Seroprevalence and Related Factors of Toxoplasma gondii in Pigeons Intended for Human Consumption in Northern China

Introduction

The pigeon is one of the most common bird species in the world. There is a long history in China of rearing pigeons, and this has recently increased due to the birds' ornamental value and also the high nutritional value of the meat and/or eggs. According to national statistics, the scale of the pigeon industry continues to grow at 10–15% a year in China (Chen 2012). However, because of the close relationship between humans and pigeons, many pathogens can be transmitted, including Chlamydia (Wang et al. 2018) and Toxoplasma gondii (Cano-Terriza et al. 2015).

T. gondii is one of the most important zoonotic foodborne pathogens since it causes toxoplasmosis. T. gondii has a broad host range, including almost all warm-blooded animals, including pigeons, as intermediate hosts (Dubey 2010, Vilares et al. 2014, Zhang et al. 2018). The definitive host is the felids (Frenkel et al. 1970, Zulpo et al. 2018), which can shed infective oocysts into the environment; these, in turn, can contaminate food/water sources and infect humans and/or other animals (Dubey 2010, Zhang et al. 2016a, Zulpo et al. 2018). Humans can also become infected via consumption of undercooked pigeon meat that contains tissue cysts (Cano-Terriza et al. 2015, Cong et al. 2017, 2018, Zou et al. 2017). In general, T. gondii infection is asymptomatic; however, it can cause abortion and fetal deformity in pregnant women and even death in patients with immune deficiencies (Tian et al. 2017, Wang et al. 2017).

Since the pigeon is one of the most important intermediate hosts of T. gondii. (De Sousa et al. 2010, Cano-Terriza et al. 2015), it is important to understand the prevalence of T. gondii infection. Although several studies have recorded the seroprevalence of T. gondii in pigeons around the world (De Sousa et al. 2010, Alvarado-Esquivel et al. 2011, De Lima et al. 2011, Karatepe et al. 2011, Khademvatan et al. 2013, Barros et al. 2014, Vilares et al. 2014, Vitaliano et al. 2014, Cano-Terriza et al. 2015), in China this has only been recorded in Gansu (Cong et al. 2012) and Guangdong Provinces (Yan et al. 2011). More importantly, people living in northern China often eat raw meat, especially pigeon meat, which increases the risk of infection (Zhang et al. 2016b). This study aims at investigating the seroprevalence of T. gondii infection in pigeons in Jilin Province, Liaoning Province, and Inner Mongolia Autonomous Region (IMAR) in Northern China and at estimating the related factors. These data could help to further control toxoplasmosis in pigeons and other hosts in China.

Materials and Methods

Results

In this study, 104 (10.80%) of 963 pigeons were found to be T. gondii-seropositive at the cut-off of 1:64. A further 68 were found to be seropositive at the cut-off of 1:64, 20 at 1:128, 12 at 1:256, and 4 at 1:512 (Table 1). The seroprevalence of T. gondii in male and female pigeons was 8.80% (41/466) and 12.68% (63/497), respectively (Table 1). The seroprevalence of T. gondii infection in adult pigeons (12.63%, 86/681) was significantly higher than that in juveniles (6.38%, 18/282) (Table 1).

Multivariable regression analysis showed strong effects of both gender (OR = 0.63, 95% CI 0.42–0.96) and age (OR = 0.45, 95% CI 0.27–0.77) on seroprevalence. Adult pigeons (12.63%, OR = 2.12, 95% CI 1.25–3.60) were found to be more susceptible than juveniles (6.38%). Moreover, male pigeons (8.80%) were considered to have lower seropositivity compared with females (12.68%, OR = 1.51, 95% CI 0.99–2.28, Table 1).

Discussion

Found worldwide, T. gondii is a food-borne zoonotic pathogen that can be transmitted to other hosts through ingestion of undercooked meat (Zou et al. 2017, Zhang et al. 2018). One meat that is commonly eaten raw or undercooked is pigeon, especially in northeastern China, despite the limited information on the seroprevalence of T. gondii infection in pigeons. IHA has been widely used to detect the seroprevalence of T. gondii in a variety of animals because it is simple, safe and has good sensitivity and specificity. Therefore, we investigated T. gondii seroprevalence in 963 pigeons in Jilin Province, Liaoning Province, and IMAR by IHA, specifically looking at differences due to region, age, and gender.

Around 10% of pigeons tested as seropositive for T. gondii antibodies, higher than feral pigeons in Southern Spain (9.2%) (Cano-Terriza et al. 2015) and Jaboticabal, Brazil (0.83%) (De Sousa et al. 2010); and also higher than domestic pigeons in Niğde region, Turkey (0.90%) (Karatepe et al. 2011) and Guangdong, China (8.7%) (Yan et al. 2011), wild pigeons (0.95%) in Niğde region, Turkey (Karatepe et al. 2011), pigeons (Columba livia) from São Paulo State, Brazil (5.04%) (De Lima et al. 2011), and wild birds in Durango, Mexico (2.6%) (Alvarado-Esquivel et al. 2011). However, the values are lower than in doves in Brazil (22.3%) (Barros et al. 2014); pigeons in Lisbon, Portugal (70.7%) (Vilares et al. 2014) and in Lanzhou, Northwest China (11.86%) (Cong et al. 2012); and birds in southwest of Iran (16.5%) (Khademvatan et al. 2013) and southeast Brazil (22.2%) (Vitaliano et al. 2014). Seroprevalence could be affected by several factors, including feeding conditions and sensitivity of the different species, which possibly account for the large variation in prevalence between these studies. Moreover, the high seroprevalence of T. gondii infection in pigeons suggests that they are a potential zoonotic risk for human toxoplasmosis.

T. gondii is an opportunistic pathogen, and previous studies demonstrated that the seroprevalence of T. gondii antibody increases with host age (Afonso et al. 2010, Alvarado-Esquivel et al. 2012, Meng et al. 2015). This phenomenon was also seen in this study: Risk of infection in adults (12.63%) was around twice (OR = 2.12, 95% CI 1.25–3.60, p = 0.0005) that in juveniles (6.38%). This may be because adults had more opportunity to come into contact with T. gondii.

In this study, females had a higher T. gondii seroprevalence and appeared to be more susceptible to infection than males, a result consistent with previous studies (Roberts et al. 1995, Bai et al. 2017). However, our finding was different from the previous studies reported that no correlation between the gender and anti-T. gondii seropositivity was found in pigs (Alvarado-Esquivel et al. 2015, Gebremedhin et al. 2015).

As a zoonotic pathogen, T. gondii is easily transmitted via ingesting meat containing oocysts or/and tissue cysts (Zhang et al. 2018). Although there have been no reports to date of toxoplasmosis related to consumption of pigeon meat in China, it is important to remain vigilant, especially in northeastern China where consumption of pigeon meat is common. To better assess the zoonotic risk of pigeon meat, T. gondii should be isolated from pigeons and further studied.

In conclusion, this is the first article of the seroprevalence of T. gondii in pigeons in Jilin Province, Liaoning Province, and IMAR in China. We found that the seroprevalence of T. gondii increased with age and was higher in females. These findings could provide useful data for effective control measures against T. gondii infection in pigeons and/or other hosts. The findings also suggest that pigeons cannot be eaten raw.