TY - JOUR
AU - Saif, L. J.
AB - ABSTRACT Members of the public are always somewhat aware of foodborne and other zoonotic pathogens; however, recent illnesses traced to produce and the emergence of pandemic H1N1 influenza virus have increased the scrutiny on all areas of food production. The Council for Agricultural Science and Technology has recently published a comprehensive review of the fate and transport of zoonotic pathogens that can be associated with swine manure. The majority of microbes in swine manure are not zoonotic, but several bacterial, viral, and parasitic pathogens have been detected. Awareness of the potential zoonotic pathogens in swine manure and how treatment, storage, and handling affect their survival and their potential to persist in the environment is critical to ensure that producers and consumers are not at risk. This review discusses the primary zoonotic pathogens associated with swine manure, including bacteria, viruses, and parasites, as well as their fate and transport. Because the ecology of microbes in swine waste is still poorly described, several recommendations for future research are made to better understand and reduce human health risks. These recommendations include examination of environmental and ecological conditions that contribute to off-farm transport and development of quantitative risk assessments. INTRODUCTION Animal manure management systems in the United States are designed to store, treat, and apply to land solid, semisolid, slurry, or liquid manure (i.e., urine and fecal material) on agricultural fields after removal from the animal environment. Manure processed in swine management systems is usually in liquid (1 to 4% solids), slurry (4 to 15% solids), or semisolid form, and land application most often involves spreading on fields as fertilizer (Dickey et al., 1981; Copeland and Zinn, 1998; Hill, 2003). The majority of these management systems are designed to reduce the concentrations of microbes found in swine manure by 90 to 99% or more (Sobsey et al., 2005) and to prevent off-farm transport of manure materials (i.e., nondischarge systems). The majority of microbes contained in swine manure are not pathogenic to humans (i.e., zoonotic). Nonetheless, the effectiveness of swine manure management systems to prevent environmental contamination with human pathogens is a concern because there are several putative environmental transmission pathways by which these zoonotic pathogens may be transported to water resources. Manure treatment systems may include multiple mechanisms of physical, biological, or chemical treatment of manure. Most treatment technologies used in swine production, however, rely on physical and biological treatment of manure to decrease nutrient and microbial concentrations before removal from the system. Table 1 provides some of the more commonly used waste management systems in swine production facilities. This review summarizes Council for Agricultural Science and Technology Special Publication No. 29, “Fate and Transport of Zoonotic Bacterial, Viral, and Parasitic Pathogens During Swine Manure Treatment, Storage, and Land Application” (Council for Agricultural Science and Technology, 2008). The Pork Check-Off commissioned this review to define the fate and transport of zoonotic pathogens after manure storage and land application to determine researchable knowledge gaps and to aid in developing research priorities related to pork production. Table 1. Waste management technologies used in swine production systems System1  Functional classification  Usage,2 %  Below-ground (deep pit) slurry storage  Storage of wastes  57.2  Solids separator  Physical treatment of wastes by removing solid fraction of slurried or semisolid wastes from liquid fraction  14.6  Single nonaerated lagoon  Storage and biological treatment of slurried or liquid wastes  22.8  Multistage nonaerated lagoon system  Storage and serial biological treatment of slurried or liquid wastes  38.6  Aerated lagoon  Storage and biological treatment of slurried or liquid wastes  0.4  Composting (including vermiculture)  Biological treatment of solid or semisolid fraction of wastes  6.7  Surface spreading or spray-field irrigation  Disposal of treated solid wastes  61    Disposal of treated semisolid wastes (surface spreading)  49.1    Disposal of treated liquid wastes (spray-field irrigation)  11.2  Subsurface soil injection  Disposal of treated slurried wastes  34.3  System1  Functional classification  Usage,2 %  Below-ground (deep pit) slurry storage  Storage of wastes  57.2  Solids separator  Physical treatment of wastes by removing solid fraction of slurried or semisolid wastes from liquid fraction  14.6  Single nonaerated lagoon  Storage and biological treatment of slurried or liquid wastes  22.8  Multistage nonaerated lagoon system  Storage and serial biological treatment of slurried or liquid wastes  38.6  Aerated lagoon  Storage and biological treatment of slurried or liquid wastes  0.4  Composting (including vermiculture)  Biological treatment of solid or semisolid fraction of wastes  6.7  Surface spreading or spray-field irrigation  Disposal of treated solid wastes  61    Disposal of treated semisolid wastes (surface spreading)  49.1    Disposal of treated liquid wastes (spray-field irrigation)  11.2  Subsurface soil injection  Disposal of treated slurried wastes  34.3  1Usage not reported for the following types of waste-handling systems: 1) confinement building under slat-scrape, gravity-drainage, or flush system (removal of semisolid, liquid, or slurried wastes from animal environment); 2) surface or subsurface flow constructed wetlands (biological treatment of liquid wastes), or 3) anaerobic digester (biological treatment of liquid and slurried wastes; methane production for energy recovery) technologies. 2Estimated percentage of US swine facilities using the system (USDA, 2002). Some facilities use more than one management technology, resulting in the total percentage exceeding 100%. View Large Table 1. Waste management technologies used in swine production systems System1  Functional classification  Usage,2 %  Below-ground (deep pit) slurry storage  Storage of wastes  57.2  Solids separator  Physical treatment of wastes by removing solid fraction of slurried or semisolid wastes from liquid fraction  14.6  Single nonaerated lagoon  Storage and biological treatment of slurried or liquid wastes  22.8  Multistage nonaerated lagoon system  Storage and serial biological treatment of slurried or liquid wastes  38.6  Aerated lagoon  Storage and biological treatment of slurried or liquid wastes  0.4  Composting (including vermiculture)  Biological treatment of solid or semisolid fraction of wastes  6.7  Surface spreading or spray-field irrigation  Disposal of treated solid wastes  61    Disposal of treated semisolid wastes (surface spreading)  49.1    Disposal of treated liquid wastes (spray-field irrigation)  11.2  Subsurface soil injection  Disposal of treated slurried wastes  34.3  System1  Functional classification  Usage,2 %  Below-ground (deep pit) slurry storage  Storage of wastes  57.2  Solids separator  Physical treatment of wastes by removing solid fraction of slurried or semisolid wastes from liquid fraction  14.6  Single nonaerated lagoon  Storage and biological treatment of slurried or liquid wastes  22.8  Multistage nonaerated lagoon system  Storage and serial biological treatment of slurried or liquid wastes  38.6  Aerated lagoon  Storage and biological treatment of slurried or liquid wastes  0.4  Composting (including vermiculture)  Biological treatment of solid or semisolid fraction of wastes  6.7  Surface spreading or spray-field irrigation  Disposal of treated solid wastes  61    Disposal of treated semisolid wastes (surface spreading)  49.1    Disposal of treated liquid wastes (spray-field irrigation)  11.2  Subsurface soil injection  Disposal of treated slurried wastes  34.3  1Usage not reported for the following types of waste-handling systems: 1) confinement building under slat-scrape, gravity-drainage, or flush system (removal of semisolid, liquid, or slurried wastes from animal environment); 2) surface or subsurface flow constructed wetlands (biological treatment of liquid wastes), or 3) anaerobic digester (biological treatment of liquid and slurried wastes; methane production for energy recovery) technologies. 2Estimated percentage of US swine facilities using the system (USDA, 2002). Some facilities use more than one management technology, resulting in the total percentage exceeding 100%. View Large BACTERIAL HAZARDS ASSOCIATED WITH SWINE MANURE Determining the environmental fate of bacterial pathogens from swine manure is extremely difficult. Biological variables include pathogen shedding by individual pigs; microbial interactions within stored manure; inoculation of stored manure each time a pig sheds pathogens; interactions with water, OM, aquatic plants, and plankton; and interactions with plants, nematodes, OM, and soil microorganisms after land application. Physical variables include type of manure storage, temperature and humidity during storage, soil type, temperature, moisture, water, pH, salinity, and rainfall events. The most studied aspect of this topic has been fecal shedding of pathogens, but understanding is still limited (USDA, 2002, 2005). Although some research indicates that pathogens in swine manure do not survive long after they are applied to the soil, other data contradict this, indicating relatively long survival times in soil and water (Table 2). There is a great need for good hypothesis-driven research to determine the factors that affect the environmental survival and persistence of zoonotic pathogens contained in swine manures. Table 2. Reported bacterial zoonotic pathogens found in swine wastes1 Bacterial pathogen  Prevalence,2 %  Survival,3 d  Swine waste  Stored wastes  Plants  Soil  Water  Salmonella  7.9 to 100  5.2 to 22  16 to 63  16 to 120  35 to 147  Enteropathogenic Escherichia coli  0 to 22  15.5 to 24  16 to 63  16 to 99  90  Campylobacter  13.5 to 73.9  10.34  16 to 63  8 to >32  2 to >60  Yersinia enterocolitica  0 to 65.4  04  Unknown  10  6 to 448  Listeria  16 to 19.8  0 to 19  42 to 128  ≤120  7 to 56  Bacterial pathogen  Prevalence,2 %  Survival,3 d  Swine waste  Stored wastes  Plants  Soil  Water  Salmonella  7.9 to 100  5.2 to 22  16 to 63  16 to 120  35 to 147  Enteropathogenic Escherichia coli  0 to 22  15.5 to 24  16 to 63  16 to 99  90  Campylobacter  13.5 to 73.9  10.34  16 to 63  8 to >32  2 to >60  Yersinia enterocolitica  0 to 65.4  04  Unknown  10  6 to 448  Listeria  16 to 19.8  0 to 19  42 to 128  ≤120  7 to 56  1Data are from Jones et al. (1976), Van Renterghem et al. (1991), Lund (1996), Guan and Holley (2003), Brandl et al. (2004), Bhaduri et al. (2005), Côté and Quessy (2005), Gütler et al. (2005), Hutchison et al. (2005a,c), Nicholson et al. (2005), Rostagno et al. (2005), USDA (2005), and Bhaduri and Wesley (2006). 2Prevalence = percentage of samples positive for the bacteria. 3Survival = length of time (in days) pathogen was detected on the soil or plant or in water. Detection of colonies of cultured organisms on agar media. 4Only one sample. View Large Table 2. Reported bacterial zoonotic pathogens found in swine wastes1 Bacterial pathogen  Prevalence,2 %  Survival,3 d  Swine waste  Stored wastes  Plants  Soil  Water  Salmonella  7.9 to 100  5.2 to 22  16 to 63  16 to 120  35 to 147  Enteropathogenic Escherichia coli  0 to 22  15.5 to 24  16 to 63  16 to 99  90  Campylobacter  13.5 to 73.9  10.34  16 to 63  8 to >32  2 to >60  Yersinia enterocolitica  0 to 65.4  04  Unknown  10  6 to 448  Listeria  16 to 19.8  0 to 19  42 to 128  ≤120  7 to 56  Bacterial pathogen  Prevalence,2 %  Survival,3 d  Swine waste  Stored wastes  Plants  Soil  Water  Salmonella  7.9 to 100  5.2 to 22  16 to 63  16 to 120  35 to 147  Enteropathogenic Escherichia coli  0 to 22  15.5 to 24  16 to 63  16 to 99  90  Campylobacter  13.5 to 73.9  10.34  16 to 63  8 to >32  2 to >60  Yersinia enterocolitica  0 to 65.4  04  Unknown  10  6 to 448  Listeria  16 to 19.8  0 to 19  42 to 128  ≤120  7 to 56  1Data are from Jones et al. (1976), Van Renterghem et al. (1991), Lund (1996), Guan and Holley (2003), Brandl et al. (2004), Bhaduri et al. (2005), Côté and Quessy (2005), Gütler et al. (2005), Hutchison et al. (2005a,c), Nicholson et al. (2005), Rostagno et al. (2005), USDA (2005), and Bhaduri and Wesley (2006). 2Prevalence = percentage of samples positive for the bacteria. 3Survival = length of time (in days) pathogen was detected on the soil or plant or in water. Detection of colonies of cultured organisms on agar media. 4Only one sample. View Large In 1999, the US General Accounting Office reported on waste management practices used in animal agriculture (US General Accounting Office, 1999), and Humenik et al. (2004) summarized environmentally superior technologies in swine production facilities. Whereas many of these practices emphasized limiting nutrient loading, runoff, and other ecologically sound practices, none specifically addressed the control of zoonotic pathogens, even though the US Environmental Protection Agency (1998) cited bacteria as one of the top 3 sources of impairment in rivers and estuaries. Zoonotic bacterial pathogens that have been associated with swine manure include Bacillus anthracis, Brucella spp., Campylobacter spp., Chlamydia spp., Escherichia coli, Leptospira spp., Listeria monocytogenes, Mycobacterium spp., Salmonella spp., and Yersinia spp. These pathogens may be transmitted either through direct contact with the manure or indirectly through the environment (Strauch and Ballarini, 1994; Pell, 1997). The most frequently studied enteric pathogens occurring in swine manure are Salmonella, E. coli, Campylobacter, Listeria, and Enterococcus. Lack of data on other bacterial pathogens in swine manure results from the difficulty in culturing and identifying them. Understanding the implications of the persistence of swine-associated zoonotic pathogens during storage, treatment, and land application is important for assessing and controlling their presence in the environment. Because the epidemiology (i.e., occurrence) of fecal shedding of the most common zoonotic bacterial enteric pathogens is well described elsewhere (USDA, 2002, 2005), this review focuses on the persistence of the best characterized bacterial pathogens (i.e., Salmonella, E. coli, Campylobacter, Listeria, and Enterococcus) contained in stored swine manure (Jones et al., 1976; Anugwa et al., 1989; Davies et al., 1997, 1998; Chinivasagam et al., 2004; Hutchison et al., 2005a), the effects of land application (Pillai et al., 1996; Lewis and Gattie, 2002; Gerba and Smith, 2005), their survival in soil (Van Renterghem et al., 1991; de Freitas et al., 2003; Santamaría and Toranzos, 2003; Brandl et al., 2004; Hutchison et al., 2004; Côté and Quessy, 2005; Nicholson et al., 2005), the effects of runoff events (Van Donsel et al., 1967; Saini et al., 2003; Tyrrel and Quinton, 2003; Malik et al., 2004), and their presence in water (Blaser et al., 1980; Lund, 1996; Jones, 2001; Nevecherya et al., 2005). Table 2 presents a summary of data on zoonotic pathogen prevalence and survival. As this table demonstrates, studies vary widely in the reported presence and survival of zoonotic pathogens, depending on the studied growth conditions, sensitivity of culture media, and swine production system. Data supporting the prevalence in swine manure are the most abundant and come from survey types of studies (Van Renterghem et al., 1991; Guan and Holley, 2003; Bhaduri et al., 2005; Gütler et al., 2005; Hutchison et al., 2005a; Nicholson et al., 2005; USDA, 2005; Bhaduri and Wesley, 2006). There is little information on the survival of these pathogens in swine manure representing on-farm conditions, where urine and feces are being added on a continual basis, because most studies take samples away from the storage unit and hold them in laboratory conditions. Unfortunately, survival studies of zoonotic pathogens from swine manure on plants (Herikstad et al., 2002; Dong et al., 2003; Kühn et al., 2003; Hutchison et al., 2005c), in the soil, and in water are limited. Effects of soil type, pH, and moisture content on the survival and persistence of swine manure pathogens have not been studied systematically. There is a need for good hypothesis-driven research on the prevalence and survival of swine manure pathogens beyond the typical survey work currently available in the literature. Further research is needed for land application of manure with regard to pathogens in bioaerosols; transport into soil, through soil, or both; and the potential to enter water via infiltration or runoff. Although the enteric pathogens have been the most studied to date, more research is needed on the amounts of other zoonotic pathogens in swine manure as well as on their survival and dissemination in soil and water. More information is needed on how different climate and soil factors affect the ability of these bacteria to persist in and be transported through soil and water. COMMON VIRUSES OF SWINE Influenza Influenza virus is a zoonotic agent that can be transmitted easily between animals and humans (Castrucci et al., 1993; Webby and Webster, 2001). The broad host range of influenza viruses includes humans, pigs, birds, marine mammals, horses, mink (Webster, 1997), cats (Thanawongnuwech et al., 2005), and dogs (Crawford et al., 2005). Infection of humans with swine influenza virus has occurred sporadically (Dacso et al., 1984; Wells et al., 1991; Alexander and Brown, 2000), causing clinical disease of varying severity and transmissibility, but occasionally, some occurrences have been fatal. There is strong evidence that swine veterinarians, swine farmers, and meat-processing workers are at increased risk of swine influenza virus infection compared with people who have no exposure to swine (Olsen et al., 2002; Myers et al., 2006). As enveloped viruses, influenza viruses are sensitive to heat, lipid solvents, detergents, irradiation, and oxidizing agents. The influenza viruses are considered environmentally labile outside the host (Quinn et al., 2002). The Centers for Disease Control and Prevention (2005) recommends chemical disinfection with a 1:10 dilution of household bleach or with any of several of the H Registered Antimicrobial Products for Medical Waste Treatment on the list of the US Environmental Protection Agency, including calcium oxide, sodium chloride, sodium dichloro-s-triazinetrione (e.g., swimming pool chlorine), glutaraldehyde, and quaternary ammonium compounds (US Environmental Protection Agency, 2005). The effectiveness of any disinfectant can be reduced in the presence of OM that alters the pH, temperature, or both. Hepatitis E Virus Swine hepatitis E virus (HEV), a novel virus closely related genetically and antigenically to human HEV, was discovered and characterized by Meng et al. (1997). Pigs experimentally and naturally infected by swine HEV remain clinically normal but develop microscopic lesions; in the United States, approximately 60 to 100% of pigs are infected (Meng et al., 1997). Cases of acute hepatitis E also have occurred in patients from industrialized countries, including the United States (Hsieh et al., 1999; van der Poel et al., 2001; Takahashi et al., 2003; Yazaki et al., 2003). The main route of transmission for HEV is believed to be fecal-oral. Cross-species infections of human and swine HEV have been documented (Meng et al., 1998a,b; Halbur et al., 2001). It has been demonstrated that infected pigs shed large amounts of viruses in feces (Meng et al., 1998b; Halbur et al., 2001; Williams et al., 2001). Because of the ubiquitous nature of swine HEV in pigs and the large amount of viruses excreted in feces, swine manure could contaminate irrigation and drinking water in nearby wells, rivers, ponds, or coastal water (Smith et al., 2001). Swine HEV has been detected in swine manure and wastewater associated with hog operations (Karetnyi et al., 1999) and in concrete pits and earthen lagoons of swine manure storage facilities (Kasorndorkbua et al., 2005). Unfortunately, it is not known how long the virus can survive in swine manure and remain infectious or what effect the manure storage and treatment will have on the infectivity of HEV. Future research is warranted to assess the survivability of HEV in swine manure and in different environmental regimens. Enteric Calciviruses (Noroviruses and Sapoviruses) Caliciviruses include Norovirus (NoV), Sapovirus (SaV), Vesivirus, and Lagovirus. Viruses in the NoV and SaV genera cause diarrhea in humans and animals and are referred to as human or animal enteric caliciviruses (Green et al., 2001). The identification of closely related animal enteric caliciviruses in pigs and the existence of recombinants within human and porcine strains (Jiang et al., 1999; Katayama et al., 2002, 2004) raise concerns regarding possible transmission between animals and humans. Wang et al. (2004) reported that porcine NoV (PoNoV) were detected only in fecal samples collected from finisher pigs, but not from those collected from nursing pigs, postweaning pigs, or sows. Most positive samples in this study were from healthy animals, indicating that, as previously observed for human NoV infections (Rockx et al., 2002), asymptomatic shedding of PoNoV occurs in adults, contributing to virus persistence in the field. Sapovirus in humans primarily has been associated with acute gastroenteritis in young children (Chiba et al., 2000). The porcine SaV has emerged as an important pathogen associated with diarrhea and subclinical infections among pigs of all ages (Wang et al., 2006; Jeong et al., 2007; Martella et al., 2008). Enteric viruses are acid stable and can survive in the gastrointestinal tract. Most viruses remain infectious after refrigeration and freezing and also retain their infectivity after heating to 60°C for 30 min. Chlorine-based disinfectants are considered the most effective against enteric viruses. After application of contaminated manure to land, the potential for environmental contamination may exist, including possible spread to other areas resulting from increased rainfall, overflow, or aerosol (Tyrrel and Quinton, 2003). Although the virus concentration will be less in water, the low infectious dose of human NoV (as few as 10 to 100 particles; Moe et al., 1999) and its ability to survive increase the risk of outbreak when contaminated water sources are used in food processing or as public water supplies (Hoebe et al., 2004; Ueki et al., 2004). For animal enteric caliciviruses, the first study to investigate the effect of environmental technologies on the fate of these pathogens in animal manure under field conditions was performed recently (Costantini et al., 2007). These authors evaluated 5 different environmental technologies and a conventional swine operation where storage and treatment of manure was in wastewater lagoons (Table 3). The porcine SaV and PoNoV were detected in fresh feces before treatment, but neither virus type was detected after any treatment. Table 3. Detection of animal enteric viruses pre- and posttreatment, as adapted from Costantini et al. (2007) Management system and treatment technology  Enteric virus1  PoNoV2  PoSaV3  RV-A3  RV-C3  Pre-4  Post-4  Pre-  Post-  Pre-  Post-  Pre-  Post-  Conventional swine operation  −  −  +  +  +  +  −  −  Aerobic upflow biofiltration  −  −  +  −  +  +  +  +  Constructed wetland  +  −  +  −  +  +  −  −  Super soil  +  −  +  −  +  +  +  +  High-rise hog building  +  −  +  −  +  +  +  +  Ambient temperature anaerobic digester  −  −  +  −  +  −  +  −  Management system and treatment technology  Enteric virus1  PoNoV2  PoSaV3  RV-A3  RV-C3  Pre-4  Post-4  Pre-  Post-  Pre-  Post-  Pre-  Post-  Conventional swine operation  −  −  +  +  +  +  −  −  Aerobic upflow biofiltration  −  −  +  −  +  +  +  +  Constructed wetland  +  −  +  −  +  +  −  −  Super soil  +  −  +  −  +  +  +  +  High-rise hog building  +  −  +  −  +  +  +  +  Ambient temperature anaerobic digester  −  −  +  −  +  −  +  −  1PoNoV = porcine Norovirus; PoSaV = porcine Sapovirus; RV-A = rotovirus group A; RV-C = rotovirus group C. A plus sign (+) indicates virus detected, and a minus sign (−) indicates none detected. 2Determined by reverse transcription-PCR with specific primers. 3Determined by reverse transcription-PCR with specific primers and ELISA. 4Pre- = pretreatment samples; Post- = posttreatment samples. View Large Table 3. Detection of animal enteric viruses pre- and posttreatment, as adapted from Costantini et al. (2007) Management system and treatment technology  Enteric virus1  PoNoV2  PoSaV3  RV-A3  RV-C3  Pre-4  Post-4  Pre-  Post-  Pre-  Post-  Pre-  Post-  Conventional swine operation  −  −  +  +  +  +  −  −  Aerobic upflow biofiltration  −  −  +  −  +  +  +  +  Constructed wetland  +  −  +  −  +  +  −  −  Super soil  +  −  +  −  +  +  +  +  High-rise hog building  +  −  +  −  +  +  +  +  Ambient temperature anaerobic digester  −  −  +  −  +  −  +  −  Management system and treatment technology  Enteric virus1  PoNoV2  PoSaV3  RV-A3  RV-C3  Pre-4  Post-4  Pre-  Post-  Pre-  Post-  Pre-  Post-  Conventional swine operation  −  −  +  +  +  +  −  −  Aerobic upflow biofiltration  −  −  +  −  +  +  +  +  Constructed wetland  +  −  +  −  +  +  −  −  Super soil  +  −  +  −  +  +  +  +  High-rise hog building  +  −  +  −  +  +  +  +  Ambient temperature anaerobic digester  −  −  +  −  +  −  +  −  1PoNoV = porcine Norovirus; PoSaV = porcine Sapovirus; RV-A = rotovirus group A; RV-C = rotovirus group C. A plus sign (+) indicates virus detected, and a minus sign (−) indicates none detected. 2Determined by reverse transcription-PCR with specific primers. 3Determined by reverse transcription-PCR with specific primers and ELISA. 4Pre- = pretreatment samples; Post- = posttreatment samples. View Large Rotavirus Rotaviruses (RV) are the leading cause of acute viral gastroenteritis in the young of both avian and mammalian species, including pigs and humans (Saif et al., 1994; Yuan et al., 2006). The RV from group A are the main agents of viral diarrhea in piglets, accounting for 53% of preweaning and 44% of postweaning diarrhea in swine (Fitzgerald et al., 1988; Saif et al., 1994; Yuan et al., 2006); non-group A can be detected within the same herd (Janke et al., 1990; Geyer et al., 1995; Kim et al., 1999). The presence of RV in livestock is a potential public health problem whose significance is increased by the detection in humans of serotypes and genotypes of animal strains and vice versa. Human strains also have been detected in pigs (Racz et al., 2000; Martella et al., 2001; Palombo, 2002). Moreover, in the last 3 yr, evidence has been reported for the presence of 3 different porcine strains circulating in humans (Laird et al., 2003; Esona et al., 2004; Varghese et al., 2004). At least 4 major conclusions can be drawn from studies of RV in the environment (Ansari et al., 1991; Pesaro et al., 1995; Brooks et al., 2005; Pillai, 2007). First, animal RV present in the farm are shed in increased concentrations. Second, they have increased environmental stability in manure, air, soil, and water. Third, they can be disseminated directly or indirectly to other geographical points inside or outside the farm. Finally, in recent years, as newer molecular diagnostic techniques have been used, evidence has been accumulating to support the potential zoonotic transmission of RV. Previous studies focused on anaerobic inactivation of animal viruses in pits, one of the most commonly used systems at that time, and indicated that at least a 4-mo period was required to inactivate RV, with a potential risk of environmental contamination as a consequence of pit breaks, infiltration into soil, or dissemination from the surface (Pesaro et al., 1995). Recently, superior environmental technologies have been developed to decrease the impact of environmental contamination by different treatments, including high-temperature anaerobic digester, biofiltration solids separation. (Humenik et al., 2004). In an attempt to study RV survival after application of these technologies, the presence of RV in fresh feces of swine and their survival after treatment were assessed (Costantini et al., 2007; Table 3). These results indicated that only the RNA of RV-A and RV-C, but not viral infectivity, was detected after treatment, indicating that all technologies were effective in reducing virus infectivity. Rotaviruses are nonenveloped viruses, resistant to inactivation by ether, chloroform, detergents, many chemical disinfectants, and antiseptics (Abad et al., 1998). Phenols, formalin, chlorine, and 95% ethanol have been shown to be effective (Sattar et al., 1994; Yuan et al., 2006). Additionally, UV inactivation has been shown to be effective for inactivation of RV (Smirnov et al., 1991; Battigelli et al., 1993; Ojeh et al., 1995). All these studies were done using viruses in buffered solutions, however, and the influence of solid organic material has not been evaluated. FATE AND TRANSPORT OF ZOONOTIC PARASITE PATHOGENS Several helminth worm and protozoal parasites of swine are infectious to humans, but human infection usually results from ingestion of raw or undercooked meat rather than from exposure to infected feces. Among the protozoal and helminth parasites known to infect both swine and humans, uncertainty regarding host specificity and parasite prevalence complicates the understanding of the human health risk associated with zoonotic parasites of swine in the United States. For example, molecular analysis of Giardia spp. has indicated that this protozoal parasite may have a moderate level of host specificity (Thompson, 2004; Cacciò et al., 2005). Of the 7 Giardia molecular assemblages, only 2, A and B, are associated with human infection. Although Cryptosporidium parvum has been isolated from 155 host species and was once thought to have little host specificity, recent molecular analysis of isolates has revealed significant differences and has identified new host-adapted species (Fayer, 2004). Even host-adapted strains, however, exhibit significant zoonotic transmission in most instances. Because animals are housed mostly on concrete instead of on soil, helminth parasites are considered well controlled. Consequently, only the nematode Ascaris and relevant protozoal parasites are discussed here. Ascaris suum Ascaris is one of the most common worms infecting humans worldwide. Approximately 25% of the global population is infected with this parasite (O'Lorcain and Holland, 2000). Human Ascaris infection is associated with Ascaris lumbricoides and pig infection with Ascaris suum. These 2 worms have identical life cycles and generally are very similar, so there is some controversy regarding whether they truly represent different species or are host-adapted subpopulations (O'Lorcain and Holland, 2000; Nejsum et al., 2005). Nonetheless, host specificity has been demonstrated, in that A. suum parasites will not reach maturity in the human intestine, and molecular studies have demonstrated that human infection with Ascaris worms molecularly identical to pig worms seems to represent a cross-infection (Anderson and Jaenike 1997). Ascaris suum remains one of the most common helminth parasites of pigs. Although intensive management and anthelmintic therapy have decreased the incidence of A. suum in swine significantly (Roepstorff, 1997), its fecundity and environmental persistence prevent its complete eradication from modern swine herds. A 5-yr study (1977 to 1981) of a single total confinement herd in Georgia found that Ascaris prevalence was greatest in gilts, ranging from 33.3 to 86.2% in gestation-age gilts compared with 6.4 to 29.2% in sows (Marti and Hale, 1986). In 1988, a US survey found that 70% of farms had evidence of this parasite (Kennedy et al., 1988). The risk of human exposure to A. suum eggs depends on the parasite burden in the herd and the persistence of infective eggs during manure storage, treatment, and disposal. According to the 2000 USDA National Animal Health Monitoring System study of swine facilities, approximately 51% of operations store swine manure in underground pits (USDA, 2002). After 4 wk of storage in untreated slurry, 80% of A. suum eggs were still able to develop; egg viability decreased under these conditions to 40% at 8 wk and to 0% at 16 wk (Gaasenbeek and Borgsteede, 1998). Anaerobic lagoon storage conditions, used by approximately 23% of US swine operations, seem to be more favorable to egg survival (USDA, 2002). Gaasenbeek and Borgsteede (1998) observed enhanced survival of A. suum eggs under anaerobic conditions compared with A. suum eggs in untreated slurry, reporting 80% viability after 12 wk. Similarly, more than 80% of eggs were viable after 20 d of anaerobic stabilization (Juris et al., 1996) in tanks designed to simulate anaerobic lagoon stabilization. Ensiling of swine manure had no effect on the observed A. suum egg count, and approximately 70% of recovered eggs remained viable after 56 d of treatment (Caballero-Hernández et al., 2004). To examine the possibility of environmental transport after land application of swine manure, egg survival was assessed in swine slurries land-applied on outdoor plots under varying conditions of sun and simulated rainfall (Gaasenbeek and Borgsteede, 1998). Survival of parasite eggs was greatest on wet, shaded plots, with at least 90% egg viability at 8 wk. On sunny (temperature not exceeding 25°C) dry plots, egg survival was least, with a 90% loss of viability observed between 2 and 8 wk. Additionally, increased relative humidity (i.e., from 77.5 to 100%) during the experiment favored egg survival (Gaasenbeek and Borgsteede, 1998). Cryptosporidium Cryptosporidium describes a genus of protozoan parasites that infect a wide range of vertebrates. Several Cryptosporidium spp. exist, most of which are host adapted, but zoonotic strains of C. parvum exist that are associated with outbreaks in several mammalian hosts. Cryptosporidium is an intracellular parasite that typically infects epithelial cells of the small intestine. But infection sites outside the intestinal tract can occur. The life cycle is direct, meaning a period of development outside the host is not required and oocysts are infective immediately when passed from infected hosts. Cryptosporidium spp. are transmitted via contaminated feed and water. Opportunities for human infection exist during exposure to infected livestock, their manure, or contaminated water. Oocysts are environmentally stable; consequently, fecal contamination of the environment can result in waterborne dissemination of oocysts and in human outbreaks associated with drinking and recreational waters. Cryptosporidiosis is a common cause of protozoal diarrhea in humans worldwide. Cryptosporidiosis is reported in swine. Although diarrhea has been the primary clinical sign, many infected pigs have concurrent infections with other enteric pathogens; some pigs apparently do not show any signs of infection. Typically, cryptosporidiosis is an infection of young animals; nursing and weaned pigs are infected more often than sows (Xiao et al., 1994). Although no published studies have examined the concentration of Cryptosporidum oocysts in swine manure, Thurston-Enriquez et al. (2005) referenced unpublished data reporting 20 to 90 oocysts found per gram of swine lagoon wastewater. The Cryptosporidium oocyst is a resistant parasitic stage and can retain its viability in typical environmental conditions. Cryptosporidium is much more resistant to decay over a wide range of temperatures (Fayer et al., 2000; Gajadhar and Allen, 2004). When Cryptosporidium oocysts were inoculated into pig slurries and persistence was measured in unstirred tanks, the time required for a 1-log reduction in oocysts ranged from 133 to 345 d in summer and 217 to 270 d in winter (Hutchison, 2005b). With the application of Cryptosporidium oocysts to soil blocks followed by intermittent irrigation under laboratory conditions, oocysts could move through some soils for more than 70 d; most oocysts remained in the upper 2 cm of the soil block (Fayer et al., 2000). In a field trial, land application of lagoon wastewaters to 1.5-m2 plots followed by simulated rainfall and collection of runoff waters resulted in the recovery of up to 2.2 × 106 oocysts (Thurston-Enriquez et al., 2005). Giardia intestinalis Giardia describes a genus of flagellate protozoan parasites of the small intestine that infect a wide range of vertebrates. Three main species have been described: Giardia angilis, Giardia muris, and Giardia intestinalis (Eligio-García and Cortes-Campos, 2005). Giardia intestinalis, also is known as Giardia duodenalis and Giardia lamblia, is the species known to infect humans (Ali and Hill, 2003; Eligio-García and Cortes-Campos, 2005). The life cycle of Giardia is direct, meaning that cysts of Giardia are infective immediately when excreted by infected hosts. The life cycle is short; cysts appear in the feces within 1 or 2 wk after infection in dogs, in which the life cycle is better understood than in swine (Bowman et al., 1999). Giardia spp. are known to infect both young and adult swine. Control and prevention of both Giardia and Cryptosporidium infections in pigs are complicated by the short life cycle, the long survival time of the infective stage in the environment, and the potential for rapid reinfection in contaminated housing of confined livestock. Transmission between animal and human hosts typically occurs through ingestion of fecally contaminated water, which can come from a variety of mammalian fecal sources. The concentration of Giardia cysts in swine lagoon wastewaters can be as great as 1,075 cysts/g (Thurston-Enriquez et al., 2005), but survival of Giardia cysts seems to be highly temperature dependent (Olson et al., 1999). For 90% degradation of cysts inoculated into mixed human and swine manure at 5°C, 129 d were required, but only 4 d were required at 25°C (Deng and Cliver, 1992). Giardia cysts are sensitive to freezing of soil, becoming noninfective after only 7 d at −4°C, but Giardia cysts were recoverable from soils maintained at 4°C for up to 8 wk. Soils maintained at 25°C inactivated Giardia cysts within 1 wk, but Giardia seems to be effectively retained in soil columns; sandy soils reduced cysts by more than 7 log, and gravel soil rarely resulted in breakthrough recovery of cysts (Hijnen et al., 2005). Up to 3.58 × 106 cysts were recovered from 0.75 × 2 m field plots after simulated rainfall (Thurston-Enriquez et al., 2005). In water, cysts survive less than 14 d at 25°C but survive up to 77 d at 4 to 8°C (Olson et al., 1999). Conclusions and Recommendations Several biological and physical variables drive the still poorly described ecology of microbes in swine manure and their fate in management systems and the environment. An evidence-based, systematic evaluation of studies characterizing the presence and abundance of zoonotic pathogens in swine manure systems and their relative contributions to the environment must be qualitative rather than quantitative in nature. Against the backdrop of a rapidly evolving and diverse industry and the continual development of new scientific methodologies is a complex ecology that cannot be characterized adequately under controlled bench-top conditions or studied adequately under field conditions. The wide variety of microbes, the animal and manure management practices, and the environmental factors that influence the presence, persistence, survival, and transport of pathogens result in an inestimable number of combinations of potential pathogen fates in the environment. Field studies that have attempted to identify transport of microbes from swine manure management systems through the environment have largely failed to confirm that the source of microbes was indeed the swine manure. In addition, dilution of pathogens in environmental media under natural conditions results in concentrations that are likely to be too small to recover except by molecular methods. Although increased concentrations of pathogens may be added to environmental media in controlled field studies to study these under more natural conditions, the risks associated with intentional introduction of pathogens to the environment are prohibitive to the conduct of research. Consequently, bench-top studies using artificial environments are designed to study the specific environmental effects on pathogens under very controlled conditions, but these fail to adequately capture the myriad processes that influence microbial fate and transport in the natural world. Nonetheless, research has characterized many of the drivers of microbial survival and transport and has provided useful information on the ecology of microbes in swine manure treatment systems and the environment. In light of the scientific gaps in the estimation of the human health risks associated with swine-related zoonotic pathogens, the following recommendations for future research directions are offered: Develop sensitive and quantitative methods of microbial recovery from manure management systems, with an emphasis on methods that recover multiple classes of pathogens at the same time; Continue molecular characterization of pathogens from both animal and human sources to identify important zoonotic pathogens in swine manure and in the environment; Develop methods to source-track microbes in environmental soils, water, and irrigated produce; Design studies examining the environmental and ecological conditions that contribute to off-farm transport of zoonotic pathogens; and Design and conduct quantitative risk assessments for common zoonotic pathogens found in swine manure. In spite of a technologically advanced industry that places emphasis on animal health and management, zoonotic pathogens are not likely to disappear from swine manure management systems. Although laboratory and environmental field data indicate that there may be a biologically significant amount of viable pathogens in the environment that may be associated with modern swine production, these amounts often are too small to quantify easily. In this setting, quantitative risk assessment may serve to bridge the gap between bench-top studies and environmental science to provide an estimate of the risk, which is difficult to assess using traditional field science methods. LITERATURE CITED Abad F. X. Pinto R. M. Bosch A. 1998. Flow cytometry detection of infectious rotaviruses in environmental and clinical samples. Appl. Environ. Microbiol.  64: 2392– 2396. https://doi.org/9647805 Google Scholar PubMed  Alexander D. J. Brown I. H. 2000. Recent zoonoses caused by influenza A viruses. Rev. Sci. Tech.  19: 197– 225. https://doi.org/11189716 Google Scholar CrossRef Search ADS PubMed  Ali S. A. Hill D. R. 2003. Giardia intestinalis. Curr. Opin. Infect. Dis.  16: 453– 460. https://doi.org/14501998 Google Scholar CrossRef Search ADS PubMed  Anderson T. J. C. Jaenike J. 1997. Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs. Parasitology  115: 325– 342. Google Scholar CrossRef Search ADS PubMed  Ansari S. A. Springthorpe V. S. Sattar S. A. 1991. Survival and vehicular spread of human rotaviruses: Possible relation to seasonality of outbreaks. Rev. Infect. Dis.  13: 448– 461. https://doi.org/1866549 Google Scholar CrossRef Search ADS PubMed  Anugwa F. O. I. Varel V. H. Dickson J. S. Pond W. G. Krook L. P. 1989. Effects of dietary fiber and protein concentration on growth, feed efficiency, visceral organ weights and large intestine microbial populations of swine. J. Nutr.  119: 879– 886. https://doi.org/2545846 Google Scholar CrossRef Search ADS PubMed  Battigelli D. A. Sobsey M. D. Lobe D. C. 1993. The inactivation of hepatitis A virus and other model viruses by UV irradiation. Water Sci. Technol.  27: 339– 342. Bhaduri S. Wesley I. 2006. Isolation and characterization of Yersinia enterocolitica from swine feces recovered during the National Animal Health Monitoring System Swine 2000 study. J. Food Prot.  69: 2107– 2112. https://doi.org/16995512 Google Scholar CrossRef Search ADS PubMed  Bhaduri S. Wesley I. V. Bush E. J. 2005. Prevalence of pathogenic Yersinia enterocolitica strains in pigs in the United States. Appl. Environ. Microbiol.  71: 7117– 7121. https://doi.org/16269749 Google Scholar CrossRef Search ADS PubMed  Blaser M. J. Hardesty H. L. Powers B. Wang W.-L. L. 1980. Survival of Campylobacter fetus ssp. jejuni in biological milieus. J. Clin. Microbiol.  11: 309– 313. https://doi.org/6892819 Google Scholar PubMed  Bowman, D. D., R. C. Lynn, and J. R. Georgi 1999. Georgis' Parasitology for Veterinarians.  7th ed. W. B. Saunders Co., Philadelphia, PA. Brandl M. T. Haxo A. F. Bates A. H. Mandrell R. E. 2004. Comparison of survival of Campylobacter jejuni in the phyllosphere with that in the rhizosphere of spinach and radish plants. Appl. Environ. Microbiol.  70: 1182– 1189. https://doi.org/14766604 Google Scholar CrossRef Search ADS PubMed  Brooks J. P. Tanner B. D. Gerba C. P. Haas C. N. Pepper I. L. 2005. Estimation of bioaerosol risk of infection to residents adjacent to a land applied biosolids site using an empirically derived transport model. J. Appl. Microbiol.  98: 397– 405. https://doi.org/15659194 Google Scholar CrossRef Search ADS PubMed  Caballero-Hernández A. I. Castrejón-Pineda F. Martínez-Gamba R. Angeles-Campos S. Pérez-Rojas M. Buntinx S. E. 2004. Survival and viability of Ascaris suum and Oesophagostomum entatum in ensiled swine faeces. Bioresour. Technol.  94: 137– 142. https://doi.org/15158505 Google Scholar CrossRef Search ADS PubMed  Cacciò S. M. Thompson R. C. A. McLauchlin J. Smith H. V. 2005. Unravelling Cryptosporidium and Giardia epidemiology. Trends Parasitol.  21: 430– 437. https://doi.org/16046184 Google Scholar CrossRef Search ADS PubMed  Castrucci M. R. Donatelli I. Sidoli L. Barigazzi G. Kawaoka Y. Webster R. G. 1993. Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology  193: 503– 506. Google Scholar CrossRef Search ADS PubMed  Centers for Disease Control and Prevention 2005. Questions and answers about the Influenza A (H2N2) panels: Destruction of the panels.  http://www.cdc.gov/flu/h2n2panelsqa.htm Accessed Jan. 10, 2009. Chiba S. Nakata S. Numata-Kinoshita K. Honma S. 2000. Sapporo virus: History and recent findings. J. Infect. Dis.  181( Suppl. 2): S303– S308. https://doi.org/10804142 Google Scholar CrossRef Search ADS PubMed  Chinivasagam H. N. Thomas R. J. Casey K. McGahan E. Gardner E. A. Rafiee M. Blackall P. J. 2004. Microbiological status of piggery effluent from 13 piggeries in the south east Queensland region of Australia. J. Appl. Microbiol.  97: 883– 891. https://doi.org/15479402 Google Scholar CrossRef Search ADS PubMed  Copeland, C., and J. Zinn 1998. Animal waste management and the environment: Background for current issues.  CRS Rep. Congr. 98-451. Natl. Counc. Sci. Environ., Washington, DC. Costantini V. P. Azevedo A. C. Li X. Williams M. C. Michel F. C.Jr. Saif L. J. 2007. Effects of different animal waste treatment technologies on detection and viability of porcine enteric viruses. Appl. Environ. Microbiol.  73: 5284– 5291. https://doi.org/17601821 Google Scholar CrossRef Search ADS PubMed  Côté C. Quessy S. 2005. Persistence of Escherichia coli and Salmonella in surface soil following application of liquid hog manure for production of pickling cucumbers. J. Food Prot.  68: 900– 905. https://doi.org/15895719 Google Scholar CrossRef Search ADS PubMed  Council for Agricultural Science and Technology 2008. Fate and transport of zoonotic bacterial, viral, and parasitic pathogens during swine manure treatment, storage, and land application.  Special Publ. No. 29. Counc. Agric. Sci. Technol., Ames, IA. Crawford P. C. Dubovi E. J. Castleman W. L. Stephenson I. Gibbs E. P. Chen L. Smith C. Hill R. C. Ferro P. Pompey J. Bright R. A. Medina M. J. Johnson C. M. Olsen C. W. Cox N. J. Klimov A. I. Katz J. M. Donis R. O. 2005. Transmission of equine influenza virus to dogs. Science  310: 482– 485. Google Scholar CrossRef Search ADS PubMed  Dacso C. C. Couch R. B. Six H. R. Young J. F. Quarles J. M. Kasel J. A. 1984. Sporadic occurrence of zoonotic swine influenza virus infections. J. Clin. Microbiol.  20: 833– 835. https://doi.org/6092435 Google Scholar PubMed  Davies P. R. Bovee F. G. Funk J. A. Morrow W. E. M. Jones F. T. Deen J. 1998. Isolation of Salmonella serotypes from feces of pigs raised in a multiple-site production system. JAVMA  212: 1925– 1929. Google Scholar PubMed  Davies P. R. Funk J. A. Morrow W. E. M. Jones F. T. Deen J. Fedorka-Cray P. J. Gray J. T. 1997. Risk of shedding Salmonella organisms by market-age hogs in a barn with open-flush gutters. JAVMA  210: 386– 389. Google Scholar PubMed  de Freitas J. R. Schoenau J. J. Boyetchko S. M. Cyrenne S. A. 2003. Soil microbial populations, community composition, and activity as affected by repeated applications of hog and cattle manure in eastern Saskatchewan. Can. J. Microbiol.  49: 538– 548. https://doi.org/14608420 Google Scholar CrossRef Search ADS PubMed  Deng M. Y. Cliver D. O. 1992. Degradation of Giardia lamblia cysts in mixed human and swine wastes. Appl. Environ. Microbiol.  58: 2368– 2374. https://doi.org/1381171 Google Scholar PubMed  Dickey, E. C., M. Brumm, and D. P. Shelton 1981. Swine Manure Management Systems.  NebGuide G80-531-A. Coop. Ext. Inst. Agric. Nat. Res., Univ. Nebraska, Lincoln. Dong Y. Iniguez A. L. Ahmer B. M. M. Triplett E. W. 2003. Kinetics and strain specificity of rhizosphere and endopyhytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl. Environ. Microbiol.  69: 1783– 1790. https://doi.org/12620870 Google Scholar CrossRef Search ADS PubMed  Eligio-García L. Cortes-Campos A. 2005. Genotype of Giardia intestinalis isolates from children and dogs and its relationship to host origin. Parasitol. Res.  97: 1– 6. https://doi.org/15940523 Google Scholar CrossRef Search ADS PubMed  Esona M. D. Armah G. E. Geyer A. Steele A. D. 2004. Detection of an unusual human rotavirus strain with G5P[8] specificity in a Cameroonian child with diarrhea. J. Clin. Microbiol.  42: 441– 444. https://doi.org/14715801 Google Scholar CrossRef Search ADS PubMed  Fayer R. 2004. Cryptosporidium: A water-borne zoonotic parasite. Vet. Parasitol.  126: 37– 56. https://doi.org/15567578 Google Scholar CrossRef Search ADS PubMed  Fayer R. Morgan U. Upton S. 2000. Epidemiology of Cryptosporidium: Transmission, detection and identification. Int. J. Parasitol.  30: 1305– 1322. https://doi.org/11113257 Google Scholar CrossRef Search ADS PubMed  Fitzgerald G. R. Barker T. Welter M. W. Welter C. J. 1988. Diarrhea in young pigs: Comparing the incidence of the five most common infectious agents. Vet. Med. Food Anim. Pract.  1: 80– 86. Gaasenbeek C. P. H. Borgsteede F. H. M. 1998. Studies on the survival of Ascaris suum eggs under laboratory and simulated field conditions. Vet. Parasitol.  75: 227– 234. https://doi.org/9637224 Google Scholar CrossRef Search ADS PubMed  Gajadhar A. A. Allen J. R. 2004. Factors contributing to the public health and economic importance of waterborne zoonotic pathogens. Vet. Parasitol.  126: 3– 14. https://doi.org/15567576 Google Scholar CrossRef Search ADS PubMed  Gerba C. P. Smith J. E.Jr. 2005. Sources of pathogenic microorganisms and their fate during land application of wastes. J. Environ. Qual.  34: 42– 48. https://doi.org/15647533 Google Scholar PubMed  Geyer A. Sebata T. Peenze I. Steele A. D. 1995. A molecular epidemiological study of porcine rotaviruses. J. S. Afr. Vet. Assoc.  66: 202– 205. https://doi.org/8691407 Google Scholar PubMed  Green, K. Y., R. M. Chanock, and A. Z. Kapikian 2001. Human caliciviruses. Pages 841–874 in Fields Virology.  4th ed. D. M. Knipe and P. M. Howley ed. Lippincott Williams and Wilkins, Philadelphia, PA. Guan T. Y. Holley R. A. 2003. Pathogen survival in swine manure environments and transmission of human enteric illness—A review. J. Environ. Qual.  32: 383– 392. https://doi.org/12708660 Google Scholar CrossRef Search ADS PubMed  Gütler M. Alter T. Kasimir S. Linnebur M. Fehlhaber K. 2005. Prevalence of Yersinia enterocolitica in fattening pigs. J. Food Prot.  68: 850– 854. https://doi.org/15830683 Google Scholar CrossRef Search ADS PubMed  Halbur P. G. Kasorndorkbua C. Gilbert C. Guenette D. Potters M. B. Purcell R. H. Emerson S. U. Toth T. E. Meng X. J. 2001. Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J. Clin. Microbiol.  39: 918– 923. https://doi.org/11230404 Google Scholar CrossRef Search ADS PubMed  Herikstad, H., S. Yang, T. J. Van Gilder, D. Vugia, J. Hadler, P. Blake, V. Deneen, B. Shiferaw, F. J. Angulo, and the FoodNet Working Group 2002. A population-based estimate of the burden of diarrhoeal illness in the United States: FoodNet, 1996–7. Epidemiol. Infect. 129:9–17.  Hijnen W. A. M. Brouwer-Hanzen A. J. Charles K. J. Medema G. J. 2005. Transport of MS2 phage, Escherichia coli, Clostridium perfringens, Cryptosporidium parvum, and Giardia intestinalis in a gravel and a sandy soil. Environ. Sci. Technol.  39: 7860– 7868. https://doi.org/16295848 Google Scholar CrossRef Search ADS PubMed  Hill V. R. 2003. Prospects for pathogen reductions in livestock wastewaters: A review. Crit. Rev. Environ. Sci. Technol.  30: 15– 22. Hoebe C. J. P. A. Vennema H. de Roda Husman A. M. van Duynhoven Y. T. H. P. 2004. Norovirus outbreak among primary schoolchildren who had played in a recreational water fountain. J. Infect. Dis.  189: 699– 705. https://doi.org/14767824 Google Scholar CrossRef Search ADS PubMed  Hsieh S. Y. Meng X. J. Wu Y. H. Liu S. T. Tam A. W. Lin D. Y. Liaw Y. F. 1999. Identity of a novel swine hepatitis E virus in Taiwan forming a monophyletic group with Taiwan isolates of human hepatitis E virus. J. Clin. Microbiol.  37: 3828– 3834. https://doi.org/10565892 Google Scholar PubMed  Humenik F. J. Rice J. M. Baird C. L. Koelsch R. 2004. Environmentally superior technologies for swine waste management. Water Sci. Technol.  49: 15– 21. https://doi.org/15137402 Google Scholar PubMed  Hutchison M. L. Walters L. D. Avery S. M. Munro F. Moore A. 2005 a. Analyses of livestock production, waste storage, and pathogen levels and prevalences in farm manures. Appl. Environ. Microbiol.  71: 1231– 1236. https://doi.org/15746323 Google Scholar CrossRef Search ADS PubMed  Hutchison M. L. Walters L. D. Moore A. Avery S. M. 2005 b. Declines of zoonotic agents in liquid livestock wastes stored in batches on-farm. J. Appl. Microbiol.  99: 58– 65. https://doi.org/15960665 Google Scholar CrossRef Search ADS PubMed  Hutchison M. L. Walters L. D. Moore A. Crookes K. M. Avery S. M. 2004. Effect of length of time before incorporation on survival of pathogenic bacteria present in livestock wastes applied to agricultural soil. Appl. Environ. Microbiol.  70: 5111– 5118. Google Scholar CrossRef Search ADS PubMed  Hutchison M. L. Walters L. D. Moore A. Thomas D. J. I. Avery S. M. 2005 c. Fate of pathogens present in livestock wastes spread onto fescue plots. Appl. Environ. Microbiol.  71: 691– 696. https://doi.org/15691918 Google Scholar CrossRef Search ADS PubMed  Janke B. H. Nelson J. K. Benfield D. A. Nelson E. A. 1990. Relative prevalence of typical and atypical strains among rotaviruses from diarrheic pigs in conventional swine herds. J. Vet. Diagn. Invest.  2: 308– 311. https://doi.org/1965637 Google Scholar CrossRef Search ADS PubMed  Jeong C. Park S. I. Park S. H. Kim H. H. Park S. J. Jeong J. H. Choy H. E. Saif L. J. Kim S. K. Kang M. I. Hyun B. H. Cho K. O. 2007. Genetic diversity of porcine sapoviruses. Vet. Microbiol.  122: 246– 257. https://doi.org/17382492 Google Scholar CrossRef Search ADS PubMed  Jiang X. Espul C. Zhong W. M. Cuello H. Matson D. O. 1999. Characterization of a novel human calicivirus that may be a naturally occurring recombinant. Arch. Virol.  144: 2377– 2387. https://doi.org/10664391 Google Scholar CrossRef Search ADS PubMed  Jones K. 2001. Campylobacters in water, sewage and the environment. J. Appl. Microbiol.  90: 68S– 79S. Google Scholar CrossRef Search ADS   Jones P. W. Bew J. Burrows M. R. Matthews P. R. J. Collins P. 1976. The occurrence of salmonellas, mycobacteria and pathogenic strains of Escherichia coli in pig slurry. J. Hyg. (Lond.)  77: 43– 50. https://doi.org/10332 Google Scholar CrossRef Search ADS PubMed  Juris P. Tóth F. Lauková A. Plachý P. Dubinský P. Sokol J. 1996. Survival of model bacterial strains and helminth eggs in the course of mesophilic anaerobic digestion of pig slurry. Vet. Med. (Praha)  41: 149– 153. https://doi.org/8693668 Google Scholar PubMed  Karetnyi, Y. V., N. Moyer, M. J. R. Gilchrist, and S. J. Naides 1999. Swine hepatitis E virus contamination in hog operation waste streams–An emerging infection? Workshop on the Effects of Animal Feeding Operations on Hydrologic Resources and the Environment.  USGS, Fort Collins, CO. Kasorndorkbua C. Opriessnig T. Huang F. F. Guenette D. K. Thomas P. J. Meng X. J. Halbur P. G. 2005. Infectious swine hepatitis E virus is present in pig manure storage facilities on United States farms, but evidence of water contamination is lacking. Appl. Environ. Microbiol.  71: 7831– 7837. https://doi.org/16332757 Google Scholar CrossRef Search ADS PubMed  Katayama K. Miyoshi T. Uchino K. Oka T. Tanaka T. Takeda N. Hansman G. S. 2004. Novel recombinant sapovirus. Emerg. Infect. Dis.  10: 1874– 1876. https://doi.org/15504283 Google Scholar CrossRef Search ADS PubMed  Katayama K. Shirato-Horikoshi H. Kojima S. Kageyama T. Oka T. Hoshino F. Fukushi S. Shinohara M. Uchida K. Suzuki Y. Gojobori T. Takeda N. 2002. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology  299: 225– 239. https://doi.org/12202225 Google Scholar CrossRef Search ADS PubMed  Kennedy T. J. Marchiondo A. A. Williams J. A. 1988. Prevalence of swine parasites in major hog producing areas of the United States. Agric. in Pract.  9: 25– 32. Kim Y. Chang K. O. Straw B. Saif L. J. 1999. Characterization of group Rotaviruses associated with diarrhea outbreaks in feeder pigs. J. Clin. Microbiol.  37: 1484– 1488. https://doi.org/10203510 Google Scholar PubMed  Kühn I. Iversen A. Burman L. G. Olsson-Liljequist B. Franklin A. Finn M. Aarestrup F. Seyfarth A. M. Blanch A. R. Vilanova X. Taylor H. Caplin J. Moreno M. A. Dominguez L. Herrero I. A. Möllby R. 2003. Comparison of enterococcal populations in animals, humans, and the environment—A European study. Int. J. Food Microbiol.  88: 133– 145. https://doi.org/14596986 Google Scholar CrossRef Search ADS PubMed  Laird A. R. Ibarra V. Ruiz-Palacios G. Guerrero M. L. Glass R. I. Gentsch J. R. 2003. Unexpected detection of animal VP7 genes among common rotavirus strains isolated from children in Mexico. J. Clin. Microbiol.  41: 4400– 4403. https://doi.org/12958276 Google Scholar CrossRef Search ADS PubMed  Lewis D. L. Gattie D. K. 2002. Pathogen risks from applying sewage sludge to land. Environ. Sci. Technol.  36: 286A– 293A. Google Scholar CrossRef Search ADS PubMed  Lund V. 1996. Evaluation of E. coli as an indicator for the presence of Campylobacter jejuni and Yersinia enterocolitica in chlorinated and untreated oligotrophic lake water. Water Res.  30: 1528– 1534. Google Scholar CrossRef Search ADS   Mackenzie J. S. Chua K. B. Daniels P. W. Eaton B. T. Field H. E. Hall R. A. Halpin K. Johansen C. A. Kirkland P. D. Lam S. K. McMinn P. Nisbet D. J. Paru R. Pyke A. T. Ritchie S. A. Siba P. Smith D. W. Smith G. A. van den Hurk A. F. Wang L. F. Williams D. T. 2001. Emerging viral diseases of Southeast Asia and the Western Pacific. Emerg. Infect. Dis.  7( 3 Suppl.): 497– 504. https://doi.org/11485641 Google Scholar CrossRef Search ADS PubMed  Malik Y. S. Randall W. Goyal S. M. 2004. Fate of Salmonella following application of swine manure to tile-drained clay loam soil. J. Water Health  2: 97– 101. https://doi.org/15387133 Google Scholar PubMed  Martella V. Bányai K. Lorusso E. Bellacicco A. L. Decaro N. Mari V. Saif L. Costantini V. De Grazia S. Pezzotti G. Lavazza A. Buonavoglia C. 2008. Genetic heterogeneity of porcine enteric caliciviruses identified from diarrhoeic piglets. Virus Genes  36: 365– 373. https://doi.org/18204823 Google Scholar CrossRef Search ADS PubMed  Martella V. Pratelli A. Greco G. Tempesta M. Ferrari M. Losio M. N. Buonavoglia C. 2001. Genomic characterization of porcine rotaviruses in Italy. Clin. Diagn. Lab. Immunol.  8: 129– 132. https://doi.org/11139206 Google Scholar PubMed  Marti O. G.Jr. Hale O. M. 1986. Parasite transmission in confined hogs. Vet. Parasitol.  19: 301– 314. https://doi.org/3705423 Google Scholar CrossRef Search ADS PubMed  Meng X. J. Halbur P. G. Haynes J. S. Tsareva T. S. Bruna J. D. Royer R. L. Purcell R. H. Emerson S. U. 1998 b. Experimental infection of pigs with the newly identified swine hepatitis E virus (swine HEV), but not with human strains of HEV. Arch. Virol.  143: 1405– 1415. https://doi.org/9722883 Google Scholar CrossRef Search ADS PubMed  Meng X. J. Halbur P. G. Shapiro M. S. Govindarajan S. Bruna J. D. Mushahwar I. K. Purcell R. H. Emerson S. U. 1998 a. Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J. Virol.  72: 9714– 9721. https://doi.org/9811705 Google Scholar PubMed  Meng X. J. Purcell R. H. Halbur P. G. Lehman J. R. Webb D. M. Tsareva T. S. Haynes J. S. Thacker B. J. Emerson S. U. 1997. A novel virus in swine is closely related to the human hepatitis E virus. Proc. Natl. Acad. Sci. USA  94: 9860– 9865. https://doi.org/9275216 Google Scholar CrossRef Search ADS   Moe, C., M. D. Sobsey, P. Stewart, and D. Crawford-Brown 1999. Estimating the risk of human calicivirus infection from drinking water.  Pages 4–6 in Proc. 1st Int. Workshop Human Caliciviruses, Atlanta, GA. Univ. Chicago Press, Chicago, IL. Myers K. P. Olsen C. W. Setterquist S. F. Capuano A. W. Donham K. J. Thacker E. L. Merchant J. A. Gray G. C. 2006. Are swine workers in the United States at increased risk of infection with zoonotic influenza virus? Clin. Infect. Dis.  42: 14– 20. https://doi.org/16323086 Google Scholar CrossRef Search ADS PubMed  Nejsum P. Frydenberg J. Roepstorff A. Parker E. D.Jr. 2005. Population structure in Ascaris suum (Nematoda) among domestic swine in Denmark as measured by whole genome DNA fingerprinting. Hereditas  142: 7– 14. https://doi.org/16970605 Google Scholar CrossRef Search ADS PubMed  Nevecherya I. K. Shestakov V. M. Mazaev V. T. Shlepnina T. G. 2005. Survival rate of pathogenic bacteria and viruses in groundwater. Water Resour.  32: 232– 237. Google Scholar CrossRef Search ADS   Nicholson F. A. Groves S. J. Chambers B. J. 2005. Pathogen survival during livestock manure storage and following land application. Bioresour. Technol.  96: 135– 143. https://doi.org/15381209 Google Scholar CrossRef Search ADS PubMed  Ojeh C. K. Cusack T. M. Yolken R. H. 1995. Evaluation of the effects of disinfectants on rotavirus RNA and infectivity by the polymerase chain reaction and cell-culture methods. Mol. Cell. Probes  9: 341– 346. https://doi.org/8569775 Google Scholar CrossRef Search ADS PubMed  O'Lorcain P. Holland C. V. 2000. The public health importance of Ascaris lumbricoides. Parasitology  121( Suppl.): S51– S71. Google Scholar CrossRef Search ADS PubMed  Olsen C. W. Brammer L. Easterday B. C. Arden N. Belay E. Baker I. Cox N. J. 2002. Serologic evidence of H1 swine influenza virus infection in swine farm residents and employees. Emerg. Infect. Dis.  8: 814– 819. https://doi.org/12141967 Google Scholar CrossRef Search ADS PubMed  Olson M. E. Goh J. Phillips M. Guselle N. McAllister T. A. 1999. Giardia cyst and Cryptosporidium oocyst survival in water, soil, and cattle feces. J. Environ. Qual.  28: 1991– 1996. Google Scholar CrossRef Search ADS   Palombo E. A. 2002. Genetic analysis of group A rotaviruses: Evidence for interspecies transmission of rotavirus genes. Virus Genes  24: 11– 20. https://doi.org/11928984 Google Scholar CrossRef Search ADS PubMed  Pell A. N. 1997. Manure and microbes: Public and animal health problem? J. Dairy Sci.  80: 2673– 2681. https://doi.org/9361239 Google Scholar CrossRef Search ADS PubMed  Pesaro F. Sorg I. Metzler A. 1995. In situ inactivation of animal viruses and a coliphage in nonaerated liquid and semiliquid animal wastes. Appl. Environ. Microbiol.  61: 92– 97. https://doi.org/7887631 Google Scholar PubMed  Pillai S. D. 2007. Bioaerosols from land-applied biosolids: Issues and needs. Water Environ. Res.  79: 270– 278. https://doi.org/17469658 Google Scholar CrossRef Search ADS PubMed  Pillai S. D. Widmer K. W. Dowd S. E. Ricke S. C. 1996. Occurrence of airborne bacteria and pathogen indicators during land application of sewage sludge. Appl. Environ. Microbiol.  62: 296– 299. https://doi.org/8572708 Google Scholar PubMed  Quinn, P. J., B. K. Markey, M. E. Carter, W. J. Donnelly, and F. C. Leonard 2002. Orthomyxoviridae. Pages 375–380 in Veterinary Microbiology and Microbial Disease.  Blackwell Science, Oxford, UK. Rácz M. L. Kroeff S. S. Munford V. Caruzo T. A. Durigon E. L. Hayashi Y. Gouvea V. Palombo E. A. 2000. Molecular characterization of porcine rotaviruses from the southern region of Brazil: Characterization of an atypical genotype G[9] strain. J. Clin. Microbiol.  38: 2443– 2446. https://doi.org/10835028 Google Scholar PubMed  Rockx B. De Wit M. Vennema H. Vinje J. De Bruin E. Van Duynhoven Y. Koopmans M. 2002. Natural history of human calicivirus infection: A prospective cohort study. Clin. Infect. Dis.  35: 246– 253. https://doi.org/12115089 Google Scholar CrossRef Search ADS PubMed  Roepstorff A. 1997. Helminth surveillance as a prerequisite for anthelmintic treatment in intensive sow herds. Vet. Parasitol.  73: 139– 151. https://doi.org/9477500 Google Scholar CrossRef Search ADS PubMed  Rostagno M. H. Gailey J. K. Hurd H. S. Mckean J. D. Leite R. C. 2005. Culture methods differ on the isolation of Salmonella enterica serotypes from naturally contaminated swine fecal samples. J. Vet. Diagn. Invest.  17: 80– 83. https://doi.org/15690959 Google Scholar CrossRef Search ADS PubMed  Saif, L. J., B. I. Rosen, and A. V. Parwani 1994. Animal rotavirus. Pages 279–367 in Viral Infections of the Gastrointestinal Tract.  2nd ed. A. Z. Kapikian ed. Marcel Dekker, New York, NY. Saini R. Halverson L. J. Lorimore J. C. 2003. Rainfall timing and frequency influence on leaching of Escherichia coli RS2G through soil following manure application. J. Environ. Qual.  32: 1865– 1872. https://doi.org/14535331 Google Scholar CrossRef Search ADS PubMed  Santamaría J. Toranzos G. A. 2003. Enteric pathogens and soil: A short review. Int. Microbiol.  6: 5– 9. https://doi.org/12730707 Google Scholar PubMed  Sattar S. A. Jacobsen H. Rahman H. Cusack T. M. Rubino J. R. 1994. Interruption of rotavirus spread through chemical disinfection. Infect. Control Hosp. Epidemiol.  15: 751– 756. https://doi.org/7890922 Google Scholar CrossRef Search ADS PubMed  Smirnov Y. A. Kapitulets S. P. Amitina N. N. Ginevskaya V. A. Kaverin N. V. 1991. Effect of UV-irradiation on rotavirus. Acta Virol.  35: 1– 6. https://doi.org/1683109 Google Scholar PubMed  Sobsey, M. D., O. D. Simmons, C. A. Likirdopulos, S. Qureshi, L. Worley-Davis, and C. M. Williams 2005. Phase 2 evaluation of alternative swine waste treatment and management technologies for control of pathogens.  Proc. 2005 Anim. Waste Manage. Symp., Research Park, NC. North Carolina State Univ., Raleigh. Strauch D. Ballarini G. 1994. Hygienic aspects of the production and agricultural use of animal wastes. Zentralbl. Veterinarmed. B  41: 176– 288. Google Scholar PubMed  Takahashi M. Nishizawa T. Miyajima H. Gotanda Y. Iita T. Tsuda F. Okamoto H. 2003. Swine hepatitis E virus strains in Japan form four phylogenetic clusters comparable with those of Japanese isolates of human hepatitis E virus. J. Gen. Virol.  84: 851– 862. https://doi.org/12655086 Google Scholar CrossRef Search ADS PubMed  Thanawongnuwech R. Amonsin A. Tantilertcharoen R. Damrongwatanapokin S. Theamboonlers A. Payungporn S. Nanthapornphiphat K. Ratanamungklanon S. Tunak E. Songserm T. Vivatthanavanich V. Lekdumrongsak T. Kesdangsakonwut S. Tunhikorn S. Poovorawan Y. 2005. Probable tiger-to-tiger transmission of avian influenza H5N1. Emerg. Infect. Dis.  11: 699– 701. https://doi.org/15890122 Google Scholar CrossRef Search ADS PubMed  Thompson R. C. A. 2004. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet. Parasitol.  126: 15– 35. https://doi.org/15567577 Google Scholar CrossRef Search ADS PubMed  Thurston-Enriquez J. A. Gilley J. E. Eghball E. 2005. Microbial quality of runoff following land application of cattle manure and swine slurry. J. Water Health  3: 157– 171. https://doi.org/16075941 Google Scholar PubMed  Tyrrel S. F. Quinton J. N. 2003. Overland flow transport of pathogens from agricultural land receiving faecal wastes. J. Appl. Microbiol.  94: 87S– 93S. https://doi.org/12675940 Google Scholar CrossRef Search ADS PubMed  Ueki Y. Akiyama K. Watanabe T. Omura T. 2004. Genetic analysis of noroviruses taken from gastroenteritis patients, river water and oysters. Water Sci. Technol.  50: 51– 56. https://doi.org/15318486 Google Scholar PubMed  USDA 2002. Part III: Reference of Swine Health and Environmental Management in the United States, 2000. Publ. N361.0902. US Dept. Agric., Anim. Plant Health Inspection Serv., Vet. Serv., Cent. Epidemiol. Anim. Health, Natl. Anim.  Health Monit. Syst., Fort Collins, CO. http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/swine/swine2000/Swine2000_dr_PartIII.pdf Accessed Jan. 3, 2010. USDA 2005. Part IV: Changes in the U.S. Pork Industry, 1990–2000. Publ. N428.0405. US Dept. Agric., Anim. Plant Health Inspection Serv., Vet. Serv., Cent. Epidemiol.  Anim. Health, Natl. Anim. Health Monit. Syst., Fort Collins, CO. http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/swine/index.htm Accessed Aug. 17 2006. US Environmental Protection Agency 1998. National water quality inventory: 1996 Report to Congress. Publ. EPA841-R-97-008. US Environ. Prot.  Agency Office of Water, Washington, DC. US Environmental Protection Agency 2005. List H: EPA's Registered Antimicrobial Products for Medical Waste Treatment.  US Environ. Prot. Agency, Washington, DC. http://www.epa.gov/oppad001/list_j_medicalwaste.pdf Accessed Sep. 14, 2006. US General Accounting Office 1999. Animal Agriculture: Waste Management Practices. Report to the Honorable Tom Harkin, ranking minority member, Committee on Agriculture, Nutrition, and Forestry, US Senate.  Publ. GAO/RCED-99-205. US General Accounting Office, Washington, DC. van der Poel W. H. Verschoor F. van der Heide R. Herrera M. I. Vivo A. Kooreman M. de Roda Husman A. M. 2001. Hepatitis E virus sequences in swine related to sequences in humans, The Netherlands. Emerg. Infect. Dis.  7: 970– 976. https://doi.org/11747723 Google Scholar CrossRef Search ADS PubMed  Van Donsel D. J. Geldreich E. E. Clarke N. A. 1967. Seasonal variations in survival of indicator bacteria in soil and their contribution to storm-water pollution. Appl. Microbiol.  16: 1362– 1370. Van Renterghem B. Huysman F. Rygole R. Verstraete W. 1991. Detection and prevalence of Listeria monocytogenes in the agricultural ecosystem. J. Appl. Bacteriol.  71: 211– 217. https://doi.org/1955415 Google Scholar CrossRef Search ADS PubMed  Varghese V. Das S. Singh N. B. Kojima K. Bhattacharya S. K. Krishnan T. Kobayashi N. Naik T. N. 2004. Molecular characterization of a human rotavirus reveals porcine characteristics in most of the genes including VP6 and NSP4. Arch. Virol.  149: 155– 172. https://doi.org/14689281 Google Scholar CrossRef Search ADS PubMed  Wang J. Mauser A. Chao S. F. Remington K. Treckmann R. Kaiser K. Pifat D. Hotta J. 2004. Virus inactivation and protein recovery in a novel ultraviolet C reactor. Vox Sang.  86: 230– 238. https://doi.org/15144527 Google Scholar CrossRef Search ADS PubMed  Wang Q. H. Souza M. Funk J. A. Zhang W. Saif L. J. 2006. Prevalence of noroviruses and sapoviruses in swine of various ages determined by reverse transcription-PCR and microwell hybridization assays. J. Clin. Microbiol.  44: 2057– 2062. https://doi.org/16757598 Google Scholar CrossRef Search ADS PubMed  Webby R. J. Webster R. G. 2001. Emergence of influenza A viruses. Philos. Trans. R. Soc. Lond.  356: 1817– 1828. Google Scholar CrossRef Search ADS   Webster R. G. 1997. Influenza virus: Transmission between species and relevance to emergence of the next human pandemic. Arch. Virol. Suppl.  13: 105– 113. https://doi.org/9413531 Google Scholar PubMed  Wells D. L. Hopfensperger D. J. Arden N. H. Harmon M. W. Davis J. P. Tipple M. A. Schonberger L. B. 1991. Swine influenza virus infections. Transmission from ill pigs to humans at a Wisconsin agricultural fair and subsequent probable person-to-person transmission. JAMA  265: 478– 481. https://doi.org/1845913 Google Scholar CrossRef Search ADS PubMed  Williams T. P. Kasorndorkbua C. Halbur P. G. Haqshenas G. Guenette D. K. Toth T. E. Meng X. J. 2001. Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J. Clin. Microbiol.  39: 3040– 3046. https://doi.org/11526125 Google Scholar CrossRef Search ADS PubMed  Xiao L. Herd R. P. Bowman G. L. 1994. Prevalence of Cryptosporidium and Giardia infections on two Ohio pig farms with different management systems. Vet. Parasitol.  52: 331– 336. https://doi.org/8073616 Google Scholar CrossRef Search ADS PubMed  Yazaki Y. Mizuo H. Takahashi M. Nishizawa T. Sasaki N. Gotanda Y. Okamoto H. 2003. Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J. Gen. Virol.  84: 2351– 2357. https://doi.org/12917455 Google Scholar CrossRef Search ADS PubMed  Yuan, L., G. W. Stevenson, and L. J. Saif 2006. Rotavirus and reovirus. Pages 435–454 in Diseases of Swine.  9th ed. B. E. Straw, J. J. Zimmerman, S. D'Allaire, and D. J. Taylor ed. Blackwell Publishing, Ames, IA. American Society of Animal Science
TI - Fate and transport of zoonotic, bacterial, viral, and parasitic pathogens during swine manure treatment, storage, and land application
JO - Journal of Animal Science
DO - 10.2527/jas.2009-2331
DA - 2010-04-01
UR - https://www.deepdyve.com/lp/oxford-university-press/fate-and-transport-of-zoonotic-bacterial-viral-and-parasitic-pathogens-0V67ko3Sxs
SP - E84
EP - E94
VL - 88
IS - suppl_13
DP - DeepDyve
ER -