Toxocara canis is a common round worm found in the small intestines of dogs; however, T. canis can also infect other animals. Infection of dogs as well as other animals takes place by ingestion of soil contaminated with eggs in dooryards and parks. The infected larvae reach the liver and are dormant in the liver parenchyme. They move slowly from place-to-place within the liver, or migrate to the lungs and other tissues, which is called as visceral larva migrans [1,2]. These encapsulated larvae in animal tissues do not grow into adult worms, but are capable of transmitting to other animals that eat the infected tissues harboring encapsulated larvae. This mode of transmission among carnivorous vertebrates has been established with experimental studies [1,3-5]. A large variety of non-canine animals can be infected with T. canis. Known paratenic hosts include mice, rats, chickens, pigeons, lambs, pigs, and cows. Animals are infected by ingestion of embryonated eggs in contaminated soil or of encapsulated larvae in the tissues of paratenic hosts.

Like animals, human infections may take place in 2 ways: 1) ingestion of embryonated eggs, and 2) transfer (ingestion) of encapsulated larvae of T. canis in the tissues of a paratenic host [2]. In certain ethnic groups, some adults tend to eat uncooked animal tissues which contain encapsulated infective larvae. After swallowing, the encapsulated larvae are liberated after hatching in the small intestine, penetrate the intestinal wall, get into the portal vein, and then reach the liver and lungs. They again become encapsulated and remain alive for a certain period. Uncooked livers of cow [3,6-8], pig [9], lamb [10], and chicken [11,12] have been reported as sources of human infections. However, epidemiologic data on the role of ingesting raw liver of animals in the transmission of T. canis from animals-to-humans is limited [8]. In order to evaluate the relationship between toxocariasis and the ingestion of raw meat, we conducted a prospective study.

One hundred four (86.7%) of the 120 patients showed positive results in Toxocara ELISA tests. Among them, 92.3% were confidently diagnosed as toxocariasis because they had no other possible causes to increase the eosinophil count. Twenty-four patients were diagnosed as other parasitic infections, as they showed positive ELISA results for C. sinensis (n = 12), P. westermani (2), sparganosis (4), and cysticercosis (6). Among the seropositive patients for toxocariasis, 87.5% had a recent history of consuming raw cow liver, whereas only 25.0% of seronegative patients had such a history. In 28 patients who ate raw cow livers frequently (4 times or more per year), the seropositive rate was 96.4%. In 45 patients who ate raw cow livers within 6 months prior to the interview, the seropositive rate was 95.6%. Twenty-one patients ate raw livers of animals other than the cow, such as pig (n = 7), dog (4), goat (3), chicken (3), rabbit (2), duck (1), and goose (1). Among these patients, 95.2% had a history of eating raw cow liver. Nineteen patients drank raw blood of animals, such as deer (n = 16), goat (2), duck (2), cow (1), pig (1), or mud turtle (1).

Table 1 presents the distribution of seropositive and seronegative patients in Toxocara ELISA. According to multivariate analyses, a recent history of eating raw cow liver was related to an increased risk of toxocariasis. Recent histories of eating raw liver of other animals, raw meat of animals, raw blood of animals, and raw freshwater fish, keeping dogs, and serologic results for other parasites were not related to an increased risk of toxocariasis.

Chops of raw cow liver are one of the popular dishes in some restaurants or buffets in Korea. Chops of raw cow liver are usually served along with usual cooked or barbecued meat. Some people believe that raw liver and meat are good for health, particularly for eyesight. In our study population, patients had a history of eating raw cow liver within 1 yr and some people ate chops of raw cow liver frequently whenever they go to meat restaurants. Not infrequently, some people eat raw liver of pigs, dogs, chickens, goat, duck, goose, or rabbits. Because of this eating habit, there are many patients with subclinical toxocariasis. Usually, they are checked by clinicians because of eosinophilia [8], or sometimes after small nodular lesions are incidentally found in the liver, lungs, or both on sonography or computed tomography [7].

The results of our study suggest that the ingestion of raw cow liver substantially increase the risk of toxocariasis. The seropositive rate in patients who ate raw cow liver was more than 3 times higher than in patients who did not eat raw cow liver. Patients who ate raw cow liver frequently or more recently showed very high seropositive rates. It appears that the seropositive rate is higher in people who had history of eating raw cow liver frequently and recently.

In spite of being seropositive for toxocariasis, some patients denied a history of ingestion of cow livers. Ingestion of raw livers of pigs, lambs, and chicken has been reported as route of human infections [9-12]. We attempted to establish a role of eating habit of raw animal livers other than cow livers in toxocariasis. There were 21 seropositive patients who had a history of eating raw livers of other animals, but they all had a history of eating cow livers as well. Therefore, we could not verify the relation between toxocariasis and ingestion of raw livers of other animals.

Several patients who denied a history of ingestion of cow livers were keeping dogs (3 in the house and the other 4 in gardens). Infection might take place by ingestion of eggs of T. canis, which were laid by their own dogs and then embryonated in their surroundings. In our study, however, the history of keeping dogs was not statistically significant in infection of T. canis. Among these 7 patients, 3 were not only keeping dogs but also ate raw meat of animals within 1 yr. In other 2 patients who were seropositive without history of raw cow liver ingestion, infection might have taken place by eating raw cow meat. They have eaten raw meat of animals without history of keeping dogs. There have been several case reports that toxocariasis probably took place by ingestion of raw meat of animals [15,16]. In animal experiments, Toxocara larvae were recovered in the lungs, liver, kidneys, brain, and also in muscles [3,17]. Tahira et al. [18] suggested the possibility of zoonotic risk of toxocariasis through eating animal meat. In our study, many adults who ate raw cow liver also ate raw cow meat. We could not make a differentiation of the patients infected through ingestion of raw cow liver from those infected through ingestion of raw cow meat.

We did not determine the route of toxocariasis in 4 patients. We cannot exclude the possibility of toxocariasis by other Toxocara spp., such as T. cati and T. leonina [19]. There may be some cross reaction of human IgG antibodies to Toxocara ES antigens to other helminthiases, such as trichinosis, fascioliasis, and strongyloidiasis [20].

The toxocariasis seropositive rate in general population is variable depending on countries; specifically, 18% in rural areas in China [21], 20% in Malaysia [22], 26% in Iran [23], 6-36% in the Czech Republic [24], 2-5% and 14-37% in urban and rural areas in the Midi-Pyrenees area in France, respectively [25], 5% in Switzerland [26], and 5% in a rural area of Korea [27]. Because dogs and cats are popular pets, there is widespread contamination of environment with infective eggs, and therefore toxocariasis is a worldwide disease, irrespective of developed or underdeveloped countries. Higher rates of seroprevalence have been reported in Indonesia (68%) and Nepal (81%) [28,29]. It was suggested that a high seroprevalence among healthy adults of Taiwanese aboriginal populations (46%) was due to their habit of eating raw liver or meat [9]. The population enrolled in this study consisted of patients with eosinophilia of unknown etiology. Thus, they showed very high rates of seropositivity for toxocariasis and a history of eating raw cow liver. Further studies on the relationship between toxocariasis and ingestion of raw food in general population with lower seropositive rate are needed.

This study had some limitations. This study was cross-sectional and thus temporal associations cannot be inferred. A bias arising from recall data based on the patient's ability to recall past history of eating raw tissue of animals cannot be avoided. We first expected the ingestion of raw liver of other animals and raw meat of animals as possible risk factors. However, only the ingestion of raw cow liver increased the risk of toxocariasis in our multivariate statistics. The two ingestion histories could not be demonstrated as risk factors because of the small numbers of cases and substantial overlapping histories of ingesting raw cow livers. Another limitation is that we did not count the amount of animal tissues ingested in determining the seropositivity of the enrolled patients. Finally, the results of this study could be different from the general people. Only a minority of Koreans eat raw cow liver. When we designed this study, we worried about a very low toxocariasis seropositive rate in general population. Therefore, we selected patients with eosinophilia.

With the limitations of our study in mind, we suggest that ingestion of raw cow liver increase the risk of toxocariasis. Ingestion of uncooked livers of paratenic hosts may also be a potential source of human toxocariasis, at least in patients with eosinophilia.