Research Article: Endemicity of Toxoplasma infection and its associated risk factors in Cebu, Philippines

Date Published: June 12, 2019

Publisher: Public Library of Science

Author(s): Rochelle Haidee D. Ybañez, Chadinne Girlani R. Busmeon, Alexa Renee G. Viernes, Jorim Z. Langbid, Johanne P. Nuevarez, Adrian P. Ybañez, Yoshifumi Nishikawa, Adriana Calderaro.

http://doi.org/10.1371/journal.pone.0217989

Abstract

Toxoplasma gondii is a single-celled intracellular apicomplexan parasite that causes toxoplasmosis. It is capable of infecting humans and nearly all warm-blooded animals including pigs, but cats are the only known definitive host. This ubiquitous zoonotic pathogen can cause abortion, stillbirth and fetal abnormalities, and has been associated with mental and behavioral changes in humans. Acute infection is potentially fatal in immunocompromised individuals. The present study aimed to assess the Toxoplasma seroprevalence in pigs, humans and cats after its initial reported detection in pigs about three decades ago in Cebu, Philippines. A total of 924 humans, 104 cats and 514 slaughter pigs were tested for antibodies against T. gondii using a commercial latex agglutination test. The results revealed positive detection rates of 26.3% (244/924) for humans, 42.3% (44/104) for cats and 13.4% (69/514) for slaughter pigs. Statistical analyses revealed that the area (P = 0.004), cat ownership (P = 0.020), the frequency of contact with cats (P < 0.0001) and consumption of street foods (P = 0.043) were significantly associated with seropositivity for T. gondii in humans. Meanwhile, the use of litter trays (P = 0.001) and contact with other animals (P = 0.007) were significantly associated with seropositivity in cats. The odds ratio for selected significant factors revealed that living in suburban areas (OR 1.66, 95% CI: 1.20–2.31), owning a cat (OR 1.482, 95% CI: 1.07–2.07) and eating street foods (OR 1.585, 95% CI: 1.01–2.48) were associated with an increased risk of T. gondii exposure in humans. In cats, the use of a litter tray (OR 4.5, 95% CI: 1.73–11.71) was associated with an increased risk of exposure. None of the profile parameters were found to be significantly associated with seropositivity in slaughter pigs (P > 0.05). This study is the first report of the serological detection of T. gondii in humans and cats in Cebu, Philippines, and the first assessment of the prevalence of the parasite in pigs in the area since its initial detection in 1982. This is also the first report documenting the seropositivity of T. gondii in pregnant women in the country. The confirmed seropositivity of T. gondii in Cebu, Philippines, in the present study implies the endemicity of toxoplasmosis in this area and highlights the need for routine testing and increased public awareness.

Partial Text

Toxoplasmosis is a public health problem worldwide. It is caused by Toxoplasma gondii, an obligate, intracellular, parasitic protozoan. It is zoonotic and is capable of infecting nearly all warm-blooded animals including humans, but cats are the only known definitive host. T. gondii reproduces in the gut of felids. After reproduction, the oocysts are shed through the feces. These environmentally-resistant oocysts can then contaminate the soil, which may be ingested by an intermediate host, such as rodents, birds or other warm-blooded animals [1]. This parasite can cause infections in humans following the ingestion of raw meat infected with tissue cysts, food or drink contaminated with oocysts, or by direct assimilation from the environment [2,3]. Vertical transmission from the infected mother to the fetus may also occur [4]. T. gondii infections in humans are generally asymptomatic or are manifested by flu-like symptoms and lymphadenopathy [5]. In young children, pregnant women, congenitally-infected fetuses and newborns, and immunocompromised people such as those with HIV/AIDS, those undergoing chemotherapy or those who have received an organ transplant, toxoplasmosis may be severe [2,6]. In most livestock animals such as poultry, pigs, and cattle, clinical toxoplasmosis is rare [2]; however, just like in humans, it mostly affects the young and fetuses. Thus, it is considered one of the most common zoonotic infections causing abortions in both humans and female animals [7–8]. Clinical signs rarely present themselves in infected cats, and if present, are caused by tissue inflammation and necrosis induced by the intracellular growth of tachyzoites [9]. Like most human and animal cases, congenital infections in cats are more severe than in adults [9–10].

Out of 924 participants, 244 (26.4%) were found to be seropositive (Table 1) from 21 different municipalities and cities in Cebu (Fig 1). Seropositivity was found to be greater among women (27%) than men (25.5%); however, sex was not found to be significantly associated with T. gondii seropositivity (P = 0.611). Students (28%) and respondents with non-health-related occupations (24.2%) were found to have higher seropositivity rates than health-related professionals (18.9%). Additionally, more seropositive participants had pet cats (35.2%) or were in frequent contact with these animals (45.4%). A higher proportion of seropositive individuals were suburban residents (35.1%) and consumed street foods (27.6%). Statistical analyses revealed no significant differences in seropositivity associated with sex or age. Furthermore, the respondents’ occupation was not significantly associated with seropositivity (P = 0.060). However, living in a suburban area (P = 0.002), cat ownership (P = 0.021), frequent contact with cats (P < 0.0001) and consumption of street foods (P = 0.044) were all found to be significantly associated with seropositivity to T. gondii in humans (Table 1). These factors were associated with an increased risk of being seropositive for T. gondii in humans with odds ratios of 1.66 (95% CI 1.20–2.31), 1.48 (95% CI 1.07–2.07), 2.43 (95% CI 1.73–3.42) and 1.58 (95% CI 1.01–2.48), respectively. Of the pregnant women tested in this study, 4 out of 18 (16.7%) were seropositive for T. gondii antibodies. The seroprevalence of T. gondii in humans in this study (26.4%) was slightly lower than the previously reported detection level (27.1%) in the Philippines using the same detection method [20]. Another report in the country showed a lower detection rate using ELISA on samples from Metro Manila (11.1%), but higher rates for Mindoro (61.2%) and Leyte (30.1%) [33]. The higher seropositivity rates among women in this study (27.0%) were similar to the findings of Salibay et al. [20] that reported 32% seropositivity. However, sex was not found to be significantly associated with seropositivity in previous or current studies in this country. The 16.7% detection rate among pregnant women in this study was comparable to that of previous studies in pregnant women in Singapore, which showed a prevalence of 17.2% [36], and in Vietnam with a seroprevalence of 11.2% [37], using immunofluorescent antibody test (IFAT) and ELISA, respectively. In Thailand, a slightly higher seroprevalence of 22% was reported in 2014 using ELISA [38]. Using the same method, 7.7% seropositivity was recently published in Taiwan [39], which is lower than that detected in the present study. However, the number of pregnant women tested was low, which is also a limitation of the current study. All of the above-mentioned reports did not find any significant association between seropositivity and risk factors, with the exception of the study by Andiappan et al. [38] that reported age, occupation (as laborers) and drinking water source as significant risk factors for Toxoplasma seropositivity in pregnant women in Thailand (P < 0.05). The present study reports the first serological detection of T. gondii in humans and cats in Cebu, Philippines, and the most recent serological status update in pigs since 1982 in the area. To the best of our knowledge, this is also the first report documenting serodetection of T. gondii in pregnant women in the country. The confirmed seropositivity of T. gondii in Cebu, Philippines, in the present study implies the endemicity of this disease in the area and highlights the need for increased public awareness in the country. Routine testing may be recommended for vulnerable populations, including pregnant women, immunocompromised individuals and those exposed to cats. An educational campaign about toxoplasmosis is needed to increase awareness among the public.   Source: http://doi.org/10.1371/journal.pone.0217989