Produce, Food Safety, and International Trade

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Summary O utbreaks of foodborne illness in the United States associated with imports of fresh produce affect not only consumers and the growers of the contaminated product, but also frequently other suppliers to the U.S. market, including U.S. producers. Because most produce is highly perishable, the United States depends on seasonal imports for a year-round supply of some items. Often by the time someone falls ill from an imported product and an investigation identifies both the product and its origin, that country may no longer be exporting the product to the United States. For example, a foreign grower may just supply the United States for a brief market window before the U.S. season begins. Of course, many foreign suppliers have much longer sea- sons. The negative publicity about an outbreak will often affect whichever suppliers are selling their product at that time—often U.S. producers—whether they had any- thing to do with the outbreak or not. The impact of a foodborne illness outbreak on trade depends on whether foreign producers can quickly correct the contamination problem and convince buy- ers that their product no longer poses a risk. This chapter reviews outbreaks of foodborne illnesses asso- ciated with Guatemalan raspberries, Mexican straw- berries (contaminated either in Mexico or the United States), and Mexican cantaloupe. In the Mexican strawberry case, after just one outbreak and an initial collapse of trade, strawberry trade rebounded in the following years. In the Guatemalan raspberry and Mexican cantaloupe cases, the U.S. Food and Drug Administration (FDA) refused to accept these products into the United States after outbreaks in consecutive years. The Guatemalan raspberry industry has never really recovered from the experience although it is now free to ship to the United States under a rigorous food safety program. The impact of the ongoing can- taloupe problem on future trade is still unknown. FDA, the Centers for Disease Control and Prevention, the produce industry, retailers, and foreign govern- ments have worked together to keep unsafe produce off the market and resolve food safety problems. The FDA's voluntary guidelines for good agricultural prac- tices (GAPs) provide recommendations to growers, both domestic and foreign, on how to reduce microbial hazards. FDA emphasizes that GAPs only reduce the risk of microbial contamination and cannot eliminate the risk. If invited by a foreign government, FDA will often visit an area associated with an outbreak to try to identify practices that are inconsistent with GAP guidelines. FDA also provides training in foreign countries on GAPs. Many individual growers have responded to increased concern about foodborne illnesses (and attendant financial losses) by improving their food safety sys- tems. Grower organizations have been instrumental in developing better food safety and traceback systems to protect the reputation of their particular crops. While individual farmers might not want a contamination problem traced to their operation, the industry as a whole is more concerned with accountability. Retailers, who face unwanted publicity in a foodborne illness outbreak, have also taken the initiative by demanding more stringent food safety programs from their suppliers. Some demand that their produce sup- pliers have third-party audits to verify that they are complying with GAP guidelines. 74 International Trade and Food Safety / AER-828 Economic Research Service/USDA Chapter 5 Produce, Food Safety, and International Trade Response to U.S. Foodborne Illness Outbreaks Associated with Imported Produce Linda Calvin 1 1 Agricultural economist with the Market and Trade Economics Division, Economic Research Service.

Transcript of Produce, Food Safety, and International Trade

Summary

Outbreaks of foodborne illness in the UnitedStates associated with imports of fresh produceaffect not only consumers and the growers of the

contaminated product, but also frequently other suppliersto the U.S. market, including U.S. producers. Becausemost produce is highly perishable, the United Statesdepends on seasonal imports for a year-round supply ofsome items. Often by the time someone falls ill from animported product and an investigation identifies both theproduct and its origin, that country may no longer beexporting the product to the United States. For example,a foreign grower may just supply the United States for abrief market window before the U.S. season begins. Ofcourse, many foreign suppliers have much longer sea-sons. The negative publicity about an outbreak will oftenaffect whichever suppliers are selling their product atthat time—often U.S. producers—whether they had any-thing to do with the outbreak or not.

The impact of a foodborne illness outbreak on tradedepends on whether foreign producers can quicklycorrect the contamination problem and convince buy-ers that their product no longer poses a risk. Thischapter reviews outbreaks of foodborne illnesses asso-ciated with Guatemalan raspberries, Mexican straw-berries (contaminated either in Mexico or the UnitedStates), and Mexican cantaloupe. In the Mexicanstrawberry case, after just one outbreak and an initialcollapse of trade, strawberry trade rebounded in thefollowing years. In the Guatemalan raspberry andMexican cantaloupe cases, the U.S. Food and DrugAdministration (FDA) refused to accept these productsinto the United States after outbreaks in consecutive

years. The Guatemalan raspberry industry has neverreally recovered from the experience although it isnow free to ship to the United States under a rigorousfood safety program. The impact of the ongoing can-taloupe problem on future trade is still unknown.

FDA, the Centers for Disease Control and Prevention,the produce industry, retailers, and foreign govern-ments have worked together to keep unsafe produceoff the market and resolve food safety problems. TheFDA's voluntary guidelines for good agricultural prac-tices (GAPs) provide recommendations to growers,both domestic and foreign, on how to reduce microbialhazards. FDA emphasizes that GAPs only reduce therisk of microbial contamination and cannot eliminatethe risk. If invited by a foreign government, FDA willoften visit an area associated with an outbreak to try toidentify practices that are inconsistent with GAPguidelines. FDA also provides training in foreigncountries on GAPs.

Many individual growers have responded to increasedconcern about foodborne illnesses (and attendantfinancial losses) by improving their food safety sys-tems. Grower organizations have been instrumental indeveloping better food safety and traceback systems toprotect the reputation of their particular crops. Whileindividual farmers might not want a contaminationproblem traced to their operation, the industry as awhole is more concerned with accountability.Retailers, who face unwanted publicity in a foodborneillness outbreak, have also taken the initiative bydemanding more stringent food safety programs fromtheir suppliers. Some demand that their produce sup-pliers have third-party audits to verify that they arecomplying with GAP guidelines.

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Chapter 5

Produce, Food Safety, and International Trade

Response to U.S. Foodborne Illness OutbreaksAssociated with Imported Produce

Linda Calvin1

1 Agricultural economist with the Market and Trade EconomicsDivision, Economic Research Service.

Introduction

The U.S. food supply is one of the safest in the world(Crutchfield and Roberts, 2000). In the mid-1990s,however, outbreaks of foodborne illnesses linked tomicrobial contamination of both domestic and importedproduce focused attention on the potential for contami-nation at the grower and shipper level (Tauxe, 1997).2

For example, in 1996 the potentially dangerous bac-terium Escherichia coli O157:H7 was linked toCalifornia lettuce associated with farm-level contamina-tion. In the same year, a very large foodborne illnessoutbreak was linked to imported Guatemalan raspber-ries contaminated at the farm level with the parasiteCyclospora. The economic impacts of outbreaks made itclear to the produce industry, particularly those sectorsassociated with contaminated produce, that improvedfood safety programs were necessary. The U.S. govern-ment also became more involved in produce food safetyat the farm and shipper level.

In the United States, responsibility for food safety ofimported foods resides with USDA’s Food Safety andInspection Service (FSIS) and the U.S. Food andDrug Administration (FDA). FSIS deals with meat,poultry, and some egg products, and FDA covers allother food products, including produce. Both agenciesrequire imported foods to meet domestic food stan-dards. FSIS allows only imports from countries withfood safety systems it deems to be equivalent to thosein the United States, thus putting the burden for safetyon the exporting country. Unlike FSIS, FDA does nothave legal authority to require that imports of theproducts it covers be produced with food systemsequivalent to those in the United States.

Food safety concerns can focus on pesticide residues,microbial and chemical contamination, and the effectsof biotechnology. FDA randomly tests both importedand domestic produce for pesticide residues. FDAalso randomly tests chemical residues, although thistesting is much more limited in scope. Concern aboutmicrobial contamination is relatively new.Biotechnology, an important determinant of tradeflows for other agricultural products, is not yet a cen-tral concern for fruit and vegetables. Traditionally,

FDA has relied on inspections at the port of entry toensure safety of the products. While this worked wellfor food safety issues such as detecting pesticideresidues exceeding U.S. tolerance levels, testing formicrobial contamination is a completely differentchallenge. The FDA tolerance for microbial pathogensis zero, so it would deny entry to any produce withcontamination that could be detected, but testing formicrobial contamination is not very successful.Microbial contamination is often low level and spo-radic so it can be difficult to detect. Also, if perishableproduce is held at the border while microbial tests arecompleted, it may deteriorate in quality to the pointwhere it cannot be sold. In comparison, if produce haspesticide residues that exceed the legal tolerance, it islikely to be pervasive and contamination would showup in random testing. FDA does targeted sampling formicrobial contamination when there are concernsabout a specific product.

In 1997, President Clinton announced the Produce andImported Food Safety Initiative, which called for addi-tional resources to improve domestic standards and toensure that imports were equally safe (Crutchfield,1999). Three broad areas of action were identified.First, the President directed FDA to seek new legalauthority to require equivalence in food safety systemsin foreign countries (but there has been no change inlegislation). Second, the initiative targeted moreresources at improving inspection activities abroad byproviding technical assistance. This has been an impor-tant means of improving food safety abroad. Third, theinitiative focused on providing guidance to bothdomestic and foreign producers on good agriculturalpractices (GAPs).

In 1998, FDA published voluntary guidelines forboth domestic and foreign producers on GAPs forreducing microbial contamination (FDA, 1998).Although voluntary, GAPs are now an important partof the produce industry. FDA does not have manda-tory food safety requirements with respect to micro-bial contamination for the fresh produce industry.This situation provides incentives to the produceindustry to voluntarily adopt GAPs and ensure thatfood safety does not become a bigger issue. FDAand the produce industry have developed a goodworking relationship and have made importantimprovements in food safety. FDA could imposemandatory food safety standards for fresh produce ifdeemed appropriate. For example, in the late 1990s,there were three foodborne illness outbreaks associ-

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2 Shippers are the first marketers in the produce distribution chainand are often involved with harvesting and packing produce, astage at which contamination may occur. Many shippers are verti-cally integrated grower-shippers.

ated with fruit juice—one E. coli O157:H7 outbreakassociated with apple juice and two Salmonella out-breaks associated with orange juice. Two peopledied. In 2001, FDA published a final rule requiringjuice processors to use hazard analysis and criticalcontrol point (HACCP) principles (FDA, 2001b).FDA also requires HACCP for seafood processors.These mandatory requirements also apply toimported products.

FDA promotes adoption of GAPs as a means to min-imize microbial contamination, instead of relying onrelatively ineffective testing at the border to detectproblem produce. According to FDA, even withGAPs it is not possible to eliminate microbial con-tamination for produce although it is possible toreduce the risk. For fresh and fresh-cut produce,there is no effective microbial elimination step suchas pasteurization for milk.

GAPs provide growers with a structure to evaluate dif-ferent practices and their potential to reduce microbialfood safety hazards so they can develop a food safetyprogram tailored to their own operations (see box 5.1).Many grower practices—such as water sampling orworker hygiene programs—could reduce the risk ofmicrobial contamination. Each grower must evaluate thebenefits and costs of investing in risk-reducing prac-tices. This assessment will vary by crop, environmentalconditions, and individual grower situation.

It is not always clear how much additional invest-ment in food safety practices is enough. A foodborneillness outbreak may occur if a farmer cuts cornersand fails to adopt a practice considered standard inthe local industry. Other outbreaks may representcases where growers and scientists misjudge what is required to prevent problems and growers underinvest in food safety practices. The science andtools available to growers to reduce the risk of con-tamination are still evolving. Of course, with uncer-tainty, growers may also overinvest in food safetyprecautions. There is always the concern that a prac-tice may be a technical but not an economic success.Some segments of the produce industry are undoubt-edly more advanced than others in their efforts toreduce these risks, but there is no systematic surveyof growers to identify their progress.

This chapter examines one aspect of the food safetyissue, the private and public responses to U.S. food-borne illness outbreaks due to microbial contamination

associated with imported produce.3 Even when thecontaminated product is imported, the U.S. industry isoften affected and both domestic and foreign growersneed to take action to protect their economic wellbeing. The chapter begins with information on micro-bial contamination of produce and the role of produceimports in U.S. consumption. Three examples of food-borne disease outbreaks follow which demonstratehow growers, grower organizations, governments inthe United States and abroad, and retailers respondedto contamination problems. The analysis also includesa brief look at the impact of contaminated imports ontrade. The three examples are: (1) imports ofGuatemalan raspberries associated with Cyclospora,(2) imports of Mexican strawberries associated withhepatitis A (contaminated either in Mexico or theUnited States), and (3) imports of cantaloupe fromMexico associated with Salmonella.4 In each case, thecontamination occurred, or may have occurred, at thegrower or shipper level. Then the analysis turns to acomparison of the private and public responses to foodsafety problems demonstrated by the three case studies.Concluding comments focus on lessons learned andareas for future research.

Foodborne Illness Outbreaks

Despite heightened concern about food safety, the vastmajority of growers for the U.S. market, both domesticand foreign, has never been involved in food safety

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3 This study does not examine pesticide residue contamination. Astudy of U.S. winter vegetable imports from Mexico showed thatpesticide residue violations were relatively infrequent (Calvin andBarrios, 1998). In 1997, FDA tested 3 percent of total shipmentsthrough Nogales, Arizona, and only about 3 percent of the testedproducts were in violation of pesticide residue standards. Of thewinter vegetables—tomatoes, bell peppers, cucumbers, eggplant,summer-type squash, and snap beans—only snap beans had anyviolations. Of course, the winter vegetable industry in Mexico iswell established. When Guatemala began exporting snow peas, anontraditional export, in the late 1980s, it had a serious problemwith pesticide residues that took several years to control. A pro-gram to pretest shipments in Guatemala to ensure they would passFDA inspections finally resolved the problem. 4 Cyclospora is a protozoan parasite that causes cyclosporiasis, apotentially debilitating diarrhea that can last for three weeks ormore. The disease is treatable and is only considered potentiallylife threatening to those with compromised immune systems. Thehepatitis A virus causes liver disease. The bacterium Salmonellacauses salmonellosis, which is characterized by diarrhea, fever, andabdominal cramps. Most people recover without treatment but itcan cause death in some cases when the infection spreads beyondthe intestines.

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There are many sources of potential microbial contam-ination for produce and some regions will face morechallenges than others. Some of the major sources atthe grower and shipper level include: soil, water, greenor inadequately composted manure, dust in the air,wild and domestic animals, human handling, and con-taminated equipment (FDA, 2001e). Sources of watercontamination include water used for irrigating, mixingwith pesticides, washing and rinsing produce, andmaking ice to cool produce. Different food safety prac-tices can mitigate the chances of contamination. Otherfactors unique to specific plants also affect the proba-bility of contamination.

Good agricultural practices (GAP) principles pro-vide growers with guidelines to reduce the potentialfor microbial contamination of their products.Guidelines cover growing, harvesting, sorting, pack-ing, and storage operations. National-level guide-lines on GAPs enhance the consistency andscientific basis of food safety programs developedby public and private institutions. Using GAPsreduces but does not eliminate all risk—an unob-tainable goal with current technologies.

Growers and shippers are directed to evaluate theiroperations in terms of water quality; manure/munici-pal biosolids; worker hygiene; field, facility, andtransport sanitation; and traceback capabilities.Traceback is the ability to track food from the con-sumer point of purchase back to the grower.Recommended practices are provided to mediate eachrisk. Since there are numerous potential ways toreduce risk, FDA encourages growers to pick themost cost-effective combination of practices.Therefore, two growers in different areas with differ-ent environmental conditions could both adhere toGAP principles but use different methods to do so.

GAP guidelines do not outline specific testing andmonitoring regimes because scientific data is lackingfor establishing more specific guidelines (FDA,2001e). The GAP guidelines state “Water qualityshould be adequate for its intended use. Where water

quality is unknown or cannot be controlled, growersshould use other good agricultural practices to mini-mize the risk of contamination.” The guidelines donot specify how to measure whether water quality isadequate; no one knows for sure and what is adequatevaries by crop. For example, irrigation water for acrop that matures on the ground may need to becleaner than water for an orchard crop.

Use of the GAP guidelines can be broken down intothree stages. First, growers and shippers can use GAPsto evaluate their food safety system and assess needs.Some large firms with food safety staff may evaluatetheir own systems. Some smaller growers might hire athird-party audit firm to do an evaluation. FDA doesnot regulate third-party audit firms. In 2001, a FDAreport estimated the cost of an evaluation at $300-$500per farm (FDA, 2001e). An evaluation would include areview of the current food safety system and an assess-ment of what additional practices might be needed toreduce the chance of contamination, including the doc-umentation necessary to assure continuous compliancewith GAPs.

Once growers have a food safety system evaluation andneeds assessment, they may decide to adopt new prac-tices to reduce risks. The cost of implementationdepends on the particular crop, the existing food safetysystem, and the environment in which the growersoperate (e.g., some areas may have more water contam-ination problems to contend with than others). Sometypical practices that a farmer might adopt couldinclude: water testing; water treatment programs; devel-opment of a documentation system to corroborate prac-tices and trace product; and provision of additionalhygiene facilities for workers.

Growers may opt to have their food safety programaudited periodically by third-party audit firms. Someretailers now require third-party audits to verify thatgrowers and shippers are in compliance with GAPs.In 2001, FDA estimated the typical cost of an audit tobe similar to the cost of an evaluation, about $300-$500 per farm (FDA, 2001e).

Box 5.1—Microbial Contamination and FDA’s Good Agricultural Practices (GAPs)

outbreaks. It is difficult to assess the exact incidence offoodborne outbreaks associated with produce and how it has changed over time. The Centers for DiseaseControl and Prevention (CDC) collect data on allreported foodborne outbreaks. The average annual num-ber of foodborne illness outbreaks associated with freshproduce, both domestic and imported, more than dou-bled between 1973-87 and 1988-91, from 4 per year to10 (Tauxe et al., 1997). The increasing trend appears tohave continued through 1997 (Sivapalasingam, 2002).More recent data are not yet available.

What does this trend indicate? The data are incompleteso it is difficult to generalize about food safety out-breaks beyond saying the number reported hasincreased. Researchers assume that most sporadic casesand many outbreaks of foodborne diseases are unre-ported since a case cannot be reported unless individu-als seek medical care. Many outbreaks are neverdefinitively linked to a particular contaminated productor source. In the case of perishable fruit and vegetables,by the time the authorities begin to investigate, thephysical evidence has usually been consumed or dis-carded. As a result, it is not possible to say anythingauthoritative about the incidence of contamination forvarious types of fruit and vegetables. It is also not possi-ble to say whether imported produce is any more proneto food safety problems than is domestic produce (Zeppet al., 1998).

The data also include outbreaks associated with con-tamination at all levels. Produce can be contaminatedat the grower or shipper level, at some intermediatelevel of the distribution system, or at the final point ofservice (retail store, foodservice establishment, or pri-vate residence, etc.). Data are limited and inconclusiveregarding what percent of outbreaks are attributable tocontamination at the grower or shipper level comparedwith other points along the distribution chain, orwhether contamination at any one level is increasing.

Efforts are underway to further investigate the inci-dence of food safety problems in produce. As part ofthe Produce and Imported Food Safety Initiative,USDA’s Agricultural Marketing Service (AMS) isimplementing the Microbiological Data Program, anonregulatory program that will provide baselineinformation on microbial contamination of produce. Aselect group of produce items, both domestic andimported, are being tested for pathogenic E. coli andSalmonella (AMS, 2001). There is industry concern,however, that since USDA is testing at terminal mar-

kets and chain store distribution centers, it will not beclear where any detected contamination occurred(Produce News, 2002). A problem might be mistak-enly attributed to the farm level when it could haveoccurred somewhere else along the distribution chain.On the other hand, a finding of no contamination atthe terminal market and chain store distribution centerlevel would shift concern towards problems at the finalpoint of service.

For the Produce and Imported Food Safety Initiative,FDA collected data on the incidence and extent ofpathogen contamination (FDA, 2001a). Beginning inMarch 1999, FDA tested domestic and imported pro-duce items for three microbial pathogens—Salmonella,Shigella, and E. coli O157:H7.5,6 Salmonella andShigella were both found in imports and domesticproducts, but no E. coli O157:H7 was found in either.The focus of these studies was to identify problemsresulting from failures to implement adequate GAPsand good manufacturing practices (GMPs).7 The test-ing program was not intended to determine whetherimported or domestic produce is more prone to safetyproblems since the statistical properties of the samplesdid not allow broad conclusions about general foodsafety of produce or comparisons between countries.

Policymakers and researchers are concerned aboutwhy reported food safety outbreaks associated withproduce are increasing. Better reporting due toimproved outbreak investigations and better diagnos-tics have undoubtedly contributed to some of theincrease (FDA, 2001e). Some scientists, however, donot believe that better reporting alone explains theincreased level of outbreaks (Tauxe et al., 1997). It isdifficult to sort out the competing factors.

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5 The Shigella bacteria causes shigellosis, an infectious diseasecharacterized by diarrhea, fever, and stomach cramps. People withsevere cases can usually be treated with antibiotics. Those withmilder cases will usually recover without antibiotics. 6 For the imported produce survey, FDA sampled broccoli, can-taloupe, celery, cilantro, culantro, loose-leaf lettuce, parsley, scal-lions, strawberries, and tomatoes from 21 countries. The cropswere selected based on a combination of five factors that con-tributed to overall food safety risk: previous association with out-breaks, structural characteristics that might provide a particularlyhospitable environment for bacteria, growing conditions, degree ofprocessing, and importance in U.S. consumption (FDA, 2001a).7 GMPs are FDA regulations for food processors. FDA recom-mends firms packing raw, intact fruit and vegetables use GMPs,but they are not required to do so. Firms packing fresh-cut prod-ucts, like bagged salads, are required to use GMPs.

One explanation for increased foodborne illnesses is newand emerging pathogens. Several outbreaks in the 1990swere due to these pathogens, and scientists had todevelop new practices to avoid contamination. Themicrobial pathogen E. coli O157:H7 was identified in1982 and was initially associated with ground ham-burger.8 In the early 1990s, E. coli O157:H7 was firstassociated with a number of produce items. The parasiteCyclospora was described definitively only in 1994 andhas been linked to numerous outbreaks since.Cyclospora has only been associated with a few prod-ucts—raspberries, basil, and lettuce—although manycases could not be traced to a particular product.

Another potential explanatory factor behind the rise inoutbreaks attributed to produce is the change in U.S.consumption habits. U.S. per capita consumption offresh fruit and vegetables (not including juices and otherprocessed products) increased from 249 pounds in 1981to 339 pounds in 2000, an increase of 36 percent. Thetypes of food consumed have also changed. The typicalgrocery store carried 345 produce items in 1998, com-pared with 173 in 1987 (Calvin et al., 2001).

Retailers now routinely provide produce items thatwere once considered seasonal on a year-round basis.Most produce is highly perishable and cannot bestored to provide a year-round supply, so imports areimportant. However, even storable produce is some-times imported; apple imports provide consumers withdifferent varieties and qualities (e.g., fresh-harvestapples from Southern Hemisphere countries during thespring versus stored apples). In 2000, importsaccounted for 19.5 percent of fresh fruit consumption(excluding bananas), up from 3.1 percent in 1975.9

Similarly, in 2000, imports accounted for 13.6 percentof fresh vegetable consumption (excluding fresh pota-toes), up from 5.7 percent in 1975 (table 5.1).

Bananas top the list of per capita fruit consumption inthe United States, with imports accounting for 99.6percent of consumption. Likewise, 76.1 percent of

pineapples, another tropical product, are imported. Fora storable crop like apples, imports are 7.2 percent ofconsumption. For grapes, which are now availableevery month of the year, the import share increasedfrom 5.9 percent in 1975 to 44.1 percent in 2000. Forthe vegetable and melon category, 37.4 percent of can-taloupe consumption was imported in 2000, up from12.4 percent in 1975. Less than 1 percent of lettuce isimported because it can be produced year-rounddomestically. Tomatoes, bell peppers, and cucumbershave high import shares due largely to winter importsfrom Mexico and increasing greenhouse imports, par-ticularly from Canada.

There is no reason, however, to assume that importsare more prone to food safety problems than domestic

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8 One of hundreds of strains of the E. coli bacterium, E. coliO157:H7 produces a powerful toxin that can cause severe illness.Infection often produces bloody diarrhea, but most people recoverwithout antibiotics or other specific treatment. Some people, par-ticularly children and the elderly, may develop hemolytic uremicsyndrome, a life-threatening disease that causes kidney failure. 9 Data are not true consumption data from consumer surveys butrather disappearance data (production for the fresh market plusimports and minus exports equals disappearance—a proxy forconsumption).

Table 5.1—Fresh fruit and vegetable consumptionand imports

Per capita Imported share ofconsumption consumption

Item 2000 1975 2000 1975

— Pounds farm weight — — Percent —

Fruit:1

Bananas 28.4 17.6 99.6 99.9Apples 17.4 19.5 7.2 2.2Oranges 11.7 15.9 8.5 0.8Grapes 7.3 3.6 44.1 5.9Peaches 5.5 5.0 6.4 0.3Grapefruit 5.1 8.4 3.0 0.6Strawberries 5.0 1.8 5.8 8.9Pears 3.2 2.7 20.6 3.5Pineapples 3.2 1.0 76.1 48.0Tangerines 2.8 2.6 25.7 9.5

Vegetables and melons:2

Potatoes 47.2 52.6 5.7 1.2All lettuce 32.0 23.5 0.7 0.0Onions 18.3 10.5 9.3 4.0Tomatoes 17.6 12.0 32.9 21.9Watermelon 13.9 11.4 11.5 5.9Cantaloupe 10.8 5.2 37.4 12.4Carrots 10.4 6.4 5.5 4.4Sweet corn 9.2 7.8 2.1 0.0Cabbage 9.1 8.9 3.5 0.3Bell peppers 7.0 2.5 19.6 12.6Cucumbers 6.4 2.8 41.4 21.6Broccoli 6.0 1.0 6.3 0.01 For citrus, the year reflects the end of the harvest; for noncitrus,the beginning of the harvest.2 ERS traditionally reports melons with vegetables. Consumption ison a calendar-year basis.

Source: Fruit and Tree Nut Yearbook, and Vegetable andSpecialties Yearbook, ERS, USDA.

produce. Many growers in foreign countries specializein exports. For example, in the Mexican winter veg-etable industry, growers are producing to comply with relevant U.S. government standards (pesticideresidues, microbial contamination, etc.) as well asdemands of their U.S. marketer and final buyers suchas a particular retail chain. Growers are well aware ofthe food safety requirements. If prices are favorable,they may sell some of their production to the domes-tic Mexican market but produce grown in Mexico forthe domestic market could not easily be sold into theU.S. market.

Much of the U.S. and foreign produce industry hasdeveloped a global focus. A network of business rela-tionships tie domestic and foreign producers andencourage high standards of food safety (see box 5.2).

However, with improvements in communications,storage technology, and transportation, it is possibleto acquire commodities from many new areas. Inrecent years, imports have arrived from many nontra-ditional suppliers. The Caribbean Basin Initiative andthe Andean Trade Preference Act have eliminated tar-iffs on many agricultural items and encouragedimports from these areas. The share of total volumeof fresh produce imports (excluding bananas) fromthree traditional suppliers—Mexico, Chile, andCanada—dropped from 81 percent in 1990 to 72 per-cent in 2000. Less traditional suppliers haveincreased their market share of imports. For example,in 1990 only 10 percent of asparagus imports camefrom Peru, compared with 47 percent in 2001.Similarly, Costa Rica and Guatemala accounted for17 percent of cantaloupe imports in 1990 and 60 per-cent in 2001.

Another consumption trend that may affect outbreaks isthe growing share of food eaten at foodservice establish-ments, potentially increasing the number of people han-dling produce before it is eaten (and the chance ofcontamination). In 2001, 47.4 percent of total foodexpenditures went to the foodservice sector, up from33.4 percent in 1970 (ERS, 2002).

Three Examples of FoodborneIllness Outbreaks Associated

With Imports

Three case studies examine recent food safety prob-lems: (1) disease outbreaks due to Cyclospora contami-

nation of Guatemalan raspberries, which began in 1996,(2) the 1997 outbreak of hepatitis A associated withstrawberries from Mexico, and (3) the 2000-2002 out-breaks due to Salmonella contamination associated withMexican cantaloupe. By coincidence, all three casesdeal with fruit but this does not imply that vegetablesare not also associated with foodborne illnesses.

Raspberries and Cyclospora

In the spring and early summer of 1996, CDC andHealth Canada received reports of more than 1,465cases of foodborne illness due to Cyclospora in theUnited States and Canada (for more details on the rasp-berry case, see Calvin et al., 2002). There were no fatal-ities. This was a very large outbreak compared to othersassociated with fresh produce. On June 8, 1996, theTexas Department of Health issued a health warningthat erroneously identified the source of the problem asCalifornia strawberries, then at peak production. OnJuly 18, 1996, the CDC and the Ontario Ministry ofHealth issued a statement reporting that Guatemalanraspberries were the most likely source of the outbreaks.The California Strawberry Commission estimated thatthis false alarm led to $16 million in lost revenue togrowers in the central coast of California during themonth of June (Mishen, 1996).

By the time raspberries were identified as the source of contamination, the Guatemalan raspberry spring sea-son was over so no immediate regulatory action wastaken. FDA and CDC sent a team of investigators toGuatemala later that year to observe growing conditionsand to better understand the berry industry there.Because the disease was relatively new to scientists, noone knew which raspberries were contaminated, howthey became contaminated, or how to solve the prob-lem. The CDC concluded, after considering the manydifferences in various aspects of the distribution systemsfor the implicated raspberries, that simultaneous andpersistent contamination on multiple farms was themost likely explanation for the outbreak (Herwaldt etal., 1997). Subsequent research, based on the events forwhich well-documented traceback data were available,indicated that the 1996 outbreak could have beenaccounted for by as few as six farms (Herwaldt et al.,1999). Traceback is the ability to track food from theconsumer point of purchase back to the grower. FDAprovided advice/technical assistance and suggestedusing GAPs (then under development), GMPs, and sani-tation standard operating procedures.

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A grower organization, the Guatemalan BerryCommission (GBC), developed a system to characterizefarms according to risk and allowed only certain farmsto export. However, the plan had no enforcement mech-anism for the 1997 spring season and another outbreakof foodborne illness (with no fatalities) in the UnitedStates and Canada was again traced to Guatemalanraspberries. Either the new practices were not com-pletely implemented, were ineffective, or were notdirected at the true source of contamination (Herwaldtet al., 1999). After consulting with FDA, the GBC vol-untarily stopped raspberry exports to the United States

on May 30, 1997. Guatemala estimated that stoppingexports in the middle of the spring season resulted in aloss of $10 million in income (Powell, 1998).

After a second season with Cyclospora contamina-tion problems, both the GBC and the government ofGuatemala realized that more stringent controls andenforcement were required. In November 1997, theGuatemalan government created a commission tolead the effort to improve food safety. This gave theGBC’s certification process enforcement power thatwas critical to making any export plan manageable.

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A firm importing produce into the United States tosupply the offseason market will want a product thatis equal in quality to their own to maintain their repu-tation. This takes planning. The pressure to coordi-nate year-round production, often in far-flunglocations, and provide food safety assurances mayfavor both horizontal and vertical integration or coor-dination (Wilson et al., 1997; Hennessey, 1996). Forexample, a U.S. grower-shipper may decide to collab-orate with a foreign grower-shipper to provide a yearround supply with particular characteristics—hori-zontal integration or coordination. A U.S. shippermay decide to collaborate with a foreign grower forthe same reason—vertical integration or coordination.

U.S. firms have many types of interests in foreignproduction to expand their season. For the U.S. firm,it is important that the foreign product be consistentwith the quality their firm sells from domesticsources. For example, a U.S. firm may grow producton its own farms in a foreign country for sale in theU.S. market. A U.S. firm might also have a joint ven-ture with a firm in a foreign country to produce acrop to be sold in the United States. In some cases,U.S. firms may merge with a foreign supplier. ManyU.S. shippers and grower-shippers also market forforeign growers and charge a sales commission.Some U.S. grower cooperatives have foreign mem-bers who must meet domestic production standards

These suppliers must develop relationships with reli-able foreign growers to provide these products.Suppliers may travel frequently to foreign productionregions to cement the relationship with their growers.The suppliers may send agronomists to check on pro-duction and crop conditions. Some even have staff liv-

ing in foreign countries. The stakes are high whenprocuring product from another country. In any ofthese situations, if the product has food safety prob-lems and cannot be sold, the U.S. supplier may nothave adequate supplies for its customers, a seriousproblem in the competitive produce industry. On theother hand, selling a substandard product may damagethe firm’s reputation if a foodborne illness outbreak istraced back to the firm. The stakes are also high for theforeign producer too. Many foreign countries havevery specialized produce industries geared almostexclusively towards exports. If products are not accept-able in the U.S. market they often have few alternativemarkets. For example, some of the products grown inMexico for export to the U.S. market, such as bell pep-pers, cherry tomatoes, and eggplant, have virtually noalternative domestic market.

Large foreign suppliers are following the same trendin horizontal and vertical integration in reverse. Forexample, some large Mexican and Chilean wintersuppliers are expanding into production or joint ven-tures in the United States and other countries to pro-vide a year-round supply for their U.S. buyers.Foreign growers have also vertically integrated byacquiring marketing operations in the United States.This provides foreign growers with the ability to bet-ter market fruit and vegetables since they directlycontrol the quality of their production. For example,many of the shippers located in Nogales, Arizona,where winter vegetables from Mexico enter theUnited States, are really just the marketing arms oflarge Mexican growers. In the 1996/97 season, 63percent of the tomatoes in Nogales were sold bythese vertically integrated, Mexican-owned firms(Calvin and Barrios, 1998).

Box 5.2—Ties That Bind the Domestic and Foreign Produce Industry

In December 1997, FDA, not yet convinced thatGuatemala had adequately addressed the Cyclosporacontamination problem, issued an import alert forGuatemala for the following spring season, puttingall shipments from the country under detention with-out physical examination (DWPE) and denyingimports entry into the United States. Denying allimports of raspberries based on country of originrather than rejecting products from a specific shipperwith problems was an unusual response, and oneused only after all other means of resolving theproblem were exhausted. Generally, FDA collectsrandom samples at the border, preventing entry ofproducts that fail inspections. FDA can also detain aproduct without physical examination if the shipperhas failed previous FDA port inspections or if FDAhas other information indicating that the productmight violate standards. The product may remain inDWPE status until the shipper proves that the prod-uct meets FDA’s standards.

Denying imports without physical evidence was veryrare in 1997, and in this case the import alert wasbased only on epidemiological evidence about pastoutbreaks and FDA observations on current produc-tion practices. Not until 2000 did FDA actuallyobserve Cyclospora on a Guatemalan raspberry (Hoet al., 2002). Since 1997, FDA has become lessreluctant to deny imports on epidemiological evi-dence alone.

FDA, Health Canada, the Canadian Food InspectionAgency, and Guatemalan officials consulted to con-sider improved intervention strategies for raspberryproduction. Beginning in the spring 1999 season, theUnited States allowed entry of raspberries producedunder the Model Plan of Excellence (MPE), a jointprogram of the GBC and the government ofGuatemala. Farmers are only allowed to join the MPEprogram and export by complying with a detailed pro-gram of food safety practices and successfully passingGuatemalan government inspections and FDA audits.Food safety practices include the use of filters forwater and better worker hygiene facilities. The pro-gram also requires a code applied to each clamshell ofraspberries, which allows traceback to an individualgrower. Traceback and traceforward capability is criti-cal in the event of a food safety problem. These toolscan be used to revoke the export authority of any firmsassociated with a food safety problem in order tomaintain the integrity of the MPE. In some cases,traceback can be used to eliminate Guatemalan rasp-

berries as a potential source of contamination. Inspring 1999, there were several outbreaks in theUnited States and Canada due to Cyclospora but theGBC could show, using its traceback and traceforwardcapabilities, that Guatemalan raspberries were notserved at the events associated with the outbreaks. In2000, there were two outbreaks associated withCyclospora contamination of raspberries traced to oneGuatemalan farm that was consequently removed fromthe MPE program. There have been no further out-breaks associated with Guatemalan raspberries since2000. In 2002, only three raspberry growers remainedin the MPE program. In 1996, before the contamina-tion problem began, the number of growers was esti-mated to be 85.

The MPE program is a process standard. GAPs, forexample, recommend that water quality be adequate forits intended use, but the MPE program requires farmersto use a nominal 1 micron filter as a prefilter to removeparticulate matter and an absolute 0.45 micron filter forwater used on plants and for employee hygiene. When afood safety problem becomes intractable, a process stan-dard may be necessary rather than relying on the moreflexible GAPs. Some firms might have been able to pro-duce a safe product without the expensive filters, so aprocess standard may introduce inefficiency. However,the MPE process standard may have resolved the foodsafety problem faster, reducing economic losses, than ifthe industry had relied on voluntary GAPs.

The problem with raspberries affected other products.U.S. demand for Guatemalan blackberries also declined;blackberries were never cited as a definitive cause of anyfoodborne illnesses in the United States, although theywere in Canada. In addition to possible food safety con-cerns, blackberries faced decreased demand becauseretailers prefer to buy a range of berry products all fromone buyer if possible. When Guatemala could provideonly blackberries, many buyers purchased berries fromother regions that could provide the desired mix ofberries. The blackberry industry has, however, faredmuch better than the raspberry industry; in 2001, U.S.imports of Guatemalan raspberries were 16 percent of1996 levels and blackberries were 55 percent of their1996 level. Guatemala has a voluntary food safety pro-gram for the much larger blackberry industry but it ismuch less rigorous than the MPE.

When confronted with the food safety problems inGuatemala, many berry shippers made alternativeplans. One Guatemalan shipper closed all his domestic

82 ● International Trade and Food Safety / AER-828 Economic Research Service/USDA

operations and began production in Mexico. A largeChilean firm that ships to the U.S. and Europe hadraspberry operations in Guatemala but after the firstoutbreak this firm stopped shipping raspberries fromGuatemala and began to develop production inMexico. This change of strategy might have occurredeven without the Cyclospora problems; it is cheaper totransport raspberries from Mexico by truck than fromGuatemala by airfreight.

While Guatemala worked to increase food safety stan-dards, other competitors, particularly Mexico, madeinroads into its spring and fall market niches in theU.S. market (fig. 5.1). Prior to the 1996 outbreaks, thesize and growth of Guatemalan and Mexican exports tothe United States were very similar. With outbreaks in1996 and 1997, many U.S. buyers decided to purchaseraspberries elsewhere. Some buyers still feel that thereis no reason to take a risk when there are alternatesources of raspberries. Others are reassured by theMPE, arguably the strictest industrywide program forraspberry production in the hemisphere.

In addition to the changes in Guatemala, the outbreaksled to improved private food safety programs for rasp-berry producers in Chile, Mexico, and the UnitedStates (although none of these countries were associ-ated with Cyclospora contamination of raspberries).After the Cyclospora problem had such an adverseimpact on the California strawberry industry, theCalifornia Strawberry Commission (CSC) developed afood safety program. California raspberry shippers(and their growers) also use this plan since all rasp-berry shippers also market strawberries.

Strawberries and Hepatitis A

In March 1997, more than 200 schoolchildren andteachers in Michigan contracted hepatitis A. Caseswere reported in other States as well (Hutin et al.,1999). It was quickly determined that the source of thecontamination was frozen strawberries processed by afirm in California. The processor had used fresh straw-berries shipped to the United States in April 1996, ayear earlier, from Baja California, Mexico. Most of theMexican berries had been sold in the fresh market andsome were sold to the processor (FAS, 1997). FDAwas able to determine that California-grown strawber-ries were not the source of contamination. However,FDA could not determine whether the Mexican-grow-ers fruit was contaminated in Mexico at the farm levelor at the California processor. The product was notcontaminated in Michigan.

General concerns about the safety of fresh strawberriesaffected demand for berries from all sources. Themonthly price received by growers fell 40 percent fromMarch to April in 1997, compared with an averagedecline of 16 percent for the years 1990-1996 and 1998-2000. Initial estimates from the CSC put losses at $15million with later estimates at $40 million, but both esti-mates are subject to debate (Richards and Patterson,1999). As some of the California growers had joint ventures in Mexico, they shared in the financial lossesthere too.

The 1996 outbreak associated with Cyclospora-contaminated raspberries, when California strawberrieswere initially and incorrectly implicated, increased thestrawberry industry’s awareness of their vulnerability tofood safety problems. Following that outbreak, the CSCbegan developing the voluntary Quality Assurance FoodSafety Program to help producers improve their foodsafety standards and mitigate microbial contamination.The CSC worked with FDA and the CaliforniaDepartment of Health Services to develop the program.This was one of the earliest good agricultural practicesprograms for the produce industry that focused on miti-gating microbial contamination. An industrywide foodsafety program is expensive and the CSC has spentabout $250,000 to date.

California standards for production practices and docu-mentation were already fairly rigorous, but the CSC’sQuality Assurance Food Safety Program strengthenedboth. Traceback is a critical part of the voluntary pro-gram. If there is a problem, the industry wants to be

Economic Research Service/USDA International Trade and Food Safety / AER-828 ● 83

Figure 5.1

U.S. imports of raspberries, 1990-2001

Metric tons

Source: U.S. Department of Commerce.

Mexico

Guatemala

1990 92 94 96 98 20000

200

400

600

800

1,000

1,200

1,400

1,600

Chile

able to say the product is not from California or tracethe product back to the field and isolate the problemfarm from the rest of the industry. Growers use a varietyof traceback systems. The best systems include informa-tion on shipper, date, field, and picker on each box.10 Itis not enough to just have safe products; growers mustbe prepared to quickly demonstrate their food safetyprogram in the case of an outbreak. The QualityAssurance Food Safety Program encourages farmers toalways have all their documents regarding food safetyready in the case of emergency. This includes docu-ments regarding water, soil, and any fruit testing; pesti-cide and fertilizer use; and records of hygiene practices.

This program was introduced in November 1996 andwas in effect, although still in its infancy, when thestrawberry problem occurred in 1997. Although the con-taminated product was frozen strawberries, consumerconfidence in fresh strawberries was also shaken. Inresponse to a second year of media scrutiny, the CSCwas prepared to deflect unwanted attention from theirindustry. The CSC announced that fresh Californiastrawberries were not responsible for the outbreak andthat because growers were using a sophisticated foodsafety program they were unlikely to ever be responsiblefor such an outbreak. Researchers estimated the impactof positive and negative publicity in this case. Pricesresponded more strongly to bad news than good news,so it is very important to prevent or stop negative public-ity as soon as possible (Richards and Patterson, 1999).11

Before the outbreak of hepatitis A associated with straw-berries, the growers in Mexico were members of theCalifornia Strawberry Commission. After the outbreak,the Commission decided to limit membership toCalifornia producers to maintain the California focusand a consistent message in its marketing program.However, because the Baja California and Californiastrawberry industries are so integrated, with growers inMexico marketing through California shippers, theMexican producers still benefited from the CSC’s foodsafety research.

Although it was never proven that the contaminationoccurred in Mexico, the outbreak had a serious impacton the Baja California, Mexico industry. The UnitedStates imports very small amounts of fresh strawber-ries—just 6 percent of total U.S. consumption in2001—and almost all of that is from Baja California,Mexico. The Baja California season runs from Januaryto July, with the highest production typically in April.Baja California production augments the low wintersupply in the United States. Figure 5.2 shows theimportance of Mexican strawberries during the winterfor firms offering a year-round supply.

The publicity surrounding the hepatitis A outbreak hadan immediate effect on fresh strawberry shippers fromBaja California. Figure 5.3 shows the precipitous declinein fresh strawberry shipments from Mexico in April1997, compared with 1996. Due to the collapse of mar-ket demand in the United States, the primary market forBaja California producers, U.S. shippers told theirMexican growers to stop harvesting, and about 200hectares of strawberries in Baja California were leftunharvested (out of 563 planted hectares).

In response to the outbreak, the Baja California straw-berry growers and their local grower organizationestablished more stringent food safety standards(FAS, 1998). Since most of their production isexported, the growers needed to ensure their productwould be accepted in the United States. Growersstarted using third-party audits immediately for straw-berries as well as other produce items. Many of thelarge U.S. third-party audit firms have operationsabroad in important growing areas. Some growers

84 ● International Trade and Food Safety / AER-828 Economic Research Service/USDA

10 In the case of strawberries, information on the picker was fairlyeasy for many shippers to incorporate into their traceback pro-grams. Because the strawberry industry uses an hourly wage aswell as a piece-rate payment, the industry already had to be able totie product to individual pickers.11 Two other aspects of the outbreak kept the news in the publiceye. The processor illegally sold the frozen berries as U.S.-grownberries to the National School Lunch Program, which requiresdomestic product (Richards and Patterson, 1999). Also, manyschoolchildren were immunized against hepatitis A as a precau-tionary measure when there was concern that some of the contami-nated product might have been served in Los Angeles area schools.

Figure 5.2

U.S. monthly strawberry shipments, 2001

1,000 cwt

Source: Agricultural Marketing Service, USDA.

Mexico

CentralCalifornia

Jan. Mar. May July Sep. Nov.0

500

1,000

1,500

2,000

2,500

3,000

California

MexicoFlorida

adopted the CSC’s food safety program. In an inte-grated industry, new practices in the United States arequickly adopted in Baja California.

FDA officials went to the California processor and theMexican strawberry fields to inspect operations butresults regarding the origin of the contamination wereinconclusive. FDA provided training on GAP recom-mendations that were just being developed. These rec-ommendations provided guidelines similar to those ofthe CSC program. The Mexican state-level departmentof agriculture was instrumental in disseminating infor-mation on FDA’s GAP recommendations to growers.Since that time, they have also hosted FDA and theCalifornia Department of Food and Agriculture,among others, for classes on food safety (Avendaño,2002). At the time of the outbreak, there was no effec-tive way to test for the presence of hepatitis A onstrawberries so there was no increased microbial sur-veillance specifically targeted at this pathogen. FDAwas also involved with the recall of frozen strawber-ries and processed products made with the berries. Inthe case of produce consumed in fresh form, there israrely any product to recall by the time an outbreak isdetected and the source is identified.

Although fresh strawberry imports from Mexico in1997 were only 47 percent of 1996 levels, imports in1998 increased to 86 percent of the earlier level. In1999, U.S. imports of fresh strawberries from Mexicowere at record levels. This outbreak had only a short-run impact on fresh trade.12 Apparently U.S. shipperswere confident that their Mexican strawberry growershad taken adequate precautions.

Cantaloupe and Salmonella

In 2000, 2001, and 2002 there were outbreaks ofSalmonella associated with Mexican cantaloupe.Mexico exports cantaloupe from various regions dur-ing its long export season; in each case, contaminatedcantaloupe came only from one region in the south.While Mexico only supplied 7.2 percent of total U.S.consumption in 2001, Mexico and Central America arethe major suppliers during the winter season (fig. 5.4shows suppliers in 1999, the last year of trade withoutSalmonella contamination problems).

In 2000, cantaloupe from southern Mexico were impli-cated in a Salmonella poona outbreak. Forty-sevenpeople became sick in March and April and by lateMay cantaloupe was implicated (Anderson et al.,2002). The outbreak occurred during the spring whenMexico ships a large volume of cantaloupe to the U.S.market. By the time the outbreak was traced to can-taloupe, the Mexican season was coming to a close.U.S. producers then bore the brunt of consumer back-lash against cantaloupe. The outbreak was traced to aparticular shipper in Arizona selling cantaloupe fromsouthern Mexico. FDA issued an import alert for thisshipper and one farm. In the fall, FDA visited the farmin southern Mexico. Although scientists are morefamiliar with Salmonella than emerging pathogens likeCyclospora, they cannot always determine exactly how

Economic Research Service/USDA International Trade and Food Safety / AER-828 ● 85

Figure 5.3

Strawberry shipments from Mexico, 1996-1997

1,000 cwt

Source: Agricultural Marketing Service, USDA.

1997

1996

Jan. Mar. May July Sep. Nov.0

50

100

150

200

250

12 U.S. imports of frozen strawberries from Mexico were higher in1997 than in the previous year. Frozen strawberries come fromcentral Mexico and were apparently not affected by concerns aboutfood safety problems in Baja California.

Figure 5.4

U.S. cantaloupe supply, 1999

1,000 cwt

*Central California shipments are estimated.Source: Agricultural Marketing Service, USDA.

Jan. Mar. May July Sep. Nov.0

1,000

2,000

3,000

4,000

MexicoTexas

CentralAmerica

California Desert

CentralCalifornia*

Arizona

Rest ofthe world

the contamination occurred and how to definitivelyresolve the problem. The primary host for Salmonellais animals, followed by humans. A firm shipping prod-uct contaminated with Salmonella is most likely fail-ing to follow GAPs and GMPs. FDA prepared anadverse findings report, which identified farm activi-ties that were inconsistent with GAPs and GMPs; FDAdoes not tell a farmer how to fix the problem. Whenthe distributor provided documentation demonstratingcorrective actions taken to respond to FDA’s adversefindings, the import alert was lifted and the firm andfarm resumed exporting to the U.S. market.

In late spring 2001, two additional outbreaks ofSalmonella attributed to cantaloupe occurred (firstSalmonella poona and then Salmonella anatum). Fiftypeople were sickened and two died from Salmonellapoona (Anderson et al., 2002; FDA, 2001c). Fewerpeople were sickened in the Salmonella anatum out-break. Although Salmonella can cause serious andsometimes fatal infections in young children, frail orelderly people, and others with weakened immune sys-tems, healthy people who become infected generallyexperience less severe medical problems. Based on thetraceback investigation, FDA determined that the con-taminated cantaloupe in 2001 came from the same farmin Mexico and shipper in Arizona that were implicatedin the 2000 outbreak. The firm is a large shipper ofwinter melons from Mexico and has been in the busi-ness for 30-40 years (The Packer, 2001). Either imple-mentation of the new practices was inadequate or thechanges failed to address the problem. Again, by thetime cantaloupe from Mexico were determined to bethe culprit, most of the Mexican shipping season wasover. FDA announced that anyone who had any can-taloupe from this company should remove it from sale,and the company issued a recall of its cantaloupe.Growers from northern Mexico were still selling smallvolumes to the United States. Some shippers in Arizonatold their Mexican growers to sell to the Mexican mar-ket. On May 25, 2001, FDA issued an import alert forthe distributor and grower that is still in effect in early2003. The firm cannot ship cantaloupe to the UnitedStates but it can still ship honeydew melons.

In May 2002, an outbreak of Salmonella poona in theUnited States and Canada was associated withMexican cantaloupe shipped through McAllen, Texas.Fifty-eight cases were identified (Anderson et al.,2002). The importing firm issued a voluntary recalland FDA issued an import alert (FDA, 2002a). Thiswas the third season of outbreaks traced to southern

Mexico. The Mexican government is investigating thesource of contamination.

U.S. cantaloupe imports from Mexico in the 2001-2002 season were 64 percent of the previous season’svolume (fig. 5.5). However, one large multinationalfirm’s decision to move operations to Central Americaaccounts for at least some of the decline. Other factorsbehind declining imports from Mexico include produc-tion problems and increasing input costs. Honeydewimports in 2001-2002 were 97 percent of the previousseason’s volume. Unlike the case in Guatemala whereproblems with raspberries affected demand for black-berries, commercial buyers do not seem to be particu-larly worried about honeydew melons from Mexico.13

Repeated outbreaks within an industry prompt severalconcerns. First, the industry fears that when people getsick, investigators may immediately, and incorrectly,focus on the product with a history of trouble. Second,the produce industry is concerned that FDA might issuea consumer warning about eating the contaminated pro-duce.14 Third, growers are concerned that if a problemlooks like it affects more than a few growers, the FDAmight decide to initiate an import alert against all pro-ducers from a particularly country, as in the case ofGuatemalan raspberries. Fourth, there is concern that anongoing problem could hurt the reputation of otherproducts from the same region. Fifth, FDA introduced amandatory food safety program for fruit and vegetablejuices after three outbreaks. FDA always has the optionof making food safety programs mandatory—somethingmost growers would like to avoid.

The California cantaloupe industry’s efforts to promotefood safety predate the 2000-2002 Salmonella outbreaksassociated with Mexican cantaloupe. Over the years,cantaloupe has been associated with several other food-borne disease outbreaks. Outbreaks of Salmonella in the

86 ● International Trade and Food Safety / AER-828 Economic Research Service/USDA

13 Although all field-grown melons mature on the ground and aretherefore exposed to potentially contaminated soil and irrigationwater, cantaloupe appear to be particularly susceptible to microbialcontamination, perhaps because of the rough webbing on the rind,which may harbor pathogens (FDA, 2001a). Smooth-skinned hon-eydew melons, which are often grown in similar areas, appear tobe less prone to contamination problems. 14 Beginning in 1995, there were numerous outbreaks traced tosprouts that the industry could not seem to resolve. In 1998, FDAwarned high-risk groups to avoid eating raw alfalfa sprouts. Thenin 1999, FDA broadened the warning to include all consumers, notjust those at high risk, and all types of raw sprouts (FDA, 1999).This warning was repeated in 2002 and expanded to include lightlycooked mung bean sprouts (FDA, 2002c).

United States in 1990, 1991, and 1997, and in Canada in1991 and 1998 were traced to cantaloupe (FDA, 2001d).In 1991, the news about contaminated cantaloupeemerged in August, when half of the large Central Valleycrop in California is shipped (fig. 5.4). The U.S. can-taloupe industry initiated a food safety program calledthe “Melon Safety Plan” (Tauxe, 1997). Once the crisiswas over, however, the program ran out of money andsputtered to a stop.

Since 1998, the California Melon Research Board,which represents all California melon producers,except watermelon growers, has spent more than$300,000 on funding melon food safety research at theUniversity of California at Davis. Growers whoremember the economic chaos of the 1991 outbreakand are concerned about the potential impact of anynew food safety problems fund the research. Thisgroup of California growers, with the largest can-taloupe production in the United States, views thisinvestment in food safety as critical for the reputationof their industry. This research focuses on Californiacantaloupe and while the general principles of thisresearch will be widely applicable, the specifics willnot. California melons are mostly field packed andforced-air cooled. In other parts of the United States,Mexico, and Central America, shed packing and cool-ing with cold water or ice are more common and thesepractices pose different food safety challenges.

Beginning in 2000, the California CantaloupeAdvisory Board (a marketing order for California can-taloupe grown north of Bakersfield) began requiringadditional traceback information on cantaloupe boxes

as part of their State marketing order (this programwas voluntary in 1999). This was not a very difficultprocess. California cantaloupe is packed in the fieldand the Board had already contracted with theCalifornia Department of Food and Agriculture toinspect cantaloupe during harvest for quality controland apply an inspection sticker to every box (growerspay the Board a per-box fee for this service).Cantaloupe from this area cannot be sold without thesticker identifying the county and shipper. The newprogram requires information on the packing date,field, and packing crew, which allows a grower totrace the problem right back to a particular part of afield. Some growers had already been providing thisadditional information. Adding this additional trace-back information to the box was neither particularlycostly nor complicated. It did take some administrativechanges, however.

To be able to require traceback, the members of theBoard had to propose a change to their marketingorder and vote on it. Their original marketing ordercovered grades and quality standards. The new marketing order specifically approves “such grade and quality standards of cantaloupes as necessary,including the marking or certification of cantaloupesor their shipping containers to expedite and implementindustry practices related to food safety” (CaliforniaDepartment of Food and Agriculture, 2000). If anotheroutbreak were to occur, this program would allow theindustry to immediately pinpoint the source of theproblem or deny that the problem is due to Californiacantaloupe, depending on the situation. This may bethe only mandatory program for produce in the UnitedStates that requires such detailed traceback informa-tion on each box.

The Mexican cantaloupe industry is also concerned.In FDA’s first round of microbial testing of produce,both imported (1999-2000) and domestic (2001-2002) shipments of cantaloupe tested positive forSalmonella. The FDA followup survey (beginning inJanuary 2001) on imported cantaloupe showed nocontaminated samples from Mexico. CDC contendsthat the interpretation of the 2001 results are limitedby the small size—only 29 samples (Anderson et al.,2002). Mexican industry insiders feel that the initialresults from the FDA served as a wake-up call togrowers; an indication that normal operations wouldnot be sufficient and that the cantaloupe industrywould have to be seen as proactive on the food safetyissue to maintain its reputation. This may be particu-

Economic Research Service/USDA International Trade and Food Safety / AER-828 ● 87

Figure 5.5

U.S. imports of cantaloupe from Mexico and Central America1,000 metric tons

Source: U.S. Department of Commerce.

Mexico

Central America

1990 92 94 96 98 20000

100

200

300

400

larly important when cantaloupe from CentralAmerica are also available during much of theMexican season. Results from the 2002 samplingprogram are not yet publicly available.

In 2001, the Mexican government agency in charge offood safety, Servicio Nacional de Sanidad, Inocuidad yCalidad Agroalimentaria (SENASICA), began devel-oping a food safety program for cantaloupe. The pro-gram is based on planting permits, productionprograms requiring GAPs and GMPs for growers andpackinghouses, and monthly melon testing. The pro-gram also includes more sophisticated traceback capa-bility. As in other cases, it is imperative to identify anygrower or packer that harms the integrity of a foodsafety program. All exports must have an internationalphytosanitary permit, which will only be issued ifcompliance with GAPs and GMPs is certified (ThePacker, 2002c). FDA and SENASICA were discussingthis program in early summer of 2002. Parts of thissystem were in place on a voluntary basis in somestates in fall 2002. Also in 2002, FDA and SENASICAbegan preparing to conduct joint training for govern-ment inspectors and farmers.

U.S. cantaloupe growers lobbied FDA to take a moreaggressive role in this evolving case (this was appar-ently not the case in the raspberry outbreaks). OnOctober 28, 2002, FDA issued an import alert againstall cantaloupe imports from Mexico (FDA, 2002d).Although the outbreaks had been traced just to twoStates in southern Mexico (Michoacan and Guerrero),FDA justified the countrywide import alert because ofFDA samples showing Salmonella contamination incantaloupe from other States (Sonora, Jalisco, Colima,Coahuila, Mexico, and Tamaulipas). Also, FDA wasconcerned that with a regional approach, melons fromrestricted regions could be commingled with melonsfrom a nonrestricted area. On November 4, 2002,Canada issued a similar import alert for all Mexicancantaloupe (CFIA, 2002).15

Mexican growers have complained about the timing ofthe decision—just as growers in Sonora were ready tobegin harvesting cantaloupe for the U.S. market. Theyalso complained that the penalties FDA is imposing

are higher than those for U.S. cantaloupe producerswith similar food safety problems. While FDA sam-ples showed Salmonella contamination in shipmentsfrom several regions of Mexico, samples from the U.S.in 2001 also showed contamination, but the U.S. grow-ers are not faced with similar restrictions (FPAA,2002). Also, for Mexican growers to be removed fromthe countrywide import alert, they will have to demon-strate higher food safety standards than U.S. growers.An individual Mexican firm can petition FDA toremove their firm from the import alert by providingdocumentation of their food safety program.According to the import alert announcement “afterreviewing these submissions, FDA, either solely or inconjunction with the relevant Mexican regulatoryauthority may conduct a limited number of onsiteinspections of the growing/processing areas to auditthe validity of the information submitted to FDA. FDAintends to give first priority to firms or growers whohave their operations inspected by a third-party auditfirm that has expertise in agricultural and transporta-tion processes.” A third-party audit showing compli-ance with GAPs will not necessarily be enough to beremoved from the import alert list. In contrast, U.S.cantaloupe growers are not required to use GAPs,although many comply voluntarily.

November 2002 saw developments on both sides of theborder. On November 8, Mexico presented a formalcomplaint to the World Trade Organization’s Sanitaryand Phytosanitary Committee claiming that the U.S.import alert against all Mexican cantaloupe was not con-sistent with U.S. trade commitments with respect to dis-crimination, protectionism, and unnecessarily traderestricting actions (SAGARPA, 2002). On November 13,the Mexican government published legislation that gavethe government legal authority to require all cantaloupegrowers to comply with the new food safety program.On November 20, importers associated with the 2000and 2001 outbreaks were indicted in the United Stateson Federal charges of “trying to impede and defeat law-ful government functions of the U.S. Customs Serviceand the U.S. Food and Drug Administration” in theirtraceback efforts (The Packer, 2002d). The importersentered a plea of not guilty and the trial, initially sched-uled for January 2003, has been delayed. On November27, 2002, FDA authorized imports from two farms fromthe northern Mexican state of Sonora (The Packer,2002e). This paper only covers events throughNovember 2002 in a case that will continue to evolve.

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15 In the raspberry case, between 1998 and 2000, either the UnitedStates or Canada had an import alert but never in the same year.Since Cyclospora was an emerging pathogen, it was not clear whatactions were adequate to resolve the problem. This inconsistency inpolicy raised concerns in Guatemala about the scientific basis oftrade policy.

Summary of Responses to Food Safety Problems

Private Response

In a food safety outbreak, the grower’s first line ofdefense is to adopt GAPs if they are not already inplace.16 Some growers develop their own food safetyprograms that are even more stringent than FDA’sGAP guidelines. However, it is often difficult todetermine how contamination occurred and whatpractices are adequate to resolve the problem. InGuatemala the problems took several seasons toresolve and the exact means of contamination wasnever determined. It is not clear how long it will taketo solve the problem in Mexico since neither theextent of the problem nor the source of contamina-tion have yet been identified.

In the past, an individual grower could adopt a betterfood safety program when faced with a food safety prob-lem, but it was difficult to signal to buyers that the firm’sproduct was safer than that of others in the industry. Inthe raspberry case, the two market leaders—large U.S.and Chilean firms—adopted new food safety programsfor all their growers in different countries. These firmsare so large that the cost of improved practices and addi-tional testing was likely small compared with the lossesassociated with a potential food safety problem anddamage to their reputation. If consumers and large-scalebuyers recognize the brand name, then these firms maybe able to maintain consumer confidence even if otherfirms’ reputations suffer from a food safety problem.

The growth in the use of third-party audits for GAPshas provided growers with a new tool to indicate thatappropriate practices are in place. An audit can reduceasymmetric information between the grower and ship-per and between the shipper and commercial buyers. Inthe late 1990s, with GAPs in place, third-party auditors

began to verify food safety programs for field opera-tions as being in compliance with these guidelines.While FDA developed GAPs, the private sector hasdeveloped the third-party auditing industry for microbialcontamination.17 There is no government oversight ofthird-party audit firms—an issue that concerns many inthe produce industry (The Packer, 2002a). Standardsmay vary between auditing firms and between retailersrequiring use of audits. Growers and shippers are con-cerned that this raises their costs if they need to havedifferent audits for different buyers.

Another concern regarding third-party audits formicrobial food safety is that this focus is relativelynew for produce. The third-party audit industry has itsroots in pesticide residue testing and auditing ofindoor HACCP programs. Examining produce for pes-ticide residues is much easier than looking for micro-bial contamination. Although adherence to GAPguidelines and successful third-party audits of foodsafety programs do not guarantee food safety, FDA isconcerned that some outbreaks have been traced backto firms that have successfully completed third-partyaudits.18 An audit can verify that growers are usingcertain food safety practices that should help reducemicrobial contamination but it is much harder toobserve the potential for contamination. For example,GAP guidelines say that water must be adequate for itsintended use. An auditor may take water samples in anattempt to provide a more comprehensive assessmentof risk. However, water samples can be problematicsince water contamination is not necessarily a constantpresence. A sample of surface water that tests negativefor microbial organisms on one day indicates nothing

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16 Of course, some firms already had sophisticated food safetypractices in place, even before the more recent concern with foodsafety. Many of the largest firms have their own food safety pro-grams with trained scientists overseeing production and packingoperations. This is particularly important for the new fresh-cutproducts like bagged salads which often have consumer-recog-nized brands. Investment in food safety protects the brand name.Branding is becoming more common in produce; in 1997, 19 per-cent of retail produce sales were branded products, compared withonly 7 percent in 1987 (Kaufman et al., 2000).

17 In 2001, USDA’s AMS began a pilot program offering third-party audits for produce in several States, the Fresh Produce AuditVerification Program (AMS, 2002). The AMS audits are similar toprivate audits. The AMS program does not seek to influence thethird-party audit industry, just to provide another source of thesame service. The program is run through the State departments ofagriculture. AMS has inspectors at shipping-point locations andhas experience working with growers. This program grew out of arequest from New Jersey growers. Currently, the program isoffered in New Jersey, California, and Oregon. It is just starting inWashington and Florida. The cost of an AMS audit is similar tothose offered by the private sector. The typical audit takes 5-6hours. In California, an audit costs $65 per hour plus $31 per hourin travel costs (The Packer, 2002b).18 This concern has become more obvious in the import alert forMexican cantaloupe, which states that FDA will conduct their owninvestigations and not rely solely on third-party audits. This is sim-ilar to FDA conducting audits of Guatemalan raspberry farms inthe early stages of the MPE program.

about the chances of contamination on another day.Tests of water from wells that are protected from sur-face contamination are more helpful; for example, ayearly sample from such a well might be sufficient todetermine the overall water quality.

Growers have another reason to adopt GAPs and usethird-party audits. In 1999, Safeway, the third largestU.S. food retailer, expanded their food safety programto require all their suppliers of certain commodities toverify that they follow government food safety stan-dards and specifications in production and packing.Some other retailers have followed suit. To qualify as aSafeway supplier, a grower must have an independentthird-party auditor verify that they are using GAPs forproduction and GMPs for packinghouses. Requiringverification of use of GAPs and GMPs was a new ideaand met with initial opposition. Domestic and importedproduce sold by Safeway must meet the same standards.Research covering a select group of U.S. fruit and veg-etable shippers indicates that in 1999, almost half ofthose studied provided third-party audits for GAPs orGMPs for at least one of their buyers. While shipperswere not always happy about complying with thisrequest, most indicated that they would implement veri-fication programs in response to changing buyer prefer-ences (Calvin et al., 2001).

In each of the case studies, shippers tried to distancethemselves from those associated with a food safetyproblem. Shippers can reduce their risk by requiringgrowers to provide third-party audits or by droppinggrowers with less sophisticated food safety programsor more challenging environments. The problems inGuatemala may have helped the small but growingindustry in Mexico since shippers could satisfy mostof their needs with Mexican raspberries. Mexico can-taloupe growers may face a similar situation in thefuture if U.S. buyers decide to reduce their risks byswitching to Central American cantaloupe.

Grower Organization Response

Grower organizations have also been important forcesfor resolving food safety problems. Beginning in themid-1990s, the fresh produce industry became awareof the potential cost of food safety problems related tocontamination at the farm level. Many trace thisheightened awareness to the well-publicized 1996 out-break of E. coli O157:H7 that was traced to mesclun(lettuce mix) grown and packed on one small farm in

California. This was the first reported multistate out-break of E. coli O157:H7 associated with lettuce(Hilborn et al., 1999). It was also one of the earliestcases clearly identifying microbial contamination atthe farm level.

Concerned about potential government regulation,the Western Grower’s Association, which representsthe California and Arizona produce industry (including almost all U.S. lettuce production), and theInternational Fresh-cut Produce Association, took theinitiative and developed their own set of guidelines forfresh produce food safety. Similarly the CSC devel-oped its own set of guidelines following the raspberrycontamination problem in 1996. FDA’s GAP guide-lines published in late 1998 built, in part, on these ear-lier industry efforts.

One grower organization has been active in providingguidance to the third-party audit industry. The UnitedFresh Fruit and Vegetable Association has developed atraining program on food safety auditing. Growerswere concerned that some auditors experienced only inindoor audits were unfamiliar with the produce indus-try and outdoor settings where some factors cannot becontrolled. This program also serves a need for contin-uing education for growers interested in evaluatingtheir own food safety programs.

Grower organizations have become more concernedabout the reputation of their crops for food safety. Avery large and important firm may be able to maintainits reputation despite the actions of others in the indus-try, but most firms must rely on the overall reputationof the industry. Retail buyers may know that a particu-lar firm has never been associated with an outbreak,has a strong food safety program, and has successfulthird-party audits for adherence to GAP principles, butconsumers generally do not have that great a knowl-edge of the industry. News reports of an outbreak asso-ciated with a particular grower may affect consumerperceptions about all growers of that product in thatsame area or anywhere else.

A grower organization’s effort to build a reputation forfood safety is a public good. At least in the short run,everyone benefits from the reputation for safety even ifthey are not investing in improved food safety. In eachof the three cases studied, grower organizations havefocused on developing systems to trace products fromfinal selling point back to the grower, which encour-ages grower responsibility and reduces the free-rider

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problem.19,20 In the case of an outbreak, a growerorganization that encourages traceback can prove tothe public that their product is not responsible for theproblem. Or, where the industry is responsible for theoutbreak, the responsible grower or growers can beidentified and damage can be limited.

In the raspberry case, the Guatemalan food safety pro-gram with its traceback and traceforward capabilitiesis mandatory. With the California StrawberryCommission, the Quality Assurance Food SafetyProgram is voluntary but the Commission is confidentthat all shippers use some sort of traceback, althoughthe degree of sophistication varies. The Baja Californiastrawberry growers appear to follow the CaliforniaStrawberry Commission’s program closely. In the caseof cantaloupe, the California Cantaloupe AdvisoryBoard’s traceback program is mandatory. Mexico’snew cantaloupe food safety program with enhancedtraceback is also mandatory.

This level of traceback capability may not be represen-tative of other industries who have not yet faced foodsafety problems, even though traceback capability isan integral part of GAPs. The difficulty of implement-ing a traceback program may vary by crop because ofparticular harvesting or marketing practices. For exam-ple, products that are packed in the field can easily belabeled with the origin of the product. If products areharvested and then packed in a central facility, a littlemore care is required to maintain traceability. Cropslike tomatoes present a particular traceability chal-lenge. They are often harvested, packed, and then sentto repackers where tomatoes from several producersmay be commingled before being resorted by maturity.

Government Response

FDA’s most important contributions to improving foodsafety for produce is the development of guidelines for

food safety practices. The value of GAPs will increaseas science provides more answers regarding how toreduce risk of microbial contamination.

Because it is so difficult to identify microbial contami-nation on produce, FDA cannot rely on random testingat the border to detect contaminated produce. FDAwill do inspections when there is reason to think theremight be a problem. Because of the problems withcantaloupe in recent years, FDA conducts microbialtesting on imported and domestic cantaloupe. Insteadof focusing on testing, FDA has concentrated much ofits efforts on education in foreign countries. All effortsto solve food safety problems abroad reduce the bur-den on the consuming public and on the FDA andCDC, which investigate outbreaks. In 1997, FDA spent6,274 hours investigating the Cyclospora-contaminatedraspberries (U.S. GAO, 1999).

When invited by a foreign government, FDA will visitindividual farms associated with contamination prob-lems and identify practices that are not consistent withGAPs. Findings compiled from these visits are used toidentify trends for future training and guidance develop-ment. FDA, in association with the University ofMaryland, teaches food safety practices in the UnitedStates and abroad through the Joint Institute of FoodSafety and Applied Nutrition. This program has pro-vided classes on GAPs. In addition, FDA provides train-ing for conducting farm investigations. In 2002, FDAconducted several training courses in Mexico on how todo farm investigations for produce.

When an outbreak is associated with imported pro-duce, FDA must determine whether the problem canbe easily solved or whether the individual firm orcountry should not be allowed to ship to the UnitedStates until the problem is fixed. Traditionally, FDArelies on laboratory identification of pathogens on aproduct before making decisions on withdrawing aproduct from the market or banning its import. This isa problem for fresh produce, which is rarely availablefor analysis when an outbreak develops. Over time,FDA has become more comfortable with making deci-sions based on epidemiological evidence alone. TheCyclospora case in Guatemala was the first big pro-duce case that relied solely on epidemiology. TheMexican Salmonella case demonstrates again thereliance on epidemiology.

The role of FDA varies depending on the case. ForGuatemalan raspberries, FDA eventually banned allimports because an individual farm could not be iden-

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19 Even before recent food safety problems and emphasis on usingGAPs, some firms voluntarily adopted traceback programs as agood business practice.20 The Federal Government does not currently require traceback nor monitor voluntary activities (Golan et al., 2002). However,the newly enacted Public Health Security and BioterrorismPreparedness and Response Act of 2002 will eventually requiresome traceability capability (FDA, 2002). Although farmers areexempt, shippers and most other firms in the distribution channelwill be required to be able to identify where any product came fromand where it went to (“one up, one down”). FDA must publish theirregulations for establishing this system by December 12, 2003.

tified and the problem seemed pervasive. FDA andCDC sent researchers to Guatemala to investigate theindustry and provide assistance in developing a pro-duction system to minimize the potential of microbialcontamination. FDA’s role in the Mexican strawberrycase appears to have been limited at the farm level,particularly since no one could determine where thecontamination occurred. In this case, however, thestrawberries were processed so FDA was involved inthe recall of the processed product. With a fresh prod-uct, there is often no product to recall. In the Mexicancantaloupe case, FDA first issued import alerts forthree firms selling cantaloupe associated withSalmonella outbreaks. In late 2002, FDA banned allcantaloupe imports from Mexico. FDA is evaluatingpetitions from individual Mexico growers for exemp-tion from the ban.

State organizations, such as the California Departmentof Food and Agriculture, are also involved in foodsafety outreach programs to producers in other coun-tries. Again, the motivation is self-interest since con-tamination problems traced to imports can have suchnegative impacts on U.S. producers.

As the case studies demonstrate, in most cases foreigngovernments have tried to resolve food safety problems,although perhaps not as aggressively as desired by theUnited States in the early stages. In Guatemala, the gov-ernment became involved in the GBC’s efforts todevelop a workable and enforceable food safety plan. Inthe strawberry case, the industry in Baja Californiaacted almost as a part of the U.S. industry and benefitedin an indirect way from food safety initiatives of theCSC. Mexican government activities appear to havebeen limited to the state level in that case. In November2002, the Mexican government put into place a foodsafety program to try to resolve the cantaloupe problem.

Conclusions

Food safety and produce trade are clearly compatible;the vast majority of imports are never associated withfood safety outbreaks. Producers in the United Statesand foreign countries, grower organizations, govern-ments, and commercial buyers are actively involved inimproving food safety.

Producers are self-motivated to provide safe producebecause of the financial consequences of an outbreaktraced back to their operation. Of course, there arealways some cases where people will not invest suffi-

ciently in food safety practices because they think theirproduct is safe or they deliberately cut corners. As trace-ability improves, however, the probability that responsi-bility for contaminated food will fall on those farmerswith inadequate food safety programs will increase.

Grower organizations are motivated because of the public good nature of a product reputation. Since an outbreak anywhere can have a negative impact on con-sumers’ perceptions of the product, grower organizationsmust do something to try to reassure the public that theirproduct is safe and distinguish themselves from othergroups of growers associated with a problem.

Fears of economic and reputation losses if a contami-nated produce item is traced to their firm motivateretailers and other commercial buyers to demand highfood safety standards. Buyers want to know about agrower’s food safety plan. Some demand third-partyverification of compliance with GAPs and GMPs.

In the United States, FDA encourages farmers to followguidelines to reduce microbial contamination in pro-duce. It does have the power to impose mandatory foodsafety programs if necessary. With respect to trade,FDA restricts imports from individual firms or all pro-ducers in a region or country when food safety prob-lems cannot be resolved. FDA has been active inpromoting improved food safety abroad. In both Mexicoand Guatemala, microbial food safety programs havetraditionally been voluntary. Government programsbecame mandatory for the particular products after foodsafety problems resulted in U.S. import alerts.

There is no reason to think that this trend toward moresophisticated food safety programs is any more diffi-cult for foreign growers to cope with than for domesticgrowers. However, increased concerns about microbialfood safety programs pose particular challenges forsmaller farmers in both the United States and foreigncountries. When there are food safety problems, thecosts of production increase for everyone producingfor the U.S. market. New fixed costs, such as purchas-ing a water filtration system, would be particularlyproblematic for small producers spreading the cost ofthe new investment over smaller volume of output.Also, smaller farmers (or geographically dispersedfarmers) might not be able to support the growerorganizations that have been so important in resolvingfood safety problems.

The case studies show that failure to resolve food safetyproblems quickly can have serious impacts on an indus-

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try and trade. A major policy challenge is to determinewhen government intervention may be required toresolve a problem. Science is not as definitive as desiredwhen trying to make decisions about trade and foodsafety. While some practices clearly increase the proba-bility of microbial contamination, it is often difficult forFDA and others to identify the source of contaminationand the new practices that would yield safer food. Thereis a chance that too aggressive a stance would unneces-sarily restrict international trade when using GAPsmight resolve the problem in the next season. In thehepatitis A outbreak linked to strawberries, if the con-tamination occurred in Mexico, use of GAPs alone mayhave been sufficient to solve the problem (or it may be asporadic problem that might pop up again in the future).Restricting trade can be economically devastating for anindustry, as in the Guatemalan raspberry case. However,the raspberry and cantaloupe cases show that it can takeseveral years to resolve a problem and in both cases theforeign governments intervened. In these cases a moremoderate response may be inadequate, leading to moreoutbreaks and economic losses in affected industries.

In each case, damage was not limited to the producersof the contaminated product. Anyone producing a prod-uct for the U.S. market, including U.S. growers, maybe caught in the consumer backlash against a productand will probably have to adopt more stringent foodsafety programs. Given the widespread impacts of foodsafety outbreaks, there may be opportunities for growerorganizations in different countries to organize jointefforts to resolve problems. Organizations would haveto weigh the negative fallout of a food safety problemoriginating with their competitors against the potentialgain if their competitors’ sales were restricted. Thecosts and benefits would vary by industry.

The case studies show the actions of growers, growergroups, and governments caught up in foodborne ill-ness outbreaks. Future research should investigate whatother sectors of the produce industry, which have notyet faced the economic disruption of a foodborne ill-ness outbreak, are doing to prepare for the possibility.

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96 ● International Trade and Food Safety / AER-828 Economic Research Service/USDA