Introduction

Miscarriage, stillbirth, premature birth, and low birth weight newborn are adverse pregnancy outcomes used as indicators for assessing the quality of maternal and child health services globally [1,2]. Among various other factors, these negative conditions can be caused by infection [3,4]. Many zoonotic pathogens including Toxoplasma gondii, Chlamydia sp., Brucella sp., and Coxiella burnetii can be transmitted from animals to pregnant women and lead to negative health consequences including adverse pregnancy outcomes [3–5]. One of the most important zoonotic disease reservoirs potentially impacting human health is domestic livestock, including cattle, camels, goats, and sheep. Small ruminants such as goats or sheep are reservoirs of many important zoonotic diseases, notably brucellosis caused by Brucella sp., coxiellosis caused by C. burnetii, and toxoplasmosis caused by T. gondii [6–8]. In endemic areas of these zoonotic pathogens, contact with infected animals and handling or ingesting raw animal products have been shown to be risk factors of these infections [9,10].

Several risk factors have been associated with human toxoplasmosis, particularly cat ownership and a history of raw meat consumption [11,12]. In pregnant women, infection with T. gondii can pose a serious risk for an adverse pregnancy outcome, including miscarriage, fetal anomaly, stillbirth, fetal growth restriction, and preterm birth [3,13]. Acute toxoplasmosis during pregnancy can also cause congenital toxoplasmosis [14]. A previous study found that women with a history of obstetric problems had a higher incidence of seropositivity for toxoplasmosis than women without any history of obstetric problems [15].

Brucellosis in humans is commonly caused by B. melitensis or B. abortus [16]. Milking animals and consumption of unpasteurized dairy products have been found to be risk factors for infecting human brucellosis [17,18]. Many studies have reported that brucellosis during pregnancy was a risk factor for obstetric complications, including congenital and neonatal infections [4,18,19]. A history of spontaneous abortion or intrauterine fetal death in pregnant women were associated with seropositivity for brucellosis [9].

Coxiellosis or Q fever in humans is primarily caused by inhalation of particles contaminated with birth secretions from an infected animal [20]. Occupational exposure to ruminants including goats is considered as a risk factor of human coxiellosis [21]. In pregnant women living in areas endemic for C. burnetii, coxiellosis during pregnancy has been associated with miscarriage and prematurity [22]. Additionally, another study reported that women with seropositivity for coxiellosis were more likely to have a previous or current obstetric complications [23].

Our study aimed to assess the seropositivities of immunoglobulin G anti-Toxoplasma gondii antibodies, immunoglobulin G anti-Brucella abortus antibodies and immunoglobulin G anti-Coxiella burnetii antibodies among pregnant women having adverse pregnancy outcomes in southern Thailand, and explore the associated factors with the seropositivities.

Methods

Results

The adverse pregnancy outcomes of the 105 included pregnant women were miscarriage (37.1%, 39/105), stillbirth (1.9%, 2/105), and premature birth or low birth weight newborn (61.0%, 64/105). Table 1 presents the demographic characteristics and related information of home animal and goat exposures. The mean age of the women was 27.9 ± 6 years. The majority were Muslim (91.4%). Half of them had graduated from secondary school and one-fifth of them were housewives. Seventy-five women (71.4%) had one or more home animals of which the most common was cats. One-third of them had experienced goat exposure with the majority of these involved in goat raising. The obstetric information of the women is presented in Table 2. Most women had attended their first ANC visit at gestational age of 12 weeks or less (86.7%) and two-thirds were multigravida (67.6%). Of the 105 women with current adverse pregnancy outcomes in our study, 32.4% had a prior history of one or more adverse pregnancy outcomes.

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Table 1. Demographic characteristics and pet ownership information including animal at home and goat exposures.

https://doi.org/10.1371/journal.pone.0216652.t001

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Table 2. Obstetric information.

https://doi.org/10.1371/journal.pone.0216652.t002

Thirty-six women with seropositive (34.3%) for antibodies against B. abortus, C. burnetii, or T. gondii. The seropositivity of IgG anti-T. gondii antibodies was highest (31.4%), followed by IgG anti-C. burnetii antibodies (1.9%), and IgG anti-B. abortus antibodies (1.0%) (Table 3). None of the women were found to be co-seropositive for antibodies against any of those three pathogens. Due to the small number of women with seropositivity for IgG anti-B. abortus and IgG anti-C. burnetii, the factors associated with being seropositive could be analyzed only for seropositivity for IgG anti-T. gondii. Women aged over 30 years or multiparous women were significantly more likely to show positive antibodies in univariate analysis, but there were no significant associations in the multiple logistic regression analysis (Table 4). The higher the woman’s age, the greater the odds ratios for positive antibodies in the dose-response relationship. Women with low education or who were a housewife were more likely to have higher odds of positive antibodies, but not to a significant level.

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Table 3. Seropositivities for IgG anti-Brucella abortus, Coxiella burnetii, and Toxoplasma gondii antibodies.

https://doi.org/10.1371/journal.pone.0216652.t003

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Table 4. Factors associated with seropositivity for IgG anti-T. gondii antibodies among pregnant women.

https://doi.org/10.1371/journal.pone.0216652.t004

Discussion

The seropositivity of IgG anti-T. gondii antibodies was more commonly found among the study women than IgG anti-C. burnetii and IgG anti-B. abortus antibodies, but with only a non-significant dose-response relationship between seropositivity for IgG anti-T. gondii and the age of the women. There was also a potential relationship between IgG anti-T. gondii seropositivity with low educational attainment and being a housewife.

Toxoplasmosis seroprevalence among women of reproductive age has been found to vary widely depending on geographical regions in the world. Globally, toxoplasmosis seroprevalence among women was reported at up to 60% regardless of pregnancy status [31,32]. In Thailand, two studies reported the overall seroprevalences in non-pregnant women were 2.6% and 2.8% [33,34]; however, other studies reported a wide variation among pregnant Thai women ranging from 5.3% to 22.0% [28,35–38]. In our study, the toxoplasmosis seroprevalence was higher than in those previous reports from Thailand, which could be explained by noting that the pregnant women in our study were women who had had an adverse pregnancy outcome.

The seropositivity for IgG anti-T. gondii antibodies was shown to increase with age, similar to the findings of previous studies [12,39], which can be explained by noting that the chance of being exposed to sources of T. gondii will naturally increase with age. The association of education with seropositivity of toxoplasmosis in previous studies varied [11,40–42]. The study in Ethiopia showed women with low educational attainment had significantly higher odds of seropositivity, while in contrast, women with higher educational attainment in Burkina Faso were also more likely to be seropositive [39,41]. In our study, women with low educational attainment had higher odds of seropositivity of toxoplasmosis, but the difference was not statistically significant, which was similar to a study from Ethiopia [42]. This variation could be explained by other related factors such as residential area of the women [43] or environmental exposure to T. gondii contaminated animals through either daily activities or occupation [41]. Housewives had non-significantly higher odds of positive antibodies against toxoplasmosis than other occupation groups, similar to a previous study [11], which may be related to higher contact with raw animal products, especially meat, during food processing at home.

Very low seroprevalences of coxiellosis and brucellosis among pregnant women were found in our study (1.9% and 1.0%, respectively). This was a similar finding in animal that the seroprevalence of animal coxiellosis and brucellosis in Thailand were low as reported by previous studies (3.9% and 1.5%, respectively) [25,44]. In contrast, previous studies conducted among people having a livestock-related occupation in Thailand found that the seroprevalences of coxiellosis and brucellosis were 42.8% and 8.8%, respectively [44,45]. This may be due to the fact that the women participating in our study were not in animal-related occupations conferring a higher risk for the studied diseases. Thus, the exposure to raw animal products, including both meat and dairy products or occupational exposure to livestock, should be considered as the more important significant potential risk factor for coxiellosis and brucellosis.

This is the first study to measure the seropositivities of toxoplasmosis, coxiellosis and brucellosis in pregnant women who had adverse pregnancy outcomes in Thailand. There were some limitations to the study. First, the seropositivity tests for all three diseases were based on single serum samples collected at the first ANC visit, not paired serum samples, in detection of acute infection using IgG status. The seropositivities for toxoplasmosis, coxiellosis and brucellosis as found in our study could reflect a past exposure with the pathogens among the women. Second, the sample size was too small to explore the associations between seropositivities and potential risk factors as in the second objective because the sample size calculation was determined according to a prevalence study for the first objective. Finally, the study setting was an area where goat rearing is common, thus the findings are not generalizable to pregnant women in other settings, but our findings can still be useful as baseline information for antenatal care in settings where animal rearing, particularly goat rearing, is common, and also help to increase awareness of zoonotic diseases affecting maternal and newborn health.

In conclusion, one-third of women with adverse pregnancy outcomes showed positive antibodies for toxoplasmosis, while coxiellosis and brucellosis were less common. For toxoplasmosis seropositivity, a dose-response relationship with age was detected, and low educational attainment and being a housewife were found to be associated risk factors.

Supporting information

Acknowledgments

This study was part of the first author’s thesis in partial fulfillment of the requirements for a Ph.D. at Prince of Songkla University, Thailand. The authors thank the Songkhla Provincial Public Health Office, as well as District Public Health Offices including Thepa District, Na Thawee District, Sabayoi District, and Chana District for providing collaboration in our contact with District Hospitals, Primary Care Units, and Health Promotion Hospitals in the four study districts. The authors also acknowledge all healthcare providers, health volunteers, and laboratorians in all study settings for their kind assistance in the collection of questionnaires, blood samples, and follow-up data.