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International Journal for Parasitology 38 (2008) 1359–1370 www.elsevier.com/locate/ijpara

Invited Review

Control of the risk of human toxoplasmosis transmitted by meat
Aize Kijlstra a,b,*, Erik Jongert c
Animal Sciences Group, Wageningen UR, P.O. Box 65, 8200 AB Lelystad, The Netherlands b Department Ophthalmology, Maastricht University, Maastricht, The Netherlands c Laboratory for Toxoplasmosis, Pasteur Institute of Brussels, Scientific Institute of Public Health, Belgium, Engelandstraat 642, 1180 Brussels, Belgium Received 14 May 2008; received in revised form 25 June 2008; accepted 29 June 2008

Abstract One-third of the human world population is infected with the protozoan parasite Toxoplasma gondii. Recent calculations of the disease burden of toxoplasmosis rank this foodborne disease at the same level as salmonellosis or campylobacteriosis. The high disease burden in combination with disappointing results of the currently available treatment options have led to a plea for more effective prevention. In this review we describe Toxoplasma as a hazard associated with the consumption of undercooked meat or meat products and provide an analysis of the various options to control the risk of human toxoplasmosis via this source. Monitoring and surveillance programs may be implemented for pre-harvest control of Toxoplasma infection of farm animals, with the reduction of environmental oocyst load as the most important milestone. Alternatively, Toxoplasma safe meat can be obtained through simple post-harvest decontamination procedures, whereby freezing the meat may currently be the best option, although new technologies using irradiation or highpressure treatment may offer promising alternatives. Influence of culture, religion and food handling customs may predispose a certain type of meat as an important source of infection, indicating that prevention needs to be tailored according to social habits in different regions in the world. The rationale for more stringent control measures to prevent toxoplasmosis both from disease and economic points of view is emphasized. Ó 2008 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
Keywords: Toxoplasma gondii; Meat; Parasite inactivation; Food safety

1. Introduction Toxoplasmosis is a disease caused by the protozoan parasite Toxoplasma gondii (Montoya and Liesenfeld, 2004) and infection with the parasite is ubiquitous throughout the world. Less than 20% of individuals develop overt disease including fever, lymph node enlargement or intraocular inflammation (Holland, 2003; AFSSA, 2005). Details concerning both asymptomatic and symptomatic infection and the risks of transmission from animals to humans in the USA were recently reviewed by Dubey and Jones (2008). In the review presented here we have focussed on meat as a source of infection, highlighting regional differ* Corresponding author. Address: Animal Sciences Group, Wageningen UR, P.O. Box 65, 8200 AB Lelystad, The Netherlands. Tel.: +31 320 238095; fax: +31 320238050. E-mail address: aize.kijlstra@wur.nl (A. Kijlstra).

ences throughout the world, and have extensively dealt with pre- and post-harvest mechanisms of control. Furthermore, the rationale for more stringent control measures to prevent toxoplasmosis both from disease and economic points of view is emphasized. More emphasis on prevention is needed because currently available antibiotic therapy seems to have little effect on mother-to-child transmission, and whether treatment affects the clinical manifestations in the newborn with congenital toxoplasmosis (CT) is still under debate (Thibaut et al., 2007). The effectiveness of antiparasitic treatment for chronic ocular toxoplasmosis has also not yet been formally demonstrated (Rothova et al., 1993; Stanford et al., 2003). Treatment failure may be related to late timing of treatment and the fact that currently available drugs cannot reach the parasite stage within tissue cysts (Dubey, 1996; Gormley et al., 1998). In humans, primary infection with the parasite before pregnancy provides complete

0020-7519/$34.00 Ó 2008 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ijpara.2008.06.002

2003. French Guiana and New Zealand (Choi et al. The observed decline in Toxoplasma seroprevalence as noted in many developed countries over past decades has been attributed to the introduction of modern farming systems resulting in a lower prevalence of Toxoplasma cysts in meat in combination with an increased use of frozen meat by consumers (Tenter et al. gondii transfer to humans Experimental infections of food animals such as cattle. special education and residential care costs (Roberts et al. to date no experimental data or studies are available to support this route of infection. 2006. Dubey.9% of cats have been found to actively shed Toxoplasma-like oocysts. 1990). gondii oocyst contamination of the environment is mostly restricted to cat defecation sites (Afonso et al.9) 63 80 252 128 80 858 Multivariate analysis data are represented from three large case-control studies and depicted as odds ratio plus confidence intervals (in brackets). 1999.. associated complications. Roghmann et al... plasmosis (Cook et al. However. are at risk (Glasner et al. rabbit. annual productivity losses. 1998. (1996) Baril et al.1–10. 2002. Diza et al. gondii is often missed as a diagnosis and it may therefore remain an under-reported disease entity (Bottieau et al.. horse. (2000) protection against congenital toxoplasmosis (Montoya and Liesenfeld. One study has shown that berries experimentally spiked with oocysts can pass T. Despite the fact that disease burden of toxoplasmosis is comparable to that of other foodborne diseases such as salmonellosis or campylobacteriosis. 2007.4–7.. gondii oocysts are difficult to distinguish from Hammondia hammondi oocysts by microscopical analysis (Schares et al. 1994). Havelaar et al. Despite the low incidence. the annual economic impact has been estimated at US$ 12 million (Roberts and Frenkel. 1999.2) No increased risk 4.1360 A. Ocular toxoplasmosis was traditionally considered to be a manifestation of congenital disease. Inhalation of dust containing oocysts has also been implicated as a means of transmission (Teutsch et al.. 2006).1–7. gondii outbreaks to oocyst contamination of drinking water in the United States. shows that most cases are due to acquired disease which means that not only pregnant women. In the UK.. which makes it the second most important foodborne infection for humans after salmonellosis (Buzby and Roberts. 50% of children presenting with chorioretinitis are due to Toxoplasma infection after birth (Stanford et al. probably leading to one or more days of work missed in mild cases (AFSSA. 3. In the UK. Dabritz et al. gondii in humans. Carme et al. 2005. and thus might also be transferred via raw vegetables and fruit. Infectious mononucleosis such as illness due to T. toxoplasmosis has received little attention from policy makers in past years (Mead et al. 1992.. 2004).5 (1.2) 3. Transmission of oocysts occurs by water and soil. A few studies have been able to link T. the fact that strict vegetarians become infected with T. 2000) (Table 1).1 (0. However. a recent study has shown that T. (1999) Cook et al.85–14) 3. Small outbreaks of toxoplasmosis have been associated with the consumption of raw meat in Korea.. Baril et al. The largest study estimated that consumption of not-well-cooked meat was the cause of infection in 30–60% of pregnant women with acute toxo- 4. despite the fact that up to 20% of infected individuals may develop clinical complications.12 (1. 1979). have shown that these animals are susceptible to T.. The costs associated with acquired toxoplasmosis have never been addressed.1 (2. E. Less than 0. but the general population. 1999)... gondii contamination by intake of oocysts . Svobodova et al. gondii shows that oocyst contamination still plays an important role in infection (Hall et al. Canada and Brazil (Bowie et al. BahiaOliveira et al. 1997. 2.. Lake et al. however. 2002). Vaillant et al. 1999. Food animal species involved in T. 2000).1 (1. 1996.1–63.. Indications that meat is a main cause of T..7 billion per year.1–27) 1. 1986.6–10.. Kemmeren et al. Although it is generally assumed that raw vegetables are a source of contamination with T. 2007).. Recent insight. 2005. Costs of CT were estimated up to US$ 1.. 2003). Kijlstra. 2007). Schares et al. The total economic impact of CT in the USA has been estimated to be as high as US$ 7. Ross et al. three large case-control studies have pinpointed uncooked meat as the most important risk factor for pregnant women (Kapperud et al. 2005.73 (1. USA France. pigs. 1996). game birds.. Kortbeek et al. Holland has estimated that approximately 2% of infected individuals will have ocular involvement (Holland.1) 3. Sources of human infection with T.. and this may be an over-estimation since T. treatment and social costs. (Childs and Seegar. 2008). gondii are oocysts shed in faeces of infected felines and tissue cysts from infected meat animals.. 2004. AFSSA. 2006). Cook et al..26 million per case.. Jones et al.. 2000).4 (1.. a Venison.. 2004).4) No increased risk No increased risk 5. Gilbert and Stanford. 2000. the economic impact of CT is high due to severity of infection. 1997. whale. gondii infection to mice (Kniel et al. 2001.. 2002). 2008).. gondii infection in humans The source by which an individual has become infected with T. In Europe. and were mainly attributed to medical costs. Jongert / International Journal for Parasitology 38 (2008) 1359–1370 Table 1 The risk of Toxoplasma gondii infection in association with the consumption of undercooked or raw meat from various species Type of meat Mutton/Lamb Pork Beef Poultry Othera Number of cases Number of controls Kapperud et al. gondii cannot be discriminated by diagnostic tests. sheep and goats. 2005)... 2008)..

1983. gondii infection in humans. Kijlstra.. In the Western world. 2000). Skinner et al. Presence of cysts .. Although studies have reported the isolation of T. 3. 1999)... 2005). Sharma et al. Chicken meat is mostly well cooked for consumption. Raw or undercooked lamb meat is considered a delicacy in certain countries such as France and is therefore considered an important source of infection in that country (AFSSA..4. van der Giessen et al. 1998.. 2000). 1995. 3. Beef Although epidemiological studies have shown that the consumption of raw or undercooked beef is considered a risk for T. 2000. gondii have been shown to harbour infectious parasites in their meat. gondii may cause a re-emergence of pork meat as an infectious meat source (Kijlstra et al. Dubey and Jones. E. Toxo & Food 2006. 2005). 1998).. 2004a. 2006). Lehmann et al.a serological survey in horses slaughtered for human consumption in Italy. gondii from caprine tissues. gondii infections (Kapperud et al.. Toxoplasma gondii infection in horses. gondii induced pathology in livestock animals and their role in the transmission of T. especially in developing countries. gondii infection in humans (Baril et al. Sroka. 2000). Tassi. 1986a. 3.. conclusive evidence is lacking to correlate this with the actual presence of infectious parasites in edible tissues from naturally infected beef (Dubey. Dubey and Thulliez. commercially produced free ranging chickens intended for meat consumption (broilers) have a limited life span and to date no recent data are available concerning T. Seroprevalence of T. In. 1984.. 2007). Davies et al. gondii to humans in the USA was recently reviewed by Dubey and Jones (2008). 2007). housing and climatic conditions (Tenter et al. most farm animals that are seropositive for T. 1988.6.. 2008). 2006. Poultry Seroprevalence of up to 65% in free ranging chickens has been reported and the presence of the parasite in meat could be shown in 81% of seropositive animals (da Silva et al. 2004a. 1980..4% of sheep were shedding T... Horses Horses can become infected with T. Goats Seroprevalence for T. Blewett et al. Due to major changes in animal production hygiene. In response to natural infection. 1967). gondii infection in pigs (Vanknapen et al. Jongert / International Journal for Parasitology 38 (2008) 1359–1370 1361 or tissue cysts. 1981.. EstebanRedondo et al.. with the exception of beef (Dubey et al. Zia-Ali et al. 1986b).2. however it can be expected that poultry kept outside has a higher chance of being infected with the parasite (Dubey et al.. modern production systems have virtually eliminated T. pp. and that seroprevalence can be high in bovine (up to 92% has been reported) (Vanknapen et al.. 1988. Currently. 1980.. may be considered as an important source of T. McColgan et al.. 1982. 2006). 1993. Pork meat is therefore not the main source of infection any more in many parts of the world. A comprehensive review on T. gondii seroprevalence in these chickens. and that following experimental infection T. Sheep All case-control studies have identified the consumption of mutton/lamb meat as a highly significant risk factor for contracting T. More et al... Adult sheep meat is often well cooked and therefore probably poses a smaller risk of infection to the consumer than lamb meat. Outbreaks have been reported following consumption of raw beef. Small ruminants such as goats are an important source of meat and milk in many undeveloped countries and may play a role as a source of infection for humans residing in these areas (Shrestha and Fahmy.3. gondii in goats can be as high as 77% and is dependent on the presence of oocysts in the environment. Italy. 96–97. Palermo. However. 3. P. no large-scale prevalence data are available on the presence of parasites in goat meat products (Dubey. 2000.. Sacks et al.A. 1975.. Schulzig and Fehlhaber. gondii and in certain regions of the world. 2007).. Dubey.. Meerburg et al. 2007). gondii in sheep can be as high as 92% in certain European countries (Tenter et al. 1997). Undercooked meat has thus been considered a main source of infection. Lunden and Uggla. increasingly popular animal friendly production systems with increased risk of exposure to T. Drinking unpasteurized (cow) milk was not associated with T. Recently a large-scale screening of sheep farms has shown that 3.. Cook et al. 2008).. 1999. 1990..1. 3. with the exception of beef (Tenter et al. Kijlstra et al. 1982. Consumption of raw goat’s milk and milk products has been linked to cases of toxoplasmosis in humans and pigs (Riemann et al. although doubt was raised whether the meat was unadulterated (Dubey and Jones. Pigs Outbreaks of acute toxoplasmosis have been described following the consumption of uncooked pork (Choi et al. 1996). gondii in their milk (Fusco et al. gondii infection in pregnant women. gondii can be isolated from their tissues. 2006. 2001. Tenter et al.. Depending on the environmental load with oocysts. 1995. van der Giessen et al. gondii infection of pork meat has dropped dramatically (Tenter et al.. 2003. the rate of T. 2007). 2008).. sheep can readily acquire toxoplasmosis (Skjerve et al. Free ranging chickens. up to 90% of the animals were shown to be seropositive (Tassi. 2003).. 1992. 2000. 2004). 3. In a study by Hellman and Tauscher the presence of viable parasites in 170 commercially obtained beef cuts was evaluated but none tested positive (Hellmann and Tauscher.5.

Viable parasites were also detected in one out of 67 cured meat samples investigated in the United Kingdom (Warnekulasuriya et al. Ross et al. Epidemiological studies and several outbreaks have identified the handling and consumption of raw or undercooked game as a source of toxoplasmosis (McDonald et al. gondii infection in pigs (Meerburg et al.1. but also via uptake of rodents carrying T. gondii infection on the farm it is necessary to identify the sources of infection in relation to the behaviour of various farm animals. 3. feed or surface water infected with oocysts shed by infected cats (Skjerve et al. Raw or undercooked horse meat is frequently consumed in countries such as Belgium. gondii prevention of herbivorous farm animals (Frenkel et al. 2005. 1995). Tenter et al. gondii DNA has recently been shown to be present in sheep milk (Fusco et al. Toxoplasma gondii ‘‘on farm risk’’ management 5. Kijlstra et al. 1995. An oral vaccine composed of live bradyzoites from an oocyst-negative mutant strain (T-263) has been effective in preventing oocyst shedding by cats (Frenkel et al. 1990. 1991. 2006). Carme et al. forage. respectively (Vikoren et al. gondii. Gamarra et al. Cook et al. Gent). 1). 1998. gondii antibodies in macropod marsupials. Antolova et al. Dubey and Jones.. 1998).. Older animals (sows) are mainly used for cured meat products and it is known that T. 4. 2007). It was recently shown that 22% of Western Grey Kangaroos are T..1362 A. E.. WAAVP.. 1990). 2007). As yet little data is available concerning the analysis of risk factors for herbivorous animals to become infected with T. 2007. Due to high demand in certain countries there is an intense trade of both farmed and natural game. Control of the presence of cats on the farm or the shedding of oocysts from these cats may play an important role in T. gondii cysts (Fig.. gondii infection via pasture. under experimental conditions (Davis and Dubey. Tassi. gondii infection depends on regional preferences for horse meat.2. gondii organisms in commercially made fresh pork sausages was recently shown in a study from Brazil (Dias et al.. gondii infection of omnivorous farm animals such as pigs has not yet been elucidated. Game An emerging risk is the increasing popularity of game meat such as roe deer. Bartova et al. gondii (Lutz.. a whole batch may become infected (Aspinall et al. 2008). In particular.. 1998). The role of horses as a source of T. 1995. 2006). 2006).. The relative role of oocysts versus tissue cysts in T.. Afonso et al. 1998. 2000. Cat control Cats with outdoor access may become infected via oocysts in the environment or by predating wildlife (Hejlicek and Literak. 2007). Woods et al. gondii infection increases with age (Tenter et al. 2003.. N.. 2005). 1991). 2000). In. 5.. 2002). Feeding of raw milk products to other animals (and humans) might also play a role in the horizontal transmission of T. 2000). Gauss et al.7. the preparation method and the seroprevalence of horses used for consumption (Gill. Tenter et al. 2002) (Fig.. Kijlstra. It has been estimated that one pig may be consumed by 200–400 individuals (Fehlhaber et al. 2000). 2001. In the event of including a few infected animals. Reshedding of oocysts has been observed after superinfection with other coccidia or after immunosuppression under experimental conditions (Dubey. 1995). ... Mixture of beef with other types of meat is general practice in minced meat preparations and could be an explanation for the observed epidemiological findings that link consumption of raw beef to T. and a study from the European Food Safety Authority has recently estimated that approximately half of the game produced in Europe may be seropositive for T.... this may be a risk factor for poultry or pigs (Weigel et al. Mateus-Pinilla et al.. No evidence is available whether naturally infected cats will reshed T. Sources of infection To prevent T. Mixed meat products Meat products are often made by mixing the meat and organs of many animals. Primary infection in cats protected these animals from oocyst reshedding up to 6 years post primary infection. gondii (EFSA. Development of an ELISA for the detection of T. wild boar or kangaroo. showed a moderate decrease in seroprevalence of farm rodents and pigs (Mateus-Pinilla et al. 2005).. Italy. Jongert / International Journal for Parasitology 38 (2008) 1359–1370 has been shown in edible tissues from horses (Alkhalidi and Dubey. Gaffuri et al. hay.. gondii infection and that the meat of infected animals contains viable tissue cysts (Canfield et al. 2004. 1995.. The actual presence of viable T. gondii.. and T. Omnivorous animals can become infected with T. 2005. 2007).. 2006. 2002). Herbivorous animals most likely contract T.. gondii similar to herbivorous animals. gondii infection in humans. 1997. A study investigating the effect of T-263 vaccination of cats on a farm. Earlier studies have indicated that kangaroos are highly susceptible to T. 5.. 2008). partly via frozen import or fresh meat imports (Reinken.. Feeding of non-pasteurized goat whey has been identified as a risk factor for T.. 2006. gondii oocysts later in life.. gondii seropositive (Parameswaran. France and Japan (Gill. Many by-products such as sausages or ham include pork meat. Kangaroo meat was implicated as the cause of an outbreak of toxoplasmosis in Australia in 1994 (Robson et al.2% of European roe deer (Capreolus capreolus) were seropositive for T.. 2008). The duration of the protective immunity has not been established and as yet this vaccine is not commercially available. 2002. 1979). Serological studies showed that between 13% and 39. Between 8% and 38% of the wild boars tested in Europe were seropositive for T. 1). gondii infection (Fusco et al. Dubey.

2004). gondii oocyst shedding. but did not result in significant protection (Buxton et al. the presence of cats on the farm should be avoided. (2) Heating of milk products. (10) Consumer education on food hygiene and decontamination procedures. 2007). Recently. Farm animal vaccination Toxoplasma gondii vaccination of farm animals is traditionally used to prevent abortions in sheep and goats. 2002). gondii rhoptry extract failed to protect animals against experimental acute toxoplasmosis.. 1. In view of the long-term oocyst survival and vertical transfer of infection in intermediate hosts (Marshall et al. gondii-free meat in 52% of vaccinated pigs after oral challenge with T. 2008). gondii vaccination programs that have a long-term food safety objective. (4) Indoor production system.and post-harvest risk management for the control of infectious sources of animal and human toxoplasmosis. 1989). Vaccination studies in sheep with a live non-persistent T.. 2007). gondii seroprevalence in pigs may take several years (Mateus-Pinilla et al. Percentages indicate highest observed seroprevalence per species. gondii oocysts (Kringel et al. Intervet) consisting of a live mutant strain (S48) that does not persist in sheep tissues is used in countries where parasite associated abortions are frequently encountered (Innes and Vermeulen. 2004). (7) Animal feed & bedding decontamination by heating.. 1991). (1) Freezing and/or heating.. Challenge of pigs vaccinated with a T. Although a farmer can vaccinate his own cats against T. this will not prevent contamination of the farm area by non-vaccinated stray or neighbour cats. however 37% of surviving animals were free of tissue cysts (Garcia et al. gondii vaccination of cats may therefore depend on government regulations.3... 2006). Recently. (5) Cat control.. vaccination with Toxovax does not eliminate vertical transmission of the parasite when infection occurs during pregnancy. Pre. increased immune responses were observed after experimental challenge. 5. It remains questionable whether cat owners can be persuaded to participate in general T. 1999). E. In order to reduce the presence of T. (8) Vaccination against tissue cyst formation (a) or oocyst shedding (b). (6) Rodent control. Vaccination of pigs with the live RH strain could reduce parasite load in the tissues of these animals (Kotula et al. Jongert / International Journal for Parasitology 38 (2008) 1359–1370 1363 Fig. Kijlstra. resulting in T. the effect of vaccination of cats on T. A commercially available tachyzoite vaccine (OvilisÒ Toxovax. . Percentages indicate the highest observed seroprevalence per animal species or the percentage of cats actively shedding oocysts. Thickness of arrows represents the likeliness of transmission without risk management procedure. resulting in Toxoplasma-free meat in two of three vaccinated animals (Jongert et al.. it was shown that intranasal vaccination of cats with crude rhoptry proteins in immune stimulating complexes (ISCOMs) prevented oocyst shedding in two out of three challenged cats (Garcia et al. However. but do not contribute towards the health status of individual cats. gondii strain (RH) encapsulated in ISCOMs or poly-lactide-co-glycolide (PLG) microspheres could induce increased immune responses after challenge. a cocktail DNA vaccine has been shown to prime the immune system of pigs against toxoplasmosis.A. gondii oocysts on a farm. A successful approach in T. (9) Serological monitoring of people at risk. (3) Animal friendly production system.

2008). . 1960) (Dubey et al. whereby the responsibility of food safety is laid in the hands of the consumer. 1). 2004b).1. Jongert / International Journal for Parasitology 38 (2008) 1359–1370 From a food safety perspective.. Havelaar et al... T. rodent control campaigns were shown to have an important impact on the production of Toxoplasma-free pigs on organic farms (Kijlstra et al. 2006). 2007). One of the problems with T. Killing the parasite Studies have indicated that T.. irradiation.2.43% to 0.. gondii by ingestion of undercooked meat was first proposed in the late 1950’s (Weinman and Chandler.85%) and storage at 4 °C (Jacobs et al.. and techniques to destroy the cyst form of the parasite were investigated (Table 2).09% (Breugelmans et al. gondii status of the original animals is not known. In view of the fact that recent studies have shown that the disease burden of acquired toxoplasmosis is also high. Few studies have evaluated effects on meat from naturally infected animals. Meat Handling. Prevention programmes have been shown to be very efficient in reducing the incidence of CT. each country should make their own risk assessment and based on the findings implement management options for efficient prevention of T. Heat treatment is the most secure method to inactivate the parasite. An outbreak of toxoplasmosis in Northern Canada’s Inuit population was ascribed to the skinning of fur and consumption of raw caribou meat from hunted game. 6.4. 1990). Nibbling of minced meat during food preparation has been shown to be a risk factor for contracting toxoplasmosis (Kapperud et al.. 1). In the case of free range farming it is necessary to take adequate measures to control rodents in the vicinity of the stables (Meerburg et al.. gondii infection via meat. On the other hand it could be used to detect T. and the way meats and meat products are prepared throughout the world. 2004). which shows that handling of infected animals may be a risk for infection (McDonald et al. Monitoring Monitoring animals at slaughter would enable the identification of farms at risk and could be used to implement changes in farm management to improve the food safety of the meat produced. no standardized reference sera or other reference materials are available and there is no laboratory certification program. Despite the fact that the disease burden of toxoplasmosis is probably as high as salmonellosis and campylobacteriosis (Kemmeren et al.1. bedding material and forage (Kijlstra et al. Raising the salt concentration or the temperature led to inactivation of the parasite (Table 2). The same study also showed that women who washed kitchen knifes infrequently after cutting meat also had an increased risk of infection. freezing. Recently. consumption and consumer attitude Knowledge of consumers about toxoplasmosis is limited and often restricted to women who have been informed about the problem during pregnancy. Early studies The hypothesis of horizontal transmission of T. To prevent oocyst contamination of food or stables it is important to keep cats out of these areas. Farm management In the case of environmental contamination with oocysts the most extreme management measure would be to keep farm animals intended for meat production inside. In this respect a freezing procedure would be the most practical risk management option. 1996). Post-harvest prevention 6. 1960).. gondii monitoring in food animals is the fact that there is no general agreement among the tests to be used. high-pressure. suggesting cross-contamination as a mechanism of transmission. gondii examined the effects of storage conditions on parasite survival and showed that parasite tissue cysts could be lysed in distilled water (Jacobs et al.. 1956). 6. and feeding of farm animals with raw milk or milk products (whey) from goats or sheep should be discouraged (Meerburg et al. gondii-infected meat and destroy the tissue cysts in the meat by specific procedures (Fig.. gondii in food animals is not monitored at slaughter whereas Salmonella and Campylobacter monitoring programs have started in many countries.1364 A. whereby the T. 2006. 7. vaccination could be employed to reduce or prevent the formation of tissue cysts in meat (Fig. Post-harvest but pre-kitchen procedures involving a combination of treatments may be implemented to assure non-infectivity of meat. A survey of 22 years of prevention showed that seroconversion rates during pregnancy could be reduced from 1. 1990). The first experiments describing the inactivation of tissue cysts of T. 2004). gondii tissue cysts in meat are susceptible to various physical procedures such as heat treatment. A separate problem is the importation of fresh meat. heat all feed administered to a temperature of at least 70 °C and provide animals with clean drinking water. Kijlstra. It should be noted that most studies were performed using experimentally infected pigs or with tissue cysts isolated from the brains of infected mice. acidity and enhancing solutions. E.. As there is a large variation in the types and amounts of meat eaten. 7. it should become evident that public health information concerning prevention of toxoplasmosis should be directed at the public at large. but survived for several weeks in the presence of physiological saline (0. For those food animals that can become infected via uptake of tissue cysts it is important to prevent access of rodents and birds into the stables. 5.

Experiments using different freezing temperatures showed that an internal temperature of À12 °C was sufficient to render the parasite non-viable (Kotula et al. and has been shown to have a considerable impact on the reduction of Escherichia coli contamination in ground beef (Berry and Bigner-George. It was observed that freezing for 2 days at À20 °C was sufficient to inactivate the parasite.2. (1960) were the first to show that heating could inactivate tissue cysts. Parasite viability was evaluated by mice or cat bioassay. gondii tissue cysts.7 °C (Kotula et al. freezing and heating on viability of Toxoplasma gondii tissue cysts Sample Tissue cysts from infected rat brain Salt 0. Limited data are available concerning consumer cooking habits and it is certainly possible that parts of meat being grilled or barbecued do not reach sufficiently high-temperatures to kill the parasite. 1992)..3% 2% 1% Temperature (°C) Time 4 18–20 18–20 18–20 50 56 50 Various 56 days 49 days 21 days 7 days 45 days 3 days 7 days 45 days immediate 2 days 4–21 days 8h 6–35 days 8h 64 h 24–48 h 0–24 days 12 h 30 min 24 h 1h 10 min 15 min Efficacya Reference À + + + + + + + À À À + À + + À + + +c + + +b + À + + Jacobs et al. showed that all meat samples were rendered non-infectious by freezing 6–35 days at À25 °C (Grossklaus and Baumgarten. At 50 °C it takes 1 h to inactivate tissue cysts (Table 2) whereas immediate destruction takes place when the internal temperature of meat reaches a temperature of 67 °C (Dubey et al. but proper tim- ing and temperature are necessary for a 100% parasite killing efficiency.1% 0.. most probably due to uneven heating (Lunden and Uggla.. c Toxoplasma gondii cysts could be isolated up to 13 days after preparation of smoked hams. This latter study thus indicates that importation of marginally frozen meats does not guarantee destruction of the parasite. À indicates that the procedure did not kill all parasites and + indicates a 100% killing effect of the procedure on the parasite.85% 6% 0. 1996). unless stated otherwise. 1990). (2006) Grossklaus and Baumgarten (1968) Hill et al.85% 2% 3.85% 0. Jacobs et al.. 1968). Cooking style has an influence on cooking temperatures and time. 2001.1–2. . b One of 54 deep frozen samples was still positive in a mouse bioassay after storage at À25 °C for 35 days. Other studies showed that at least 3 days at À20 °C were required to inactivate isolated tissue cysts (Djurkovic-Djakovic and Milenkovic. (1991) Hill et al.. (1965) Scupin (1968) Kotula et al. Kijlstra. (2004) Dubey et al. Freezing of meat by consumers is widely applied in westernized countries. The loss of sensory quality may be an important factor in consumers’ attitudes towards freezing of meat.85% 0.9 °C and 11 days at À6. Rhee et al. 2006). Jongert / International Journal for Parasitology 38 (2008) 1359–1370 Table 2 Effect of salting. (1990) Sommer et al. and that parasites in meat from experimentally infected pigs did not survive when frozen for 4 days at À7 °C to À12 °C (Kuticic and Wikerhauser. (2004) Djurkovic-Djakovic and Milenkovic (2000) Hill et al. (2006) Kuticic and Wikerhauser (1996) Lunden and Uggla (1992) Pork meat spiked with Toxoplasma cysts 2% 1% 4 4 67 À20 15% NaNO3/NaCl 5 À12 Various enhancing solutions 4 À25 Various enhancing solutions 4 À7 to À12 Meat from experimentally infected pigs Meat from infected sheep a Salt & sugar Smoking 4 <50 Efficacy was scored as À or +. 2003). Freezing and heating The effect of freezing on T.A. E. (1960) 1365 Tissue cysts from infected mouse brain Dubey (1997) 4 4 À20 Hill et al. 7. The primary control factor for prevention of T. gondii infection via meat consumption is adequate cooking and prevention of cross-contamination (McCurdy et al. In general. gondii-infected mice. freezing can inactivate the T.. gondii cyst viability was first described in 1965 (Sommer et al. 1991). 1965). Cooking infected meat in a microwave does not guarantee killing of the parasite.85% 0.1% 0% 0. 1991). Experiments with meat from pigs that were fed with T. 2000). Toxoplasma gondii tissue cysts remained viable up to 22 days at À1 and À3.

2004).. gondii DNA in commercially available swine sausages but bio-assays could not detect the presence of viable tissue cysts in these samples (de Oliveira Mendonca et al. viable parasites have not been isolated from commercial cuts of beef meat. 2006).3. the former can be localized and inactivated whereas prevention of the latter source is more complex (Dubey. indicating that prevention needs to be tailored according to social habits per country or region of the world. salt used for preparing sausages may inactivate T. 2008). 1997). Meat from grazing animals such as sheep and goats can be considered as important potential sources of T. Curing of lamb meat with salt and sugar for 64 h at 4 °C or smoking salt-injected meat at temperatures not exceeding 50 °C for 24–28 h were effective in killing T. is a preventable disease entity. 2006). caused by the consumption of infected meat... Pumping and curing meat A number of studies have addressed the effect of curing procedures such as salting.1366 A.. Aymerich et al. The high prevalence of toxoplasmosis in certain areas of the world has been associated with the consumption of raw sausages (Buffolano et al. gondii infection via this source (Fig.. while the addition of tripolyphosphate salts had no effect on parasite viability (Hill et al. However. gondii (Jamra et al. gondii infection for humans. 1997). gondii infection. Kuticic and Wikerhauser. Studies by Dubey have shown that 6% NaCl can kill the isolated tissue cyst. we review the data implicating meat as an important source of infection and describe strategies to reduce the risk of human T. gondii cysts were detected in freshly prepared swine sausages in other experiments (Dias et al. Although the relative role of tissue cysts versus oocysts in human toxoplasmosis is not exactly clear and may differ between countries. religion..7 kGy (Dubey et al. Kijlstra. 1996.. The relative role of these routes of transmission are not exactly known since disease manifestations cannot be distinguished according to source of infection.85% salt. Isolated tissue cysts can survive for 56 days in a solution of 0. Consumption of horse.4% lactate salt solutions into experimentally infected pig meat could kill the parasite but that a 1% NaCl solution provided variable results. Other studies indicated that depending upon the time of incubation. independent of the temperature used (Dubey. smoking or fermentation on tissue cyst survival. 1991). 1). 1986. Pub- 7. Sroka et al. The relative role of infection sources therefore comes from epidemiological studies. different sources of meat may act as most important infection source for a certain population. Conclusion Toxoplasma gondii is a ubiquitous parasite that can infect almost any warm-blooded animal. Infection in humans usually occurs via the consumption of cysts in undercooked meat (products) or by the uptake of soil or water contaminated by oocysts from feline faeces. gondii infections in meat producing animals such as pigs. 2005). 2004.. 1997). New developments in the knowledge of T. game and chicken can also be considered to play a role in horizontal transmission of T. 1994. Epidemiological case-control studies have attributed the main source of infection in Europe to undercooked meat. keeping animals indoors and preventing access of other animals. Irradiation and high-pressure Gamma irradiation of tissue cysts can render the parasite inactive at doses between 0.3% (Dubey.4 and 0. 2005). and food preparation methods. The parasite has a complex life cycle and multiple routes of infection are possible.4. Modern production technologies have shown that this is feasible and have led to a marked decrease of T. Depending on culture. 49 days at 2% and 21 days at 3. This may be due to confounding factors in epidemiological studies such as general meat knowledge of the respondents. 1996).. However. and thus a few infected animals may lead to T. Dias et al. 1992). E. Dubey and Thayer. viable T. Curing of meat products often involves the mixing of meat from various animals from different farms and sometimes from different farming systems (organic and regular). 2006) but negative effects on meat colour and texture have to be addressed . the adverse effects of irradiation on colour have a major impact on the use of this technology and in certain countries large-scale implementation is restricted due to poor consumer acceptance (Brewer. Toxoplasmosis in humans. gondii contamination of a whole batch of cured meat products. It should be noted that the above experiments were performed with the VEG strain and that the effect of strain differences with regard to viability following treatment with enhancing solutions has not been investigated yet.. Curing of meat has historically been introduced to preserve meat. gondii (Lunden and Uggla. 2004. gondii to humans. PCR studies have demonstrated the presence of T. Despite epidemiological studies pointing to beef as a source of T. In this report. and no laboratory tests are available to distinguish an infection by oocysts from an infection by tissue cysts. 8. Preventing infection of food animals can be achieved by giving animals sterilized feed and water. 2004. in particular on the presence of other meat sources in products sold as beef (adulteration) and meat mixtures where beef is a component amongst others. High-pressure treatment using 300 MPa can inactivate T. More recent data have shown that injection of >2% NaCl and/or >1. gondii infection in humans. before this method can be developed for routine decontamination (Cheftel and Culioli. Jongert / International Journal for Parasitology 38 (2008) 1359–1370 7. The difference between these two studies may be ascribed to the time interval between sausage preparation and bioassay in mice. the associated disease burden and the current inability to pharmacologically kill the tissue cyst stage of the parasite demand stricter monitoring and surveillance of the infection in both humans and food animals. gondii tissue cysts (Lindsay et al.

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