Farmed wild boars exposed to Toxoplasma gondii and Trichinella spp.

doi:10.1016/j.vetpar.2011.12.026

Veterinary Parasitology

Volume 187, Issues 1–2, 8 June 2012, Pages 323-327

https://doi.org/10.1016/j.vetpar.2011.12.026 Get rights and content

Abstract

The meat of wild boar (Sus scrofa L.) can be a source of human infections with zoonotic parasites Toxoplasma gondii and Trichinella spp. We screened 197 wild boar sera collected at slaughter from 25 Finnish farms in 2007–2008 for serological evidence of infections with these parasites. Using a commercial direct agglutination test at a serum dilution of 1:40, T. gondii-specific IgG antibodies were detected in 65 (33.0%) samples, on 14 (56.0%) farms. Females, animals older than 24 months, animals of small herds, and animals originating from south-western parts of Finland were more often T. gondii-seropositive than were males, younger animals, animals of larger herds, and animals originating from the north and east, respectively. Four (2.0%) of the sera, originating from three (12.0%) farms, tested Trichinella-seropositive with an in-house ELISA and a conservative cut-off for seropositivity. One farm had both T. gondii- and Trichinella-seropositive animals. Taken together, an infection source had been present on 16 (64.0%) farms, and 69 (35.0%) of the 197 farmed wild boars intended for human consumption had specific serological evidence of exposure to a zoonotic parasite.

Introduction

The European wild boar (Sus scrofa L.) is a popular game animal species whose meat is also available for consumers as a farmed delicacy. Unfortunately, it can be a source of zoonotic parasites, such as Toxoplasma gondii and Trichinella spp., if enjoyed undercooked (EFSA, 2005, EFSA, 2007). At the slaughterhouse level, meat intended for retail is monitored for Trichinella, but not for T. gondii infections.

Although many epidemiological and parasitological studies of wild boar pertain to free-ranging animals (e.g. for T. gondii, reviewed by Fornazari et al., 2009), investigating the role of farmed wild boars as hosts for zoonotic parasites is also of both public health and veterinary importance. Contrary to expectations for free-ranging game animals, farmed animals could be at least partly protected from such infections. In Finland, approximately 100 free-ranging wild boars are shot by hunters every year, and 600 farmed wild boars are slaughtered for meat. This serological survey aimed to estimate the exposure of the farmed wild boar population to T. gondii and Trichinella spp.

Section snippets

Farms and animals

This survey was part of a nationwide epidemiological study for which a sampling frame was compiled from the official records of Finnish wild boar farmers. All 117 farms were contacted and 32 (45% of active farms) participated in the study. The farmers sampled their wild boars at slaughter and provided the background information on the animals and farms.

For this survey, we selected serum samples from 2007 to 2008 to obtain a sufficient sample size, calculated based on expected seroprevalences of

Prevalences

T. gondii-specific IgG antibodies were detected in 65 (33.0%; 95% CI 26.7–39.8%) sera (Table 1). At least one T. gondii-seropositive animal was found on 15 (60.0%; 95% CI 40.2–77.6%) farms (Fig. 1).

Based on the cut-off that we set, four (2.0%; 95% CI 0.6–4.8%) samples were interpreted as Trichinella-seropositive (Table 1). Three (12.0%; 95% CI 3.1–29.3%) farms had at least one Trichinella-seropositive animal. In general, higher ODs seemed to be clustered on some of the farms (Fig. 2).

Indirect

Discussion

The T. gondii seroprevalence in Finnish farmed wild boars (33%) was seven times higher than the seroprevalence in captive wild boars in Brazil (4.5%) despite our higher threshold for defining a positive sample (Fornazari et al., 2009). The method used in the Brazilian study is fundamentally the same as the direct agglutination test used in our study.

The Trichinella seroprevalence in Finnish farmed wild boars (2%) was lower than the previous estimate (11%) (Sukura et al., 2001). However, that

Conflict of interest statement

The authors declare no conflicts of interest.

Acknowledgements

The authors thank the farmers for their contribution in sampling the animals, the personnel of the Quality Game Farming project for their assistance, and Antti Oksanen for commenting on the manuscript during its preparation. Financial support was provided by the Finnish Ministry of Agriculture and Forestry, the Association for Animal Disease Prevention (ETT), and the Mercedes Zachariassen Foundation.

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Toxoplasma gondii is an important zoonotic parasite worldwide, but it has received limited attention in Ukraine. A seroepidemiological study was conducted and samples from 452 wild boars that had been hunted in 2006–2011 in 23 of the 25 regions of Ukraine were tested to estimate T. gondii seroprevalence. A locally available commercial enzyme-linked immunosorbent assay (ELISA) was used for the investigation. Additionally, we tested 92 of the sera using a widely used commercial multi-species ELISA and an indirect immunofluorescence antibody test (IFAT). With the locally available ELISA, 35 of the 452 wild boars tested positive, yielding a seroprevalence estimate of 7.7% (95% confidence interval 5.5–10.5). The seropositive wild boars originated from eight of the regions. Using the majority criteria, 10/92 samples tested using both ELISAs and the IFAT were considered positive, yielding an estimated seroprevalence of 10.9% within the subset of samples. The highest seroprevalence was observed in wild boars hunted in Luhans'k (30.0%), Odesa (17.7%) and Kharkiv (12.7%). Seroprevalence was higher in older animals (13.3% for age group >12 months and 7.7% for age group ≤12 months). This is the first seroepidemiological study of T. gondii in wild boars in Ukraine. Assuming that seropositivity indicates presence of infectious parasites in the tissues, eating undercooked meat of wild boars hunted in Ukraine could be a potential source of infection to other hosts, including humans.
Epidemiology of Trichinella in the Arctic and subarctic: A review
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Citation Excerpt :
Corresponding percentages for T. nativa were 62.5, 74.7, and 90.2, respectively. Antibodies against Trichinella were detected in 11% of 99 and 2% of 197 farmed Finnish wild boars that had been tested negative for muscle larvae in meat inspection (Sukura et al., 2001; Jokelainen et al., 2012). The seropositive wild boars had possibly been exposed to T. nativa, which has low infectivity to swine, including wild boar (Kapel, 2001).
The finding of Trichinella in the Arctic was foreseen because captive polar bears and arctic foxes had been found infected during the first decades of the 20th century. Human trichinellosis outbreaks were reported to have taken place in 1944 in Franz Josef Archipelago and 1947 in Greenland, and previous outbreaks in Greenland also appeared to have been trichinellosis. Now, it is known that Trichinella parasites thrive in the Arctic and subarctic and pose a risk for public health. We collated the available information, which show that infection prevalences are high in many animal host species, and that outbreaks of human trichinellosis have been described also recently. The species diversity of Trichinella in the Arctic and subarctic is relatively high, and the circulation is in non-domestic cycles with transmission by predation, scavenging and cannibalism. There are also sporadic reports on the synanthropic species Trichinella spiralis in arctic wild mammals with little known or assumed contact to potential synanthropic cycles. In this paper, we summarize the knowledge on epidemiology of Trichinella parasites in the circumpolar Arctic and subarctic regions, and discuss the challenges and solutions for their control.
All about Toxoplasma gondii infections in pigs: 2009–2020
2020, Veterinary Parasitology
Citation Excerpt :
Most data were from hunted wild swine. The prevalence was generally low in a few samples from farmed boars in China (9.9%, Bai et al., 2017), Denmark (28.0%, Laforet et al., 2019), Finland (33.0%, Jokelainen et al., 2012), Latvia (20.3%, Deksne and Kirjusina, 2013), and Ukraine (6.6%, Galat et al., 2018). These pigs are probably slaughtered for general human consumption.
Toxoplasma gondii infections are common in humans and animals worldwide. Toxoplasma gondii infection in pigs continues to be of public health concern. Pigs are important for the economy of many countries, particularly, USA, China, and European countries. Among the many food animals, pigs are considered the most important for T. gondii transmission in USA and China because viable parasites have rarely been isolated from beef or indoor raised chickens. Besides public health issues, T. gondii causes outbreaks of clinical toxoplasmosis in pigs in China, associated with a unique genotype of T. gondii (ToxoDB genotype #9 or Chinese 1), rarely found in other countries. The safety of ready to eat pork products with respect to T. gondii infection is a matter of recent debate. Here, we review in detail seroprevalence, prevalence of viable and nonviable T. gondii, epidemiology, risk assessment, diagnosis, and curing of pork products containing T. gondii for the past decade. This review will be of interest to biologists, parasitologists, veterinarians, and public health workers.
Seroprevalence of Toxoplasma gondii in domestic pigs, sheep, cattle, wild boars, and moose in the Nordic-Baltic region: A systematic review and meta-analysis
2019, Parasite Epidemiology and Control
Toxoplasma gondii is an important foodborne zoonotic parasite. Meat of infected animals is presumed to constitute a major source of human infection and may be a driver of geographical variation in the prevalence of anti-T. gondii antibodies in humans, which is substantial in the Nordic-Baltic region in northern Europe. However, data on seroprevalence of T. gondii in different animal species used for human consumption are scattered.
We conducted a systematic review of seroprevalence studies and meta-analysis to estimate the seroprevalence of T. gondii in five animal species that are raised or hunted for human consumption in the Nordic-Baltic region: domestic pigs (Sus scrofa domesticus), sheep (Ovis aries), cattle (Bos taurus), wild boars (Sus scrofa), and moose (Alces alces). We searched for studies that were conducted between January 1990 and June 2018, and reported in articles, theses, conference abstracts and proceedings, and manuscripts. Subgroup analyses were performed to identify variables influencing the seroprevalence.
From a total of 271 studies identified in the systematic review, 32 were included in the meta-analysis. These comprised of 13 studies on domestic pigs, six on sheep, three on cattle, six on wild boars, and four on moose. The estimated pooled seroprevalence of T. gondii was 6% in domestic pigs (CI_95%: 3–10%), 23% in sheep (CI_95%: 12–36%), 7% in cattle (CI_95%: 1–21%), 33% in wild boars (CI_95%: 26–41%), and 16% in moose (CI_95%: 10–23%). High heterogeneity was observed in the seroprevalence data within each species. In all host species except wild boars, the pooled seroprevalence estimates were significantly higher in animals >1 year of age than in younger animals. Not all studies provided information on animal age, sensitivity and specificity of the serological method employed, and the cut-off values used for defining an animal seropositive.
A substantial proportion of animals raised or hunted for human consumption in the region had tested positive for T. gondii. This indicates widespread exposure to T. gondii among animals raised or hunted for human consumption in the region. Large variations were observed in the seroprevalence estimates between the studies in the region; however, studies were too few to identify spatial patterns at country-level.
A systematic review and meta-analysis on the global seroprevalence of Trichinella infection among wild boars
2018, Food Control
Citation Excerpt :
We performed subgroup analyses to find source of heterogeneity, but it remained high after subgroup analysis. We assumed that differences in study design or sampling strategy, characteristics of the serological assays used, different positive cut-off values and different sources of animals studied (e.g., Cuttell et al., 2014 studied wild boar from a low risk region and Jokelainen, Näreaho, Hälli, Heinonen, and Sukura (2012) used farmed wild boar in their study) could be reasons for high heterogeneity. Despite the aforementioned limitations, the analysis and interpretation presented here furthers our understanding of the global seroprevalence of Trichinella infection among wild boar.
Trichinellosis, caused by the parasitic nematode Trichinella spp. is a widespread foodborne zoonotic disease and is a public health concern in many countries. Wild boar is the second most important source of trichinellosis for humans. We conducted a systematic review and meta-analysis to evaluate the global seroprevalence of Trichinella infection among wild boar. We searched five major databases for studies reporting Trichinella spp. seroprevalence in wild boar between January 1995 and January 2018. Inclusion and exclusion criteria were applied. A random-effects model was used to estimate the pooled seroprevalence of Trichinella in wild boar. A total of 21 studies involving 16,327 wild boar from 15 countries were included in this meta-analysis. The pooled seroprevalence for Trichinella infection in wild boar was 6% (95% CI: 3–10%; 1084/16327). The estimated seroprevalence in North America was 9% (95% CI, 1–25%), in Europe 7% (95% CI, 3–13%), in Asia 3% (95% CI, 0.0–11%) and in Oceania 3% (95% CI, 2–4%). Geographical location, gender and age were not significantly associated with seropositivity. In sub-group analysis, the pooled seroprevalence of Trichinella infection in wild boar when ELISA was used as the diagnostic test (16%; 95% CI, 4–34%) was significantly higher when compared to western blot (4%; 95% CI, 0–12%). These results emphasize that wild boars are a potential source for acquisition of Trichinella infection in humans, and surveillance programs should be implemented in high-risk countries.
The global seroprevalence of Toxoplasma gondii among wild boars: A systematic review and meta-analysis
2017, Veterinary Parasitology
Citation Excerpt :
Whereas, the seroprevalence of T. gondii decreases in subarctic and arctic areas (higher altitude than 65°), where environment temperature is low and domestic cats are rare, and, when present are mostly kept indoors. In support of this statement, a geographical north-south gradient in seroprevalence of T. gondii was estimated in domestic moose, sheep, farmed wild boars, and lynx in Finland (Jokelainen et al., 2010, 2012, 2013). Moreover, Flegr et al. (2014) showed that prevalence of human toxoplsmosis decreases with an increase in geographical latitude.
This systematic review and meta-analysis study was performed to evaluate the worldwide seroprevalence of Toxoplasma gondii among wild boar. We searched PubMed, Science Direct, Web of Science, Cochrane, Scopus, EBSCOhost and Google Scholar databases for studies reporting T. gondii seroprevalence in wild boars between January 1995 and March 2017. Inclusion and exclusion criteria were applied. We estimated the pooled seroprevalence of T. gondii in wild boars using a random-effects model, and evaluated overall seroprevalence in different geographical areas. A total of 43 articles that included 16788 wild boar from 23 countries fulfilled our eligibility criteria. Of these, 4759 wild boar had been defined T. gondii seropositive and we estimated the pooled worldwide seroprevalence of toxoplasmosis in wild boars to be 23% (95% CI: 19–27%). The pooled seroprevalence in North America (32%, 20–45%; odds ratio [OR] 2.09) and Europe (26%, 21–30%; OR 1.72), was higher than Asia (13%, 5–23%). The lowest seroprevalence was estimated in South America (5%, 3–8%). An increased seropositivity was observed with elevation in geographical latitude. In subgroup analyses, the pooled seroprevalence of T. gondii was higher in wild boar older than 12 months of age (28%, 22–35%; OR 1.57) compared to those up to 12 months of age (20%, 16–25%). Our findings suggest that wild boar have an important role in human infection and the epidemiological cycle of T. gondii infection.

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Veterinary Parasitology

Abstract

Introduction

Section snippets

Farms and animals

Prevalences

Discussion

Conflict of interest statement

Acknowledgements

References (19)

Toxoplasmosis in pigs – The last 20 years

Vet. Parasitol.

Toxoplasma gondii infection in wild boars (Sus scrofa) bred in Brazil

Vet. Parasitol.

Detection of trichinellosis in pigs by artificial digestion and enzyme immunoassay

J. Food Prot.

Diagnosis of swine trichinosis by enzyme-linked immunosorbent assay (ELISA) using an excretory-secretory antigen

Vet. Parasitol.

Toxoplasma gondii in wild cervids and sheep in Finland: North–south gradient in seroprevalence

Vet. Parasitol.

Control of trichinellosis by inspection and farm management practices

Vet. Parasitol.

Transmission dynamics of Toxoplasma gondii on a pig farm

Infect. Genet. Evol.

Sylvatic Trichinella spp. Infection in Finland

J. Parasitol.

Opinion of the Scientific Panel on Biological Hazards on “Risk assessment of a revised inspection of slaughter animals in areas with low prevalence of Trichinella”

EFSA J.

Cited by (34)

Seroprevalence of Toxoplasma gondii in wild boars (Sus scrofa) hunted in Ukraine

Epidemiology of Trichinella in the Arctic and subarctic: A review

All about Toxoplasma gondii infections in pigs: 2009–2020

Seroprevalence of Toxoplasma gondii in domestic pigs, sheep, cattle, wild boars, and moose in the Nordic-Baltic region: A systematic review and meta-analysis

A systematic review and meta-analysis on the global seroprevalence of Trichinella infection among wild boars

The global seroprevalence of Toxoplasma gondii among wild boars: A systematic review and meta-analysis

Short communicationFarmed wild boars exposed to Toxoplasma gondii and Trichinella spp.

Abstract

Introduction

Section snippets

Farms and animals

Prevalences

Discussion

Conflict of interest statement

Acknowledgements

Vet. Parasitol.

Vet. Parasitol.

J. Food Prot.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Infect. Genet. Evol.

Sylvatic Trichinella spp. Infection in Finland

J. Parasitol.

Opinion of the Scientific Panel on Biological Hazards on “Risk assessment of a revised inspection of slaughter animals in areas with low prevalence of Trichinella”

EFSA J.

Short communication
Farmed wild boars exposed to Toxoplasma gondii and Trichinella spp.