Document Detail

A Review of Foodborne Bacterial and Parasitic Zoonoses in Vietnam.
Jump to Full Text
MedLine Citation:
PMID:  24162798     Owner:  NLM     Status:  Publisher    
Abstract/OtherAbstract:
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.
Authors:
Juan J Carrique-Mas; J E Bryant
Related Documents :
24959328 - Estimation of costs for control of salmonella in high-risk feed materials and compound ...
24779468 - Seasonal prevalence of antibodies to leptospira interrogans in antillean manatees from ...
22458938 - Enrichment of extruded snack products with co-products from chestnut mushroom (agrocybe...
25058878 - Chemistry and multibeneficial bioactivities of carvacrol (4-isopropyl-2-methylphenol), ...
12741458 - Therapeutic potential of gastric electrical stimulation for obesity and its possible me...
25055188 - Nutritional status of women and child refugees from syria - jordan, april-may 2014.
Publication Detail:
Type:  JOURNAL ARTICLE     Date:  2013-10-26
Journal Detail:
Title:  EcoHealth     Volume:  -     ISSN:  1612-9210     ISO Abbreviation:  Ecohealth     Publication Date:  2013 Oct 
Date Detail:
Created Date:  2013-10-28     Completed Date:  -     Revised Date:  -    
Medline Journal Info:
Nlm Unique ID:  101222144     Medline TA:  Ecohealth     Country:  -    
Other Details:
Languages:  ENG     Pagination:  -     Citation Subset:  -    
Affiliation:
Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 764 Vo Van Kiet, W.1, Dist.5, Ho Chi Minh City, Vietnam, jcarrique-mas@oucru.org.
Export Citation:
APA/MLA Format     Download EndNote     Download BibTex
MeSH Terms
Descriptor/Qualifier:

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-ta): Ecohealth
Journal ID (iso-abbrev): Ecohealth
ISSN: 1612-9202
ISSN: 1612-9210
Publisher: Springer US, Boston
Article Information
Download PDF
© The Author(s) 2013
OpenAccess:
Received Day: 10 Month: 3 Year: 2013
Revision Received Day: 10 Month: 6 Year: 2013
Accepted Day: 24 Month: 9 Year: 2013
Electronic publication date: Day: 26 Month: 10 Year: 2013
pmc-release publication date: Day: 26 Month: 10 Year: 2013
Print publication date: Year: 2013
Volume: 10First Page: 465 Last Page: 489
PubMed Id: 24162798
ID: 3938847
Publisher Id: 884
DOI: 10.1007/s10393-013-0884-9

A Review of Foodborne Bacterial and Parasitic Zoonoses in Vietnam
Juan J. Carrique-MasAff1 Address: +84-8-39237954 jcarrique-mas@oucru.org
J. E. BryantAff1
Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 764 Vo Van Kiet, W.1, Dist.5, Ho Chi Minh City, Vietnam

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.


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).


References
Adler B,de la Pena Moctezuma A. Leptospira and leptospirosisVeterinary MicrobiologyYear: 201014028729619345023
Anderson N,Luong TT,Vo NG,Bui KL,Smooker PM,Spithill TW. The sensitivity and specificity of two methods for detecting Fasciola infections in cattleVeterinary ParasitologyYear: 199983152410392764
Anh NT,Madsen H,Dalsgaard A,Phuong NT,Thanh DT,Murrell KD. Poultry as reservoir hosts for fishborne zoonotic trematodes in Vietnamese fish farmsVeterinary ParasitologyYear: 201016939139420149548
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. Plant-borne human contamination by fascioliasisAmerican Journal of Tropical Medicine and HygieneYear: 20067529530216896136
Beleneva I. Incidence and characteristics of Staphylococcus aureus and Listeria monocytogenes from the Japan and South China seasMarine Pollution BulletinYear: 20116238238720947102
Bodhidatta L,Lan NT,Hien BT,Lai NV,Srijan A,Serichantalergs O,et al. Rotavirus disease in young children from Hanoi, VietnamThe Pediatric Infectious Disease JournalYear: 20072632532817414396
Boqvist S,Chau BL,Gunnarsson A,Engvall EO,Vagsholm I,Magnusson U. Animal- and herd-level risk factors for leptospiral seropositivity among sows in the Mekong Delta, VietnamPreventive Veterinary MedicineYear: 20025323324511830296
Boqvist S,Thu HTV,Vagsholm I,Magnusson U. The impact of Leptospira seropositivity on reproductive performance in sows in southern Viet NamTheriogenologyYear: 2002581327133512387346
Cadilhon J,Moustier N,Poole N,Tam P,Fearne P. Traditional vs. modern food systems? Insights from vegetable supply chains to Ho Chi Minh City (Vietnam)Development Policy ReviewYear: 2006243149
Chai JY,Darwin Murrell K,Lymbery AJ. Fish-borne parasitic zoonoses: status and issuesInternational Journal for ParasitologyYear: 2005351233125416143336
Chau TT,Campbell JI,Schultsz C,Chau NV,Diep TS,Baker S,et al. Three adult cases of Listeria monocytogenes meningitis in VietnamPLoS MedicineYear: 20107e100030620668655
Chau TTH,Campbell J,Schultsz C,Nguyen C,To D,Baker S,et al. Three adult cases of Listeria monocytogenes meningitis in VietnamPLoS MedicineYear: 20107e100030620668655
Chen Y,Guo Y,Wang Z,Liu X,Liu H,Dai Y,et al. Foodborne disease outbreaks in 2006 report of the National Foodborne Disease Surveillance Network, ChinaWei Sheng Yan JiuYear: 20103933133420568464
Chi TT,Dalsgaard A,Turnbull JF,Tuan PA,Murrell KD. Prevalence of zoonotic trematodes in fish from a Vietnamese fish-farming communityJournal of ParasitologyYear: 20089442342818564743
Choi D,Lim JH,Lee KT,Lee JK,Choi SH,Heo JS,et al. Cholangiocarcinoma and Clonorchis sinensis infection: a case–control study in KoreaJournal of HepatologyYear: 2006441066107316480786
Clinton White J. Mandell G,Bennet J,Dolin RCryptosporidium speciesPrinciple and Practice of Infectious DiseasesYear: 2010PhiladelphiaChurchill Livingstone/Elsevier35473586
Coker RJ,Hunter BM,Rudge JW,Liverani M,Hanvoravongchai P. Health in Southeast Asia 3. Emerging infectious diseases in southeast Asia: regional challenges to controlLancetYear: 201137759960921269678
Conlan JV,Vongxay K,Fenwick S,Blacksell SD,Thompson RC. Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia?Trends in ParasitologyYear: 20092539840319717341
Dang TC,Yajima A,Nguyen VK,Montresor A. Prevalence, intensity and risk factors for clonorchiasis and possible use of questionnaires to detect individuals at risk in northern VietnamTransactions of the Royal Society of Tropical Medicine and HygieneYear: 20081021263126818632126
De NV. Fish-borne trematodes in VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 200435299301
De NV,Le TH. Human infections of fish-borne trematodes in Vietnam: prevalence and molecular specific identification at an endemic commune in Nam Dinh provinceExperimental ParasitologyYear: 201112935536121959023
De NV,Murrell KD,Cong LD,Cam PD,Chau LV,Toan ND,et al. The food-borne trematode zoonoses of VietnamThe Southeast Asian Journal of Tropical Medicine and Public HealthYear: 200334Suppl 1123412971505
Do TT,Bui TT,Molbak K,Phung DC,Dalsgaard A. Epidemiology and aetiology of diarrhoeal diseases in adults engaged in wastewater-fed agriculture and aquaculture in Hanoi, VietnamTropical Medicine & International HealthYear: 200712Suppl 2233318005312
Doanh PN,Shinohara A,Horii Y,Habe S,Nawa Y,Le NT. Description of a new lung fluke species, Paragonimus vietnamensis sp. nov. (Trematoda, Paragonimidae), found in northern VietnamParasitology ResearchYear: 20071011495150117674049
Doanh PN,Shinohara A,Horii Y,Habe S,Nawa Y,Le NT. Discovery of Paragonimus proliferus in Northern Vietnam and their molecular phylogenetic status among genus ParagonimusParasitology ResearchYear: 200810267768318071749
Doanh PN,Shinohara A,Horii Y,Habe S,Nawa Y. Discovery of Paragonimus westermani in Vietnam and its molecular phylogenetic status in P. westermani complexParasitology ResearchYear: 20091041149115519083013
Doanh PN,Dung do T,Thach DT,Horii Y,Shinohara A,Nawa Y. Human paragonimiasis in Viet Nam: epidemiological survey and identification of the responsible species by DNA sequencing of eggs in patients’ sputumParasitology InternationalYear: 20116053453721946337
Dorny P,Somers R,Cam Thi Dang T,Khong Nguyen V,Vercruysse J. Cysticercosis in Cambodia, Lao PDR and VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 200435223226
Dorny P,Somers R,Vercruysse J. Response to comment on: Human tapeworms in north VietnamTransactions of the Royal Society of Tropical Medicine and HygieneYear: 2007101629630
Drew TW. The emergence and evolution of swine viral diseases: to what extent have husbandry systems and global trade contributed to their distribution and diversity?Revue Scientifique et TechniqueYear: 2011309510621809756
Drury R. Hungry for success: urban consumer demand for wild animal products in VietnamConservation and SocietyYear: 20119247257
Dubey JP,Huong LT,Sundar N,Su C. Genetic characterization of Toxoplasma gondii isolates in dogs from Vietnam suggests their South American originVeterinary ParasitologyYear: 200714634735117442492
Dubey JP,Huong LT,Lawson BW,Subekti DT,Tassi P,Cabaj W,et al. Seroprevalence and isolation of Toxoplasma gondii from free-range chickens in Ghana, Indonesia, Italy, Poland, and VietnamJournal of ParasitologyYear: 200894687118372623
Dyar OJ,Hoa NQ,Trung NV,Phuc HD,Larsson M,Chuc NT,et al. High prevalence of antibiotic resistance in commensal Escherichia coli among children in rural VietnamBMC Infectious DiseasesYear: 2012129222512857
EFSAThe European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010EFSA JournalYear: 2012102597
Ellerbroek L,Narapati D,Tai NP,Poosaran N,Pinthong R,Sirimalaisuwan A,et al. Antibiotic resistance in Salmonella isolates from imported chicken carcasses in Bhutan and from pig carcasses in VietnamJournal of Food ProtectionYear: 20107337637920132687
Erhart A,Dorny P,Van De N,Vien HV,Thach DC,Toan ND,et al. Taenia solium cysticercosis in a village in northern Viet Nam: seroprevalence study using an ELISA for detecting circulating antigenTransactions of the Royal Society of Tropical Medicine and HygieneYear: 20029627027212174775
Fayer R. Cryptosporidium: a water-borne zoonotic parasiteVeterinary ParasitologyYear: 2004126375615567578
Galan-Puchades MT,Fuentes MV. Diagnosis of human cysticercosis and Taenia asiaticaAmerican Journal of Tropical Medicine and HygieneYear: 200981116519996453
Garin B,Gouali M,Wouafo M,Perchec AM,Thu PM,Ravaonindrina N,et al. Prevalence, quantification and antimicrobial resistance of Campylobacter spp. on chicken neck-skins at points of slaughter in 5 major cities located on 4 continentsInternational Journal of Food MicrobiologyYear: 201215710210722607809
Geurden T,Somers R,Thanh NT,Vien LV,Nga VT,Giang HH,et al. Parasitic infections in dairy cattle around Hanoi, northern VietnamVeterinary ParasitologyYear: 200815338438818328629
Gibson-Kueh S,Yang R,Thuy NT,Jones JB,Nicholls PK,Ryan U. The molecular characterization of an Eimeria and Cryptosporidium detected in Asian seabass (Lates calcarifer) cultured in VietnamVeterinary ParasitologyYear: 2011181919621641722
Graham JP,Leibler JH,Price LB,Otte JM,Pfeiffer DU,Tiensin T,et al. The animal–human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainmentPublic Health ReportsYear: 200812328229919006971
Ha TA,Pham TY. Study of Salmonella, Campylobacter, and Escherichia coli contamination in raw food available in factories, schools, and hospital canteens in Hanoi, VietnamAnnals of the New York Academy of SciencesYear: 2006108126226517135522
Hall G,Kirk MD,Becker N,Gregory JE,Unicomb L,Millard G,et al. Estimating foodborne gastroenteritis, AustraliaEmerging Infectious DiseasesYear: 2005111257126416102316
Hedegaard Clausen J,Madsen H,Murrell KD,Van PT,Thu HN,Do DT,et al. Prevention and control of fish-borne zoonotic trematodes in fish nurseries, VietnamEmerging Infectious DiseasesYear: 2012181438144522932069
Hien BT,Trang do T,Scheutz F,Cam PD,Molbak K,Dalsgaard A. Diarrhoeagenic Escherichia coli and other causes of childhood diarrhoea: a case–control study in children living in a wastewater-use area in Hanoi, VietnamJournal of Medical MicrobiologyYear: 2007561086109617644717
Ho Dang Trung N,Le Thi Phuong T,Wolbers M,Nguyen Van Minh H,Nguyen Thanh V,Van MP,et al. Aetiologies of central nervous system infection in Viet Nam: a prospective provincial hospital-based descriptive surveillance studyPLoS ONEYear: 20127e3782522662232
Hoa NT,Chieu TTB,Dung SD,Long NT,Quoc T,Hieu TQ,et al. S. suis serotype 2 and PRRSV in pigs, Vietnam 2010Emerging Infectious DiseasesYear: 20131933133323343623
Holland WG,Luong TT,Nguyen LA,Do TT,Vercruysse J. The epidemiology of nematode and fluke infections in cattle in the Red River Delta in VietnamVeterinary ParasitologyYear: 20009314114711035232
Hong TTT,Linh NQ,Ogle B,Lindberg JE. Survey on the prevalence of diarrhoea in pre-weaning piglets and on feeding systems as contributing risk factors in smallholdings in central VietnamTropical Animal Health and ProductionYear: 20063839740517165611
HPA (2013) Table of Zoonotic Diseases and Organisms. http://www.hpa.org.uk/Topics/InfectiousDiseases/InfectionsAZ/Zoonoses/TableZoonoticDiseases. Accessed March 12, 2012.
Hubalek Z. Emerging human infectious diseases: anthroponoses, zoonoses, and sapronosesEmerging Infectious DiseasesYear: 2003940340412643844
Huong LT,Dubey JP. Seroprevalence of Toxoplasma gondii in pigs from VietnamJournal of ParasitologyYear: 20079395195217918384
Huong LT,Ljungstrom BL,Uggla A,Bjorkman C. Prevalence of antibodies to Neospora caninum and Toxoplasma gondii in cattle and water buffaloes in southern VietnamVeterinary ParasitologyYear: 19987553579566094
Indrawattana N,Nibaddhasobon T,Sookrung N,Chongsa-Nguan M,Tungtrongchitr A,Makino S,et al. Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methodsJournal of Health, Population and NutritionYear: 2011292638
Isenbarger D,Hien B,Ha H,Ha T,Bodhidatta L,Pang L,et al. Prospective study of the incidence of diarrhoea and prevalence of bacterial pathogens in a cohort of Vietnamese children along the Red RiverEpidemiology and InfectionYear: 200112722923611693500
Jenkins MB,Liotta JL,Lucio-Forster A,Bowman DD. Concentrations, viability, and distribution of Cryptosporidium genotypes in lagoons of swine facilities in the Southern Piedmont and in coastal plain watersheds of GeorgiaApplied and Environment MicrobiologyYear: 20107657575763
Jittapalapong S,Nimsupan B,Pinyopanuwat N,Chimnoi W,Kabeya H,Maruyama S. Seroprevalence of Toxoplasma gondii antibodies in stray cats and dogs in the Bangkok metropolitan area, ThailandVeterinary ParasitologyYear: 200714513814117141415
Khan MI,Ochiai RL,von Seidlein L,Dong B,Bhattacharya SK,Agtini MD,et al. Non-typhoidal Salmonella rates in febrile children at sites in five Asian countriesTropical Medicine & International HealthYear: 20101596096320545918
Kino H,Inaba H,Van De N,Van Chau L,Son DT,Hao HT,et al. Epidemiology of clonorchiasis in Ninh Binh Province, VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 1998292502549886107
Ky H,Van Chap N. Radioclinical aspects of cerebral and muscular cysticercosis: 20 casesJournal of NeuroradiologyYear: 200027264266
Lan-Anh NT,Phuong NT,Murrell KD,Johansen MV,Dalsgaard A,Thu LT,et al. Animal reservoir hosts and fish-borne zoonotic trematode infections on fish farms, VietnamEmerging Infectious DiseasesYear: 20091554054619331729
Laras K,Van CB,Bounlu K,Tien NTK,Olson JG,Thongchanh S,et al. The importance of leptospirosis in Southeast AsiaAmerican Journal of Tropical Medicine and HygieneYear: 20026727828612408667
Le Bas C,Tran TH,Nguyen TT,Dang DT,Ngo CT. Prevalence and epidemiology of Salmonella spp. in small pig abattoirs of Hanoi, VietnamAnnals of the New York Academy of SciencesYear: 2006108126927217135524
Le TX,Rojekittikhun W. A survey of infective larvae of Gnathostoma in eels sold in Ho Chi Minh CitySoutheast Asian Journal of Tropical Medicine and Public HealthYear: 20003113313711023080
le Xuan T,Rojekittikhun W,Punpoowong B,le Trang N,Hien TV. Case report: intraocular gnathostomiasis in VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 20023348548912693580
Le TH,De NV,Agatsuma T,Blair D,Vercruysse J,Dorny P,et al. Molecular confirmation that Fasciola gigantica can undertake aberrant migrations in human hostsJournal of Clinical MicrobiologyYear: 20074564865017135435
Le TH,De NV,Agatsuma T,Thi Nguyen TG,Nguyen QD,McManus DP,et al. Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in VietnamInternational Journal for ParasitologyYear: 20083872573018031748
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,Verbrugh HA. Antimicrobial resistance among pathogenic bacteria in Southeast AsiaSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 20124338542223082591
Linh BK,Thuy DT,My LN,Sasaki O,Yoshihara S. Application of agar gel diffusion test to the diagnosis of fasciolosis in cattle and buffaloes in the Red River Delta of VietnamJapan Agricultural Research QuarterlyYear: 200337201205
Liu X,Chen Y,Wang X,Ji R. Foodborne disease outbreaks in China from 1992 to 2001 national foodborne disease surveillance systemWei Sheng Yan JiuYear: 20043372572715727189
Liu XM,Chen Y,Fan YX,Wang MQ. Foodborne diseases occurred in 2003—report of the National Foodborne Diseases Surveillance System, ChinaWei Sheng Yan JiuYear: 20063520120416758972
Luu QH,Tran TH,Phung DC,Nguyen TB. Study on the prevalence of Campylobacter spp. from chicken meat in Hanoi, VietnamAnnals of the New York Academy of SciencesYear: 2006108127327517135525
Mai NT,Hoa NT,Nga TV,le Linh D,Chau TT,Sinh DX,et al. Streptococcus suis meningitis in adults in VietnamClinical Infectious DiseasesYear: 20084665966719413493
Mas-Coma S. Epidemiology of fascioliasis in human endemic areasJournal of HelminthologyYear: 20057920721616153314
Mayer DA,Fried B. The role of helminth infections in carcinogenesisAdvances in ParasitologyYear: 20076523929618063098
Montoya J,Boothroyd J,Kovacs J. Mandell G,Bennet J,Dolin RToxoplasma gondiiPrinciple and Practice of Infectious DiseasesYear: 2010PhiladelphiaChurchill Livingstone/Elsevier34953526
Nga TV,Parry CM,Le T,Lan NP,Diep TS,Campbell JI,et al. 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 VietnamTransactions of the Royal Society of Tropical Medicine and HygieneYear: 2012106263422137537
Ngan PK,Khanh NG,Tuong CV,Quy PP,Anh DN,Thuy HT. Persistent diarrhea in Vietnamese children: a preliminary reportActa PaediatricaYear: 199281Suppl 38112412612286020
Nghia HD,Hoa NT,le Linh D,Campbell J,Diep TS,Chau NV,et al. Human case of Streptococcus suis serotype 16 infectionEmerging Infectious DiseasesYear: 20081415515718258097
Nghia HD,le Tu TP,Wolbers M,Thai CQ,Hoang NV,Nga TV,et al. Risk factors of Streptococcus suis infection in Vietnam. A case–control studyPLoS ONEYear: 20116e1760421408132
Ngo TH,T TBC,Tran TTN,Nguyen VD,Campbell J,Pham HA,et al. Slaughterhouse pigs are a major reservoir of Streptococcus suis Serotype 2 capable of causing human infection in southern VietnamPLoS ONEYear: 20116e1794321464930
Nguyen TV,Le Van P,Le Huy C,Weintraub A. Diarrhea caused by rotavirus in children less than 5 years of age in Hanoi, VietnamJournal of Clinical MicrobiologyYear: 2004425745575015583308
Nguyen D,Le P,Huyn L,Truong C. Dieu tra tinh hinh nhiem vi khuan va phan tich cac yeu to lien quan voi mot so benh vi khuan lay sang nguoi tren dan bo sua tai tp. Ho Chi MinhKhoa học kỹ thuật thú yYear: 2006134346
Nguyen ST,Nguyen DT,Le DQ,Le Hua LN,Van Nguyen T,Honma H,et al. Prevalence and first genetic identification of Cryptosporidium spp. in cattle in central Viet NamVeterinary ParasitologyYear: 200715035736117964078
Nguyen TH,Nguyen VD,Murrell D,Dalsgaard A. Occurrence and species distribution of fishborne zoonotic trematodes in wastewater-fed aquaculture in northern VietnamTropical Medicine & International HealthYear: 200712Suppl 2667218005317
Nguyen TG,Van De N,Vercruysse J,Dorny P,Le TH. Genotypic characterization and species identification of Fasciola spp. with implications regarding the isolates infecting goats in VietnamExperimental ParasitologyYear: 200912335436119733565
Nguyen TG,Le TH,Dao TH,Tran TL,Praet N,Speybroeck N,et al. Bovine fasciolosis in the human fasciolosis hyperendemic Binh Dinh province in central VietnamActa TropicaYear: 2011117192220920452
Nguyen ST,Honma H,Geurden T,Ikarash M,Fukuda Y,Huynh VV,et al. Prevalence and risk factors associated with Cryptosporidium oocysts shedding in pigs in central VietnamResearch in Veterinary ScienceYear: 20129384885222342125
Nissapatorn V,Noor Azmi MA,Cho SM,Fong MY,Init I,Rohela M,et al. Toxoplasmosis: prevalence and risk factorsJournal of Obstetrics and GynaecologyYear: 20032361862414617462
Olsen A,le Thuan K,Murrell KD,Dalsgaard A,Johansen MV,De NV. Cross-sectional parasitological survey for helminth infections among fish farmers in Nghe An province, VietnamActa TropicaYear: 200610019920417141724
Painter JA,Hoekstra RM,Ayers T,Tauxe RV,Braden CR,Angulo FJ,et al. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008Emerging Infectious DiseasesYear: 20131940741523622497
Pegues D,Miller SI. Mandell G,Bennet J,Dolin RSalmonella species, including Salmonella typhiPrinciple and Practice of Infectious DiseasesYear: 2010PhiladelphiaChurchill Livingstone/Elsevier28872903
Pham Duc P,Nguyen-Viet H,Hattendorf J,Zinsstag J,Dac Cam P,Odermatt P. Risk factors for Entamoeba histolytica infection in an agricultural community in Hanam province, VietnamParasites & VectorsYear: 2011410221663665
Phan TT,Khai LTL,Ogasawara N,Tam NT,Okatani AT,Akiba M,et al. Contamination of Salmonella in retail meats and shrimps in the Mekong Delta, VietnamJournal of Food ProtectionYear: 2005681077108015895745
Phan M,Ersboll A,Do D,Dalsgaard A. Raw-fish-eating behavior and fishborne zoonotic trematode infection in people of northern VietnamFoodborne Pathogens and DiseaseYear: 2011825526021117922
Phuc PD,Konradsen F,Phuong PT,Cam PD,Dalsgaard. Practice of using human excreta as fertilizer and implications for health in Nghe An province, VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 20063722222916771238
Pozio E,Hoberg E,La Rosa G,Zarlenga DS. Molecular taxonomy, phylogeny and biogeography of nematodes belonging to the Trichinella genusInfection, Genetics and EvolutionYear: 2009960661619460327
Queuche F,Van Cao V,Le Dang H. Endemic area of paragonimiasis in VietnamSanteYear: 199771551599296804
Sery V,Zastera M,Prokopec J,Radkovsky J,The PH,Canh DT. To the problem of toxoplasmosis in VietnamBulletin of the Institute of Maritime and Tropical Medicine in GdyniaYear: 1988391811853270582
Sieu TP,Dung TT,Nga NT,Hien TV,Dalsgaard A,Waikagul J,et al. Prevalence of Gnathostoma spinigerum infection in wild and cultured swamp eels in VietnamJournal of ParasitologyYear: 20099524624819245276
Smythe LD,Wuthiekanun V,Chierakul W,Suputtamongkol Y,Tiengrim S,Dohnt MF,et al. The microscopic agglutination test (MAT) is an unreliable predictor of infecting Leptospira serovar in ThailandAmerican Journal of Tropical Medicine and HygieneYear: 20098169569719815889
Somers R,Dorny P,Nguyen VK,Dang TC,Goddeeris B,Craig PS,et al. Taenia solium taeniasis and cysticercosis in three communities in north VietnamTropical Medicine & International HealthYear: 200611657216398757
Somers R,Dorny P,Geysen D,Nguyen LA,Thach DC,Vercruysse J,et al. Human tapeworms in north VietnamTransactions of the Royal Society of Tropical Medicine and HygieneYear: 200710127527716806333
Sotelo J. Neurocysticercosis: eradication of cysticercosis is an attainable goalBritish Medical JournalYear: 200332651151212623885
Suzuki K,Kanameda M,Inui K,Ogawa T,Nguyen VK,Dang TT,et al. A longitudinal study to identify constraints to dairy cattle health and production in rural smallholder communities in Northern VietnamResearch in Veterinary ScienceYear: 20068117718416481015
Ta YT,Nguyen TT,To PB,da Pham X,Le HT,Alali WQ,et al. Prevalence of Salmonella on chicken carcasses from retail markets in VietnamJournal of Food ProtectionYear: 2012751851185423043836
Taira N,Yoshifuji H,Boray JC. Zoonotic potential of infection with Fasciola spp. by consumption of freshly prepared raw liver containing immature flukesInternational Journal for ParasitologyYear: 1997277757799279579
Taylor WRJ,Giang VT,Thai QN,Duong VD,Viet KN,Cap TN,et al. Acute febrile myalgia in Vietnam due to trichinellosis following the consumption of raw porkClinical Infectious DiseasesYear: 200949E79E8319712034
Thai KTD,Binh TQ,Giao PT,Phuong HL,Hung LQ,Van Nam N,et al. Seroepidemiology of leptospirosis in southern Vietnamese childrenTropical Medicine & International HealthYear: 20061173874516640627
Thai TH,Hirai T,Lan NT,Yamaguchi R. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North VietnamInternational Journal of Food MicrobiologyYear: 201215614715122497836
Thang NM,Popkin BM. Patterns of food consumption in Vietnam: effects on socioeconomic groups during an era of economic growthEuropean Journal of Clinical NutritionYear: 20045814515314679380
Thi NV,Dorny P,La Rosa G,Long TT,Van CN,Pozio E. High prevalence of anti-Trichinella IgG in domestic pigs of the Son La province, VietnamVeterinary ParasitologyYear: 201016813614019962244
Thompson CN,Phan VT,Le TP,Pham TN,Hoang LP,Ha V,et al. Epidemiological features and risk factors of Salmonella gastroenteritis in children resident in Ho Chi Minh City, VietnamEpidemiology & InfectionYear: 20121411604161323010148
Thu ND,Dalsgaard A,Loan LT,Murrell KD. Survey for zoonotic liver and intestinal trematode metacercariae in cultured and wild fish in An Giang Province, VietnamKorean Journal of ParasitologyYear: 200745455417374978
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,Nguyen H. Mot so dac diem trong hoi chung au trung di chuyen noi tang do gium dua cho Toxocara canisY Hoc Tp Ho Chi MinhYear: 20014192197
Tran VH,Tran TK,Nguye HC,Pham HD,Pham TH. Fascioliasis in VietnamThe Southeast Asian Journal of Tropical Medicine and Public HealthYear: 200132Suppl 2485012041604
Tran TP,Ly TL,Nguyen TT,Akiba M,Ogasawara N,Shinoda D,et al. Prevalence of Salmonella spp. in pigs, chickens and ducks in the Mekong Delta, VietnamJournal of Veterinary Medical ScienceYear: 2004661011101415353859
Trung D,Van N,Waikagul J,Dalsgaard A,Chai JY,Sohn WM,et al. Fishborne zoonotic intestinal trematodes, VietnamEmerging Infectious DiseasesYear: 2007131828183318258031
Udonsom R,Lekkla A,Chung P,Cam P,Sukthana Y. Seroprevalence of Toxoplasma gondii antibody in Vietnamese villagersSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 200839141818567438
Uga S,Hoa NT,le Thuan K,Noda S,Fujimaki Y. Intestinal parasitic infections in schoolchildren in a suburban area of Hanoi, VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 2005361407141116610642
Uga S,Hoa NT,Noda S,Moji K,Cong L,Aoki Y,et al. Parasite egg contamination of vegetables from a suburban market in Hanoi, VietnamNepal Medical College JournalYear: 200911757819968142
Van CTB,Thuy NTT,San NH,Hien TT,Baranton G,Perolat P. Human leptospirosis in the Mekong Delta, Viet NamTransactions of the Royal Society of Tropical Medicine and HygieneYear: 19989262562810326104
Van TT,Moutafis G,Istivan T,Tran LT,Coloe PJ. Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistanceApplied and Environment MicrobiologyYear: 20077368856890
Verle P,Kongs A,De NV,Thieu NQ,Depraetere K,Kim HT,et al. Prevalence of intestinal parasitic infections in northern VietnamTropical Medicine & International HealthYear: 2003896196414516309
Vien CV,Phue NC,Ha LD,Tuan LM,Van NT,Pao TC,et al. Paragonimiasis in Sin Ho District, Lai Chau Province, Viet NamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 199728Suppl 1469656347
Vijayan VK. Parasitic lung infectionsCurrent Opinion in Pulmonary MedicineYear: 20091527428219276810
Vo ATT,van Duijkeren E,Fluit AC,Heck M,Verbruggen A,Maas HME,et al. Distribution of Salmonella enterica serovars from humans, livestock and meat in Vietnam and the dominance of Salmonella typhimurium phage type 90Veterinary MicrobiologyYear: 200611315315816337754
Vu Nguyen T,Le Van P,Le Huy C,Nguyen Gia K,Weintraub A. Etiology and epidemiology of diarrhea in children in Hanoi, VietnamInternational Journal of Infectious DiseasesYear: 20061029830816458564
Wagenaar JFP,Falke THF,Nam NV,Binh TQ,Smits HL,Cobelens FGJ,et al. Rapid serological assays for leptospirosis are of limited value in southern VietnamAnnals of Tropical Medicine and ParasitologyYear: 20049884385015667716
Waikagul J,Diaz Camacho P. Fried DMABGnathostomiasisFood-borne parasitic zoonoses: fish and plant-borne parasitesYear: 2007New YorkSpringer235261
Wertheim HF,Nghia HD,Taylor W,Schultsz C. Streptococcus suis: an emerging human pathogenClinical Infectious DiseasesYear: 20094861762519191650
Wertheim HF,Nguyen HN,Taylor W,Lien TT,Ngo HT,Nguyen TQ,et al. Streptococcus suis, an important cause of adult bacterial meningitis in northern VietnamPLoS ONEYear: 20094e597319543404
Willingham AL 3rd,De NV,Doanh NQ,Cong LD,Dung TV,Dorny P,et al. Current status of cysticercosis in VietnamThe Southeast Asian Journal of Tropical Medicine and Public HealthYear: 200334Suppl 1355012971506
Willingham AL III,Wu H-W,Conlan J,Satrija F. Combating Taenia solium cysticercosis in Southeast Asia: an opportunity for improving human health and livestock productionAdvances in ParasitologyYear: 20107223526620624534
Xiao L,Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmissionInternational Journal for ParasitologyYear: 2008381239125518479685
Xuan LT,Hoa PL,Dekumyoy P,Hoan NH,Khuong LH,Van TT,et al. Gnathosthoma infection in south VietnamSoutheast Asian Journal of Tropical Medicine and Public HealthYear: 200435Suppl. 1979915272751
Xuan LT,Hung NT,Waikagul J. Cutaneous fascioliasis: a case report in VietnamAmerican Journal of Tropical Medicine and HygieneYear: 20057250850915891121
Yu H,Jing H,Chen Z,Zheng H,Zhu X,Wang H,et al. Human Streptococcus suis outbreak, Sichuan, ChinaEmerging Infectious DiseasesYear: 20061291492016707046

Tables
[TableWrap ID: Tab1] Table 1 

Studies investigating the contributions of non-typhoidal Salmonella (NTS) to human diarrhoeal disease in Vietnam.


Citation Study date Study location Sample size Age Study type NTS prevalence Other aetiologies and observations
Ngan et al. (1992) 1988–1989 Hanoi 83 diarrhoea cases <3 years Hospital-based study No cases detected 24% had ETEC isolated, 8% had EPEC, 5% rotavirus, 6% Candida, and 4% Giardia lamblia
Isenbarger et al. (2001) 1998–1999 Red River Delta (3 communes) 1,655 healthy children in longitudinal study; 2,160 diarrhoea cases; 203 controls <5 years Longitudinal (community), hospital-based case-control study 0.8% cases, 1% controls Diarrhoea incidence: 1.3 episodes/child/year. Only bacterial aetiologies investigated: Main aetiologies (cases vs. controls): Campylobacter spp. (6.8 vs. 3.8%), Shigella spp. (6.5 vs. 1.5%), ETEC (6.5 vs 4.4%)
Bodhidatta et al. (2007) 2001 Hanoi 291 diarrhoea cases; 291 controls <5 years Hospital-based case-control study 7% cases; 1% controls Main aetiologies (cases vs. controls): Rotavirus (31% vs. 3%); Aeromonas (15% vs. 8%); Astrovirus (12% vs. 1%); Shigella (9% and 1%); Campylobacter (4% and 0%); Adenovirus (4% vs. 1%) and ETEC (3.0% vs. 0%)
Nguyen et al. (2004); Vu Nguyen et al. (2006) 2001–2002 Hanoi 587 diarrhoea cases; 249 controls <5 years Hospital-based case-control study No cases detected Main aetiologies (cases vs. controls): Rotavirus (46.7 vs. 3.6%), EAEC (11.6% vs. 7.2%), EPEC (6.6 vs. 4.4%), ETEC (2.2 vs. 0.4%); Shigella spp. (4.8 vs. 0%). Campylobacter isolation not attempted.
Khan et al. (2010) 2001–2003 International study including hospital in Hue (central Vietnam) 3611 febrile patients 5 to 15 years Hospital-based No cases detected S. typhi detected in 18 cases (0.5%) in Hue; International study. Other sites in Pakistan, India, and Indonesia also included
Hien et al. (2007) 2002–2004 Hanoi; suburban area using wastewater for agriculture and aquaculture 222 children enrolled in longitudinal study; 111 diarrhoea cases; 111 controls <6 years Longitudinal (community), hospital-based case-control study 3.6% cases; 2.7% controls Diarrhoea incidence: 0.63 episodes/child/year. Aetiologies (cases vs. controls): Rotavirus (17.1% vs. 4.5%), Entamoeba hystolitica (15.3% vs. 4.5%), diarrhoeagenic E. coli (22.5 vs. 23.4%), Shigella spp. (6.0 vs. 0%), Campylobacter spp. (1.8 vs. 1.8%)
Do et al. (2007) 2002–2004 Red River Delta 636 healthy adults in longitudinal study; 163 cases and 163 controls 15–70 years Longitudinal (community), hospital-based case–control study 0.6% cases; 3.1% controls Diarrhoea incidence: 0.28 episodes per adult per year. Aetiologies (cases vs. controls): E. hystolitica (9.9 vs. 0%); Diarrhoeagenic E. coli (13.5 vs. 9.8%); Shigella (3.1 vs. 1.2%); C. jejuni (0.6 vs. 0%); rotavirus (3.7 vs. 0.6%)
Thompson et al. (2012) 2009–2010 HCMC 1,419 diarrhoea cases <5 years Hospital-based study 5.4% cases (of which 58% were Group B) Main independent risk factors: diarrhoeal contact (OR = 6.0) and living in a household with >2 children (OR = 2.3)

[TableWrap ID: Tab2] Table 2 

Studies investigating NTS in food animals, meat and processed meat products of Vietnam.


Citation Study date Study location Sampling site, species, sample type Sample size NTS prevalence; additional observations NTS serovars
Tran et al. (2004) 2000 Mekong Delta (6 provinces) Animals in farms: pigs (faeces), chickens and ducks (caecal samples) 439 pigs, 302 chickens, 357 ducks Prevalence in pig, chicken and duck samples was 5.2, 7.9, and 8.7%, respectively. Higher prevalence on small-scale farms than industrial farms Most common serovars: S. Javiana and S. Derby (pigs); S. Emek and S. Javiana (chickens); S. typhimurium and S. Weltvreden (ducks)
Vo et al. (2006) 2004 South Vietnam (13 provinces) Pigs, cattle, chickens, ducks (carcasses, faeces, meat) at farms and abattoirs; Human (faeces) Pigs (534), Cattle (390), Chickens (257), Ducks (34) Prevalence in pigs, cattle, chicken and duck samples: 49.4, 27.4, 38.5, 20.5%, respectively. Most common serovars: S. typhimurium and S. Anatum (pigs); S. Emek and S. Blockley (poultry); S. Anatum, S. Weltevreden, and S. Lexington (15.9%) (cattle)
Hong et al. (2006) 2004 Central Vietnam Pigs on smallholder farms (faeces) 100 farms; 90 piglets with diarrhoea, 63 piglets without diarrhoea No difference in prevalence of NTS in piglets with and without diarrhoea (10 and 11% positive, respectively)
Phan et al. (2005) 2000–2001 Mekong Delta Fresh meat and shrimps from the market 718 samples of meat (pork, duck, beef, chicken) and shrimps 70% (pork); 49% (beef); 24% (shrimps); duck (22%); 21% (chicken) Most common serovars: S. Derby, S. Weltrvreden, and S. London (pork); S. Weltevreden, S. London, S. Dessau (beef); S. Emek, S. typhimuirum, S. Dessau (chicken); S. Lexington, S. Derby, and S. Dessau (duck); S. Dessau, S. Weltvreden and S. Tennessee (shrimps)
Van et al. (2007) Unknown HCMC Fresh meat market samples 130 samples of meat 64% (pork); 62% (beef); 18% (chicken).
Ha and Pham (2006) 2003–2004 Hanoi Meat samples from factory, schools, hospital canteens 177 meat samples 8.3% poultry meat; 1.2% other meat
Thai et al. (2012) 2007–2008 Northern Vietnam Retail supermarkets 586 meat samples 39.6% (pork); 42.9% (chicken) Most common serovars: S. Emek, S. Infantis, S. Blockey, and S. Anatum (chicken); S. Anatum, S. Derby, S. typhimurium and S. Infantis (pork)
Le Bas et al. (2006) Unknown Hanoi 15 pig slaughterpoints (faeces, carcass swabs) 117 faeces (caeca) and 46 carcass swabs 52% (faeces) and 96% (carcass swabs)
Ellerbroek et al. (2010) Unknown Hanoi 6 pig slaughterpoints (lymph nodes) 178 lymph nodes Prevalence from backyard small-scale farms (43%) versus intensive farms (29%) S. Derby (50%); S. typhimurium (27%). Most S. typhimurium isolates were phage type DT22
Ta et al. (2012) Unknown Six provinces (different regions) Wet markets and supermarkets (chicken carcasses) 1,000 carcasses 46%; no significant difference between study sites, temperature at retail, or wet markets versus supermarkets

[TableWrap ID: Tab3] Table 3 

Published surveys of Toxoplasma gondii in humans and domestic animal species in Vietnam.


Citation Study date Study location Species Details Sample size Overall prevalence; additional observations
Sery et al. (1988) 1984 Suburban Hanoi and Hoa Binh (northern mountain region) Human Healthy individuals, all ages 259 (140 from Hanoi, 119 from Hoa Binh) 24.3% (Hoa Binh); 15.7% (suburban Hanoi); Higher prevalence in early childhood than middle age.
Huong et al. (1998) 1995 Near HCMC Cattle, buffalo Cross-bred Frisian-Zebu cattle 200 of each species 10.5% (cattle) and 3% (buffalo)
Dubey et al. (2008) 2003 Mekong Delta (6 provinces) (and 6 other countries: Ghana, Indonesia, Poland and Italy Chickens From 38 different farms 330 24.2% seropositive by MAT
Huong and Dubey (2007) 2003–2005 Southern Vietnam (Dong Nai, Tien Giang provinces) Pigs 587 27.2% seropositive in market weight pigs (6 months). Prevalence higher in older pigs
Dubey et al. (2007) 2006 Mekong Delta (7 provinces) Domestic dogs 42 50% seropositive; experimental infections of naive cats with tissues from 8 dogs with high titres demonstrated transmission in 100% cases; high genetic similarity between T.gondii isolates from Vietnam and South America
Udonsom et al. (2008) 2007 Three provinces: Nghe An and Lao Cai (north) and Tien Giang (Mekong Delta) Humans Rural 650 Overall prevalence 4.2%; Highest in Nghe An (6.4%), followed by Lao Cai (4.7%) and Tien Giang (1.1%)

[TableWrap ID: Tab4] Table 4 

Published surveys of Taeniasis/Cysticercosis in humans in Vietnam.


Citation Study date Study location Type of study Details Sample size Overall prevalence; additional observations
Erhart et al. (2002) 1999 Bac Ninh (Red River Delta) Survey using serum cysticercosis prevalence Healthy individuals, all ages 210 5.7%; 5/12 seropositive individuals reported history of epilepsy.
Verle et al. (2003) 1999 Hoa Binh (north-western Vietnam) Survey of gastrointestinal helminth infection 6 ethnic groups 526 households (2,522 samples) Taenia eggs detected in 0.1% stool samples. One person had subcutaneous nodules that were diagnosed as cysticercosis by biopsy
Somers et al. (2007) 2002–2003 Northern Vietnam (14 provinces) Hospital-based Patients 65 patients from 14 hospitals 55.4% specimens identified as T. asiatica; 38.5% T. saginata and 6.2% T. solium tested by mitochondrial 12S rDNA by PCR
Somers et al. (2006) 2003–2004 Bac Kan (far northern province); Ha Tinh (central Vietnam); Hai Duong (Red River Delta) Survey using serum (prevalence of cysticercosis) and faeces (prevalence of taeniasis) Healthy individuals from 3 areas:
1. Bac Kan (rural, mountainous)
2. Ha Tinh (rural, coastal)
3. Hai Duong (peri-urban, costal)
303 (mountainous region); 179 (rural coastal region);
229 (peri-urban, coastal region)
Study investigating helminth infections. 5.3% (Bac Kan); 0.6% (Ha Tinh); 0% (Hai Duong)

[TableWrap ID: Tab5] Table 5 

Published surveys of Fasciola spp. in humans and ruminants in Vietnam.


Citation Study date Study location Species Sample collections Sample size Overall prevalence; additional observations
Tran et al. (2001a, b) 1997–2000 Hospitals in central and southern Vietnam Humans Stools from hospitalized patients with confirmed Fasciola infection 500 Largest number of cases from central provinces of Khanh Hoa, Binh Dinh and Quang Nga; prevalence per site per year unknown
Verle et al. (2003) 1999 Hoa Binh (north-western Vietnam) Humans Stools from healthy community cohorts (6 ethnic groups) 2,522 from 526 households No Fasciola eggs detected
Holland et al. (2000) 1999–2000 Hanoi province (northern Vietnam) Cattle Faeces 119 22% Fasciola egg-positive; positives only among animals >3 months; no evidence of seasonality
Linh et al. (2003) 2000–2002 Hanoi province (northern Vietnam) Cattle/buffalo Faeces and livers 30 cattle, 2 water buffalo 62% Fasciola egg-positive, and 100% positive for worms in liver tissue
Anderson et al. (1999) 2002 Hanoi city (northern Vietnam) Cattle Faeces and livers 92 78.3% cattle had Fasciola in liver. Positive correlation between age of cattle and number of liver flukes
Suzuki et al. (2006) 2002–2003 Hanoi province (northern Vietnam) Cattle 99 smallholder dairy farms; 4 time points; faeces 263 cattle 10% Fasciola egg-positive in June; 26% egg-positive in March; significant association between poor reproductive performance and Fasciola infestation
Uga et al. (2005) 2003–2004 Suburban Hanoi (northern Vietnam) Humans Stools from adolescents (14–15 years) 116 1% Fasciola egg-positive. The most frequently detected helminths were: Trichuris trichiura (67%), Ascaris lumbricoides (34%) and hookworm (3%)
Geurden et al. (2008) 2006 Red River Delta (5 provinces) Cattle Faeces 334 cattle 28% Fasciola egg-positive (3-24 moths); 39% prevalence in cattle >2 years
Nguyen et al. (2011) 2008 Binh Dinh (central Vietnam) Cattle Faeces and sera 825 cattle 54.9% Fasciola egg-positive and 72.2% Fasciola seropositive

[TableWrap ID: Tab6] Table 6 

Published surveys of foodborne trematode zoonoses (FTZ) in humans and animals in Vietnam.


Citation Study date Study location Sample collections Sample size Overall prevalence; additional observations
Phan et al. (2011) Unknown Nam Dinh province (Red River Delta) Faeces of farming household members 180 32.2% FZT egg-positive; 8% did not report eating raw fish; OR = 2.3 for consuming raw fish (vs. no consumption); OR = 3.6 for eating raw fish in restaurants vs. eating raw fish at home
De (2004) 1976–2002 15 provinces all over the country Healthy individuals, domestic dogs and cats ~30,000 Overall 21% FZT egg-positive for C. siniensis/O. viverrini. Highest in Nam Dinh (37.5%) and lowest in Thai Binh (0.2%). Prevalence 3 times higher among men. Peak in 40-50 years. Prevalence in dogs (28.6%) and 64.2% in cats. 7/10 species of fresh water fish infected with metacercaria
Kino et al. (1998) 1997 Ninh Binh province (Red River Delta) Faeces from healthy individuals; tissues of farmed fish 306 13.7% FZT egg-positive for C. siniensis; Males higher prevalence than females (23 vs. 1.5%); prevalence increase with age; prevalence of metacercaria in silver carp >56%; prevalence of cercaria among Melanoides tuberculatus snails (13%)
Dang et al. (2008) 1999/2000 Ninh Binh province (Red River Delta) Faeces from healthy individuals 1,115 26.1% FZT egg-positive; males higher prevalence than females; All adult parasites recovered were C. sinensis; association between FZT positivity and consumption of raw fish
Olsen et al. (2006) 2004 Nghe An (north-central Vietnam Faeces of fish farmers 964 0.6% FZT egg-positive for FZT; 0.7% for Fasciolopsis buski; infection prevalences of Ascaris lumbricoides, Trichuris trichiura and hookworm were 34.8, 50.7 and 51.3%, respectively
Trung et al. (2007) 2005 Nam Dinh province (Red River Delta) Faeces of healthy individuals; positive individuals examined for adult parasites after treatment with praziquantel 615 (33 examined twice) 65% FZT egg-positive; Among treated and re-examined patients: 51% positive with C. sinensis. Other species identified were Haplorchis pumilio (100%); H. taichui (70%); H yokogawai (3%); Stellantchasmus falcatus (6%); Fascilopsis buski (3%)
Chi et al. (2008) 2005 North-central Vietnam Tissues of tilapia and 6 carp species from 53 fish farms 716 12–61% FZT metacercaria positive species included FZT H. pumilio, H. taichui, H. yokogawai, Centrocestus formosanus, S. falcatus and Echinochasmus japonicus; similar prevalence in nursery and grow-out ponds
Lan-Anh et al. (2009) 2005 Nghe An (north-central Vietnam) Faeces of terrestrial farm species 35 domestic cats, 80 domestic dogs, and 114 pigs 48% egg FZT positive (cats); 35% (dogs); 14% (pigs)
Nguyen et al. (2007a, b) 2005–2006 Nghe An (north-central Vietnam Tissues of tilapia and carp fish reared on wastewater-fed ponds 1,200 Overall ~4.8% FTZ metacercaria positive (higher in warmer months). All metacercariae recovered were of the family Heterophyidae. Tilapia and 3 species of carp were infected
Thu et al. (2007) 2005–2006 Mekong Delta Tissues of catfish and snakehead fish 852 31% FZT metacercaria positive; 10% positive for zoonotic species, including O. viverrini (1.9%), H. pumilio (2.8%) and Procerovum spp. (5.6%)
Anh et al. (2010) 2009 Nam Dinh province (Red River Delta) Liver tissues from poultry from 60 fish farms 50 (chickens); 50 (ducks) Identified Centrocestus formosanus and Echnostoma cinetorchis
De and Le (2011) 2009/2010 Nam Dinh (Red River Delta) Faeces of healthy individuals; positive individuals examined for adult parasites after treatment with praziquantel 405 (10 examined twice) 32.2% FZT egg-positive; 29.3% in males and 16.0% in females. 385 adult flukes from 10 patients identified: C. sinensis (14.6%), Haplorchis taichui (32.3%), Haplorchis pumilio (52.08%) and Centrocestus formosanus (1.0%)

[TableWrap ID: Tab7] Table 7 

Paragonimus spp. Studies in Humans in Vietnam.


Citation Study date Study location Sample collections Sample size Overall prevalence; additional observations
Queuche et al. (1997) 1993 Lai Chau (northern Vietnam) Sputum of patients with pulmonary disease; faeces of healthy people 155 patients; 225 healthy; 125 children 8–18 years; 16 domestic dogs; 15 pigs 28% of patients had eggs in sputum; Mean age 11 years; 2 of 155 patients had CNS symptoms; 5% healthy people were egg-positive; associations with consuming freshwater crabs; 5/16 dogs and 2/15 pigs tested positive for adult lung flukes
Vien et al. (1997) 1994/1995 Lai Chau (northern Vietnam) Sputum of chronic respiratory disease patients 44 2 of 44 with CNS symptoms; 100% of cases egg-positive; most cases had eaten insufficiently roasted crabs
Doanh et al. (2011) Unknown Three provinces: Lai Chau, Yen Bai (north) and Quan Tri (central) Sputum of healthy patients 590 12, 4 and 0% seropositive from Lai Chau, Yen Bain and Quan Tri, respectively; sequences from eggs from sputum of six individuals identified Paragonimus heterotremus

[TableWrap ID: Tab8] Table 8 

Summary of main challenges and suggested priority research areas on FBZ in Vietnam.


Foodborne pathogen Data on prevalence/ incidence in humans Data on animal reservoir Challenges for Vietnam Suggested areas of research
Non-typhoidal Salmonella (NTS) infection Responsible for ~0–7% of diarrhoea in <5 year children; limited data on serovar distribution in humans. High levels of NTS carriage among adults; some evidence for person-to-person transmission among children High prevalence and variability of serovars in poultry, pigs, fish/seafood and meat products Meeting export targets of meat products will require improved control of NTS in fish, pigs and poultry Attribution studies in humans; impact of urbanization and backyard farming on human immunity; Antimicrobial resistance; NTS diversity within backyard versus industrialized production systems
Campylobacter spp. infection Responsible for ~4–40% of diarrhoeal cases in <5 year children (Red River Delta) Very high prevalence in chicken carcasses and meat products High levels of multi-resistance including ciprofloxacin resistance Risk factors and attribution studies among clinical cases; prevalence and genetic diversity in backyard versus industrialized production systems, and along processing/ retailing market chains; impact of urbanization and backyard farming on human immunity
Streptococcus suis infection Most common cause of adult bacterial meningitis; majority of cases caused by S. suis serotype 2; approximately 5–43 confirmed cases per year in Vietnam High (>40%) carriage in upper respiratory tract (tonsils) of market weight swine; predominance of S. suis 2; epidemiological interactions with viral infections (e.g. PRRSv) Improved control over illegal marketing of ill pigs; hygiene and health quality standards in slaughter/processing facilities Estimation of burden of disease using combined indicators for human morbidity/mortality and economic losses to swine sector; risk factors for pig colonization; development of porcine vaccines and novel diagnostic tools for herd management and risk mitigation
Listeriosis Three clinical case reported from north Vietnam with meningitis in 2008/2009 No data Possible increased incidence in coming years, due to greater consumption of packed food items including soft cheeses, meat and fish Consumer perceptions of risk, health and safety in relation to highly processed foods; enhanced surveillance among high risk groups; investigation in food processing plants
Toxoplasmosis No published data on human clinical cases. Seroprevalence in humans ranging between 1.1 and 6.4%. Higher (7.7–11%) among pregnant women and drug users in some Very high prevalence in domestic dogs and pigs (>50%); lower in cattle and buffalo (3–10%) Unknown risks due to poor understanding of principle zoonotic reservoir Enhanced surveillance among pregnant women and neonates to estimate burden of disease; prevalence of oocysts in cats, dogs, dog meat and treated and untreated wastewater
Cryptosporidiosis No published data on human clinical cases. At least two studies of paediatric diarrhoea failed to identify Cryptosporidium High prevalence of C. parvum and C andersoni in cattle; Cryptosporidirum spp. oocysts found in pigs and farmed fish but not speciated Risks associated with uncontrolled urbanization, peri-urban agriculture, waste water treatment and climate change Etiological and syndromic studies of enteric disease in humans and animals; development of informal networks for reporting and investigating suspect foodborne outbreaks
Giardiasis No published data on human clinical cases. 4% carriage of G. lamblia among healthy subjects in north Vietnam 50% of calves near Hanoi found positive by feacal microscopy; however, dominant species may be non-zoonotic G. duodenalis Risks associated with uncontrolled urbanization, peri-urban agriculture, waste water treatment and climate change Etiological and syndromic studies of enteric disease; species diversity in farm animals and farmed ’wild’ exotic species; risk factor studies; detection of oocysts in vegetables, treated and untreated wastewater
Taeniasis/ cysticercosis In the late 1990s, approximately 100–150 cases/year with cerebral cysticercosis in northern Vietnam. Human surveys (2003/2004) using stool egg counts suggest low level prevalence of (0.2–7.2%). Likely to be circumscribed to certain areas in Vietnam Multiple species identified from pigs and domestic dogs, including T. solium, T saginata asiatica Probable future reductions in prevalence/incidence due to changes in swine production Seroepidemiological and clinical studies. Identify host species of T. s. asiatica; studies investigating prevalence of Taenia eggs in the environment
Fascioliasis >1,000 patients/year reported in central provinces, especially Quang Nai; seroprevalence ~8% in some areas; diagnostic case reports increasing Hyper-endemic in ruminants of central provinces (>70% in adult cattle); high level species diversity; hybrid species identified (F. gigantica and F. hepatica) Risks associated with changes in forage production for beef and dairy cattle Detection of metacercariae in leaf vegetables; ecologic determinants of disease transmission; risk assessment; development of novel indicators to estimate combined disease burden in humans and animals
Leptospirosis Highly seroprevalence in southern Vietnam suggesting endemicity. Responsible for 2–8% cases of acute jaundice. Main serovars identified Seramanga and Bataviae Hyper-endemic in pigs in the Mekong Delta Very common in kidneys in fattening pigs. Main serovars Bratislava, Iterohaemorrhagiae, Automnalis and Pomona Estimate burden of infection by targeting patients with suspect hepatic and haemorrhagic syndromes. Investigate main reservoirs of infection including rats, pigs, dogs and cattle
Trichinellosis Decreasing incidence in recent years; small outbreaks in northwest Seroprevalence in swine ~14–20% in some areas Probable future reductions in prevalence/incidence due to changes in swine production Role of rodents in transmission; risks associated with specific culinary practice
Fishborne zoonotic trematode (FZT) infection High rates of asymptomatic carriage in humans living in Red River Delta provinces (>75%) High species diversity including both pathogenic and non-pathogenic flukes of multiple genera Risks associated with expansion of aquaculture industry, waste water treatment and climate change Enhanced surveillance to estimate disease burden; detection of FZT in fish; risk assessment; intervention studies; ecologic determinants of disease transmission


Article Categories:
  • Review

Keywords: Keywords Vietnam, foodborne zoonoses, livestock, aquaculture, human–animal interface.

Previous Document:  The Absence of Zoonotic Agents in Invasive Bullfrogs (Lithobates catesbeianus) in Belgium and The Ne...
Next Document:  AAV1.NT-3 gene therapy for Charcot-Marie-Tooth neuropathy.