Background

With the rapid development of social economy and living standards, an increasing number of cats and dogs are raised as pets by many families in China [1]. Until now, there are over 50 million pet dogs and 40 million pet cats in China [2]. Considering the huge number of pets in China and the association with their owners, it is necessary for pet owners to know about the information of the zoonotic diseases transmitted by pets [3]. Toxoplasma gondii is an important zoonotic parasite belonging to Phylum Apicomplexa that is commonly found in warm-blooded vertebrates, including humans and birds [4]. It has been calculated that nearly one-third of the global population has been infected by this parasite [5]. Cats, definitive hosts for this parasite, can discharge oocysts in their feces, resulting in soil contamination with oocysts [5]. Human can infect with this parasite through ingesting raw or undercooked meat containing T. gondii cysts, or through ingesting water or food contaminanted with T. gondii sporulated oocysts [4, 5].

Many studies have been conducted to explore the potential transmission situation of some zoonotic protozoan diseases between pets and humans all over the world [4, 6, 7]. However, limited information about T. gondii infection in pet owners in China can be obtained [8]. Thus, the present study was conducted with the aim to explore the T. gondii seroprevalence in pet cats and their owners for the first time in Jilin province, northeastern China.

Results

In this study, a total of 62 cat sera out of 306 examined pet cats (20.3%) were seropositive for T. gondii with titers of 1:25 found in 15 pet cats, 1:50 in 9 pet cats, 1:100 in 9 pet cats, 1:200 in 7 pet cats, 1:400 in 10 pet cats, 1:800 in 9 pet cats, and ≥ 1:1600 in 3 pet cats (Table 1). Considering the species of pet cats, T. gondii seroprevalence was ranged from 0 in American Shorthair cat to 26.2% in Chinese Lihua cat (Table 1). T. gondii seroprevalence in pet cats from Changchun, Jilin and Liaoyuan were 23.1, 19.8 and 16.9%, respectively. In view of the age of pet cats, the cats were in the 2–3 year old age group have the highest T. gondii seroprevalence (22.1%), followed by the ≤1-year old age pet cats (19.8%), and > 3-year old age pet cats (17.6%). Female pet cats (22.3%) had a higher T. gondii seroprevalence than male pet cats (18.4%). Moreover, pet cats from rural areas (30.4%) had a significantly higher seroprevalence than those from urban areas (15.2%) (p = 0.002).

Table 1 Seroprevalence of T. gondii infection in pet cats in northeastern China
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The results of testing the T. gondii antibodies in the owners of pet cats showed that 18.1% (72/397) owners of pet cats were seropositive for T. gondii. Of these, T. gondii IgG and IgM antibodies were found in 16.9% (67/397) and 1.3% (5/397) of the owners of pet cats, respectively. With a view to the age of owners of pet cats, T. gondii seroprevalence was ranged from 12.6% in the 31- to 40-year old age group to 24.0% in the ≤20-year-old age group (Table 2). The seroprevalence of T. gondii infection in owners of pet cats from Changchun, Jilin, and Liaoyuan were 20.8, 18.4, and 13.9%, respectively. Male owners of pet cats (19.4%) had a litter higher seroprevalence than female owners (17.1%). Moreover, owners of pet cats living in rural areas (28.9%) had a significantly higher seroprevalence than those living in urban areas (12.0%) (p < 0.001). Owners of pet cats who had the habit of fecal harmless treatment (11.3%), had a lower seroprevalence compared with those who did not have this habit (19.3%), however the difference was not significant (p > 0.05). In addition, 39.8% (158/397) owners of pet cats have the knowledge of zoonotic protozoan diseases, in this case, owners of pet cats who understood knowledge of zoonotic protozoan diseases (10.1%) have a significantly lower seroprevalence than those who did not understand knowledge of zoonotic protozoan diseases (23.4%) (p < 0.001).

Table 2 Seroprevalence of T. gondii infection in the owners of pet cats in northeastern China
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Discussion

In this study, we reported the evidence for the seroprevalence of T. gondii infection in pet cats and their owners in Jilin province, northeastern China for the first time. The proportion of T. gondii positive in the sera of pet cats and their owners were 20.3% (62/306) and 18.1% (72/397), respectively. The T. gondii seroprevalence in pet cats in this study (20.3%) was a median of 20.3% T. gondii seroprevalence in cats including stray and pet cats reported by a systematic review and meta-analysis of the seroprevalence of T. gondii in cats in mainland China from 1995 to 2016 [9], but a litter lower than 21.67% T. gondii seroprevalence in pet cats in Shandong province, eastern China [8].

In China, toxoplasmosis is still an important public health problem because there is an increasing number of AIDS patients, and the number of people living with HIV and AIDS in China is nearly 1,000,000 [10]. It is well known that cats play a crucial role in the transmission of T. gondii [4, 5]. In this case, pet cats could be a significantly potential cause of human toxoplasmosis because they frequently intimate contact with their owners. In China, owners of pet cats like to take their pets for a walk in the morning and evening time and the pet cats are free-roaming and might be exposed to T. gondii existed in the environment. After this, millions of environmentally-resistant oocysts might be excreted in cat feces, resulting in health risks to animals and humans [5, 11]. Previous studies have showed that the presence of cats at home induces the risk of exposure to T. gondii [12, 13]. Thus, it is very necessary to publicize the information of zoonotic protozoan diseases caused by pets to the public. Coincidentally, we found that the owners of pet cats who understood knowledge of zoonotic protozoan diseases (10.1%) have a significantly lower seroprevalence than those who did not understand knowledge of zoonotic protozoan diseases (23.4%) (p < 0.001). Therefore, publicity work should be taken to publicize the dangers and protection methods of zoonotic protozoan diseases caused by pets [1]. Furthermore, another known factor that contributes to the maintenance and dissemination of this disease, especially in rural environments, owners of pet cats consuming contaminated vegetables and fruits from home grown and poor sanitary conditions (untreated water). These factors increase the chances of getting infected more than owners of pet cats who live in cities. This is consistent with our research results that owners of pet cats living in rural areas (28.9%) had a significantly higher seroprevalence than those living in urban areas (12.0%) (p < 0.001).

Continuing evidence suggests that waterborne transmission of T. gondii to humans is common, through the spread of T. gondii oocysts by the overland runoff [14]. Thus, fecal harmless treatment of cats can cut down the environmental contamination with T. gondii oocysts existed in cat feces [15]. However, owners of pet cats who had the habit of fecal harmless treatment (11.3%), had a lower seroprevalence compared with those without this habit (19.3%) in the present study, however the difference was not significant (p > 0.05). Such a large quantity gap of sample-size between owners of pet cats who had the habit of fecal harmless treatment and those without the habit of fecal harmless treatment. Anyway, if we want to cut down the environmental contamination with T. gondii oocysts, we must hygienically dispose cat feces in the first place.

Conclusions

We firstly showed that the seroprevalence of T. gondii infection in pet cats and their owners is common in Jilin province, northeastern China. Thus, some control measures should be implemented to reduce T. gondii infection in pet cats, and the owner of pets, in the studied regions and elsewhere in China, such as publicity work and fecal harmless treatment.

Materials and methods

Northeast China is an important pet breeding and breeding base in China, and Jilin Province (40°50′ ~ 46°19′ N; 121°38′ ~ 131°19′ E) is located in the central part of Northeast China. Due to geographical advantages and suitable environment, many residents here like to keep cats. The present study was approved by the Animal Ethics Committee of Jilin Agricultural University. From January 2017 to October 2018, 306 pet cats were randomly selected from three regions (Changchun, Jilin, Liaoyuan) in Jilin province (Fig. 1). Questionnaires were provided to cat owners requesting data about each sampled animal. Collected data included information on the species, region, age, gender, and residence area of the pet cat, and their owner’s age, region, gender, residence area, understanding knowledge of zoonotic protozoan diseases and how to deal with feces. Before blood collection of pet cats, a permission was obtained from each pet cat owner and then a local veterinary practitioner was employed to collect the blood samples from the medial saphenous vein of each pet cat. Moreover, we explained the purpose and process of this study to the pet owners and a permission was given to us from the pet owners. After that, nearly 2 ml blood samples were got from the venous blood of each owner by a professional nurse. All blood samples were left about 4 h at 4 °C and then centrifugated at 1500×g for 5–10 min to isolate the serum. After isolation, the serum were stored in Eppendorf tubes at − 20 °C before the next step.

Fig. 1
figure 1

Map showing three cities in Jilin province, northeastern China, where pet cats sampling was performed. A, Changchun; B, Jilin; C, Liaoyuan

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In this study, sera of pet cats were tested for anti-T. gondii antibodies using a modified agglutination test (MAT) [16, 17]. Slightly, sera were added to the “U” bottom of 96-well microtiter plates, and diluted 2-fold starting from 1:25 to 1:1600. The sera was considered T. gondii-positive when the MAT titers ≥25 [10]. Suspicious serum samples were re-tested. Moreover, positive and negative controls were included in all tests. To detect T. gondii IgG and IgM antibodies in sera of owners, commercially available enzymelinked immunosorbent assay (ELISA) kits (Haitai Co., Ltd., China) were used following the instructions of the manufacturer. All samples were run in duplicate. SAS version 9.1 was used to do the statistical analysis. p value < 0.05 was used to determine statistically significant by a Chi-square test.