Prevalence of antibodies against Toxoplasma gondii in pets and their owners in Shandong province, Eastern China

Significant strides have been made in the prevention and treatment of parasitic diseases. However, many parasites remain a common cause of morbidity and mortality in pet animals and can also pose a threat to the environmental and public health [1]. One of these parasitic diseases is toxoplasmosis, an important zoonotic parasite disease caused by the opportunistic protozoan Toxoplasma gondii. This parasite can infect almost all domesticated and wild animals, and humans [2, 3]. Cats represent the only definitive host of T. gondii, with many animals, including dogs, serving as the intermediate host. Humans acquire T. gondii infection via ingestion of undercooked or raw meat containing T. gondii cysts, or through ingesting food or water contaminated with cat-derived T. gondii oocysts [3, 4].

Cats and dogs are the most popular pets, and play a significant role in people’s daily life [5] - bringing many benefits to humans’ physical and mental health [6]. In China, pet ownership is becoming more common [7]; with rapid economic and social development. This increase in pet ownership has been considered as an indicator of the improved socioeconomic status of the Chinese society [8]. The population of cats and dogs being kept as pets in China, are approaching 100 and 200 million, respectively [9]. In Beijing, the number of pet dogs increased from 100,000 to 1.5 million between 2001 and 2007. Dogs and cats are also used in rural areas of China to guard homes and limit the spread of rats.

Despite the increasing popularity of dogs and cats as pets, they can be a source of many zoonotic diseases to humans [10–13]; especially children, the elderly and immunocompromised individuals [14–16]. Both humans and pets (dogs and cats) are known to be susceptible to infection with the agent that causes toxoplasmosis. A recognition of the potential transmission of many parasitic zoonoses from pets to humans has led to a worldwide increase in the number of studies of T. gondii infection in pets [4, 17, 18] - including mainland China [19, 20]. However, nothing is known about the prevalence of T. gondii infection in pet owners in China.

The aim of the present study, was to determine the seroprevalence of T. gondii infection in pet dogs and cats, and their owners, in Shandong province, eastern China. The serological findings provide evidence that pet ownership can significantly increase the risk for pet-associated zoonotic T. gondii infection in humans.

In the present study, the serological evidence for the presence of T. gondii infection in pet dogs and cats, and their owners in Shandong province, eastern China is reported. We demonstrated that T. gondii seroprevalence in pets and pet owners was 18.61% and 18.04%, respectively. Seroprevalence of T. gondii in cats was 21.67%, being slightly lower than the 24.5% seroprevalence detected in cats in mainland China, from 1991 to 2015 [20]. Seroprevalence T. gondii in dogs was 15.56% - higher than the 11.1% seroprevalence previously reported in pet dogs in China [19].

The association between cat ownership and increased seropositivity of T. gondii is to be anticipated, because cats - serving as the definitive host of this parasite - play a key role in the transmission of T. gondii to humans [21]. In the studied regions, cats are used mainly to control rats and mice, or as a pet. Cats become infected with T. gondii when they prey on infected rodents or birds. This is followed by excretion of millions of environmentally-resistant oocysts in cat feces, causing health risks to animals and humans [3, 22]. The presence of cats at home increases the risk of exposure to T. gondii, as reported previously [23].

Dogs, on the other hand, are a dead-end intermediate host and do not produce T. gondii T. gondii oocysts; and might be considered less important to the zoonotic transmission of T. gondii. However, dogs can ingest oocysts from cat feces, by coprophagia, which pass intact [24] and even viable [25] through their gut into the feces. Some dogs have a tendency to roll in pungent substances, such as cat feces. This behaviour means that dogs can mechanically spread T. gondii oocysts, contaminating the environment [24] and infecting humans - accidentally through ingestion of oocysts from dog fur while petting them [26]. The ingestion of improperly-cooked infected meat, can be a source of transmission to people in areas where selling dog meat for human consumption is permitted [27].

Our study also found that female pet owners (24.39%, 60/246) had a significantly higher seroprevalence than male pet owners (10.75%, 23/214; P < 0.001) (Table 2). This may be due to various factors. In China, women are responsible for taking care of pet animals at home, handling raw meat and vegetables, and performing household cleaning tasks. These factors can increase their contact with cats and dogs, and their feces, thus increasing opportunities of acquiring the infection compared with men. With this in mind, women should follow basic hygienic measures to limit exposure to zoonotic agents; including wearing gloves and masks when handling cat feces, together with hygienic disposal of cat feces and frequent hand-washing - particularly before preparing food.

There is increasing evidence for the importance of waterborne transmission of T. gondii to humans, via the dissemination of oocysts through surface water [28]. Therefore, proper disposal of cat litter can reduce environmental contamination with oocysts excreted in cat feces [29]. Although pet owners who used their hands to dispose pet feces (18.97%) had a higher seroprevalence compared with those who used gloves (12.86%), the difference was not statistically significant (P > 0.05). This may be due to a large difference in the sample-size between people who disposed pet feces using gloves, and those using bare hands. Regardless, cat feces must be hygienically disposed of, in order to reduce the environmental contamination with T. gondii oocysts.

In China, approximately 1 in 5 pet cats is T. gondii-seropositive, and this may impose a significant risk as the number of owners, and their interactions with cats, is increasing [20]. Cats and dogs are known to harbor other protozoal species [17], helminthes [30], and many other types of pathogens, such as fungal, viral, and bacterial agents [31], and may constitute potential reservoirs to their owners. Therefore, the epidemiological and public health importance of zoonotic infections, in pet dogs and cats in China, should be investigated in future studies. In the interim, we advocate the implementation of better measures to improve personal hygiene; and to maintain good pet-keeping management practice, which will ultimately help in reducing the risk of T. gondii infection, and other zoonoses, in humans.

The present results show that the seroprevalence of T. gondii infection in pets and their owners in Shandong province, eastern China, was high and poses significant health risks to the local community. Our study provides evidence, that an association exists between the ownership of pet cats or dogs, and an increased risk for T. gondii infections in pet owners. Therefore, it is imperative to implement control measures to reduce T. gondii prevalence in pets, and pet owners, in the studied regions and elsewhere in China. It remains to be determined, whether or not pets and their owners may have been exposed to the same environmental source of T. gondii infection; and the directionality of transmission between pets and pet owners requires further investigation.