The dynamics of Trichinella spiralis epidemiology: Out to pasture?

The great public health success in prevention of human trichinellosis has resulted in a decades-long decline in the incidence and health impact of this zoonosis. The important elements of this achievement include improvement in animal husbandry practices, meat inspection, consumer education, and medical care. Most outbreaks now involve consumption of infected game. However, domestic pork still accounts for many outbreaks, mostly in Eastern Europe and Argentina, where traditional small, "backyard" rearing of pigs for household and local use often involve high risk rearing practices, especially the feeding of food waste. Although commercially produced pork under controlled management now accounts for about half of the world's pork production the demand by consumers, especially in Europe and North America, for free-range pork is increasing. Because of the varying degrees of outdoor exposure in free-range systems, there is concern that such exposure increases the risk of spillover of Trichinella spiralis, (also Trichinella britovi and Trichinella pseudospiralis in Europe) from wild animal reservoirs. This review examines the knowledge gaps hindering the risk assessments needed to provide the producers with guidelines for achieving the food safety assurance demanded by consumers.

Two-year intervention trial to control of fish-borne zoonotic trematodes in giant gourami (Osphronemus goramy) and striped catfish (Pangasianodon hypophthalmus) in nursery ponds in the Mekong Delta, Vietnam.

Fish-borne zoonotic trematode parasites (FZT) pose a food safety and public health problem in Vietnam. The transmission cycle is complex as domestic animals, especially dogs, cats, fish-eating birds and pigs together with humans serve as reservoir hosts and contribute to FZT egg contamination of aquaculture ponds and the environment. This intervention trial was conducted to determine the effectiveness of various on-farm interventions, including reduction in FZT egg contamination through treatment of infected people and domestic animals, reduction in snail density through mud removal from aquaculture ponds prior to fish stocking, and various other measures in reducing FZT infection in juvenile striped catfish (Pangasianodon hypophthalmus) and giant gourami (Osphronemus goramy). Interventions were implemented on 5 farms for each fish species during production cycles in 2009 and 2010 while 5 similar farms for each species served as control. For both fish species, both prevalence and intensity of infection did not differ significantly between intervention and non-intervention farms prior to the interventions. The interventions significantly reduced both prevalence and intensity of FZT infection in the juvenile fish compared to control ponds. For giant gourami, odds of infection in intervention ponds was 0.13 (95% CL: 0.09-0.20; p<0.001) of that in non-intervention ponds after the 2009 trial and 0.07 (0.03-0.14; p<0.001) after the 2010 trial. For striped catfish, these figures were 0.17 (0.08-0.35; p<0.001) after the 2009 trial while after the 2010 trial all ponds with interventions were free from infection. Metacercariae intensity (no. of metacercariae/fish) in giant gourami from intervention ponds was 0.16 (0.11-0.23; p<0.001) of that in fish from non-intervention ponds after the 2009 trial and 0.07 (0.04-0.15; p<0.001) after the 2010 trial; for striped catfish these figures were 0.18 (0.09-0.36; p<0.001) and 0.00 (confidence limits not estimated), respectively. The aquaculture farm pond intervention approaches taken in this trial have the potential to reduce or eliminate FZT infections in fish and may be implemented across the entire region if adjusted to local conditions and fish species.

Effect of pond water depth on snail populations and fish-borne zoonotic trematode transmission in juvenile giant gourami (Osphronemus goramy) aquaculture nurseries.

Infection with fish-borne zoonotic trematodes (FZT) is an important public health problem in many parts of Southeast Asia. People become infected with FZT when eating raw or undercooked fish that contain the infective stage (metacercariae) of FZT. The parasites require specific freshwater snails as first intermediate host and a variety of fish species, both wild caught and cultured, as second intermediate host. Aquaculture production has grown almost exponentially in SE Asia and in order to produce fish free from FZT metacercariae, it is important to mitigate factors promoting transmission to fish. Here we report results from a cross-sectional study to look at the association between pond depth and infection with FZT in giant gourami nursery ponds. Density of intermediate host snails was positively associated with pond depth (count ratio associated with a 1m increase in pond depth was 10.4 (95% C.L.: 1.61-67.1, p<0.5)) and this may partly explain the higher prevalence and intensity of FZT infection in juvenile fish. High fry stocking density (>200 fry m(-3)) was associated with lower host snail density (count ratio=0.15) than low stocking density (<100 fry m(3)). Ponds stocked with 100-200 fry m(-3) had snail counts 0.76 (95% C.L.: 0.33-1.75, p n.s.) of those in ponds stocked with fry density of <100 fry m(-3). Since density of intermediate snail hosts was associated with FZT transmission to fish, effort should be taken to reduce snail density prior to stocking the fry, but focus should also be on habitats surrounding ponds as transmission may occur through cercariae produced outside ponds and carried into ponds with water pumped into ponds.

Zoonotic foodborne parasites and their surveillance.

Humans suffer from several foodborne helminth zoonotic diseases, some of which can be deadly (e.g., trichinellosis, cerebral cysticercosis) while others are chronic and cause only mild illness (e.g., intestinal taeniosis). The route of infection is normally consumption of the parasite's natural host as a human food item (e.g., meat). The risk for infection with these parasites is highest wherever people have an inadequate knowledge of infection and hygiene, poor animal husbandry practices, and unsafe management and disposal of human and animal waste products. The design of surveillance and control strategies for the various foodborne parasite species, and the involvement of veterinary and public health agencies, vary considerably because of the different life cycles of these parasites, and epidemiological features. Trichinella spiralis, which causes most human trichinellosis, is acquired from the consumption of pork, although increasingly cases occur from eating wild game. For cysticercosis, however, the only sources for human infection are pork (Taenia solium) or beef (T. saginata). The chief risk factor for infection of humans with these parasites is the consumption of meat that has been inadequately prepared. For the pig or cow, however, the risk factors are quite different between Trichinella and Taenia. For T. spiralis the major source of infection of pigs is exposure to infected animal meat (which carries the infective larval stage), while for both Taenia species it is human faecal material contaminated with parasite eggs shed by the adult intestinal stage of the tapeworm. Consequently, the means for preventing exposure of pigs and cattle to infective stages of T. spiralis, T. solium, and T. saginata vary markedly, especially the requirements for ensuring the biosecurity of these animals at the farm. The surveillance strategies and methods required for these parasites in livestock are discussed, including the required policy-level actions and the necessary collaborations between the veterinary and medical sectors to achieve a national reporting and control programme.

Prevalence and intensity of fish-borne zoonotic trematodes in cultured freshwater fish from rural and urban areas of northern Vietnam.

Consumption of raw freshwater fish produced in both rural farm and urban wastewater ponds is a common practice in Vietnam. The present study assessed the risk of fish-borne zoonotic trematode (FZT) infection from fish raised in both these aquaculture systems in northern Vietnam. The diversity, prevalence, and infection intensity of FZT metacercariae in 1,500 freshwater fish collected from 6 sites located in rural and urban areas in northern Vietnam were investigated. The specific diagnosis of species was made by morphologic methods. The overall FZT prevalence in fish from both urban wastewater ponds and rural farm ponds was 11.2%. In wastewater ponds, the overall prevalence was 5.1%, ranging from 2.0% in tilapia to 7.3% in common and grass carp. In fish from farm ponds, the prevalence was 17.3%, and ranged from 6.7% in mud carp to 26.7% in common carp. The mean intensity of FZT infection was also higher in fish from farm ponds than that in fish from wastewater ponds (6.0% and 8.4%, respectively). The FZT species recovered from infected fish included both liver (Clonorchis sinensis) and intestinal flukes (Haplorchis taichui, Haplorchis pumilio, and Centrocestus formosanus). The prevalence of FZT in fish raised in these common farm systems represents a significant public health risk for a population with a strong cultural preference for consuming raw or inadequately prepared fish. These research results should encourage the public health and agriculture sectors to conduct the risk factor research required to develop control programs for FZT.

Population dynamics and intra-litter transmission patterns of Isospora suis in suckling piglets under on-farm conditions.

The aim of this study was to investigate the intra-litter infection dynamics of Isospora suis under natural conditions, and to study any association between parasite transmission and the contamination level of the farrowing pen by applying different interventions in order to reduce the transmission of I. suis infection within the litter. The study was divided in 2 trials including in total 22 litters (254 piglets). The first trial included 4 litters (where standard procedures practiced routinely on the farm piglets were applied) and the piglets were followed coprologically from farrowing until 2 weeks after weaning. The sows of those litters were also examined at various intervals before and after farrowing. The second trial included the application of 3 different management procedures: (A) standard farm hygiene and management procedures, (B) standard farm hygiene and management procedures+the first piglets found to excrete I. suis oocysts in each pen were removed from the pen, and (C) reduced cleaning. Each procedure was studied in 2 litters. This was replicated 3 times to yield a total of 18 litters. The results suggested that (i) the sow does not play an important role in transmission of I. suis in the farrowing pen; (ii) in natural infections, both the age of the piglet age at onset of oocyst excretion and the oocyst excretion patterns may vary considerably; (iii) the course of oocyst excretion or development of diarrhoea is related to the time of initial infection and (iii) piglets, which are heavy at birth, are more prone to acquire I. suis infection. Moreover, it was demonstrated that cleaning could be an effective means of restricting the spread of the parasite within the litter and thus the development of diarrhoea.

The effect of inulin on new and on patent infections of Trichuris suis in growing pigs.

The objective of this experiment was to investigate the potential influence of inulin on the establishment of new and patent infections of Trichuris suis in growing pigs. Two experimental diets were formulated based on barley flour with either added insoluble fibre from oat husk (Diet 1) or a pure inulin (16%) supplementation (Diet 2). Twenty-eight 10-week-old pigs were divided randomly into 4 groups (Groups 1-4) each of 7 pigs. After 3 weeks adaptation to the experimental diets all pigs were infected with a single dose of 2000 infective T. suis eggs. Group 1 was fed Diet 1 until 7 weeks post-infection (p.i.) and Group 3 until 9 weeks p.i., Group 2 was fed Diet 2 until 7 weeks p.i., Group 4 was fed Diet 1 until week 7 p.i. and was switched-over from Diet 1 to Diet 2 until week 9 p.i. Seven weeks p.i. pigs in Groups 1 and 2 were slaughtered, and pigs in Groups 3 and 4 were slaughtered at 9 weeks p.i. Trichuris suis worm burdens were determined for all pigs. Inulin-fed pigs (Group 2) exhibited an 87% reduction in EPG, compared to the pigs on standard diet (Group 1) (P < 0.0001). The number of worms recovered at week 7 p.i. from pigs on the inulin diet (Group 2) was significantly reduced by 71%, compared to the pigs on standard diet (Group 1) (P < 0.01). At week 9, worm recovery in pigs on the inulin diet switch protocol (Group 4) was reduced by 47% compared to the control pigs in Group 3 (P < 0.01). Further, the inulin-fed pigs exhibited a significant reduction in female worm fecundity and worm large intestine location was more distal compared to those from pigs on standard diet. These results demonstrate that inclusion of the highly degradable fructose polymer inulin in the diet leads to significant reductions in T. suis establishment, egg excretion, and female worm fecundity and can be used as a treatment for patent infections.

Anti-Trichinella antibodies detected in chronically infected horses by IFA and Western blot, but not by ELISA.

In the Balkan countries, where trichinellosis is a re-emerging zoonosis, it is of great importance to determine Trichinella infection prevalence among the major hosts, including horses. One method for monitoring prevalence is serological surveillance; however, the validity of serological methods in horses is not well understood. The dynamics of anti-Trichinella IgG production and circulating excretory/secretory (ES) antigens were investigated in three horses experimentally-infected with Trichinella spiralis. Horses were slaughtered at 32 week post infection (p.i.). Low worm burdens were found in all three animals. Anti-Trichinella IgG was detected up to 32 weeks p.i. by an indirect immunofluorescence assay (IFA) and by Western blot (Wb), but not by ELISA. The ELISA test detected antibodies for only a short period of time (up to 18 weeks p.i. using ES antigen or up to 20 weeks p.i. using tyvelose-BSA antigen). The presence of circulating muscle larvae ES antigen in sera of infected horses was observed by dot blot from the 4th week p.i. up to the 32nd week p.i.

Epidemiology of Trichinella infection in the horse: the risk from animal product feeding practices.

A discovery in 2002 of a Trichinella spiralis-infected horse in Serbia offered an opportunity to conduct needed epidemiological studies on how horses, considered herbivores, acquire a meat-borne parasite. This enigma has persisted since the first human outbreaks from infected horse meat occurred in then 1970s. The trace back of the infected horse to a farm owner was carried out. Interviews and investigations on the farm led to the conclusion that the owner had fed the horse food waste in order to condition the horse prior to sale. Further investigations were then carried out to determine the frequency of such practices among horse owners. Based on interviews of horse producers at local horse markets, it was revealed that the feeding of animal products to horses was a common practice. Further, it was alleged that many horses, particularly those in poor nutritional condition would readily consume meat. A subsequent series of trials involving the experimental feeding of 219 horses demonstrated that 32% would consume meat patties. To confirm that horses would eat infected meat under normal farm conditions, three horses were offered infected ground pork balls containing 1100 larvae. All three became infected, and at necropsy at 32 weeks later, were still positive by indirect IFA testing, but not by ELISA using an excretory-secretory (ES) antigen. This result indicates that further study is needed on the nature of the antigen(s) used for potential serological monitoring and surveillance of horse trichinellosis, especially the importance of antigenic diversity. The experimentally-infected horses also had very low infection levels (larvae per gram of muscle) at 32 weeks of infection, and although the public health consequences are unknown, the question of whether current recommended inspection procedures based on pepsin digestion of selected muscle samples require sufficient quantities of muscle should be addressed. It is concluded that horses are more willing to consume meat than realized and that the intentional feeding of animal products and kitchen waste is a common occurrence among horse owners in Serbia (and elsewhere?). This is a high risk practice which demands closer scrutiny by veterinary and food safety authorities, including the implementation of rules and procedures to ensure that such feeds are rendered safe for horses, as is now required for feeding to swine.

Effects of short-chain fatty acids and lactic acids on survival of Oesophagostomum dentatum in pigs.

The direct influence of intracaecal infusion of short-chain fatty acids (SCFA) and lactic acids (LA) on already established Oesophagostomum dentatum infection in cannulated pigs was investigated. We tested the hypothesis that the previously discovered anti-parasitic effect of inulin is mediated through its metabolic products SCFA and LA by infusing into cannulated pigs these compounds in amounts approximating to those produced in the pigs large intestine and caecum during the metabolism of inulin. The experiment comprised of 18 pigs--2 groups of 9 pigs in each. The normal diet used in the experiment was based on barley flour with insoluble fibre from oat husk with added soybean meal, vitamins and minerals. After 2 weeks of adaptation to the diet all the pigs were inoculated with 6,000 infective larvae of O. dentatum. Six weeks later, surgery on all pigs was performed to install cannulas into caeci. At 7 weeks post-infection (p.i.) the SCFA and LA infusion was initiated in Group 1 (experimental) pigs; at the same time pigs in Group 2 (controls) were infused with saline. At week 10 p.i., all pigs were killed and their worm burdens determined. SCFA and LA infused pigs exhibited markedly reduced fecal egg counts and worm recoveries (98 and 92% reduction, respectively, compared to saline controls). The results from this study demonstrate that SCFA and LA have a significant negative influence on established O. dentatum infection in growing pigs. The results also show that the type of dietary carbohydrates fed and its intestinal degradation can yield metabolic by products that profoundly influence helminth survival.