Seroprevalence of and Risk Factors for Toxoplasma gondii in the US Swine Herd Using Sera Collected During the National Animal Health Monitoring Survey (Swine 2006)

The United States Department of Agriculture (USDA) initiated the National Animal Health Monitoring System (NAHMS) in 1983 to collect, analyse and disseminate data on animal health, management and productivity in US domestic livestock populations, including swine. The programme includes an on‐farm serological sampling component which can be used to monitor seroprevalence of various pathogens, including Toxoplasma gondii. The purpose of this study was to determine the seroprevalence of T. gondii in grower/finisher pigs using sera collected during NAHMS Swine 2006 and to determine farm level factors associated with differences in seroprevalence on farms where sera was collected during the Swine 2006 survey. Sera and data on management practices for this study were collected from 185 grower/finisher swine production sites located in 16 states accounting for >90% of US swine production (Arkansas, Colorado, Iowa, Illinois, Indiana, Kansas, Michigan, Minnesota, Missouri, Nebraska, North Carolina, Ohio, Pennsylvania, South Dakota, Texas and Wisconsin). A total of 6238 sera were tested for T. gondii antibodies using a commercial ELISA assay (Vet. Parasitol. 128 , 2005, 177). Seroprevalence in this study, as determined by ELISA, was 2.6%, with a herd prevalence of 21.6% and a mean within‐herd prevalence of 2.7%. Analysis of swine management practices indicated that rodent control methods and carcass disposal methods were associated with differences in the number of T. gondii positive samples on farm. These results are consistent with current epidemiological knowledge of the transmission of Toxoplasma on the farm (ingestion of organic matter containing oocysts, or ingestion of infected animal tissues). Production practices which eliminate these sources of exposure can reduce the risk of Toxoplasma infection in pigs, and reduce the likelihood of human infection from consumption of infected pork.     

Comparison of Different Commercial Serological Tests for the Detection of Toxoplasma gondii Antibodies in Serum of Naturally Exposed Pigs

Toxoplasma gondii is the aetiological agent of the zoonotic disease toxoplasmosis and transmitted among other ways by chemically and physically untreated, that is, raw pork to humans. The detection of Toxoplasma gondii is impossible by currently practiced meat inspection, but serological tests can be used to detect Toxoplasma gondii antibodies in pig herds and can consequently be helpful to identify potentially contaminated pork. Therefore, appropriate serological tests are required. In this study, serum samples of 1368 naturally exposed slaughter pigs from 73 Austrian farms were collected. Serum samples of at least 16 slaughter pigs per farm were tested. The prevalence of Toxoplasma gondii antibodies in serum was measured by a commercial available modified agglutination test (MAT) and compared to three different commercial available enzyme‐linked immunosorbent assays (ELISA). The MAT detected 6.5%, ELISA I 6.7%, ELISA II 4.8% and ELISA III 4.3% of the pigs as Toxoplasma gondii antibody positive. The agreement, according to the kappa coefficient (κ), was substantial between the MAT and ELISA I (κ = 0.62), II (κ = 0.64) and III (κ = 0.67). A better agreement was determined between ELISA I and II (κ = 0.715), ELISA I and III (κ = 0.747) and ELISA II and III (κ = 0.865). At least one pig per farm was detected Toxoplasma gondii antibody positive in 17 (23.3%) farms by the MAT, 26 (35.6%) farms by ELISA I, 16 (21.9%) farms by ELISA II and 11 (15.1%) farms by ELISA III. Pig farms with a high number of Toxoplasma gondii antibody‐positive pigs or high antibody titres were identified by all of the four used serological tests. Concerning the occurrence of Toxoplasma gondii antibodies in Austrian pig farms, a monitoring and surveillance programme would be reasonable to find high‐risk farms.     

Infection with Toxoplasma gondii during Pregnancy: Seroepidemiological Studies in Austria

Seropositivity among pregnant woman in Austria has decreased from 48% to 50% at the end of the 1970s to 35% in recent years. Despite this decrease, knowledge of possible sources and risk factors for Toxoplasma infection remains important. We reviewed seroepidemiological studies that were undertaken to assess the roles of undercooked meat and oocysts in cat faeces as potential sources of infection in pregnant women. Improved management and hygiene in pig herds raised in confinement have resulted in less contact of pigs with cats and a decrease of infected pigs within one decade from 14% in 1982 to 0.9% in 1992. In Austrian wild boar populations, however, seroprevalences remained essentially unchanged during the same decade (18% in 1983 and 19% in 1990–1993). Austrian sheep and goats are usually kept on small farms where cats abound and are predominantly seropositive (66% in sheep and 69% in goats). The seroprevalence in cats has decreased from approximately 81% in 1987 to 59% in 1996; presumably because of cats’ increased consumption of processed food. Despite the decrease of infection in pregnant women via the cat‐to‐pig pathway, it may be offset by a recent concomitant increase in mutton consumption. Free‐ranging chickens are a good indicator of the prevalence of T. gondii oocysts in the soil because chickens are ground feeders. Antibodies to T. gondii, as evaluated by the modified agglutination test, were found in 36% of chickens from 12 Austrian ‘biofarms’. Because Austrians rarely consume raw pork, the fraction of human T. gondii infections associated with pig meat consumption is likely small. As meat consumption and lifestyle patterns change in Austria, the risk of human infection with T. gondii via different pathways needs re‐evaluation and targeted educational efforts to control transmission.     

Prevalence of anti-<Emphasis Type="Italic">Toxoplasma gondii</Emphasis> antibodies in sport horses from Qazvin,Iran

In the present study, the prevalence of antibodies to Toxoplasma gondii in sport horses of Qazvin was examined using modified agglutination test (MAT). On 52 horse sera totally examined for anti-Toxoplasma antibodies, 37 horses (71.2%) were seropositive by MAT. Results of the present study showed a high rate of Toxoplasma infection in horses in Qazvin area. More comprehensive study on equine toxoplasmosis is recommended.     

Seroprevalence and risk factors associated with Toxoplasma gondii infection in pig farms from Catalonia, north-eastern Spain

Seroprevalence and associated risk factors for Toxoplasma gondii infection in pigs were analyzed in 1202 sera samples, including sows and pigs of three, seven, 11, 15 and 20 weeks of age, from 23 farms in Catalonia, north-eastern Spain. Antibodies were tested by the modified agglutination test (MAT) at titers ?1:25. Antibodies to T. gondii were found in 228 samples (19.0%; 95% CI: 16.8-21.2). The individual prevalence in animals higher than 7 weeks of age was 22.8% (174/762; 95% CI: 16.6-29.0) and the within-farm prevalence ranged from 7.1% to 36.4%. Statistically significant differences were found among age classes. The risk factors significantly associated with T. gondii seroprevalence were the presence of cats, percentage of mortality at weaning and the presence of outdoor facilities in the farms. The seroprevalence observed in the present study indicates widespread exposure to T. gondii among domestic pigs in Catalonia, which may have important implications for public health.     

Prevalence of antibodies to toxoplasma gondii in cattle and swine in the Netherlands: Towards an integrated control of livestock production

Summary

Serological surveys of the prevalence of antibodies against Toxoplasma gondii were carried out amongst swine and cattle in the Netherlands. Data were analysed according to the different categories of animals. The results show very low seroprevalences of Toxoplasma gondii in finishing pigs (1.8%) and in fattening calves (1.2%). In sows and dairy cattle, respectively, seroprevalences of 30.9% and 27.9% respectively, were found, demonstrating clearly the environmental infection pressure and illustrating the importance of housing and management in establishing low infection rates.

Substantially different seroprevalences were found between dairy cattle sampled in the North and in the South of the Netherlands (13.1% and 42.6%, respectively).

The infection rates in the samples from finishing pigs, fattening calves, and dairy cattle demonstrate that seroprevalences in individual farms or herds may differ considerably. Investigation of the factors involved can be useful in determining the causes of infection and for developing measures with regard to prevention. The very low seroprevalences in finishing pigs and fattening calves indicate, however, that the production of toxoplasma‐free meat may be well within reach in modern husbandry.

Since farm animals easily are infected, serological screening of individual farms or herds for the absence of T. gondii infection, as a part of the Integrated Quality Control programme, can be helpful in determining the quality of livestock production and in developing certain standards of hygiene for individual farms.     

Meat Juice Serology and Improved Food Chain Information as Control Tools for Pork‐Related Public Health Hazards

The seroprevalence of Salmonella spp., pathogenic Yersinia spp., Toxoplasma gondii and Trichinella spp. was studied in 1353 finishing pigs from 259 farms that were allocated according to farm types: large fattening farms (≥1000 pig places), small fattening farms (< 1000 pig places) and farrow‐to‐finish farms. The antibodies were analysed with commercial ELISA kits in meat juice samples that were collected at Finnish slaughterhouses. Salmonella antibodies were rare (3% of pigs, 14% of farms) when the cut‐off optical density (OD) value 0.2 was used. Antibodies to pathogenic Yersinia spp. and T. gondii were detected in 57% of pigs and 85% of farms (OD ≥0.3) and in 3% of pigs and 9% of farms (OD ≥0.15), respectively. No antibodies to Trichinella spp. were detected (OD ≥0.3). The European Food Safety Authority (EFSA) considers Salmonella spp., Yersinia enterocolitica, T. gondii and Trichinella spp. as the most relevant biological hazards in the context of meat inspection of pigs. The seroprevalence of these important zoonotic pathogens was low in Finland, except that of Yersinia. The seroprevalence of Toxoplasma was significantly higher in pigs originating from small‐scale fattening farms (P < 0.05). Strong positive correlation was observed at the animal level between Salmonella and Yersinia seropositivity and between Salmonella and Toxoplasma seropositivity (P < 0.05). We suggest that these results reflect the level and importance of biosecurity measures applied on the farms. Meat juice serology at slaughter is a useful tool for targeting measures to control these pathogens. The information obtained from analyses should be used as part of the food chain information (FCI).     

Sero-epidemiological investigation of bovine toxoplasmosis in traditional and smallholder cattle production systems of Tanga Region,Tanzania

In view of the worldwide importance of Toxoplasma gondii and the fragmented information on the seroprevalence of the disease in animals in Tanzania, a study, using the modified Eiken latex agglutination test (LAT), was conducted from May 2003 to January 2004 to determine the prevalence of antibody to T. gondii in 130 randomly selected farms comprising 655 cattle. The overall seroprevalence of T.gondii antibodies in cattle and farms were 3.6% and 13%, respectively. Risk factors for animal and herd-level toxoplasmosis seropositivity were tested using multivariable logistic regression to control for confounding factors. Cattle managed under traditional husbandry practises were more likely to be seropositive than those managed under smallholder practises (48% versus 4.7%; p < 0.01). Herd size of ≥ 9 cattle were at greater risk of acquiring infection than herds holding fewer animals [≤ 9 cattle], (odd ratio [OR] = 3.99; 95% confidence interval [CI], 0.97–16.48; P = 0.001). We concluded that seroprevalence at herd level was high and relatively low at animal level, possibly due to the reduced susceptibility of cattle to T.gondii infection as compared to goats and sheep. The high seroprevalence in animals managed by traditional husbandry practise suggests that the parasite is widely distributed in the environment and could pose a public health threat to the people living in those areas.     

Molecular genotyping and serological evaluation of Toxoplasma gondii in mothers and their spontaneous aborted fetuses in Southwest of Iran

BackgroundGiven the lack of routine screening and the high prevalence of toxoplasmosis in pregnant women in Iran, the current study aimed to find out the rate and features of Toxoplasma gondii infection in the spontaneously aborted human fetuses in Kohgiluyeh and Boyer-Ahmad Province, Southwestern Iran.MethodsThis cross-sectional study was performed on 100 spontaneously aborted fetuses’ tissues and their mother blood samples. The mothers’ sera were evaluated for anti-Toxoplasma antibodies while their buffy coat and aborted fetuses tissues were evaluated for Toxoplasma DNA. PCR product at GRA6 locus was sequenced and phylogenetic analysis was done. Likewise, quantitative Real-Time PCR was performed to find out the parasite burdens in mothers buffy coat and fetuses tissues.ResultsUsing serological method, anti-Toxoplasma IgG and IgM antibodies were detected in 7 (7%) and 3 (3%) out of 100 sera from women with spontaneous abortion. Real-time PCR method detected T. gondii DNA in the buffy coat of one seronegative and 2 (out of 3) IgM seropositive cases. None of the samples from aborted fetuses were infected with T. gondii. BLAST and phylogenetic analysis showed that the sequenced isolates belonged to type I of T. gondii and two identified T. gondii isolates were taxonomically grouped into one clade.ConclusionOur findings revealed type I genotype of T. gondii in two mothers with spontaneous abortion, without fetus involvement. It is necessary to examine more aborted fetuses’ samples from different geographical areas to determine the association between Toxoplasma genotype and abortion.     

Seropositivity of Toxoplasma gondii in domestic donkeys (Equus asinus) and isolation of T. gondii from farm cats

Donkeys (Equus asinus) are used as both companion and working animals throughout the world and in some countries, their meat and milk are used for human consumption. Here we report the first serological survey of Toxoplasma gondii in donkeys in the United States. Serum samples from 373 donkeys from eight farms in five states were tested for T. gondii antibodies by the modified agglutination test (MAT). Twenty-four of 373 (6.4%) of donkeys were seropositive, with MAT titers ranging from 25 to ≥200. All seropositive donkeys were Miniature breed. Seropositivity prevalence was 7.0% in female donkeys (20/282) and 4.1% in male donkeys (4/91). No donkeys less than 24 months of age (129) were seropositive, suggesting postnatal transmission of infection. Domestic cats were present on six of the eight farms. Three cats from one farm had MAT titers of 200. Viable T. gondii was isolated from the hearts of two cats, but not from brain tissues. Genotyping of isolate DNA extracted from culture-derived tachyzoites using 10 PCR-restriction fragment length polymorphism (RFLP) markers (SAG1, SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, PK1, L358 and Apico loci) revealed that both isolates were clonal Type II (ToxoDB PCR-RFLP genotype #1). This is the first serological survey for T. gondii in donkeys in the United States, and suggests that donkey milk and meat should be considered as a potential source for human infection. The role of barn cats in the transmission of T. gondii to donkeys on farms warrents further investigation.     

Toxoplasma gondii in Ireland: Seroprevalence and Novel Molecular Detection Method in Sheep,Pigs, Deer and Chickens

Toxoplasma gondii is among the most studied parasites worldwide but there is not much information about it published in Ireland. The objectives of this study were to determine the seroprevalence of T. gondii in sheep, pigs, deer and chickens and the molecular detection of T. gondii DNA in muscle tissue. Serum samples were collected from these species at the time of slaughter at Irish abattoirs during 2007 and tested for anti‐T. gondii antibodies using a commercial semi‐quantitative latex agglutination test. Antibodies (titre ≥1 : 64) were found in 36% (105/292) sheep, 4.7% (15/317) pigs and 6.6% (23/348) deer. In chickens, 18% (65/364) had antibody titres, ranging between 1 : 5 and 1 : 1024. Significant (P ≤ 0.05) age‐related differences in seroprevalence were found in adult sheep (58.1%) and pigs (23.1%). Significant gender differences in seroprevalence was also found in sheep with more females (43%) than males (22.4%) being positive. However, when adjusted for age through logistic regression gender was no longer significant. Seroprevalence was also evaluated on farm locations grouped to NUTS level 3, but the prevalence was too low to draw any statistical conclusions. Using a nested PCR, the presence of T. gondii DNA was detected in diaphragm samples from 3.6% (3/83) sheep, 13.0% (3/23) pig and 4.2% (3/71) deer. Meat digestion liquids from a Trichinella spp. survey in pigs were also used for the first time to detect T. gondii. Toxoplasma gondii DNA was detected in 50% (10/20) of pooled samples. This is the first in depth study of T. gondii seroprevalence in animals in Ireland and a novel method, using digestion liquid from pooled diaphragm samples, for PCR detection in pigs is described.     

Serological Survey of Toxoplasma gondii Infection in the Domestic Goose (Anser domestica) in Southern China

In the present study, the antibodies to Toxoplasma gondii in 191 farm‐bred and 83 house‐bred geese (Anser domestica) were assessed for the prevalence of T. gondii infection in southern China with the modified agglutination test. Antibodies to T. gondii (MAT ≥ 1 : 5) were found in 27 (14.14%) of farm‐bred geese and 14 (16.87%) of house‐bred geese. Geese infected with T. gondii may be a source of T. gondii infection for humans and cats.     

Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in sheep from Mossoró, Rio Grande do Norte, Brazil

Toxoplasma gondii is an obligate intracellular parasite with a variety of hosts, responsible for reproductive problems and economic losses in sheep flocks. Neospora caninum was recently identified and its clinical presentation in sheep is similar to that of toxoplasmosis, which can cause repeated abortions, though less frequently in this species. In order to confirm the prevalence of these agents in the city of Mossoró, Rio Grande do Norte, Brazil, 409 serum samples from adult sheep (364 females and 45 males) were tested by the indirect immunofluorescence antibody test, using cut-off point at a dilution of 1:64 and 1:50 for T. gondii and N. caninum, respectively. From the 35 properties examined, 23 (65.7%) had at least one seropositive animal for T. gondii and six (17.1%) for N. caninum. The prevalence of seropositive animals for T. gondii was 20.7% and for N. caninum 1.8%. There was no association between the presence of the agent’s antibody and gender, reports of reproductive problems and presence of dogs and/or cats in the properties. T. gondii is well distributed and N. caninum has low prevalence in sheep and in the properties of the studied region.     

Antibody Prevalence and Risk Factors for Toxoplasma gondii Infection in Women from Multan,Pakistan

Toxoplasma gondii infections are prevalent in humans and warm‐blooded animals. Maternal infections during pregnancy may have devastating consequences for transplacentally infected neonates. This study was conducted to examine the seroprevalence of antibodies to T. gondii in pregnant women of childbearing age and determine risk factors associated with pregnancy history, pet ownership, social and cultural factors at Nishtar Hospital, Multan. Samples were collected from 403 women and examined using a commercially available enzyme‐linked immunosorbent assay (ELISA). The overall prevalence of antibodies to T. gondii was 17.6% (71) in the 403 samples collected from women. Antibodies to T. gondii were present in 19.4% (45) of 232 pregnant women and 15.2% (26) of the samples from 171 non‐pregnant women. This study identified miscarriage history, pet ownership, type of residence, marital status, source of drinking water and eating habits as significant (P < 0.05) risk factors associated with the presence of antibodies to T. gondii infection. Seroprevalence was not significantly different (P > 0.05) in women from different ethnic groups based upon lifestyle and culture.     

Investigations with enzyme-linked immunosorbent assays for Trichinella spiralis and Toxoplasma gondii in the Dutch 'Integrated Quality Control for finishing pigs' research project.

In the framework of the Dutch field trial 'Integrated Quality Control (IQC) for finishing pigs' ELISA (screening) techniques were used to detect animals seropositive for Toxoplasma gondii and/or Trichinella spiralis. The aim was to determine whether farms which consistently delivered seropositive pigs could be detected and monitored (defined as 'problem farms'). The investigation involved 120 farms and three slaughterhouses, and a total of 23,348 serum samples were examined. In addition, all pigs were also screened for the presence of Trichinella spiralis with the digestion method (pooled samples). The prevalence of seropositivity for Trichinella spiralis and Toxoplasma gondii was 0.3% and 2.1% respectively. Parasitological examinations concerning T. spiralis were negative. Considering the characteristics of the used methodology, the conclusion was drawn that there were no parasitological or serological indications for T. spiralis infections, and that with respect to T. gondii the infection rate seemed to be equally low for all farms involved. In addition, a longitudinal pilot study during a whole finishing period was undertaken at two finishing farms. Animals seropositive for Toxoplasma gondii were found from the earliest days of the finishing period. Housing and management may (still) play an important role in the prevention of contact with this parasite.     

The role of rodents and other wildlife in the epidemiology of swine toxoplasmosis

Two swine production units and their contiguous wildlife populations were used for this study. These herds were located 7 miles apart in the major swine producing area of south central Georgia. Herd A had a Toxoplasma gondii antibody prevalence of 27.6% in all ages of swine sampled, with an increased incidence of 13.6% over a 5-month period. This herd was maintained under a semi-range condition. The swine in Herd B were maintained exclusively in concrete floored, enclosed buildings. This herd had a 0.85% T. gondii prevalence. Rodents and a few other wildlife and domestic species were trapped in or around both herds. These animals were examined for Toxoplasma antibodies using the same test procedure utilized for swine sera, the indirect immunofluorescent (IIF) test. Additionally, rodent tissues were homogenized and suspensions prepared for interperitoneal (I/P) inoculation into CF₁ laboratory mice.Rodents and wildlife species examined were: Mus musculus, Peromyscus leucopus, Rattus norvegicus, Sigmodon hispidus, Procyon lotor, and Didelphis marsupalis. Feral and domestic animals other than swine that also were tested for the presence of T. gondii antibodies included two cats, two horses, and a dog. The overall prevalence of T. gondii antibodies in all non-porcine species examined was 67% for those animals in and around the premises of Herd A, and 63% for those in and around Herd B.Toxoplasma infectivity of rodents whose tissues were processed and inoculated into laboratory mice correlated well with the results of the IIF test on the serum of these wild rodents. No tachyzoites of T. gondii were found in the peritoneal exudate of laboratory mice post I/P inoculation with wild rodent tissue, with one exception.While there was no significant difference in Toxoplasma infectivity in non-porcine species on these two premises, management practices appeared to be the determining factor in swine infection with T. gondii. Excluding wildlife precluded infection.     

What Do We Know About Risk Factors for Infection in Humans with Toxoplasma gondii and How Can We Prevent Infections?

Fourteen case–control studies evaluating the importance of different risk factors for infection of humans with Toxoplasma gondii were identified. Surprisingly, up to two‐thirds of infections could not be explained by risk factors such as consuming raw or undercooked meat or poor kitchen hygiene. Few studies reported population attributable risk, and when reported, it was low. Protocols including questionnaires used for collecting data, age and socio‐economic groups studied, and sample sizes varied among studies. There is a need for carefully planned, case–control studies to identify sources of infection with T. gondii in humans. New risk factors, such as the manufacture of organic meat, and possible ways to sterilize meat to inactivate T. gondii tissue cysts are discussed.     

Toxoplasma gondii seroprevalence in veterinarians in Finland: Older age,living in the countryside,tasting beef during cooking and not doing small animal practice associated with seropositivity

Practising veterinary medicine has an inherent risk of exposure to zoonotic agents, including the protozoan parasite Toxoplasma gondii. We screened sera of veterinarians authorized to work in Finland for the presence of specific immunoglobulin G antibodies against T. gondii with an enzyme‐linked fluorescent assay, and evaluated potential risk factors for T. gondii seropositivity from extensive questionnaire data with almost 1,300 quantitative variables. We used a causal diagram approach to address the complexity of the life cycle of the parasite and its numerous possible transmission routes, and built a multivariable binomial logistic regression model to identify risk factors that are particularly relevant for veterinarians. The samples and questionnaire data were collected in 2009. Altogether, 294 veterinarians, almost 15% of the Finnish veterinary profession, were included in the study. The median age was 39 years, and the majority, 86%, were women. Altogether, 43 (14.6%; 95% confidence interval: 10.9–19.0) of the 294 veterinarians tested seropositive for T. gondii. According to the final model, veterinarians who were at least 40 years old had 2.4 times higher odds to be seropositive than younger veterinarians; veterinarians who lived in the countryside had 4.0 times higher odds to be seropositive than veterinarians who lived in towns; female veterinarians who tasted beef during cooking had 2.6 times higher odds to be seropositive than male veterinarians who did not taste beef during cooking; and veterinarians who did not do small animal practice had 2.3 times higher odds to be seropositive than those who did. The results illustrate the numerous transmission routes of T. gondii.