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Infectious Disease Movement in a Borderless World: Workshop Summary 2 Travel, Conflict, Trade, and Disease OVERVIEW The essays collected in this chapter examine how travel, armed conflict, and trade move people—as well as animals, plants, and products made from them—and how these movements influence patterns of infectious disease transmission. The discussion begins with an exploration of the role of the global traveler in the emergence of infectious disease by workshop speaker Mary Wilson of Harvard, who illustrates the profound impact of recent increases in the volume, speed, and reach of global travel. “Humans can reach almost any part of the earth today within the incubation period for most microbes that cause disease in humans,” Wilson writes. “Travel is also discontinuous, often including many stops and layovers along the way. This means that travelers are part of the dynamic global process of moving biota, along with trade, which moves plants, animals, and other materials.” Moreover, she observes, several other trends—including growth in human and food animal populations and urbanization—further contribute to infectious disease emergence. Travelers can serve as sentinels for disease, and thereby contribute to the global disease surveillance system, as Wilson demonstrates through key findings by the decade-old GeoSentinel Surveillance Network regarding transmission of falciparum malaria and dengue fever. The network gathers information on ill international travelers and migrants from 42 travel and tropical medicine clinics on six continents in order to provide early alerts about unusual infections or infections in unusual locations or populations. Studying travelers can help characterize “global microbial traffic,” Wilson concludes. Travel, migration, and displacement are significant characteristics of armed
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Infectious Disease Movement in a Borderless World: Workshop Summary conflict that contribute to increased risk of infectious disease. Certain categories of infectious diseases tend to increase during war, according to workshop speaker Barry Levy of Tufts University; these include diarrheal diseases and acute respiratory infections, as well as measles, malaria, meningococcal disease, and tuberculosis. In the chapter’s second paper, Levy discusses major causes—apart from injury—that contribute to the increased incidence of infectious diseases during wartime: reduced availability of health services, environmental damage, and forced migration. Interestingly, Levy notes that whereas one might expect HIV transmission to increase during war due to concomitant increases in several risk factors for its transmission, “several studies have demonstrated that HIV incidence has generally decreased during war—only to increase again after conflict has ended.” Moreover, he adds, “there have been many successful HIV/AIDS prevention and treatment programs during armed conflict.” Absent the cessation of armed conflict, the war-related burden of infectious disease can be addressed through attention to specific war-associated risk factors, as well as through a host of measures (e.g., surveillance, preparedness) that apply to any high-risk situation, Levy explains. He also notes the importance of protecting health care workers and preserving health-supporting infrastructure, which may be supported by maintaining their neutrality both during war and in its aftermath. Like travel, globalized trade is vast, rapid, on the rise, and a significant risk factor for infectious disease emergence. In the chapter’s third essay, workshop speaker Ann Marie Kimball, of the University of Washington, and co-author Jill Hodges present case studies of several emerging infectious diseases, including H5N1 influenza and bovine spongiform encephalopathy (BSE), and their relationship to “risky” trade practices in food production and medicine. “While microbial risks have been globalized along with commerce, the corresponding health and protective measures for the most part have not,” the authors observe. The International Health Regulations (IHR) 2005 “provides some important safeguards to help limit the international spread of infectious disease,” they note, but these regulations require support for both capacity building and community building if their intent is to be fulfilled. Responding to some of the disease threats described in the previous three essays is the daunting task taken on by workshop speaker David Acheson of the Food and Drug Administration (FDA). He describes the agency’s response to two recent challenges to the security of the U.S. food supply—the 2008 outbreak of Salmonella Saintpaul and the deliberate contamination of imported wheat gluten with melamine—in his contribution to this chapter. He also discusses changes in FDA’s food security efforts to respond to such threats by seeking to understand where and when they arise, to anticipate their potential to spread globally, and to use risk-based inspections to detect them before an outbreak occurs in the United States; these include efforts under way to increase the FDA’s presence in foreign countries, to develop model systems for risk-based inspections, and to make use
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Infectious Disease Movement in a Borderless World: Workshop Summary of inspection and testing data generated by industry or other “third parties” to increase the breadth and depth of their surveillance. GLOBAL TRAVEL AND EMERGING INFECTIONS Mary E. Wilson, M.D., F.A.C.P., F.I.S.D.A.1 Harvard University Humans travel in numbers and at speeds unprecedented in history (IOM, 2003; Wilson and Chen, 2008). Travelers visit remote areas as well as major population centers. Humans may be displaced because of social, economic, or political upheavals or extreme events and environmental disasters (IOM, 2008). The elimination of spatial and temporal barriers, especially by long-distance air transport, means that humans can reach almost any part of the Earth today within the incubation period for most microbes that cause disease in humans. Travel is also discontinuous, often including many stops and layovers along the way. This means that travelers are part of the dynamic global process of moving biota, along with trade, which moves plants, animals, and other materials (Wilson, 1995b). Natural movement of animals via migration, and transport of seeds, microbes, and other materials via water and air currents, is the backdrop against which massive travel and trade are occurring in today’s world (Wilson, 1995a). One consequence of this movement is the juxtaposition of species that have never before had physical proximity. The contact between microbes, humans, and animals may result in infection, which may or may not be expressed in disease or death. Another potential consequence of the movement of species, such as arthropods, mammals and other animals, and plants, whether intentional or inadvertent, is the establishment of species in new geographic areas (Tatem et al., 2006). These introductions may cause major changes in the existing ecosystem, including marine ecosystems. Many examples exist of the harmful effects of invasive species, though many species of well-regarded plants and animals in the Americas were not native to the Americas (Crosby, 1972). Characteristics of Global Travel Global travel has increased as reflected in Figure 2-1, showing numbers of international tourist arrivals from 1950 though 2005 and the projections until 2020. In addition to the marked increase in the overall number, there has also been a shift in areas visited by travelers, especially to areas in Asia. The 2006 figures from the World Tourism Organization showed the most rapid relative increase was to sub-Saharan Africa (UNWTO, 2008b). Travel between regions 1 Associate Professor of Global Health and Population, Harvard School of Public Health; Associate Clinical Professor, Harvard Medical School. E-mail: email@example.com.
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-1 International tourist arrivals by region (in millions), 1950-2020. SOURCE: Reprinted with permission from UNWTO (2008a). was increasing faster than travel within regions, and air transport was growing at a faster pace than ground and water transport. Figure 2-2 shows the breakdown by means of transport, with air travel accounting for 46 percent of transport (UNWTO, 2008). The shifts in destination mean more people will be traveling to low-latitude countries—areas with greater species richness (Guernier et al., 2004) and often characterized by poor sanitation and limited infrastructure, a milieu where risk for exposure to common and previously unidentified microbes may be higher. In looking ahead, it is unclear to what extent the current dramatic changes in the global economy will affect numbers of travelers or favored destinations. Political instability and disease outbreaks can also influence travel destinations, sometimes abruptly. A vivid example of the rapid increase in travel is the outline of lifetime tracks by David Bradley (1989; figure also reproduced in Cliff and Haggett, 2004), who recorded the life travel over four male generations in his own family (Figure 2-3). The linear scale for the spatial movement increases by a factor of 10 for each generation (Cliff and Haggett, 2004). Similar findings were noted in a study which showed that spatial mobility, taking into account all forms of transportation, of the French population between 1800 and 2000 increased 1,000-fold (Grubler and Nakicenovic, 1991). Using numbers from the U.S. Census Bureau and the United Nations World Tourism Organization (UNWTO, 2008c), one can calculate that the world population between 1950 and 2007 increased 2.6-fold, whereas the international tourist arrivals increased 35-fold. Although individuals
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-2 Inbound tourism by means of transport. SOURCE: Reprinted with permission from UNWTO (2008a). on average are traveling much greater distances, González and colleagues found that individual human trajectories showed high degrees of temporal and spatial regularity, with individuals returning to a few highly frequented locations (González et al., 2008). Population Size, Density, Location, and Proximity to Animals This increase in human movement is not occurring as an isolated event. Today, the global human population is the largest ever recorded—and so is the population of food animals. About half of the people on Earth live in urban areas, the largest fraction ever (Wilcox et al., 2008). These human hosts provide expanded opportunities for viral replication and mutation events. Most of the population and projected growth are in low-latitude urban areas—regions that are home to sprawling megacities, many surrounded by vast slum areas that lack clean water and sanitary facilities (Figure 2-4). Animals such as dogs, chickens, cows, and rats live in and near human living quarters, which have been assembled from whatever materials can be found. Individuals who inhabit these areas often work in major metropolitan areas, so they have regular contact with large, dense human populations in high-rise buildings and other built environments. Residents
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-3 Life travel over four male generations in the same family. SOURCE: Adapted from Bradley (1989) and reprinted from Cliff and Haggett (2004) with permission from Oxford University Press. of periurban slums may also visit family in rural areas, thus potentially providing a link from rural to urban populations and to the rest of the world. Changes in the environment, including extreme weather events, can favor the appearance of some infections and can also displace populations (IOM, 2008). Animals have been the origin of many of the recently identified emerging infectious diseases, including HIV/AIDS, H5N1 avian influenza, severe acute respiratory syndrome (SARS) (Jones et al., 2008; Wang et al., 2008), and swine-origin H1N1 influenza A (Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, 2009; Smith et al., 2009a). Populations of animals have expanded rapidly, in large part to accommodate the desire for more animal protein in the diet, which has coincided with the economic resources to buy it. In China, for example, at the time of the 1968 influenza pandemic, the size of the human population was 790 million, the pig population 5.2 million, and the poultry population 12.3 million. By 2005, while the human population in China increased less than two-fold, the pig population increased about 100-fold to 503 million and the poultry population increased 1,000-fold to 13 billion (Osterholm, 2005).
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-4 Juxtaposition of urban slums and modern buildings in São Paulo, Brazil. SOURCE: Image courtesy of Zema Fontoura. Concentrated animal feeding operations, where large numbers of genetically similar animals are raised in concentrated areas—so-called factory farms—are becoming increasingly common in the United States and other countries (Pew Commission, 2008). Unfortunately, little systematic surveillance of influenza and other potential pathogens in swine populations is routinely done, a shortcoming highlighted by the emergence and spread of a reassortant influenza in 2009 (Smith et al., 2009a). Roles of the Traveler Human travelers can easily carry person-to-person transmitted infections to any part of the world. An example is the human immunodeficiency virus (HIV), which was introduced to all areas of the world almost exclusively by travelers (Perrin et al., 2003). Recently, swine-origin H1N1 has spread globally, its movement hastened by global air travel. Although drug-resistant forms of tuberculosis can emerge in settings with inadequate and inappropriate treatment regimens, humans also transport and transmit tuberculosis, including multidrug resistant (MDR) and now extensively resistant (XDR) forms of tuberculosis, in geographic areas far from the point of acquisition (Jassal and Bishai, 2009; Oeltmann et al., 2008). Although tuberculosis is an old disease and is present worldwide,
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Infectious Disease Movement in a Borderless World: Workshop Summary the incidence of infection and the levels of drug resistance vary enormously by population and geographic area. In 2008, the overall incidence of tuberculosis in the United States was 4.2 cases per 100,000 population (CDC, 2009). The rate in persons who were foreign born was 10 times higher than the rate in persons who were U.S. born, reflecting the vast differences in rates of tuberculosis around the world. A number of countries have annual incidence rates exceeding 300 per 100,000. Figure 2-5 displays the geographic spread of XDR tuberculosis between December 2006 and June 2008. The traveler can serve in many roles (Wilson, 2003). Nonimmune travelers are at risk for a number of infections that exist primarily in tropical areas. Vaccines and drugs are available today to reduce the risk for many of these infections, such as yellow fever and malaria. Travelers were important historically in the spread of infections and remain so today, perhaps to an even greater extent (Colizza et al., 2006). They can also carry microbes with resistance genes, even if they are unaware of it. Travelers today continue to spark outbreaks of measles in populations that do not have high levels of immunity. It is easy to see how travelers could play a key role in the global epidemiology of infections that are transmitted from person to person, such as HIV, SARS, tuberculosis, influenza, and measles (Hufnagel et al., 2004), but they are also important in the spread of some vector-borne infections, as will be discussed below. Receptivity to Introductions Geographic areas and populations vary in their receptivity to introductions of potential pathogens that can cause human disease. Multiple factors are in play. The physicochemical environment may preclude the presence of a necessary mosquito vector or essential intermediate host. The physical environment may also influence transmission dynamics. For example, influenza has a strong seasonal pattern, especially in temperate regions. This seasonality is influenced by the humidity; recent studies suggest that absolute humidity is a more useful measure than relative humidity. The absolute humidity affects influenza virus transmission and virus survival. Absolute humidity can explain 90 percent of the variability of influenza virus survival, whereas relative humidity can explain only 36 percent of variation (Shaman and Kohn, 2009). Hence, travelers with influenza returning to temperate areas during hot, humid months are unlikely to spark epidemic spread (Lowen et al., 2008), though focal outbreaks in contained, air-conditioned spaces (e.g., air-conditioned nursing homes and barges) have been reported during hot, humid weather. Influenza outbreaks in the Southern Hemisphere occur during hot-weather months in the Northern Hemisphere; in the tropics influenza can circulate throughout the year. Analysis of H3N2 epidemics worldwide between 2002 and 2007, including those in temperate regions, suggested that they were seeded annually by viruses that had first appeared in East and Southeast Asia (Russell et al., 2008). These viral strains appeared to have evolved from other Asian strains.
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-5 Countries with XDR tuberculosis cases in December 2006 and June 2008. SOURCE: Reprinted from Lancet Infectious Diseases, Jassal and Bishai (2009), with permission from Elsevier. Copyright 2009.
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Infectious Disease Movement in a Borderless World: Workshop Summary Other local factors that affect the receptivity of individuals and a population to introduction of a new infection include housing, sanitation, and living conditions. Good nutrition can reduce the vulnerability to some infections or diminish their severity. Populations may be immune because of vaccination or prior infection. Human behavior and activities influence exposure to a number of infections (e.g., sexually transmitted infections). And finally, good surveillance and wider access to good medical care may reduce the burden of an infection in a population and allow it to be brought under control. In addressing the question of how controllable an infection is that is directly transmitted from person to person, a key factor is the proportion of transmission that occurs before onset of symptoms or during asymptomatic infection (Fraser et al., 2004). Public health measures are most likely to be effective when little or no infection is transmitted during asymptomatic infection. Figure 2-6 displays four FIGURE 2-6 How controllable is an infection? Plausible ranges for the key parameters R0 and θ for four viral infections of public concern are shown as shaded regions. The size of the shaded area reflects the uncertainties in the parameter estimates. SOURCE: Fraser et al. (2004).
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Infectious Disease Movement in a Borderless World: Workshop Summary infections that are transmitted from person to person: SARS, smallpox, influenza, and HIV. Fortunately, the fever caused by infection with the SARS coronavirus preceded onset of transmissibility, meaning that with strict surveillance for symptoms and isolation of those with symptoms, it became possible to interrupt the transmission of this infection. Influenza, on the other hand, is more difficult to contain because transmission may begin before onset of symptoms, and infected patients may have little or no fever. Based on epidemiological analyses, Fraser et al. (2009) estimated the basic reproductive number of the swine-origin H1N1 influenza A virus in the range of 1.4 to 1.6. Vector-borne Infections Vector-borne infections can also be introduced into new geographic areas by travelers, though the vulnerable areas are restricted to those with competent mosquito or other arthropod vectors. Because important vectors, such as Aedes aegypti and Aedes albopictus, can be dispersed by trade (especially via ships), more human-inhabited areas of the world are infested with these potential vectors than ever before (Tatem et al., 2006). Aedes aegypti thrives in an urban environment, and today about 2.5 to 3 billion people live in tropical and subtropical areas infested with this mosquito. Two vector-borne infections, dengue fever and chikungunya infection, which have expanded in distribution in recent years, illustrate multiple contributions to this dynamic process and spread. Dengue virus is causing more infections, including more cases of severe and complicated dengue fever, than ever before (Wilder-Smith and Gubler, 2008). Although multiple factors contribute, three forces described above are especially important: urbanization with major expansion of populations living in tropical and subtropical areas; population size; and rapid, frequent travel of viremic humans to areas infested with competent vectors. Lax vector control programs and urban settings that lack piped water (so residents must store water in their homes) and are littered with used tires, discarded plastic cups, and other trash with standing water that allow breeding of mosquito vectors exacerbate the problem. Today, the dengue viruses have a much larger host population in which to replicate, recombine, and mutate than ever before, given the size of the human population. Zanotto and colleagues (1996) found that the number of dengue lineages has increased roughly in parallel with the size of the human population over the past 200 years (Figure 2-7). More urban areas in tropical and subtropical regions now have a population size large enough (estimated to be between 150,000 and 1 million) to allow the ongoing circulation of dengue viruses. An increasing number of geographic areas are experiencing cocirculation of more than one dengue serotype, setting the stage for secondary infections and more severe disease.
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-13 Salmonella Saintpaul outbreak traceback and distribution. Partial view of the traceback and distribution of peppers from Mexico, July 16-22, 2008. SOURCE: FDA (2008b).
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Infectious Disease Movement in a Borderless World: Workshop Summary with increasing frequency, can best be prevented and addressed. The investigation led us to a distributor in McAllen, Texas, where we found positive pepper samples. They had received their jalapeno peppers from a packing facility in Nueva Leone, Mexico, so we returned to an entirely different part of that country to inspect pepper farms. On July 30, we found the outbreak strain, Salmonella Saintpaul, in irrigation water and on remaining peppers on a farm in Tamaulipas, Mexico. Melamine in Pet Food This investigation began with reports of sick pets from consumers, and also from a pet food company whose research animals developed kidney failure following routine taste tests (FDA, 2008a). The only associated change in pet food formulation was the source of the wheat gluten it contained. Once this was recognized, we soon determined that scraps from affected pet food manufacturers were being used to produce food for livestock, which could in turn introduce the adulterant into foods consumed by humans. Thus, melamine was traveling up the food chain, beginning with food ingredient manufacturers, and onward to feed mills, to poultry farms and hog farms, and from there to chicken and pork in supermarkets. A joint risk assessment was conducted between the FDA and the U.S. Department of Agriculture (USDA) to determine if the levels in poultry and pork were of a concern to public health. The assessment concluded the levels were not a public health concern. We also discovered that not only was this wheat gluten coming into the United States, but a U.S. company was also importing it to Canada. We alerted the Canadian authorities, who found that the gluten was being used there to make fish feed that was being shipped back into the United States. The complete U.S. distribution chain of the melamine-contaminated wheat gluten is shown in Figure 2-14. It makes the point that contaminants—including pathogens—connected to food may be disseminated through vast and complex systems that profoundly affect international trade and economic relationships, as other workshop participants noted. Time for a New Approach In light of these complexities, the FDA is attempting to change its approach by becoming more proactive in addressing food safety by addressing the whole supply chain. One important route to this goal is to conduct targeted, risk-based inspections, but these may be difficult to identify. Risk-based inspections are dependent on having adequate data, analytical capabilities, and inspectors. Currently such inspections are conducted at ports of entry, where it is decided whether a given product made in a foreign country and shipped to the United States will be inspected or tested for chemical or microbiological contamination, based on the various factors such as the nature of the product, its origin and
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 2-14 Sequence of events—different routes of melamine-contaminated wheat gluten into the United States. SOURCE: Food and Drug Administration. destination, and the past inspection history of similar products. This procedure, euphemistically called a “snapshot,” examines only one point in the distribution chain: importation. In the future, our goal is to gain greater assurance for the complete supply chain—from grower to manufacturer to shipper to importer to distributor to retailer—of imported food products. This is going to require a multifaceted approach that includes more inspections. There are significant challenges and scarce resources for pursuing inspections of overseas growers and manufacturers, among them the sheer numbers (approximately 200,000, as previously noted) of registered foreign food facilities. There is no way, despite some peoples’ wishes, that we could inspect and sample every import at the port of entry. Rather, we must try to optimize inspection based on risk. We cannot simply test or inspect our way to safe food and having appropriate preventive controls throughout is a key step. Risk-Based Inspections To pursue a risk-based approach to food safety, we need leverage with foreign governments and with industry in order to gather information on the status of foreign growers, manufacturers, and foreign governments. Using these data, we must conduct effective analyses to inform risk-based decisions at the port of
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Infectious Disease Movement in a Borderless World: Workshop Summary entry. Finally, rather than determining whether to examine food products on a case-by-case basis, we need to build a decision-making system. We are currently using a prototype of such a system, which we call PREDICT, to maximize the use of FDA data in making risk-based decisions. PREDICT software allows the FDA to make risk-based decisions for import inspections and has the capacity to receive new datasets as other data streams come online. A pilot project, conducted in the Port of Los Angeles, employed PREDICT to make inspection decisions regarding seafood, for which clear inspection standards had already been established. In this trial, PREDICT prompted inspectors to detect contaminated foods more frequently than did the existing inspection system (known as OASIS). The FDA is currently attempting to expand PREDICT, recognizing that this system is only as good as the data provided to it. Increased Foreign Presence Another way the FDA is supporting a more proactive stance on addressing threats to the globalized food supply is by establishing a greater foreign presence. To that end, we recently opened three offices in China—in Beijing, Shanghai, and Guangzhou—staffed by about a dozen permanent FDA employees. Although their staffs are too small to conduct significant numbers of inspections, these foreign offices will be able to strengthen relationships with the Chinese government that will improve our ability to exchange information and deal with contamination issues as they arise, and potentially before they become problems for the United States. In order to situate FDA personnel throughout the world, we are opening similar outreach offices in New Delhi and Mumbai, India; in central South America; and in Europe. Increased Inspections Currently the FDA performs between 100 and 155 inspections of foreign food manufacturers per year. We plan to perform 1,000 such inspections per year by 2011. While we recognize that we cannot inspect our way to safe food, we think that targeted inspections associated with the most potentially risky products are an important move forward. Use of Third-Party Data The food industry extensively inspects and tests foods that are imported into the United States. Can the FDA make use of this information? Recognizing that this is a potentially contentious issue (see below), our goal is to examine the process surrounding third-party certifications and determine how the FDA can use that information to better protect the public and make maximal use of resources. One aspect of this is to use standards for third parties that provide information
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Infectious Disease Movement in a Borderless World: Workshop Summary supplied to the FDA, whether it is derived from state agencies, foreign governments, or private third parties. We then want to be able to use that information to inform the risk-based inspection process. Currently, the PREDICT model at ports of entry operates primarily on U.S. compliance data. Incorporating inspection data and information from overseas and from industry into our analyses should improve our ability to make risk-based decisions. Ensuring Confidence Any risk-based decision-making system that employs third-party data must be completely transparent, and it must be clear that providing data to the FDA will not enable industry or importers to bypass inspections at the port of entry. In order to increase confidence in such a system by all stakeholders—which include companies, consumers, regulators, and Congress—the FDA issued a guidance document in January 200912 describing attributes that a third-party certification program should have in order for the FDA to have confidence in the quality of the audit conducted by the program. It also provides information on the certification process, including guidance on application, certification, recertification, and withdrawal of certification. In order to determine how such a third-party certification program might operate, the FDA has established a pilot program focused on aquacultured shrimp. We issued a Federal Register Notice13 asking for volunteers among companies that import shrimp into the United States to submit an application to this certification program. By processing these applications, we hope to determine infrastructure needs for handling these kinds of data, find out whether importers can meet our data standards, and establish processes for evaluating third-party certification programs. This pilot program does not guarantee entry into the U.S. market by participating shrimp importers. We are not using the data they provide to make importation decisions; rather, this pilot study should identify strengths and weaknesses in our developing third-party certification program and help us learn how to make such a program transparent and credible. Conclusion The regulatory challenges involved in providing safe food to the United States will increase as globalization of the food system continues. The complexities of the food supply are enormous, and there is considerable economic benefit in making food distribution as rapid and efficient as possible. It is therefore 12 Guidance for Industry Voluntary Third Party Certification Programs for Foods and Feeds. See http://www.fda.gov/oc/guidance/thirdpartycert.html. 13 See http://www.regulations.gov/fdmspublic/component/main?main=DocumentDetail&o=090000648066388c; Docket No.: FDA-2008-N-0382.
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