Abstract
Vietnam has experienced unprecedented economic and social development in recent years, and the livestock sector is undergoing significant transformations. Although food animal production is still dominated by small-scale ‘backyard’ enterprises with mixed crop–livestock or livestock–aquatic systems, there is a trend towards more intensive and vertically integrated operations. Changes in animal production, processing and distribution networks for meat and animal products, and the shift from wet markets to supermarkets will undoubtedly impact food safety risks in Vietnam in unforeseen and complex ways. Here, we review the available published literature on bacterial and parasitic foodborne zoonoses (FBZ) in Vietnam. We report on clinical disease burden and pathogen prevalence in animal reservoirs for a number of important FBZ, and outline opportunities for future research.
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Introduction
Foodborne zoonoses (FBZ) are human infections transmitted through ingested food and caused by pathogens whose natural reservoir is a vertebrate animal species (Hubalek 2003). In industrialized countries, ~20% people suffer annually from foodborne infections (Hall et al. 2005; Painter et al. 2013); the fraction attributable to zoonotic organisms is ~50% (Liu et al. 2004, 2006; Chen et al. 2010; EFSA 2012). In Vietnam, suspect outbreaks of foodborne disease are reported to the Vietnam Food Administration (VFA) (http://vfa.gov.vn). In 2011, 148 outbreaks were reported, with 38,915 cases, 3,663 hospitalizations and 27 deaths. In most cases, FBZ aetiologies remain undetermined, and the relative disease burden compared to other infectious diseases cannot be readily quantified.
Some characteristics of animal production and food consumption habits in Vietnam that may promote zoonotic disease transmission include: (1) high density of both human and animal populations living in close proximity; (2) a predominance of smallholder production systems with mixed species and little/no biosecurity; (3) the presence of abattoirs and wet markets operating with rudimentary hygiene, limited cold chain for distribution and low levels of meat inspection; (3) widespread consumption of raw/undercooked blood, meat, fish, organ tissues, raw leaf vegetables and wild animal products and (4) use of untreated wastewater and sewage for agriculture. For these reasons, Vietnam and South East Asia are often considered a hotspot for emerging infectious diseases (Coker et al. 2011). Indeed, the threat of emerging viral pathogens has received significant international attention, while the burden of endemic (predominantly bacterial and parasitic) zoonoses remains largely neglected. Within the last two decades, Vietnam has undergone extraordinary development. Changes underway involve rapid urbanization, intensification of animal production, modernization of food marketing systems and changes in food consumption habits. These changes will undoubtedly have major impacts on human exposures to animal pathogens, and hence the overall risk of zoonotic disease transmission. Despite significant investments in improved disease surveillance systems, information on FBZ is not readily available, and veterinary services are chronically under-resourced. The objectives of this review paper are to highlight knowledge gaps on FBZ and suggest priorities and specific areas for future research.
Methods
We reviewed the available published literature in English from Vietnam on bacterial and parasitic FBZ from 1991 until January 2013. We searched PubMed for articles on food and waterborne zoonotic pathogens listed by the UK Health Protection Agency (HPA 2013), plus: ‘yersiniosis’ and ‘Yersinia enterocolitica’, ‘Fasciola’, ‘fascioliasis’, ‘Angiostrongylus cantonensis’, ‘fishborne trematodes’ and ‘Paragonimus’. Each search term was used in combination with ‘Vietnam’ and ‘Viet Nam’. We also used the same search terms to identify relevant articles published in the following Vietnamese public health and veterinary journals: (1) Tạp chì phòng 
bệnh 
rét và các bệnh ký sinh trùng (Journal of Prevention of Malaria and Parasitology); (2) Khoa học kỹ thuật thú y (Journal of Veterinary Medicine); (3) Y học thực hành (Medical Practice); (4) Y học tp. HCM (Medicine in Ho Chi Minh City); (5) Tạp chí Y học dự phòng (Journal of Preventive Medicine). None of these journals is electronically indexed. Although the emergence of antimicrobial resistance (AMR) is of paramount importance to food safety and public health in Vietnam (Dyar et al. 2012; Lestari et al. 2012), we have chosen not to address AMR, as this topic merits an extensive review on its own. Similarly, due to space limitations, we have not covered viral FBZ. We document available data on diverse FBZ, including human clinical impact and prevalence/incidence data within animal reservoirs, with a specific focus on the current situation in Vietnam.
Bacterial FBZ
Non-Typhoid Salmonella (NTS)
Non-typhoidal Salmonella (NTS) infections are caused by serovars of Salmonella enterica other than (non zoonotic) S. typhi or S. Paratyphi. Most NTS serovars are presumed to be zoonotic and potentially pathogenic to humans. NTS infections are typically self-resolving gastroenteritis, although complications may occur in children (<5 years), elderly and immunodeficient patients (Pegues and Miller 2010). NTS may infect a wide range of animals (both domestic and wild), but the vast majority do not to cause detectable pathology in the reservoir host.
In Vietnam, improvements in sanitation have resulted in dramatic reductions of typhoid over recent decades. In southern Vietnam, S. typhi cases reduced from 497 in 1994 to 34 in 2008, with a concurrent increase of invasive cases of NTS (from 9 to 24) (Nga et al. 2012). Studies on NTS in humans in Vietnam are summarized in Table 1. NTS prevalence in various farm animals (pre-slaughter) and in slaughter and retail facilities is summarized in Table 2. Detected levels in meat are high, suggesting widespread contamination during slaughtering/processing. Contaminated fish products likely reflect widespread use of animal/human sewage in aquaculture. Serovar or molecular data from animals and humans are limited, so it is difficult to establish the main sources of human infection. Epidemiological data suggests that person-to-person transmission plays a major role (Thompson et al. 2012). NTS carriage has been detected in ~5% of healthy adults (personal communication).
Campylobacteriosis
Globally, Campylobacter is the single most common human bacterial diarrhoeal pathogen, and together with NTS, account for ~90% of foodborne bacterial disease. In Vietnam, as in other countries, C. jejuni is the dominant species found in paediatric clinical cases (~85%) (Isenbarger et al. 2001), with the remainder due to C. coli.
Reported Campylobacter prevalence in Vietnamese poultry meat ranges from 28 to 31% (Ha and Pham 2006; Luu et al. 2006). A 2005–2006 investigation of Campylobacter spp. at slaughterpoints in five cities worldwide indicated lowest prevalence in Ho Chi Minh City (HCMC) (15.3%, vs. an overall prevalence of 65.5%); 74% were C. lari, 9% C. coli, 4% C. jejuni and 13% other species. Semi-industrial poultry slaughtering was associated with lower contamination than informal direct slaughter by sellers (Garin et al. 2012). In Vietnam, there are no published data on pre-slaughter (on-farm) prevalence or Campylobacter species diversity.
The relative contribution of Campylobacter and NTS to diarrhoea is not particularly high, and asymptomatic infections appear to be common (Table 1). Given the widespread prevalence of NTS and Campylobacter in food products, and the intense human–animal exposures for most rural Vietnamese, the low incidence of clinical disease may reflect high levels of population immunity.
Listeriosis
Listeria monocytogenes causes abortion and sepsis-like infection in humans, especially among immunocompromised individuals, neonates, pregnant women and the elderly. Clinical L. monocytogenes infection was confirmed in 2008–2009, among three patients with meningitis in Hanoi (Chau et al. 2010; Tran et al. 2010). Listeriosis has been linked to consumption of unpasteurised soft cheeses, processed meat and fish products. A study of fish and seafood products from Nha Trang Bay (central Vietnam) identified L. monocytogenes in 5.8% (Beleneva 2011).
There are no data on prevalence of L. monocytogenes in meat products in Vietnam, but studies in the region (Thailand) suggest a high prevalence of L. monocytogenes in raw meats, especially in those sold in supermarkets (Indrawattana et al. 2011). In Vietnam, meat is increasingly bought from supermarkets, especially in urban areas.
Streptococcus suis
Streptococcus suis is an emerging human infection in Vietnam. The clinical picture is typically severe, and may involve skin, respiratory, neurological, cardiovascular and gastrointestinal systems. The largest S. suis outbreak recorded occurred in China in 2005, with 215 confirmed cases among pig slaughterers (Yu et al. 2006). Aetiological studies in Vietnam of cerebrospinal fluid from >2,000 patients (1996–2010) with suspect CNS infection have identified S. suis serotype 2 in 8.9–33.6% diagnosed patients (Mai et al. 2008; Wertheim et al. 2009b; Ho Dang Trung et al. 2012), confirming S. suis as the most frequent cause of bacterial meningitis in adults. About 66% patients experienced hearing loss as a sequela (Mai et al. 2008). Serotype 2 accounts for 96% of human cases, but other serotypes (i.e. 16, 14) have also occurred (Nghia et al. 2008). A case–control study identified the following risk factors: (1) eating undercooked pig blood/intestine; (2) occupation related to pigs; and (3) exposure to pigs while having skin injuries (Nghia et al. 2011). Due to poorly regulated marketing systems, ill pigs may enter the food chain, thus posing a significant risk to both slaughterhouse workers and consumers. Consumption of pig blood, intestines and organ meats is common in Vietnam (Wertheim et al. 2009a).
Streptococcus suis carriage rates of 41% (n = 542) have been identified in healthy Vietnamese pigs. Serotype 2 appears to be dominant (14%), followed by serotypes 3, 21, 21 and 16 (Ngo et al. 2011). High numbers of pigs infected with Porcine Respiratory Reproductive Syndrome (PRRS) virus have tested positive for S. suis in blood, indicating concurrent viraemic and bacteraemic infections (Hoa et al. 2013).
Leptospirosis
Leptospirosis is caused by several pathogenic species within the genus Leptospira. Humans become infected through cuts, skin abrasions or by drinking contaminated water. Symptoms can range from mild, influenza-like illness to severe infection with renal and hepatic failure, pulmonary distress and death (Adler and de la Pena Moctezuma 2010).
Studies of acute jaundice in Hanoi and HCMC from 1993 to 1997 (n = 550 patients) reported 8 and 2% leptospirosis, respectively. The most commonly identified serovars were Seramanga and Bataviae (Laras et al. 2002). A serosurvey in the Mekong Delta reported high seropositivity (21%) among 36–45 year olds, with detection of Bataviae (21.7%), Panama (15.2%), Icterohaemorrhagiae (13.7%), and Australis (8.7%). In that study, walking barefoot was a significant risk factor for seropositivity, but not contact with animals (Van et al. 1998). A 2003 survey of children (n = 961) in southern Vietnam identified anti-Leptospira IgG in 12.8%, a 1.5:1 male: female ratio of seropositivity, and significant association with swimming in rivers. Based on IgG seroconversion, a 0.99% annual incidence was estimated (Thai et al. 2006).
Leptospiras have a broad range of animal reservoirs. Most studies in Vietnam have focused on pigs due to their impact on swine reproduction. In the Mekong Delta, Bratislava, Icterohaemorrhagiae, Automnalis, Grippotyphosa and Pomona are the most common serovars, with higher prevalence in small-scale farms compared to large holdings (Boqvist et al. 2002a, b). In general, there appears to be little overlap between serovars in pigs and humans; however, there is a paucity of surveillance data on which to judge exposures and epidemiological associations. The diffuse clinical picture and lack of straightforward diagnostics for leptospirosis (Wagenaar et al. 2004; Smythe et al. 2009) hamper adequate case reporting from Vietnam.
Parasitic FBZ
Toxoplasmosis
Toxoplasmosis is caused by the larval stage of the protozoan Toxoplasma gondii. Humans become infected by ingesting cysts (from undercooked meat/viscera), or oocysts released from the definitive host (the domestic cat) that contaminate food, water or the environment. Clinical signs range from mild to severe due to invasion of muscle, brain and eyes. Congenital toxoplasmosis occurs due to primary maternal infection during gestation (Montoya et al. 2010).
In Vietnam, a number of T. gondii serosurveys have been conducted (Table 3). Human seroprevalence is not particularly high (1–24%); in animals it ranges from low/medium (3% buffalo, 10% cattle) to high (23% pigs; 29% poultry; 50% domestic dogs). There are no published data on prevalence in domestic cats. Pigs are likely to play a major role in T. gondii infection, since pork is the most commonly consumed meat. In Thailand, a high prevalence in stray dogs has also been reported (Jittapalapong et al. 2007). Domestic dogs may also be relevant to transmission, since stray dogs are often imported from Thailand to supply dog meat restaurants. In southeast Asia, culinary habits (e.g. eating undercooked meat) and low water quality may be a more significant risk factor for T. gondii than cat ownership (Nissapatorn et al. 2003).
Cryptosporidiosis
Cryptosporidiosis is caused by protozoa of the genus Cryptosporidium. Of ~20 Cryptosporidium species, seven are zoonotic (Fayer 2004), the most common one being C. parvum bovine genotype 2. Transmission is through ingested contaminated water and vegetables, although person-to-person transmission has been also documented. Most outbreaks have been attributed to C. parvum and linked to a waterborne source (Clinton White 2010). Studies in Vietnam have not found evidence of Cryptosporidium clinical disease among children with diarrhoea (Uga et al. 2005; Bodhidatta et al. 2007).
Cattle are thought to be the most common source of C. parvum genotype 2, although infection of pigs has also been described (Jenkins et al. 2010). A study of 266 cattle in three central provinces found 33.5% C. parvum positive (Nguyen et al. 2007a). Another study from the Red River Delta failed to detect Cryptosporidium among 68 healthy calves, but found 50% positive for Giardia (Geurden et al. 2008). A Cryptosporidium prevalence of 18% among diarrheic pigs of central Vietnam was reported (Nguyen et al. 2012), however, speciation was not performed, thus the implications for zoonotic transmission were unclear. C. parvum has been detected in farmed fish from southern Vietnam in association with wastewater used in aquaculture (Gibson-Kueh et al. 2011).
Giardiasis
Giardia lamblia is a protozoan cause of diarrhoea found in soil, food, and water contaminated with faeces from infected humans or animals. G. lamblia has a very broad host range, and some subtypes/species are zoonotic. Recent molecular analysis of specific genetic assemblages suggests a high degree of host-specificity, with limited potential to infect humans (Xiao and Fayer 2008). A study on children less than 3 years old with severe diarrhoea in Hanoi identified G. lamblia among 2.4% (Ngan et al. 1992). Healthy people (N = 2,522) in north-western Vietnam had a surprisingly high prevalence (4.1%) (Verle et al. 2003). A study in calves less than 3 months old showed that Giardia spp. were the most prevalent parasites (50%); further characterization of 17 isolates indicated that all were non-zoonotic G. duodenalis (Geurden et al. 2008). Both Giardia and Cryptosporidium represent a challenge to safe drinking and recreational water supplies, due to their resistance to chlorine and environmental persistence.
Taeniasis/Cysticercosis
Taeniasis and cysticercosis are distinct disease entities caused by different life stages of Taenia spp. Taeniasis refers to human enteric infection with the adult tapeworm, after ingestion of taenid cysts (cysticerci) present in undercooked beef (T. saginata) and pork (T. solium and T. asiatica). Cysticercosis are infections caused by ingestion of taenid eggs. Over the past decades, incidence of cysticercosis has decreased substantially worldwide owing to improved animal husbandry, sanitation and better meat inspection (Sotelo 2003).
Studies on taeniasis and cysticercosis in humans are shown in Table 4. During the 1990s, approximately 100–150 patients with neurocysticercosis were annually referred to Hanoi hospitals (Ky and Van Chap 2000). In addition, serosurveys published in Vietnamese suggest a large variation in prevalence among adults (0.2–7.2%) (Willingham et al. 2003).
Pig infections with cysticerci may result in reduced carcass value or full condemnation. A 1989–1992 study of meat carcasses in Hanoi indicated low prevalence (<0.1%). A 1999–2000 swine serosurvey indicated ~10% prevalence of cysticerci; however, cysts were T. hydatigena, for which the domestic dog is the final host (Dorny et al. 2004). Taenid eggs and T. solium cysts have been found in vegetables and dog meat sold in Hanoi (Uga et al. 2009; Willingham et al. 2010). Eating raw/pickled pork (i.e. ‘nem chua’) may be a major risk factor, as well as agricultural use of human wastewater as fertilizer (Dorny et al. 2004). To date, T. asiatica has not been reported from pigs in Vietnam, suggesting there may be other non-porcine intermediate hosts (Dorny et al. 2007). It is not yet clear whether T. asiatica causes cysticercosis (Galan-Puchades and Fuentes 2009). The presence of both T. saginata and T. asiatica in Vietnam may limit transmission of the more serious T. solium infection due to cross-protection (Conlan et al. 2009).
Trichinellosis
Trichinellosis is caused by ingestion of encysted larvae of the genus Trichinella, predominantly from contaminated pork. T. spiralis is the most common species, found in pigs, wild boars and other species (Pozio et al. 2009). In humans, the clinical spectrum ranges from mild fever to myalgia and fulminating fatal disease. Like cysticercosis, the incidence of Trichinellosis has been decreasing worldwide over the last century. Data on Trichinella from Vietnam are limited to a few reports of sporadic outbreaks (~25 cases each) reported since 1970 in remote northern provinces (Dien Bien, Yen Bai and Son La), all traced back to consumption of undercooked/fermented pork (Taylor et al. 2009). A 2008–2009 serosurvey for T. spiralis in 1,035 free-roaming pigs reported age-dependent increases in seroprevalence, with overall seropositivity of 20%, and Trichinella larvae in 14.5% (Thi et al. 2010).
Fascioliasis
Fascioliasis is caused by liver flukes of two species, Fasciola hepatica and F. gigantica. Humans become infected through ingestion of water or freshwater plants with adherent metacercaria (Mas-Coma 2005; Ashrafi et al. 2006) or juvenile forms (Taira et al. 1997). The parasite requires replication in Lymnea snails as intermediate hosts.
In Vietnam, fascioliasis has been increasingly diagnosed since the 1990s, mostly in ruminant-producing areas during the rainy season (De et al. 2003) (Table 5). Aberrant clinical forms (cutaneous fascioliasis) have been reported in association with F. gigantica (Xuan et al. 2005; Le et al. 2007). A hybrid of F. hepatica and F. gigantica has been reported from humans, cattle (Le et al. 2008) and goats (Nguyen et al. 2009). Parasite burdens are likely to have important economic repercussions for livestock production.
It is unclear whether increasing case numbers of fascioliasis represent disease emergence or improved laboratory diagnostics and reporting. Changes in environmental factors and/or livestock production (i.e. increasing stocking densities, use of cattle faeces as fertilizer) may contribute to transmission (Tran et al. 2001b; De et al. 2003).
Fish-Borne Zoonotic Trematodes (FZT)
FZT comprise a large group of flukes of the families Heterophyidae, Echinostomatidae and Opistorchiidae (Chai et al. 2005). Adult liver flukes live in the biliary tract of a range of vertebrates. Eggs are released in the environment; the miracidium penetrates freshwater snail tissues, where it develops into free-swimming cercariae that infect cyprinid freshwater fish. Within the fish host, parasites invade muscle and transform into metacercariae that are infectious for humans. Although most human FZT infections are subclinical, Clonorchis sinensis and Opistorchis verrini may cause chronic liver infection, pancreatitis, cholangitis and cancer (Choi et al. 2006; Mayer and Fried 2007). C. sinensis is widely distributed in East Asia and is endemic to the Red River Delta, whereas O. viverrini is present in Laos, Cambodia, Thailand and southern Vietnam.
Approximately, one million people are infected with FZT in Vietnam (Kino et al. 1998). Overall, low to moderate levels of FZT are found within healthy individuals. Epidemiological studies indicate significant geographic variability, associations with culinary habits, and widespread infection of diverse animal species (Table 6). During 2009–2010, an intervention study in 18 fish nurseries introduced snail control by pond draining and treatment of humans and domestic cats. Examination of ~15,000 fish after 9 weeks of intervention indicated moderate success in reducing fish infection rates with FZT (Hedegaard Clausen et al. 2012). Given that human, pig and poultry excreta are commonly used as fish feed, and that snails and fish are fed to poultry, it is likely that multiple vertebrate species play a role in maintaining FZT transmission. There are strong economic and trade incentives to reduce transmission to promote successful development of aquaculture exports.
Paragonimiasis
Paragonimiasis is a lower respiratory tract infection caused by lung Paragonimus flukes. Humans become infected through consumption of infective metacercariae from raw or undercooked crustaceans. Eggs are voided by infected people in sputum or faeces; in the environment, the parasite goes through several stages involving snails and then crayfish or crabs as hosts. Symptoms are sometimes mistaken with chronic tuberculosis (Vijayan 2009). Clinical cases in Vietnam have been documented from mountainous regions, linked to consumption of infected crabs (Table 7). Vietnamese domestic dogs and pigs infected with Paragonimus have been reported (Queuche et al. 1997). Species identified from Vietnam include P. heterotremus, P. vietnamiensis, P. proliferus (northern mountainous areas) and P. westermani (central Vietnam) (Doanh et al. 2007, 2008, 2009). In spite of mass screening, treatment and education programmes, paragonimiasis remains a problem in a limited number of areas of the country.
Gnathostomiasis
Gnathostomiasis occurs wherever consumption of raw fish is common. Human infections are acquired by ingestion of advanced third stage larvae (AL3) of Gnathostoma spp. present in fish species. Humans are paratenic hosts; the larvae commonly migrate through subcutaneous tissues, visceral organs and the central nervous system. G. spinigerum is the most common species in Southeast Asia, usually found in swamp eels (Monopterus albus) (Waikagul and Diaz Camacho 2007).
Until 1998 only three cases of G. spinigerum had been documented in Vietnam; however, introduction of serological tests since then led to hundreds of cases since. A study indicated that 63.8% had cutaneous and 14.7% had visceral manifestations (Xuan et al. 2004). Severe eye infection due to G. spinigerum was reported in the Mekong Delta (Xuan le et al. 2002). Market surveys of eels (n = 1,081) in HCMC identified G. spinigerum AL3 in 0.11% (Le and Rojekittikhun 2000). Prevalence was higher in wild-caught eels and at the end of the rainy season (Sieu et al. 2009).
Other FBZ Reported in the Vietnamese Literature
Between 2006 and 2011, 413 human cases and three anthrax deaths were reported in northern Vietnam. All had a history of slaughtering/eating dead ruminants (Tran and Pham 2012). Studies on suspect cases of Toxocara canis using serology confirmed 83 visceral and 33 ocular infections (Tran et al. 2001a; Le et al. 2012). A 2004 serological study of 1,201 dairy cattle in HCMC reported negative results for M. bovis (ELISA) and Brucella spp. (Nguyen et al. 2006).
Discussion
Our review of 95 publications reveals the highly diverse range of endemic pathogens associated with FBZ in Vietnam. Although a systematic ranking of disease burden associated with FBZ is not possible at this time, the pathogens fall largely into three groups: (1) pathogens that are relatively more common as causes of clinical disease in Vietnam than in developed temperate-zone countries; (2) pathogens known to be present in Vietnam that are not responsible for a particularly high disease burden; and (3) FBZ which may be fairly common, but for which the dearth of either research or surveillance data in Vietnam prohibits making any valid assessments of relative burden.
In the interest of maximizing development impacts and pursuing a One Health research agenda, there are clear imperatives to prioritize research on zoonoses within group 1 that also cause significant production losses and incur the highest economic costs to farmers. We suggest that Streptococcus suis, Leptospira, Fasciola and fish-borne trematode infections meet these criteria, and that a better understanding of the transmission ecology of these pathogens within smallholder production systems could readily generate improved control options with benefits to both human and animal health. In contrast, Campylobacter and NTS belong to the second category of FBZ, for which the clinical disease does not appear to rank particularly high; although elsewhere in the world Campylobacter and NTS are dominant causes of foodborne diarrhoea, and are the focus of intense multinational control efforts. The influence of human–animal contact rates and human population immunity to Campylobacter and NTS merits further research, since future changing patterns of exposure may drive a shift in the age-related incidence of infection. Unfortunately, the majority of pathogens fall within category 3, for which data sources are entirely inadequate to estimate burden.
Potential impacts of ongoing urbanization and economic development on FBZ in Vietnam are summarized in Table 8, alongside suggested areas for further research and improved surveillance. Surveillance of FBZ remains one of the weakest aspects of the health systems in Vietnam. In most cases, hospitals do not carry out routine diagnosis of most bacterial and parasitic FBZ. Serious diseases such as leptospirosisa and toxoplasmosis are often not adequately diagnosed and reported.
The pace of industrialization of Vietnam’s farming systems varies by sector and region. The trend is towards increasing farm sizes with higher stocking densities and modern management (all-in all-out systems, synchronized breeding, etc.). In the last decade, central decisions made at the Ministry of Agriculture and Rural Development and the Department of Livestock Production to promote restructuring of the poultry sector was viewed as a way to improve control of highly pathogenic avian influenza (HPAI). Although consolidation undoubtedly provides many more opportunities for increased biosecurity at the farm level, it may also increase vulnerabilities to dissemination of pathogens across the food chain. Changes in pathogen exposure, increased stress and breed and management factors may alter herd/flock immunity and pathogen population dynamics. The risk of pathogen emergence in modern versus traditional production systems has received some attention, but largely in relation to viruses (Drew 2011; Graham et al. 2008). It remains to be seen whether knowledge gained on drivers of viral emergence can be generalized to bacterial and parasitic FBZ.
In spite of government efforts to promote consolidation, smallholder mixed crop–livestock production remains dominant in Vietnam. Use of animal/human excreta and feed leftovers is common, especially within the ‘VAC system’ (Vuon = garden, Ao = pond and Chuong = pig pen) (Pham Duc et al. 2011). Such integrated systems provide efficient nutrient recycling, but also may promote transmission of parasites whose life cycles involve invertebrates. VAC systems are now less common in Vietnam than a few decades ago, due to alternatives for use of animal excreta (i.e. biogas) as well as increasing constraints on land use and increased land costs. Government programmes and development projects aimed at improving sanitation have resulted in safer human waste disposal. Where human excreta are used as fertilizer, a minimum of 6-month retention period is recommended to ensure pathogen inactivation. The level of compliance with this norm is not known, although some data suggests good adherence (Phuc et al. 2006). VAC systems are of course particularly vulnerable to fish-borne trematode infections, whereas industrial aquaculture operations provide increased investments in infrastructure for both quality and safety control, through the use of commercial laboratories for pathogen screening and chemical pest control of invertebrates. In the swine sector, investments in housing and improved nutrition are expected to reduce the burden of parasitic diseases such as taeniasis/cysticercosis and trichinellosis. Intensified bovine and dairy production may increase the risk of introducing cattle-associated FBZ such as bovine tuberculosis and brucellosis. Finally, for target organisms that are particularly associated with processed animal foods, such as listeriosis, increased consumption of processed food items such as soft cheeses, sausages and pates may result in increased incidence unless production of these commodities is adequately regulated.
In Vietnam, per capita ingestion of animal protein has steadily increased over the last few years (Thang and Popkin 2004) and in urban areas, the consumption of chilled, frozen and processed meat is rapidly increasing (Anon. 2011). Modern retail outlets (supermarkets, convenience stores, etc.) now account for >15% of total food distribution (Cadilhon et al. 2006), and fast-food restaurants are rapidly proliferating. Consumption of wild-animal meat has also been increasing among wealthy sectors of the population; these ‘exotic’ products pose novel and unforeseen food safety risks (Drury 2011).
In the past, regulation of food safety in Vietnam has been hampered by highly decentralized authority for monitoring value chains. A Food Safety Law (No. 55/QH12/2010) seeks to impact quality control of slaughter and processing facilities within food distribution networks, in part through clarifying new standards and regulatory policies. Examples include the development of certification systems for good food production and slaughtering practices, increase traceability and strengthening of penalties for marketing uncertified animals. Better control of food chains is likely to improve control of diseases associated with unregulated marketing (i.e. S. suis). In addition, measures such as zoning regulations on the proximity of production units close to open waterways or urban centres have been introduced. Although the impetus for many of these reforms is driven by the threat of avian influenza pandemics, the measures will likely have an impact both on disease transmission and cultural practices. Efforts to expand export markets of agricultural commodities are also providing an incentive to improve quality controls and laboratory testing; these developments are likely to be driven by the private sector and will target organisms such as NTS to meet international regulatory standards.
In summary, the rapid intensification of animal food production systems and urbanization in Vietnam will undoubtedly change the landscape of food safety risks, introducing both new opportunities for control and prevention, as well as new vulnerabilities for the spread of disease. Within this context, the key for understanding and monitoring changes will be a strengthened infrastructure for surveillance, both of human clinical disease and within the veterinary community.
References
Adler B, and de la Pena Moctezuma A (2010). Leptospira and leptospirosis. Vet Microbiol 140:287-296.
Anderson N, Luong TT, Vo NG, Bui KL, Smooker PM, and Spithill TW (1999). The sensitivity and specificity of two methods for detecting Fasciola infections in cattle. Vet Parasitol 83:15-24.
Anh NT, Madsen H, Dalsgaard A, Phuong NT, Thanh DT, and Murrell KD (2010). Poultry as reservoir hosts for fishborne zoonotic trematodes in Vietnamese fish farms. Vet Parasitol 169:391-394.
Anonymous (2011) Packaged Food in Vietnam. International Markets Bureau. Agriculture and Agri-Food, Government of Canada. http://ats.agr.gc.ca/ase/5822-eng.htm. Accessed January 10, 2013.
Ashrafi K, Valero MA, Massoud J, Sobhani A, Solaymani-Mohammadi S, Conde P, et al. (2006). Plant-borne human contamination by fascioliasis. Am J Trop Med Hyg 75:295-302.
Beleneva I (2011). Incidence and characteristics of Staphylococcus aureus and Listeria monocytogenes from the Japan and South China seas. Marine Pollution Bulletin 62:382-387.
Bodhidatta L, Lan NT, Hien BT, Lai NV, Srijan A, Serichantalergs O, et al. (2007). Rotavirus disease in young children from Hanoi, Vietnam. Pediatr Infect Dis J 26:325-328.
Boqvist S, Chau BL, Gunnarsson A, Engvall EO, Vagsholm I, and Magnusson U (2002a). Animal- and herd-level risk factors for leptospiral seropositivity among sows in the Mekong Delta, Vietnam. Preventive Veterinary Medicine 53:233-245.
Boqvist S, Thu HTV, Vagsholm I, and Magnusson U (2002b). The impact of Leptospira seropositivity on reproductive performance in sows in southern Viet Nam. Theriogenology 58:1327-1335.
Cadilhon J, Moustier N, Poole N, Tam P, and Fearne P (2006). Traditional vs. modern food systems? Insights from vegetable supply chains to Ho Chi Minh City (Vietnam). Development Policy Review 24:31-49.
Chai JY, Darwin Murrell K, and Lymbery AJ (2005). Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35:1233-1254.
Chau TT, Campbell JI, Schultsz C, Chau NV, Diep TS, Baker S, et al. (2010). Three adult cases of Listeria monocytogenes meningitis in Vietnam. PLoS Med 7:e1000306.
Chau TTH, Campbell J, Schultsz C, Nguyen C, To D, Baker S et al (2010) Three adult cases of Listeria monocytogenes Meningitis in Vietnam. PLoS Medicine 7:e1000306.
Chen Y, Guo Y, Wang Z, Liu X, Liu H, Dai Y, et al. (2010). [Foodborne disease outbreaks in 2006 report of the National Foodborne Disease Surveillance Network, China]. Wei Sheng Yan Jiu 39:331-334.
Chi TT, Dalsgaard A, Turnbull JF, Tuan PA, and Murrell KD (2008). Prevalence of zoonotic trematodes in fish from a Vietnamese fish-farming community. J Parasitol 94:423-428.
Choi D, Lim JH, Lee KT, Lee JK, Choi SH, Heo JS, et al. (2006). Cholangiocarcinoma and Clonorchis sinensis infection: a case-control study in Korea. J Hepatol 44:1066-1073.
Clinton White J (2010). Cryptosporidium species. Pages 3547-3586 in G. Mandell, J. Bennet, and R. Dolin, editors. Principle and Practice of Infectious Diseases. Churchill Livingstone Elsevier, Philadelphia.
Coker RJ, Hunter BM, Rudge JW, Liverani M, Hanvoravongchai P (2011). Health in Southeast Asia 3: Emerging infectious diseases in southeast Asia: regional challenges to control. Lancet 377: 599-609.
Conlan JV, Vongxay K, Fenwick S, Blacksell SD, and Thompson RC (2009). Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia? Trends Parasitol 25:398-403.
Dang TC, Yajima A, Nguyen VK, and Montresor A (2008). Prevalence, intensity and risk factors for clonorchiasis and possible use of questionnaires to detect individuals at risk in northern Vietnam. Trans R Soc Trop Med Hyg 102:1263-1268.
De NV (2004). Fish-borne trematodes in Vietnam. Southeast Asian J Trop Med Public Health 35: 299-301.
De NV, and Le TH (2011). Human infections of fish-borne trematodes in Vietnam: prevalence and molecular specific identification at an endemic commune in Nam Dinh province. Exp Parasitol 129:355-361.
De NV, Murrell KD, Cong LD, Cam PD, Chau LV, Toan ND, et al. (2003). The food-borne trematode zoonoses of Vietnam. The Southeast Asian journal of tropical medicine and public health 34 Suppl 1:12-34.
Do TT, Bui TT, Molbak K, Phung DC, and Dalsgaard A (2007). Epidemiology and aetiology of diarrhoeal diseases in adults engaged in wastewater-fed agriculture and aquaculture in Hanoi, Vietnam. Trop Med Int Health 12 Suppl 2:23-33.
Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, and Le NT (2007). Description of a new lung fluke species, Paragonimus vietnamensis sp. nov. (Trematoda, Paragonimidae), found in northern Vietnam. Parasitol Res 101:1495-1501.
Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, and Le NT (2008). Discovery of Paragonimus proliferus in Northern Vietnam and their molecular phylogenetic status among genus Paragonimus. Parasitol Res 102:677-683.
Doanh PN, Shinohara A, Horii Y, Habe S, and Nawa Y (2009). Discovery of Paragonimus westermani in Vietnam and its molecular phylogenetic status in P. westermani complex. Parasitol Res 104:1149-1155.
Doanh PN, Dung do T, Thach DT, Horii Y, Shinohara A, and Nawa Y (2011). Human paragonimiasis in Viet Nam: epidemiological survey and identification of the responsible species by DNA sequencing of eggs in patients’ sputum. Parasitol Int 60:534-537.
Dorny P, Somers R, Cam Thi Dang T, Khong Nguyen V, and Vercruysse J (2004). Cysticercosis in Cambodia, Lao PDR and Vietnam. Southeast Asian J Trop Med Public Health 35:223-226.
Dorny P, Somers R, and Vercruysse J (2007). Response to comment on: Human tapeworms in north Vietnam. Transactions of the Royal Society of Tropical Medicine and Hygiene 101:629-630.
Drew TW (2011). The emergence and evolution of swine viral diseases: to what extent have husbandry systems and global trade contributed to their distribution and diversity? Rev Sci Tech 30:95-106.
Drury R (2011). Hungry for success: urban consumer demand for wild animal products in Vietnam. Conservation and Society 9:247-257.
Dubey JP, Huong LT, Sundar N, and Su C (2007). Genetic characterization of Toxoplasma gondii isolates in dogs from Vietnam suggests their South American origin. Vet Parasitol 146:347-351.
Dubey JP, Huong LT, Lawson BW, Subekti DT, Tassi P, Cabaj W, et al. (2008). Seroprevalence and isolation of Toxoplasma gondii from free-range chickens in Ghana, Indonesia, Italy, Poland, and Vietnam. J Parasitol 94:68-71.
Dyar OJ, Hoa NQ, Trung NV, Phuc HD, Larsson M, Chuc NT, et al. (2012). High prevalence of antibiotic resistance in commensal Escherichia coli among children in rural Vietnam. BMC Infect Dis 12:92.
EFSA (2012). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2010. EFSA Journal 10:2597.
Ellerbroek L, Narapati D, Tai NP, Poosaran N, Pinthong R, Sirimalaisuwan A, et al. (2010). Antibiotic Resistance in Salmonella Isolates from Imported Chicken Carcasses in Bhutan and from Pig Carcasses in Vietnam. Journal of Food Protection 73:376-379.
Erhart A, Dorny P, Van De N, Vien HV, Thach DC, Toan ND, et al. (2002). Taenia solium cysticercosis in a village in northern Viet Nam: seroprevalence study using an ELISA for detecting circulating antigen. Trans R Soc Trop Med Hyg 96:270-272.
Fayer R (2004). Cryptosporidium: a water-borne zoonotic parasite. Vet Parasitol 126:37-56.
Galan-Puchades MT, and Fuentes MV (2009). Diagnosis of human cysticercosis and Taenia asiatica. Am J Trop Med Hyg 81:1165; author reply 1166.
Garin B, Gouali M, Wouafo M, Perchec AM, Thu PM, Ravaonindrina N, et al. (2012). Prevalence, quantification and antimicrobial resistance of Campylobacter spp. on chicken neck-skins at points of slaughter in 5 major cities located on 4 continents. International Journal of Food Microbiology 157:102-107.
Geurden T, Somers R, Thanh NT, Vien LV, Nga VT, Giang HH, et al. (2008). Parasitic infections in dairy cattle around Hanoi, northern Vietnam. Vet Parasitol 153:384-388.
Gibson-Kueh S, Yang R, Thuy NT, Jones JB, Nicholls PK, and Ryan U (2011). The molecular characterization of an Eimeria and Cryptosporidium detected in Asian seabass (Lates calcarifer) cultured in Vietnam. Vet Parasitol 181:91-96.
Graham JP, Leibler JH, Price LB, Otte JM, Pfeiffer DU, Tiensin T, et al. (2008). The animal–human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainment. Public Health Rep 123:282-299.
Ha TA, and Pham TY (2006). Study of Salmonella, Campylobacter, and Escherichia coli contamination in raw food available in factories, schools, and hospital canteens in Hanoi, Vietnam. Ann N Y Acad Sci 1081:262-265.
Hall G, Kirk MD, Becker N, Gregory JE, Unicomb L, Millard G, et al. (2005). Estimating foodborne gastroenteritis, Australia. Emerg Infect Dis 11:1257-1264.
Hedegaard Clausen J, Madsen H, Murrell KD, Van PT, Thu HN, Do DT, et al. (2012). Prevention and control of fish-borne zoonotic trematodes in fish nurseries, Vietnam. Emerg Infect Dis 18:1438-1445.
Hien BT, Trang do T, Scheutz F, Cam PD, Molbak K, and Dalsgaard A (2007). Diarrhoeagenic Escherichia coli and other causes of childhood diarrhoea: a case-control study in children living in a wastewater-use area in Hanoi, Vietnam. J Med Microbiol 56:1086-1096.
Ho Dang Trung N, Le Thi Phuong T, Wolbers M, Nguyen Van Minh H, Nguyen Thanh V, Van MP, et al. (2012). Aetiologies of central nervous system infection in Viet Nam: a prospective provincial hospital-based descriptive surveillance study. PLoS One 7:e37825.
Hoa NT, Chieu TTB, Dung SD, Long NT, Quoc T, Hieu TQ, et al. (2013). S. suis serotype 2 and PRRSV in pigs, Vietnam 2010. Emerg Infect Dis 19:331-333.
Holland WG, Luong TT, Nguyen LA, Do TT, and Vercruysse J (2000). The epidemiology of nematode and fluke infections in cattle in the Red River Delta in Vietnam. Vet Parasitol 93:141-147.
Hong TTT, Linh NQ, Ogle B, and Lindberg JE (2006). Survey on the prevalence of diarrhoea in pre-weaning piglets and on feeding systems as contributing risk factors in smallholdings in Central Vietnam. Tropical Animal Health and Production 38:397-405.
HPA (2013) Table of Zoonotic Diseases and Organisms. http://www.hpa.org.uk/Topics/InfectiousDiseases/InfectionsAZ/Zoonoses/TableZoonoticDiseases. Accessed March 12, 2012.
Hubalek Z (2003). Emerging human infectious diseases: anthroponoses, zoonoses, and sapronoses. Emerg Infect Dis 9:403-404.
Huong LT, and Dubey JP (2007). Seroprevalence of Toxoplasma gondii in pigs from Vietnam. J Parasitol 93:951-952.
Huong LT, Ljungstrom BL, Uggla A, and Bjorkman C (1998). Prevalence of antibodies to Neospora caninum and Toxoplasma gondii in cattle and water buffaloes in southern Vietnam. Vet Parasitol 75:53-57.
Indrawattana N, Nibaddhasobon T, Sookrung N, Chongsa-Nguan M, Tungtrongchitr A, Makino S, et al. (2011). Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methods. J Health Popul Nutr 29:26-38.
Isenbarger D, Hien B, Ha H, Ha T, Bodhidatta L, Pang L, et al. (2001). Prospective study of the incidence of diarrhoea and prevalence of bacterial pathogens in a cohort of Vietnamese children along the Red River. Epidemiol Infect 127:229-236.
Jenkins MB, Liotta JL, Lucio-Forster A, and Bowman DD (2010). Concentrations, viability, and distribution of Cryptosporidium genotypes in lagoons of swine facilities in the Southern Piedmont and in coastal plain watersheds of Georgia. Appl Environ Microbiol 76:5757-5763.
Jittapalapong S, Nimsupan B, Pinyopanuwat N, Chimnoi W, Kabeya H, and Maruyama S (2007). Seroprevalence of Toxoplasma gondii antibodies in stray cats and dogs in the Bangkok metropolitan area, Thailand. Vet Parasitol 145:138-141.
Khan MI, Ochiai RL, von Seidlein L, Dong B, Bhattacharya SK, Agtini MD, et al. (2010). Non-typhoidal Salmonella rates in febrile children at sites in five Asian countries. Trop Med Int Health 15:960-963.
Kino H, Inaba H, Van De N, Van Chau L, Son DT, Hao HT, et al. (1998). Epidemiology of clonorchiasis in Ninh Binh Province, Vietnam. Southeast Asian J Trop Med Public Health 29:250-254.
Ky H, and Van Chap N (2000). Radioclinical aspects of cerebral and muscular cysticercosis: 20 cases. Journal of Neuroradiology 27:264-266.
Lan-Anh NT, Phuong NT, Murrell KD, Johansen MV, Dalsgaard A, Thu LT, et al. (2009). Animal reservoir hosts and fish-borne zoonotic trematode infections on fish farms, Vietnam. Emerg Infect Dis 15:540-546.
Laras K, Van CB, Bounlu K, Tien NTK, Olson JG, Thongchanh S, et al. (2002). The importance of leptospirosis in Southeast Asia. American Journal of Tropical Medicine and Hygiene 67:278-286.
Le Bas C, Tran TH, Nguyen TT, Dang DT, Ngo CT (2006) Prevalence and epidemiology of Salmonella spp. in small pig abattoirs of Hanoi, Vietnam. Annals of the New York Academy of Sciences 1081:269–272.
Le TX, and Rojekittikhun W (2000). A survey of infective larvae of Gnathostoma in eels sold in Ho Chi Minh City. Southeast Asian J Trop Med Public Health 31:133-137.
Xuan le T, Rojekittikhun W, Punpoowong B, Trang le N, and Hien TV (2002). Case report: intraocular gnathostomiasis in Vietnam. Southeast Asian J Trop Med Public Health 33:485-489.
Le TH, De NV, Agatsuma T, Blair D, Vercruysse J, Dorny P, et al. (2007). Molecular confirmation that Fasciola gigantica can undertake aberrant migrations in human hosts. J Clin Microbiol 45:648-650.
Le TH, De NV, Agatsuma T, Thi Nguyen TG, Nguyen QD, McManus DP, et al. (2008). Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. Int J Parasitol 38:725-730.
Le A, Pham MH, Le TH (2012) Mot so dac diem dich te hoc nhiem Toxocara tren benh nhan may day man tinh nhiem Toxocara tai Vien 103. Tạp chì phòng chống bệnh sốt rét và các bệnh ký sinh trùng 52–58.
Lestari ES, Severin JA, and Verbrugh HA (2012). Antimicrobial resistance among pathogenic bacteria in Southeast Asia. Southeast Asian J Trop Med Public Health 43:385-422.
Linh BK, Thuy DT, My LN, Sasaki O, Yoshihara S (2003). Application of agar gel diffusion test to the diagnosis of fasciolosis in cattle and buffaloes in the Red River delta of Vietnam. Japan Agricultural Research Quarterly 37:201-205.
Liu X, Chen Y, Wang X, and Ji R (2004). [Foodborne disease outbreaks in China from 1992 to 2001 national foodborne disease surveillance system]. Wei Sheng Yan Jiu 33:725-727.
Liu XM, Chen Y, Fan YX, and Wang MQ (2006). [Foodborne diseases occurred in 2003–report of the National Foodborne Diseases Surveillance System, China]. Wei Sheng Yan Jiu 35:201-204.
Luu QH, Tran TH, Phung DC, and Nguyen TB (2006). Study on the prevalence of Campylobacter spp. from chicken meat in Hanoi, Vietnam. Ann N Y Acad Sci 1081:273-275.
Mai NT, Hoa NT, Nga TV, Linh le D, Chau TT, Sinh DX, et al. (2008). Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis 46:659-667.
Mas-Coma S (2005). Epidemiology of fascioliasis in human endemic areas. J Helminthol 79:207-216.
Mayer DA, and Fried B (2007). The role of helminth infections in carcinogenesis. Adv Parasitol 65:239-296.
Montoya J, Boothroyd J, and Kovacs J (2010). Toxoplasma gondii. Pages 3495-3526 in G. Mandell, J. Bennet, and R. Dolin, editors. Principle and Practice of Infectious Diseases. Churchill Livingstone Elsevier, Philadelphia.
Nga TV, Parry CM, Le T, Lan NP, Diep TS, Campbell JI, et al. (2012). The decline of typhoid and the rise of non-typhoid salmonellae and fungal infections in a changing HIV landscape: bloodstream infection trends over 15 years in southern Vietnam. Trans R Soc Trop Med Hyg 106:26-34.
Ngan PK, Khanh NG, Tuong CV, Quy PP, Anh DN, and Thuy HT (1992). Persistent diarrhea in Vietnamese children: a preliminary report. Acta Paediatr 81 Suppl 381:124-126.
Nghia HD, Hoa NT, Linh le D, Campbell J, Diep TS, Chau NV, et al. (2008). Human case of Streptococcus suis serotype 16 infection. Emerg Infect Dis 14:155-157.
Nghia HD, Tu le TP, Wolbers M, Thai CQ, Hoang NV, Nga TV, et al. (2011). Risk factors of Streptococcus suis infection in Vietnam. A case-control study. PLoS One 6:e17604.
Ngo TH, T.B.C. T, Tran T.T.N., Nguyen V. D., Campbell J, Pham H.A., et al. (2011). Slaughterhouse Pigs Are a Major Reservoir of Streptococcus suis Serotype 2 Capable of Causing Human Infection in Southern Vietnam. PLoS One 6:e17943.
Nguyen TV, Le Van P, Le Huy C, and Weintraub A (2004). Diarrhea caused by rotavirus in children less than 5 years of age in Hanoi, Vietnam. J Clin Microbiol 42:5745-5750.
Nguyen D, Le P, Huyn L, Truong C (2006) Dieu tra tinh hinh nhiem vi khuan va phan tich cac yeu to lien quan doi voi mot so benh vi khuan lay sang nguoi tren dan bo sua tai tp Ho Chi Minh. Khoa học kỹ thuật thú y 13:43-46.
Nguyen ST, Nguyen DT, Le DQ, Le Hua LN, Van Nguyen T, Honma H, et al. (2007a). Prevalence and first genetic identification of Cryptosporidium spp. in cattle in central Viet Nam. Vet Parasitol 150:357-361.
Nguyen TH, Nguyen VD, Murrell D, and Dalsgaard A (2007b). Occurrence and species distribution of fishborne zoonotic trematodes in wastewater-fed aquaculture in northern Vietnam. Trop Med Int Health 12 Suppl 2:66-72.
Nguyen TG, Van De N, Vercruysse J, Dorny P, and Le TH (2009). Genotypic characterization and species identification of Fasciola spp. with implications regarding the isolates infecting goats in Vietnam. Exp Parasitol 123:354-361.
Nguyen TG, Le TH, Dao TH, Tran TL, Praet N, Speybroeck N, et al. (2011). Bovine fasciolosis in the human fasciolosis hyperendemic Binh Dinh province in Central Vietnam. Acta Trop 117:19-22.
Nguyen ST, Honma H, Geurden T, Ikarash M, Fukuda Y, Huynh VV, et al. (2012). Prevalence and risk factors associated with Cryptosporidium oocysts shedding in pigs in Central Vietnam. Res Vet Sci 848-52:848-852.
Nissapatorn V, Noor Azmi MA, Cho SM, Fong MY, Init I, Rohela M, et al. (2003). Toxoplasmosis: prevalence and risk factors. J Obstet Gynaecol 23:618-624.
Olsen A, Thuan le K, Murrell KD, Dalsgaard A, Johansen MV, and De NV (2006). Cross-sectional parasitological survey for helminth infections among fish farmers in Nghe An province, Vietnam. Acta Trop 100:199-204.
Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, et al. (2013). Attribution of Foodborne Illnesses, Hospitalizations, and Deaths to Food Commodities by using Outbreak Data, United States, 1998–2008. Emerg Infect Dis 19:407-415.
Pegues D, and Miller SI (2010). Salmonella species, including Salmonella typhi. Pages 2887-2903 in G. Mandell, J. Bennet, and R. Dolin, editors. Principle and Practice of Infectious Diseases. Churchill Livingstone Elsevier, Philadelphia.
Pham Duc P, Nguyen-Viet H, Hattendorf J, Zinsstag J, Dac Cam P, and Odermatt P (2011). Risk factors for Entamoeba histolytica infection in an agricultural community in Hanam province, Vietnam. Parasit Vectors 4:102.
Phan TT, Khai LTL, Ogasawara N, Tam NT, Okatani AT, Akiba M, et al. (2005). Contamination of Salmonella in retail meats and shrimps in the Mekong Delta, Vietnam. Journal of Food Protection 68:1077-1080.
Phan M, Ersboll A, Do D, and Dalsgaard A (2011). Raw-fish-eating behavior and fishborne zoonotic trematode infection in people of northern Vietnam. Foodborne Pathogens And Disease 8:255-260.
Phuc PD, Konradsen F, Phuong PT, Cam PD and Dalsgaard (2006). Practice of using human excreta as fertilizer and implications for health in Nghe An province, Vietnam. Southeast Asian Journal of Tropical Medicine and Public Health 37:222-229.
Pozio E, Hoberg E, La Rosa G, and Zarlenga DS (2009). Molecular taxonomy, phylogeny and biogeography of nematodes belonging to the Trichinella genus. Infect Genet Evol 9:606-616.
Queuche F, Cao Van V, and Le Dang H (1997). [Endemic area of paragonimiasis in Vietnam]. Sante 7:155-159.
Sery V, Zastera M, Prokopec J, Radkovsky J, The PH, and Canh DT (1988). To the problem of toxoplasmosis in Vietnam. Bull Inst Marit Trop Med Gdynia 39:181-185.
Sieu TP, Dung TT, Nga NT, Hien TV, Dalsgaard A, Waikagul J, et al. (2009). Prevalence of Gnathostoma spinigerum infection in wild and cultured swamp eels in Vietnam. J Parasitol 95:246-248.
Smythe LD, Wuthiekanun V, Chierakul W, Suputtamongkol Y, Tiengrim S, Dohnt MF, et al. (2009). The microscopic agglutination test (MAT) is an unreliable predictor of infecting Leptospira serovar in Thailand. Am J Trop Med Hyg 81:695-697.
Somers R, Dorny P, Nguyen VK, Dang TC, Goddeeris B, Craig PS, et al. (2006). Taenia solium taeniasis and cysticercosis in three communities in north Vietnam. Trop Med Int Health 11:65-72.
Somers R, Dorny P, Geysen D, Nguyen LA, Thach DC, Vercruysse J, et al. (2007). Human tapeworms in north Vietnam. Trans R Soc Trop Med Hyg 101:275-277.
Sotelo J (2003). Neurocysticercosis: eradication of cysticercosis is an attainable goal. Bmj 326:511-512.
Suzuki K, Kanameda M, Inui K, Ogawa T, Nguyen VK, Dang TT, et al. (2006). A longitudinal study to identify constraints to dairy cattle health and production in rural smallholder communities in Northern Vietnam. Res Vet Sci 81:177-184.
Ta YT, Nguyen TT, To PB, Pham da X, Le HT, Alali WQ, et al. (2012). Prevalence of Salmonella on chicken carcasses from retail markets in Vietnam. J Food Prot 75:1851-1854.
Taira N, Yoshifuji H, and Boray JC (1997). Zoonotic potential of infection with Fasciola spp. by consumption of freshly prepared raw liver containing immature flukes. Int J Parasitol 27:775-779.
Taylor WRJ, Giang VT, Thai QN, Duong VD, Viet KN, Cap TN, et al. (2009). Acute Febrile Myalgia in Vietnam due to Trichinellosis following the Consumption of Raw Pork. Clinical Infectious Diseases 49:E79-E83.
Thai KTD, Binh TQ, Giao PT, Phuong HL, Hung LQ, Van Nam N, et al. (2006). Seroepidemiology of leptospirosis in southern Vietnamese children. Tropical Medicine & International Health 11:738-745.
Thai TH, Hirai T, Lan NT, and Yamaguchi R (2012). Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 156:147-151.
Thang NM, and Popkin BM (2004). Patterns of food consumption in Vietnam: effects on socioeconomic groups during an era of economic growth. Eur J Clin Nutr 58:145-153.
Thi NV, Dorny P, La Rosa G, Long TT, Van CN, and Pozio E (2010). High prevalence of anti-Trichinella IgG in domestic pigs of the Son La province, Vietnam. Veterinary Parasitology 168:136-140.
Thompson CN, Phan VT, Le TP, Pham TN, Hoang LP, Ha V et al (2012) Epidemiological features and risk factors of Salmonella gastroenteritis in children resident in Ho Chi Minh City, Vietnam. Epidemiol Infect 141:1604–1613.
Thu ND, Dalsgaard A, Loan LT, and Murrell KD (2007). Survey for zoonotic liver and intestinal trematode metacercariae in cultured and wild fish in An Giang Province, Vietnam. Korean J Parasitol 45:45-54.
Tran D, Pham H (2012). Mot so dac diem dich te hoc benh than o nguoi mien bac Viet Nam, 2006–2011.
22.Tran H, Tran KD, Tran H, Le T, and Nguyen H (2001a). Mot so dac diem trong hoi chung au trung di chuyen noi tang do gium dua cho Toxocara canis. Y Hoc Tp. Ho Chi Minh 4:192-197.
Tran VH, Tran TK, Nguye HC, Pham HD, and Pham TH (2001b). Fascioliasis in Vietnam. The Southeast Asian journal of tropical medicine and public health 32 Suppl 2:48-50.
Tran TP, Ly TL, Nguyen TT, Akiba M, Ogasawara N, Shinoda D, et al. (2004). Prevalence of Salmonella spp. in pigs, chickens and ducks in the Mekong Delta, Vietnam. J Vet Med Sci 66:1011-1014.
Trung D, Van N, Waikagul J, Dalsgaard A, Chai JY, Sohn WM, et al. (2007). Fishborne zoonotic intestinal trematodes, Vietnam. Emerg Infect Dis 13:1828-1833.
Udonsom R, Lekkla A, Chung P, Cam P, and Sukthana Y (2008). Seroprevalence of Toxoplasma gondii antibody in Vietnamese villagers. Southeast Asian J Trop Med Public Health 39:14-18.
Uga S, Hoa NT, Thuan le K, Noda S, and Fujimaki Y (2005). Intestinal parasitic infections in schoolchildren in a suburban area of Hanoi, Vietnam. Southeast Asian J Trop Med Public Health 36:1407-1411.
Uga S, Hoa NT, Noda S, Moji K, Cong L, Aoki Y, et al. (2009). Parasite egg contamination of vegetables from a suburban market in Hanoi, Vietnam. Nepal Med Coll J 11:75-78.
Van CTB, Thuy NTT, San NH, Hien TT, Baranton G, and Perolat P (1998). Human leptospirosis in the Mekong delta, Viet Nam. Transactions of the Royal Society of Tropical Medicine and Hygiene 92:625-628.
Van TT, Moutafis G, Istivan T, Tran LT, and Coloe PJ (2007). Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Appl Environ Microbiol 73:6885-6890.
Verle P, Kongs A, De NV, Thieu NQ, Depraetere K, Kim HT, et al. (2003). Prevalence of intestinal parasitic infections in northern Vietnam. Trop Med Int Health 8:961-964.
Vien CV, Phue NC, Ha LD, Tuan LM, Van NT, Pao TC, et al. (1997). Paragonimiasis in Sin Ho District, Lai Chau Province, Viet Nam. Southeast Asian J Trop Med Public Health 28 Suppl 1:46.
Vijayan VK (2009). Parasitic lung infections. Curr Opin Pulm Med 15:274-282.
Vo ATT, van Duijkeren E, Fluit AC, Heck M, Verbruggen A, Maas HME, et al. (2006). Distribution of Salmonella enterica Serovars from humans, livestock and meat in Vietnam and the Dominance of Salmonella Typhimurium Phage Type 90. Veterinary Microbiology 113:153-158.
Vu Nguyen T, Le Van P, Le Huy C, Nguyen Gia K, and Weintraub A (2006). Etiology and epidemiology of diarrhea in children in Hanoi, Vietnam. Int J Infect Dis 10:298-308.
Wagenaar JFP, Falke THF, Nam NV, Binh TQ, Smits HL, Cobelens FGJ, et al. (2004). Rapid serological assays for leptospirosis are of limited value in southern Vietnam. Annals of Tropical Medicine and Parasitology 98:843-850.
Waikagul J, and Diaz Camacho P (2007). Gnathostomiasis. Pages 235-261 in D. M. a. B. Fried, editor. Food-borne parasitic zoonoses: Fish and plant-borne parasites. Springer, New York.
Wertheim HF, Nghia HD, Taylor W, and Schultsz C (2009a). Streptococcus suis: an emerging human pathogen. Clin Infect Dis 48:617-625.
Wertheim HF, Nguyen HN, Taylor W, Lien TT, Ngo HT, Nguyen TQ, et al. (2009b). Streptococcus suis, an important cause of adult bacterial meningitis in northern Vietnam. PLoS One 4:e5973.
Willingham AL, 3rd, De NV, Doanh NQ, Cong LD, Dung TV, Dorny P, et al. (2003). Current status of cysticercosis in Vietnam. The Southeast Asian journal of tropical medicine and public health 34 Suppl 1:35-50.
Willingham AL, III, Wu H-W, Conlan J, and Satrija F (2010). Combating Taenia solium Cysticercosis in Southeast Asia: An Opportunity for Improving Human Health and Livestock Production. Advances in Parasitology 72:235–266.
Xiao L, and Fayer R (2008). Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol 38:1239-1255.
Xuan L. T, Hoa PL, Dekumyoy P, Hoan NH, Khuong LH, Van TT, et al. (2004). Gnathosthoma infection in south Vietnam. Southeast Asian J Trop Med Public Health 35 (Suppl. 1):97-99.
Xuan LT, Hung NT, and Waikagul J (2005). Cutaneous fascioliasis: A case report in Vietnam. American Journal of Tropical Medicine and Hygiene 72:508-509.
Yu H, Jing H, Chen Z, Zheng H, Zhu X, Wang H, et al. (2006). Human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis 12:914-920.
22.Acknowledgments
The authors want to express their gratitude to Ms Dong Thi Thanh Trang for helping with the translation of Vietnamese journal articles. Work has been co-funded by ZoNMW/WOTRO (The Netherlands), VIBRE Project (No. 205100012) and the Vietnam Initiative on Zoonotic Infections (VIZIONS), part of the Wellcome Trust Major Overseas Programme (UK).
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Carrique-Mas, J.J., Bryant, J.E. A Review of Foodborne Bacterial and Parasitic Zoonoses in Vietnam. EcoHealth 10, 465–489 (2013). https://doi.org/10.1007/s10393-013-0884-9
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DOI: https://doi.org/10.1007/s10393-013-0884-9