 4. Types of ready-to-eat organic vegetables (n=3200)

Organic vegetable type

Number of samples

(%)

Those grown in close proximity or in contact with soil (n=2349):

Broccoli

209

(7)

Cabbage

159

(5)

Carrot

478

(15)

Cauliflower

70

(2)

Celeriac

11

(<1)

Celery

193

(6)

Cress

12

(<1)

Lettuce

415

(13)

mushrooms

425

(13)

Radish

17

(<1)

Spring onions

87

(3)

Water cress

65

(2)

Other (spinach, leeks, shallots, chard)

208

(7)

Non-soil contact vegetables (n-851): 

Cucumber

221

(7)

Pepper

184

(6)

Tomato

428

(13)

Other (baby corn, cherry tomato)

18

(<1)

Total

3200

(100)

Type of Outlet

Over three-quarters (79%; 2528/3200) of samples were collected from supermarkets, 214 (7%) from health food shops, 175 (5%) from farm shops/markets, 70 (2%) from greengrocers, 54 (2%) from doorstep box-scheme deliveries, 37 (1%) from market stalls, and 24 (1%) from warehouse/storage areas. Other outlets (butchers, garden centre, nursery shop, and organic product specialist) accounted for 76 (2%). For 36 (1%) of outlets visited this information was not recorded (Fig. 2).

Figure 2 Ready-to-Eat Organic Vegetables Collected from Retail Outlets (n = 3200)

Packaging & Display

Of the ready-to-eat organic vegetables sampled (3200), 2586 (81%) were pre-packed vegetables and 567 (18%) were unwrapped or loose on sale. For the remaining 47 (1%) of samples this information was not recorded. The vast majority of samples obtained from supermarkets (96%; 2434/2528) were pre-packed. Most of the samples (96%; 3067/3200) collected were displayed and stored in a clean environment as judged by the Sampling Officer, while 59 (2%) were not. For 74 (2%) of samples this information was not recorded. A quarter of samples (24%; 770) collected had visible soil contamination, however most did not (73%; 2339). For the remaining 91 (3%) of samples this information was not recorded. Of the samples that did have visible soil contamination most were unwrapped or loose on sale (78%; 590/770).

Country of Origin

Of the 3200 organic vegetables sampled, the majority were imported (70%; 2240) with most originating from Spain (31%) and the Netherlands (15%) (Table 5). Of the 30% (943) of samples produced in the UK, nearly a quarter (24%; 226/943) originated in England, however most (67%; 634/943) samples specified UK only.

Table 5. Country of origin of ready-to-eat organic vegetables collected (n=3200)

Country of Origin

Number of samples

(%)

United Kingdom (n=943):

943

(30)

   England

226

(24.0)

   Northern Ireland

72

(7.0)

   Scotland

8

(7.0)

   Wales

63

(7.0)

   UK

634

(67.0)

Other EC Countries (n=1774):

   Austria

6

(<1)

   Belgium

47

(2)

   France

90

(3)

   Germany

1

(<1)

   Greece

2

(<1)

   Ireland

2

(<1)

   Italy

176

(5)

   Netherlands

464

(15)

   Portugal

7

(<1)

   Spain

979

(31)

Third Countries n=316):

   Argentina

8

(<1)

   Canary Islands

38

(1)

   Channel Islands

1

(<1)

   Egypt

23

(1)

   Israel

162

(5)

   Mexico

51

(2)

   Morocco

1

(<1)

   New Zealand

10

(<1)

   Tunisia

3

(<1)

   USA

17

(<1)

   Zambia

1

(<1)

   Zimbabwe

1

(<1)

Produce of two or more countries (not UK)

19

(<1)

Not recorded

148

(5)

Total

3200

(100)

Identification as organic (Certification Body Number)

The majority (81%; 2585/3200) of organic ready-to-eat vegetable samples were identified as organic by labelling containing a UK certification body number (Fig. 3), and of these almost three-quarters (74%; 1919) were by the Soil Association. The remainder (11%; 364) was identified as organic by other EC Member State certification bodies. However, for 252 (8%) of samples this information was not known.

Figure 3 Ready-to-Eat Vegetables Identified as Organic (Certification Body Number) (n = 3200)

Discussion

This study has shown that the vast majority (99.5%) of the uncooked ready-to-eat organic vegetables sampled at retail in the UK were of satisfactory/acceptable microbiological quality. Only 0.5% were classed as unsatisfactory according to published guidelines 12. Unsatisfactory results were due to E. coli and Listeria spp. (not L. monocytogenes) counts at 102 cfu/g or more. E. coli is a faecal organism and both E. coli and Listeria spp. are environmental microorganisms that are found in soil and water. Therefore, vegetables may easily become contaminated with these bacteria. However, the absence of pathogens (L.monocytogenes, Salmonella, Campylobacter, and E. coli 0157) and the low incidence (1.5%) of E. coli and Listeria spp. associated with these organic vegetables indicates that overall agricultural, hygiene, harvesting, and production practices were good.

The greatest growth in organic sales has been through the main multiple retailers (supermarkets). More consumers will have access to these outlets on a national basis than can be reached by other distribution methods, such as farmers' markets and box schemes 5. In this study over three-quarters (79%) of vegetables were collected from supermarkets and this may reflect the continued phenomenal growth of the organic market that has occurred since 1998/99 (annual market growth of 100% during the last two years) 5, 17 Overall, 80% of fresh fruit and vegetables sold in the UK are imported 3. A lower proportion (70%) of imported vegetables was examined in this study. However, vegetables were collected during the months of May and June and this may reflect market supply due to the issue of seasonality. Presentation of organic vegetables sold by supermarkets is generally in a pre-packed format. This is partly to do with the need to retain the integrity of the organic vegetables as well as to provide information to consumers via labelling 3. This is reflected by the findings in this study where most (81%) of the organic vegetables sampled were pre-packed.

Between 1992 and 1999 foodborne outbreaks made up over a third (35%; 1408/4083) of general outbreaks reported from England and Wales, and of these foodborne outbreaks, ready-to-eat fruit and vegetables accounted for a very small proportion (4.3%; 60 affecting 2170 people)11. This is the first such study to provide information on the microbiological quality on uncooked ready-to-eat organic vegetables. This study was not a comparative study and therefore did not aim to produce conclusive evidence that organically produced vegetables are more or less microbiologically safe than those produced conventionally. Such an investigation would also require a detailed microbiological risk assessment to be undertaken. However, all food sold, whether organically or conventionally produced must by law satisfy food safety requirements 20. The information and experience gained from this study could help to determine the requirements for further studies into this product area. In addition, information from the study can be used to help formulate microbiological guidelines.

Acknowledgments

The authors would like to thank all the staff in the Environmental Health Departments throughout the UK who collected samples for this study, and all the staff in both PHLS and non-PHLS laboratories who performed microbiological examination. Thanks are extended to FSML (CPHL) for typing isolates, to David Lock at LACOTS for coordinating the participation of Environmental Health Officers (EHOs), to Francis Blake from the Soil Association for advice on the sampling protocol, and to Lillian Hucklesby for entering the data.

References

1. British Standards Institution (BSI). BS EN ISO 11290-2 1998. Microbiology of food and animal feeding stuffs-Horizontal method for the detection and enumeration of Listeria monocytogenes. Part 2: Enumeration method, 1998. London: BSI.

2. Council Regulation 2092/91/EEC of 22 July 1991 on organic production of agricultural products and indications referring thereto on agricultural products and foodstuffs. Official Journal of the European Communities 1991; L198/1-15.

3. Durbury R: Fruit and Vegetables. In Handbook of Organic Food Processing and Production, (Eds. Wright S, and McCrea D). London: Blackie Academic Press, 2000, pp 78-91.

4. Food Standards Agency (FSA). Position Paper: Food Standards Agency view on organic foods, 23 August 2000. http://www.foodstandards.gov.uk/pdf_files/organicview.pdf 

5. House of Commons, Agriculture Committee Second Report: Organic Fanning, I. 20 January 2001. London: The Stationary Office.

6. House of Lords Select Committee on The European Communities Sixteenth Report. Organic Farming and the European Union, 20`h July 1999: London: The Stationary Office.

7. Institute of Food Science and Technology (IFST). Organic Food. International Food Safety News 1999; 8 (1): 2-6.

8. Ministry of Agriculture, Fisheries and Food (MAFF). A study on Farm Manure Applications to Agricultural Land and an Assessment of the Risks of Pathogen Transfer into the Food Chain, 2000. London: MAFF.

9. Ministry of Agriculture, Fisheries and Food. Organic Foods. Food Safety Information Bulletin 1998; 101 pp 8587.

10. Food Safety Act 1990, Code of Practice No 7: - Sampling for Analysis and Examination. London: FSA, 2000.

11. O' Brien S, Mitchell RT, Gillespie I and Adak GK (PHLS CDSC) The Microbiological Status of Ready-To- Eat Fruit and Vegetables 2000. Discussion Paper ACM/476 of the Advisory Committee on the Microbiological Safety of Food (ACMSF). http://www.foodstandards.gov.uk/pdf_files/papers/acm476.pdf 

12. Public Health Laboratory Service (PHLS). Guidelines for the Microbiological Quality of Some Ready-To-Eat foods sampled at the Point of Sale. Communicable Disease Public Health 2000; 3: 163-137.

13. Public Health Laboratory Service (PHLS). Standard Methods for Food Products. Direct Enumeration of Escherichia coli. Standard Method: F20, 1998. London: PHLS.

14. Public Health Laboratory Service (PHLS). Standard Methods for Food Products. Detection of Campylobacter spp. Standard Method: F21, 1998. London: PHLS.

15. Public Health Laboratory Service (PHLS). Standard Methods for Food Products. Detection of Salmonella spp. Standard Method: 1713, 1998. London: PHLS.

16. Public Health Laboratory Service (PHLS). Standard Methods for Food Products. Detection of Escherichia coli 0157 by Immunomagnetic Bead Separation. Standard Method: 1717, 1998. London: PHLS.

17. Soil Association (SA) Memorandum Submitted by the Soil Association (1762) In House of Commons Second Report, Organic Farming, II. 2e January 2001. London: The Stationery Office.

18. Soil Association. Briefing sheet - Food Safety and Organic Products ` Dispelling the Myths' 2000. Soil Association, Bristol. www.soilassociation.org.uk .

19. Soil Association. The Organic Food and Farming Report 1999. Soil Association: Bristol.

20. The Food Safety Act 1990 (Chapter 16) London: The Stationery Office.

21. The Organic Products Regulations 1992, Sl No. 2111. HMSO: London.

Annex 1: Participating PHLS Groups, Laboratories and Local Authority Food Liaison Groups and number of samples

Table la. Participating PHLS Groups, Public Health Laboratories and number of samples

PHLS group

Public Health Laboratory

Number of samples*

 

Chelmsford

152

 

Luton

151

 

Norwich

148

London & Southeast

Ashford

126

 

Brighton

216

 

London FWE Unit'

343

 

Reading

108

 

WEMS2

126

Midlands

Birmingham

81

 

Coventry

123

 

Shewsbury

100

 

Stoke

64

Northwest

Chester

181

 

Preston

146

North

Hull

62

 

Leeds

59

 

Middlesborough

67

 

Newcastle

89

South West

Bristol

147

 

Exeter

128

 

Gloucester

74

 

Hereford

49

 

Plymouth

59

 

Truro

65

Trent

Leicester

128

 

Lincoln

159

 

Sheffield

40

Wales

Cardiff

60

 

Carmarthen

51

 

Rhyl

30

Total

3332

1, London Food, Water & Environmental Unfit, CPHL
2, Wessex Environmental Microbiological Services

Table 1b. Participating Non-PHLS Laboratories and number of samples

Non-Public Health Laboratory

Number of samples*

Aberdeen City Council

13

Belfast City Hospital

81

Dumfries Galloway

2

Dundee City Council

9

Fife Area Laboratory, Kirkcaldy

15

Glasgow Scientific Services

31

Kettering Laboratory Services

4

Kings Lynn & West Norfolk 

8

Northumberland General Hospital

1

Public Analyst Aberdeen

1

Royal Alexandra, Paisley

2

Worcester Royal Infirmary

32

Worcestershire Scientific

21

Total

220

* Includes the 352 samples (not ready-to-eat organic vegetables) not included in the analysis.

Table lc. Local Authority Food Liaison Groups and number of sample

Local Authority Food Liaison Group

Number of samples*

Berkshire Food Coordinating Group

64

Cambridge Food Liaison Group

41

Cheshire Food Liaison Group

101

Cornwall CEHOS Food Sub-Group

65

Cumbria IEHO Food Safety Group

5

Derbyshire Food Liaison Group

20

Devon Food Safety Group

118

Dorset Food Group

35

Durham Food Liaison Group

17

East Sussex Food Liaison Group

86

Essex Food Group

103

Gloucester Food Safety Group

74

Greater Manchester Food Liaison Group

73

Hampshire & Isle Of Wight Food Advisory Group

84

Hereford & Worcester CEHOS Food Working Group

105

Herts & Beds IEHO And Chief Officers Food Group

84

Humberside Food Liaison Group

53

IEHO Buckinghamshire Branch Food Group

57

Kent Food Technical Group

126

Lancashire Assn Of CEHOS, Food Officer Group

63

Leicestershire Food Liaison Group

127

LFCG1 North East Sector

91

LFCG South East Sector

71

LFCG South West Sector

67

LFCG North West Sector

114

Lincolnshire Coordinating Group

89

Merseyside Food Sub-Group

62

North Yorkshire CEHOS Group

91

Northamptonshire

77

Northern Ireland Food Group

80

Northumberland Food Safety Group

21

Norfolk Food Liaison Group

120

Nottingham District Food Group

69

Oxfordshire CC Food Sub-Group

27

Scottish Food Coordinating Committee

72

Shropshire Food Liaison Group

43

Somerset Food Liaison Group

69

South Yorkshire Food Forum

20

Staffordshire Food Safety Group

71

Suffolk Food Liaison Group

38

Surrey Food Liaison Group

63

Tees Valley Food Safety Group

31

Tyne & Wear Food Control Group

58

Wales North Group

48

Wales South East Group

46

Wales South West Group

76

Warwickshire Food Liaison Group

46

West Midlands Food Liaison Group (inc. Black Country)

129

West of England Food Liaison Group

82

West Sussex Food Liaison Group

78

West Yorkshire Principal Food Officers Group 

27

Wiltshire Food Group

70

Not stated

5

Total

3552

1, London Food Coordinating Group
* Includes the 352 samples (not ready-to-eat organic vegetables) not included in the analysis.

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