Toxoplasma gondii Seropositivity and Associated Risk Factors in Cats ( Felis catus ) in Three Provinces in Northeastern China from 2013 to 2019

Introduction

With the improvement of living standard, more and more people are keen to start raising companion animals in China. Because of the special relationship among cats and humans, they can transfer many pathogens to humans, including Toxoplasma gondii (Nayeri Chegeni et al. 2019; Qin et al. 2020; Esteves et al. 2014). T. gondii, a kind of cosmopolitan protozoan parasite with a complex life cycles, including the asexual stage and sexual stage (in definitive hosts), is the causative agent of toxoplasmosis (Daryani et al. 2014; Cong et al. 2016; Sharif et al. 2015; Zhang et al. 2015).

As the most common feline definitive host, cats play a vital role in the transmission of T. gondii, whose infected feces may become a potential resource causing toxoplasmosis outbreaks (Ding et al. 2017; Tehrani-Sharif et al. 2015). Humans acquire toxoplasmosis mainly through ingestion of unwashed food or water containing oocysts shed by cats, as well as consumption of undercooked or raw meat containing tissue cysts, and usually without any symptoms (Khan and Noordin, 2019; Meng et al. 2015). However, T. gondii infection in pregnant women and HIV/AIDS patients can cause a series of disease and even death (Bowen et al. 2016; Zhang et al. 2015).

Because toxoplasmosis is seriously harmful to the human and animals, and cats play an important role in the spread of the disease, whose investigation in cats is significant and imminent. Although T. gondii infection in cats have been reported in many countries around the world (Amouei et al. 2019; Sukhumavasi et al. 2012; Waap et al. 2012; Lilly and Wortham 2013; Switzer et al. 2013; Can et al. 2014; Cerro et al. 2014), limited information was available in China. T. gondii infection in cats has been reported in Guangzhou (Zhang et al. 2009), Guizhou (Li et al. 2015), Beijing (Qian et al. 2012), Jiangsu (Hou et al. 2018), and Lanzhou (Wu et al. 2011; Cong et al. 2016) up to present, but data in northeastern China are limited.

The objectives of this study were to estimate T. gondii seroprevalence in domestic cats and stray cats in Jilin, Liaoning, Heilongjiang province, northeastern China, and access the risk factors associated with T. gondii infection. Moreover, the study provides the foundation information for control of toxoplasmosis prevalence in cats, other animals, and humans.

Materials and Methods

Results and Discussion

Toxoplasma gondii is widely distributed among cats in China and the prevalence from different regions varied. Cats in Central China (32.3%) had a higher seroprevalence than in other region wide (Eastern, 24.9%; Western, 17.4%) distributed among cats in China (Ding et al. 2017). But the rate in northeastern China is unclear. In this study, we investigated T. gondii seroprevalence in domestic cats and stray cats from seven cities in Heilongjiang province, Jilin province, and Liaoning province, northeastern China. In this study, 163 (19.1%, 95% CI: 16.4–21.7) out of 864 cats were seropositive to T. gondii tested by IHA with titers of 1:64 in 51, 1:128 in 40, 1:256 in 20, 1:512 in 12 and ≥1:1024 in 4 in cats (Table 1). The overall T. gondii seroprevalence was 19.1% (95% CI: 16.4–21.7). The highest seroprevalence with 19.6% (95% CI: 15.5–23.7) in Heilongjiang, followed by Liaoning province (19.1%, 95% CI: 14.4–23.8) and the lowest seroprevalence in Jilin province with 18.3% (95% CI: 13.4–23.2). The warm climates are conducive to the survival of oocysts and the activity of intermediate hosts. Studies have shown that oocysts can be infectious for up to 1.5 years in warm climates (Ding et al. 2017). Low rainfall and temperature in northeastern China may be one reason why the seroprevalence of T. gondii in cats is lower than that in other areas located in warm climates, such as Guizhou (63.16%) (Li et al. 2015), Beijing (57.8%) (Qian et al. 2012), Turkey (42–48%) (Can et al. 2014), and Sri Lanka (30.2%) (Kulasena et al. 2011). This is only one of the geographic differences that account for the prevalence of T. gondii. Other factors such as local economic conditions, dietary habits, and abundance of wild hosts can account for the difference (Dubey, 2010).

Stray cats and domestic cats, the most important definitive hosts for T. gondii, are closely related to humans (Lilly and Wortham, 2013; Tehrani-Sharif et al. 2015). Table 2 presents the relationship between T. gondii-seropositivity in cats in this study, based on regions, genders, type, ages, and collection year groups with univariate analysis. The cat's way of life has negative effect on the risk of T. gondii infection (OR = 0.28, 95% CI: 0.19–0.40). The effect of other variables on the results was not significant. The seroprevalence of T. gondii was higher in stray cats (36.8%, 95% CI: 29.8–43.7) in comparison with pet cats (14.2%, 95% CI: 11.6–16.8). This could be due to stray cats have more opportunities to exposure to T. gondii in the natural environment. Similar results were found in Spain (Miró et al. 2004), Tehran (Haddadzadeh et al. 2006), and Brazil (Coelho et al. 2011). This higher seroprevalence in stray cats living outdoors, hunt and may feed on debris and garbage contaminated with oocysts and wild birds infected by T. gondii infected and rodents, may be related to their hunting and eating habits, increasing the risk of ingesting parasites. In contrast, about 11.7% of wild birds in northeastern China infected by toxoplasma, and other animals of varying degrees of toxoplasma infection, including chicken, duck, goose, horse, donkey, and sheep (Wang et al. 2014, Wu et al. 2017), provide extra risk of infection for cats, especially feral cat feces reinfect the animals. Therefore, the resulting cycle brings difficulty to prevention and control. Furthermore, it is worth noting that human might be in closer contact with domestic cats, although domestic cats have a lower seroprevalence than stray cats. The related studies showed that the serological seroprevalence of pet owners was higher than that of normal people (Cong et al. 2018). With the rapid social changes in China, the number of domestic cats is also increasing rapidly. Humans acquire toxoplasmosis mainly through ingestion of oocysts shed by cats, it is worth noting that most cats only shed oocysts for about 1 week in their life. Cats seroconverted during the second and third week after they were fed tissue cysts or they had shed oocysts. Seronegative cats are either recently infected and shedding or have never been exposed (Dubey et al. 2009). To sum up, a lot of seropositive cats have already shed oocysts and caused widespread environmental contamination. This should be of public health department concern and the government should set up more stray animal shelters to control the number of stray cats. Pet owners should also reduce their cats' outdoor activities and avoid to feed them raw. In this study, 163 (19.1%, 95% CI: 16.4–21.7) out of 864 cats were seropositive to T. gondii tested by IHA with titers of 1:64 in 51, 1:128 in 40, 1:256 in 20, 1:512 in 12, and ≥1:1024 in 4 in cats (Table 1). The overall T. gondii seroprevalence was 19.1% (95% CI: 16.4–21.7) (Table 2). It is not conducive to the survival of oocysts and the activity of intermediate hosts due to the low rainfall and low temperature in northeastern China, the serological positive rate of T. gondii in cats is lower than that in other areas located in other areas with warm climates, such as Guizhou (63.16%) (Li et al. 2015), Beijing (57.8%) (Qian et al. 2012), Turkey (42–48%) (Can et al. 2014), and Sri Lanka (30.2%) (Kulasena et al. 2011). In warm climates, oocysts can be infectious for up to 1.5 years. This is only one of the geographic differences that account for the prevalence of T. gondii. Other factors such as local economic conditions, dietary habits, and abundance of wild hosts can account for the difference (Ding et al. 2017).

Large number of studies have showed T. gondii seroprevalence increases with age (Cong et al. 2016; Meng et al. 2015; Zhang et al. 2015); the same trend has also been found in this study, but the difference was not statistically significant (p > 0.05) (Table 2). In this study, the seroprevalence of T. gondii in cat declined from 2013 to 2019. The stray animals can be detrimental to humans since they are associated with the occurrence of biting incidents, transmission of diseases, damage to wild animal populations, accidents, and pollution. In view of such situations, local governments have taken out some strategies. On the one hand, the mode of keeping cats has transferred to adopt stray animals as pets rather than purchasing due to government incentives. For example, many cities hold adoption days regularly to provide opportunities for these people. Other measures refer to reduce the number of cats in the wild, such as the establishment of animal shelters, where the stray animals were given better living conditions and healthier diets to avoid infection. The decreasing seroprevalence year by year is related to these behaviors. In fact, there are many reasons for getting infected with Toxoplasma, and no generalizations should be made. Factors include cultural environment, economic conditions, and urban and rural differences. For example, low seroprevalence (7.3–11%) in Bangkok, Thailand, was attributed to religious culture, which thinks that it is sinful to kill any pet for most (95%) people in Thailand are believing in Buddhism, including cats, of which ∼15,000 cats (30 × 500 temples) living permanently around Buddhist temples are fed with a diet cooked by the public or monks (Dubey et al. 2009). On the other hand, the difference between city and country is also a factor. Cats living in the countryside have more chances to prey on mice than cats living in apartments (Must et al. 2015).

In summary, this study suggests existence of the T. gondii infection in cats in Jilin province, Heilongjiang province, and Liaoning province, northeastern China. This study provided foundation data for prevention and control of T. gondii prevalence in these regions. Way of life are highly related to T. gondii infection in cats in the investigation areas. These results suggest that T. gondii antibodies were common in cats in northeastern China. Pet owners should avoid cat hunting and getting raw meat to reduce the further spread of the parasites, and should pay attention to the harmless handling of feces when cleaning up the litter. The higher positive rates of free-roaming cats suggested that these cats had already shed oocysts that caused contamination and constituted a long-term source of infection for other hosts. The effective control over the number of stray animals should continue to be performed strictly.