U. S. Department of Health and Human Services
U. S. Food and Drug Administration
Center for Food Safety and Applied Nutrition
Office of Plant and Dairy Foods and Beverages
January 2003

EXECUTIVE SUMMARY

In March of 2000, the Food and Drug Administration (FDA) initiated a 1000 sample survey focused on high volume domestic fresh produce (the Domestic Produce 1000 Sample Survey). Cantaloupe, celery, cilantro, loose-leaf lettuce, parsley, scallions (green onions), strawberries and tomatoes were collected and analyzed for Salmonella, and E. coli O157:H7. In addition, cantaloupe, celery, parsley, scallions, and tomatoes were also analyzed for Shigella. This survey was the domestic complement to the FY 1999 Imported Produce Survey (http://www.cfsan.fda.gov/~dms/prodsur6.html).¹

Of 1028 domestic samples that were collected and analyzed, 99% were not contaminated with Shigella, Salmonella, and/or E. coli O157:H7. Eleven samples (1% of the total number sampled) were contaminated with either Shigella or Salmonella while 0% of the produce items were contaminated with E. coli O157:H7. Of the 11 contaminated samples, six (55%) were contaminated with Salmonella and 5 (45%) were contaminated with Shigella.

For regulatory follow-up, domestic samples that were found to be violative were reported to the collecting district and the Center for Food Safety and Applied Nutrition's (CFSAN) Case Processing Contact. Violative domestic produce could either be reconditioned or destroyed. Firms with violative produce were encouraged to conduct voluntary recalls. Follow-up investigations were conducted at three violative farms to determine potential sources of contamination.

BACKGROUND

Although the incidence of foodborne illnesses linked to fresh produce is low, over the last several years the proportion of foodborne illnesses associated with domestic and imported fresh fruits and vegetables has increased. In January of 1997, President Clinton announced a Food Safety Initiative designed to improve the safety of the nation's food supply. The Department of Health and Human Services (DHHS), the Department of Agriculture (USDA), and the Environmental Protection Agency (EPA) sent a report to the President, in May of 1997, that identified fresh produce as an area of concern. In October of 1997, President Clinton announced a plan entitled Produce & Imported Foods Safety Initiative to provide further assurance that fruits and vegetables consumed by the American public meet the highest health and safety standards.

The challenges in this area are self-evident. Most fresh fruits and vegetables are grown in non-sterile environments. Growers have less control over conditions in the field compared to an enclosed production facility. The surfaces of produce have natural microflora composed of microorganisms that are generally not significant to human health. However, low-level contamination of produce with pathogenic microorganisms may sporadically occur. Harvesting, washing, cutting, slicing, packaging and transporting offer opportunities for produce contamination. Most fresh produce is likely to be consumed raw without undergoing processes, such as cooking, that inactivate harmful microorganisms.

In October of 1998, the Food and Drug Administration (FDA) released a guidance document entitled "Guidance for Industry - Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables." This document outlines good agricultural and good manufacturing practices (GAPs and GMPs) to reduce the risk of microbial contamination of fresh produce. This voluntary guidance does not impose unnecessary or unequal restrictions or barriers on either domestic or foreign products. Areas covered by the guide include water quality, manure management, worker training, field and facility sanitation, and transportation. Guidelines are set to control potential sources of contamination throughout the production process, from the farm to point-of-sale. In the absence of use of GAPs and GMPs, the risk of microbial contamination increases along with the likely extent of the contamination. Implementing GAPs and GMPs increases the assurance that microbial safety hazards will be minimized.

To assist in the development of policy for the Produce & Imported Foods Safety Initiative, the Center for Food Safety and Applied Nutrition (CFSAN) needed data on the incidence and extent of pathogen contamination on selected produce. In FY 99, the FDA issued a field assignment designed to collect 1000 samples of high-volume imported produce items (FY 99 Imported Produce Survey). The report for that assignment can be found at http://www.cfsan.fda.gov/~dms/prodsur6.html. Due to elevated levels of pathogens (Salmonella and Shigella) found on cilantro, culantro, and cantaloupe samples collected during the FY 99 assignment, the FDA issued a follow-up assignment, the FY 01 300-Sample Follow-up Survey of Imported Produce. That assignment focused on cantaloupe, cilantro, culantro, and tomatoes. Results of that assignment can be found in Table 3 of this report.

As a complement to the FY 99 Imported Produce Survey, the FDA issued a domestic produce survey in May of 2000. The study again focused on high-volume produce that is generally consumed raw. The eight commodities that were selected for the domestic survey were cantaloupe, celery, cilantro, loose-leaf lettuce, parsley, scallions, strawberries, and tomatoes. Target collection areas were established so that each commodity was to be collected from districts where a significant portion of the crop is usually grown.

The objectives of the domestic produce survey were to:

• collect and analyze samples of domestic fresh produce to determine the incidence of microbial contamination on these commodities;
• undertake appropriate regulatory follow-up if violative samples were found, to protect U.S. consumers and encourage firms to implement practices to minimize microbial contamination on fresh produce; and
• obtain data to focus future research, risk assessment, industry training and food safety policy for the purpose of reducing foodborne illnesses resulting from contaminated fresh produce.

Our purpose was not to attempt to detect every incidence of low-level, sporadic contamination but to detect those levels of contamination that might result from a failure to follow adequate GAPs and GMPs as specified by FDA guidance.

PROCEDURES FOR COLLECTION AND ANALYSIS

Criteria for Selection of Commodities in Survey

The commodities that were collected and analyzed for the domestic produce survey were similar to those collected and analyzed during the imported produce survey, with some exceptions. For an explanation of the criteria used for selection of commodities sampled for the imported produce survey, see the FY 99 FDA Survey of Imported Produce at http://www.cfsan.fda.gov/~dms/prodsur6.html.

Sample Collection

Only produce grown in the United States was collected for analysis. Collection was carried out according to the schedule compiled by the FDA specifying the type of produce each district was to collect and where that produce should have been harvested.

Samples were collected aseptically, primarily from packinghouses, but were also collected from repackers and wholesalers, if the grower was identifiable. Samples were shipped under refrigeration to the servicing laboratory designated for the district that collected the sample. Samples were not frozen at any time prior to microbial analysis. Each sample consisted of ten (10) sub-samples. For cilantro, loose-leaf lettuce, parsley, and scallions, enough product was collected for each sub-sample to equal 454 grams (16 oz.). For cantaloupe and celery, each sub-sample consisted of one head/bunch of produce, or, two heads/bunches if necessary to reach the minimum sub-sample weight of 454 g. For bulk shipments of strawberries and tomatoes, each sub-sample consisted of 454 g of product. If the product was shipped in retail-sized containers, enough containers were collected to equal 454 g per sub-sample.

Microbial Analysis

Produce was prepared in a manner that closely simulated minimal consumer preparations (e.g., visible dirt removed, stems and roots trimmed, outer leaves removed), but did not include a thorough wash step. Individual sub-samples were used to prepare a "sub-sample rinse" which required the sample to be weighed and added to an appropriate amount of buffer solution to obtain a 1:1 ratio. The sample was agitated at 100 rpm for five (5) minutes to release and distribute the bacteria from the surface of the produce into the buffer solution.

For testing Salmonella or Shigella, the sub-sample rinses were composited, i.e., 10 sub-sample rinses were combined into two composites of five sub-sample rinses each. For E. coli O157:H7, however, each sub-sample was analyzed separately.

REGULATORY FOLLOW-UP FOR VIOLATIVE SAMPLES

Regulatory follow-up for this assignment was consistent with that of other FDA programs and/or assignments. If any of the microorganisms (Salmonella, Shigella, E. coli O157:H7) were detected and confirmed, the collecting district and the CFSAN Case Processing Contact were notified immediately. If the firm had held product pending the results of the test, the district encouraged the firm to either recondition the product to destroy the pathogen, or, to destroy the product if reconditioning was not feasible. If the firm had distributed the product, the collecting district encouraged the firm to conduct a voluntary recall. In cases where the lot was still available, the district office pursued seizure as appropriate provided that interstate commerce was documented. In situations where no interstate commerce was documented, the appropriate state officials were notified.

RESULTS

Primarily due to extreme weather conditions (drought), the original collection schedule was modified. The scheduled completion date of May 31, 2001 was extended and the assignment was completed on January 8, 2002. A total of 1028 samples were collected, with between 85 and 198 samples collected for each produce item.

Data Analysis

Fourteen (14) FDA district offices collected produce samples: Atlanta, Baltimore, Dallas, Denver, Detroit, Florida, Kansas City, Los Angeles, New Jersey, New Orleans, New York, San Francisco, Seattle, and Southwest Imports. The samples represented produce grown in the following 18 states: Alabama, Arizona, California, Colorado, Florida, Georgia, Iowa, Louisiana, Maryland, Michigan, New Jersey, North Carolina, New York, Ohio, Oklahoma, South Carolina, Texas, Virginia.

Incidence by Produce Item

Of the 1028 samples, 1017 (98.9%) tested negative for pathogen contamination while 11 (1.1%) of the samples were positive for pathogen contamination (Salmonella or Shigella). E. coli O157:H7 was not found on any of the produce samples. Table 1 shows the number of samples collected and analyzed and the number of confirmed positives for each produce item.

One or more samples of cantaloupe, cilantro, lettuce, parsley, and scallions were positive for pathogen contamination. Cantaloupes had the highest number of positive samples (5), followed by scallions (3), cilantro, lettuce and parsley (1 each).

When adjusted to account for the number of samples collected of each commodity, scallions had the highest rate of contamination (3.2%) of the total 93 samples collected. Cantaloupe also had a high rate of contamination (3.0%), with 164 samples collected and 5 positive samples. One of 85 cilantro samples was positive for pathogen contamination, giving a violation rate of 1.2%. One of 90 parsley samples (1.1%) was found to be contaminated as well as one of 142 (0.7%) lettuce samples.

Incidence by Pathogen

Table 2 shows the incidence of the pathogens on produce samples confirmed positive for contamination. No samples were positive for E. coli O157:H7. Of the 11 confirmed positive domestic produce samples, 6 were positive for Salmonella while the other 5 samples were positive for Shigella.

The incidence of Salmonella on the total number of produce items sampled was 0.6% (6/1028) and the incidence of Shigella was 0.5%.

Similarities And Differences Between Findings Of The Domestic Produce And Imported Produce Surveys

The imported and domestic produce surveys were designed to provide data to CFSAN on the incidence and extent of pathogen contamination on selected domestic and imported produce. This information is needed in order to develop policy and guidance for the Produce & Imported Foods Safety Initiative and to focus education/outreach efforts. The intent was not to draw quantitative comparisons between the incidence of contamination of domestic and imported produce. A larger sample size is needed in order to make these comparisons. However, the surveys were designed to allow the agency to make some qualitative comparisons in order to better understand the potential risks associated with select produce items.

During the follow-up imported produce survey, 257 samples were collected with one cilantro sample positive for Salmonella and one tomato sample positive for Salmonella. However, for these purposes, only the 1000 sample imported produce survey will be used for comparisons with the 1000 sample domestic produce survey. Both imported and domestic cantaloupe was found to have a high rate of contamination in the 1000 sample surveys. Overall, 7.3% of imported cantaloupe and 3.0% of all domestic cantaloupe sampled were contaminated with either Salmonella or Shigella. The microorganism of primary concern, Salmonella, was found on 73% of imported violative cantaloupes and on 80% of violative domestic cantaloupes.

Of the imported produce samples collected during the 1000 sample survey, in addition to cantaloupe, cilantro (9.0%), celery (3.6%), and parsley (2.4%) were violative. Domestically, in addition to cantaloupe, scallions (3.2%), cilantro (1.2%), and parsley (1.1%) were found to be violative.

Although the number of domestic tomatoes sampled was large (198), no pathogen contamination was detected on any sample. Imported tomatoes showed no signs of pathogen contamination in the initial imported produce survey. However, in the follow-up imported produce survey, there was one positive out of 169 tomato samples. Imported strawberries had less than a 1% rate of contamination and no domestic strawberry samples were violative.

REGULATORY FOLLOW-UP

Regulatory follow-up for this assignment was consistent with that of other FDA programs and/or assignments. For all 11 violative samples that were found, the FDA determined whether any portion of the lot from which the contaminated sample came was still in commerce. In all cases, since the product was a fresh produce item with a short shelf-life, the entire lot had been sold and consumed or discarded. Therefore, the product was not available for voluntary recall by the violative firms.

The presence of violative samples led state officials to initiate farm investigations and the FDA to perform three follow-up farm investigations. The state investigators and the FDA officials found no specific problem areas on the farms that could be identified as the source of the contamination. However, this is not unusual as environmental and other production factors may change between the time contamination occurs and when investigators reach a farm. The investigations allowed officials to examine farm facilities and observe standard practices to help identify sources of contamination and possible appropriate corrective actions. Implementing GAPs and GMPs increases the assurance that microbial safety hazards will be minimized. A farm that does not follow GAPs and GMPs increases the risk for contaminating produce with microorganisms of concern such as Salmonella, Shigella, or E. coli O157:H7.

¹ The FDA issued a follow-up assignment to the FY99 Imported Produce Survey, the FY01 300 Sample Follow-up Survey of Imported Produce. Although this report is mainly focused on the results of the Domestic Produce Survey, data from the follow-up assignment are reported in this document.

Guidance for Industry -- Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables

Domestic Produce Sampling Assignment - DOEP #00-16 May 2000