https://orcid.org/0000-0003-0355-5063
Figures
Abstract
This study assessed the prevalence of co-infections (human immunodeficiency virus, hepatitis B, and syphilis) and associated risk factors for Toxoplasma gondii infection among pregnant women in Mampong Municipality, Ghana. A cross-sectional design was used to recruit 201 pregnant women from six health facilities conveniently. Participants’ socio-demographics, clinical and environmental data were collected using a structured questionnaire. Using 2 ml of blood, T. gondii seroprevalence was determined by the TOXO IgG/IgM Rapid Test Cassette. Data was analyzed using descriptive and logistic regression analysis with SPSS version 27 to determine the prevalence and associations of T. gondii infection with other variables, respectively. The seroprevalence of T. gondii was 49.75%, of which 40.30%, 2.49%, and 6.97% tested positive for IgG, IgM, and IgG/IgM, respectively. Co-infection of toxoplasmosis with viral hepatitis B, human immunodeficiency virus (HIV), and syphilis rates were 15%, 1%, and 4%, respectively and were not risk factors for T. gondii transmission. Educational level and residential status were associated with toxoplasmosis [p < 0.05]. Participants with higher education had a reduced risk of T. gondii infections compared to a lower level of education [AOR = 0.39 (0.13, 0.99) p = 0.049]. Similarly, the risk of T. gondii infection was significantly lower among individuals residing in peri-urban [AOR = 0.13 (0.02–0.70), p = 0.02] and urban areas [AOR = 0.10 (0.02–0.78), p = 0.03] compared to those in rural areas. Backyard animals with extensive and semi-intensive systems, without veterinary care, and contact with animal droppings and water sources were significant risk factors for T. gondii infection [p < 0.05]. Miscarriage was associated with T. gondii infection [p < 0.05]. The burden of T. gondii infection was high among the study population, posing a risk of mother-to-child transmission. Key risk factors included low education, rural residence, backyard animal exposure, poor hygiene, and unsafe water sources. Toxoplasmosis was associated with miscarriage; thus, integrating it into routine antenatal screening could improve pregnancy outcomes. Health promotion interventions such as education on zoonotic risks, improved sanitation, safe water practices, and veterinary care for domestic animals are recommended to reduce infection risk among pregnant women.
Citation: Assoah E, Yar DD, Amissah-Reynolds PK, Balali GI, Addy R, Zineyele JK (2025) Co-infections and risk factors of Toxoplasma gondii infection among pregnant women in Ghana: A facility-based cross-sectional study. PLoS One 20(5): e0324950. https://doi.org/10.1371/journal.pone.0324950
Editor: Masoud Foroutan, Abadan University of Medical Sciences, IRAN, ISLAMIC REPUBLIC OF
Received: March 10, 2025; Accepted: May 3, 2025; Published: May 28, 2025
Copyright: © 2025 Assoah et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Globally, parasitic zoonoses are on the rise, affecting more than 4 billion people, with over 200,000 deaths recorded annually [1,2]. In low-income countries, neglected parasitic diseases such as ascariasis, amebiasis, giardiasis, toxoplasmosis, etc., continue to cause significant public health challenges, with enormous morbidity and mortality [3]. Toxoplasma gondii is known to infect vertebrate animals and humans [4,5], with 25.7% and 33.8% reported among the general human population and pregnant women, respectively [6,7]. The most significant burden is in developing countries, linked to poor sanitation and a lack of quality health services [7–10]. Children and pregnant women are generally more vulnerable to T. gondii infection due to their weaker immunity [11]. Pregnant women infected with T. gondii in the first trimester can invade the placenta, causing inflammation and damage to arteries and veins that may block the flow of blood and nutrient exchange between the mother and fetus, resulting in spontaneous abortion [12]. Meanwhile, T. gondii infection in the second and third trimesters may cause congenital toxoplasmosis, leading to mental retardation, auditory defects, and chorioretinitis [13,14].
In Ghana, policies for screening expectant mothers exist for a range of maternal infections with potential for vertical transmission such as viral hepatitis, HIV/AIDS, syphilis and malaria, to improve pregnancy outcomes and neonatal health [15,16]. The prevalence of toxoplasmosis among pregnant women in Ghana is among the highest in the world (81–90%), with possible dire consequences on pregnancy outcomes [7,17]. Nevertheless, there is no policy for T. gondii screening during pregnancy in the country. However, in Europe (Austria, France, and Slovenia), mandatory national policies for prenatal serological screening and treatment for T. gondii infection have significantly reduced congenital toxoplasmosis [18]. Early detection and administration of anti-Toxoplasma prophylaxis during pregnancy prevent congenital transmission and reduce sequelae in neonates [18].
Over the past two decades, significant progress has been made in maternal health in Ghana. Notwithstanding, maternal and neonatal morbidity and mortality are still on the increase, attributable to failure to screen and treat these diseases, including toxoplasmosis [19]. Several studies have assessed the prevalence of T. gondii infection among expectant mothers, with limited focus on its comorbidity with maternal infections and its transmission dynamics in Ghana [17,20]. Meanwhile, data on miscarriages among pregnant women over the last decade in the Mampong Municipality is on the rise [21]. However, the proxy determinants of the high miscarriage rates are uncertain and could be linked to toxoplasmosis and co-infections [22].
There is limited literature on the causal relationship between transmission dynamics and co-infection of T. gondii with HIV, viral hepatitis B, and syphilis in pregnancy in the Municipality. Hence, this study investigated the prevalence of co-infections (HIV, hepatitis B, and syphilis) and associated risk factors for T. gondii infection among pregnant women in Mampong Municipality, Ghana.
2. Materials and methods
Study design
This was a facility-based cross-sectional study that assessed the burden and concurrence of Toxoplasma gondii infection with HBV, HIV, and syphilis among pregnant women attending antenatal care (ANC) services in health facilities. The study also examined the risks of T. gondii transmission in the Mampong Municipality. Following the approval of the study on 11th August 2023, participant recruitment and data collection commenced on 15th August 2023 and concluded on 15th May 2024.
Study area
This study was conducted in the Asante Mampong Municipality of the Ashanti Region of Ghana. The study was conducted in six health facilities in five communities, with Mampong as its capital town, Dadease, Krobo, Asaam, and Kofiase. The municipality has a total population of 116,632, with females slightly more than males [23]. The municipality has an average temperature of 28°C with a relative humidity of 63% [23]. The main economic activity in the municipality is agricultural activities, including animal farming, engaging around 67.30% of the workforce [23,24]. Most households in the Municipality own domesticated animals, such as sheep, goats, poultry, cattle, cats, and dogs.
Study site
Data for the study were collected from the various health facilities with maternal and laboratory departments in the municipality. Mampong Government Hospital-Maternity Home, Calvary Health Center, Sister Phillipah Maternity Home and Clinic, Krobo-Dadease Health Center, Asaam Health Center, and Kofiase Health Center were used for the study, which has most pregnant women attending ANC. These facilities were purposefully chosen based on their distinct characteristics that would ensure balanced urban and rural data to reduce bias. The facilities were categorized into government and private hospitals, health centres, and clinics. This approach consequently yielded a substantial dataset suitable for making inferences.
Study population and sample size
Pregnant women of reproductive age (15–49 years) visiting the six selected health facilities for prenatal care and related services in the Mampong municipality were included in the study. Participants who had undergone laboratory and ultrasonography tests confirming their pregnancy and had lived in the study area for at least six months were recruited for the study. A sample size of 201 was estimated based on the toxoplasmosis prevalence rate of 92%, using Cochran’s formula as previously described [25,26].
Data collection tools and techniques
A structured questionnaire consisted of four sections, including socio-demographic characteristics such as age, religion, education, and residential status; obstetric variables such as trimester and gravidity; laboratory test results such as HBV, HIV, and syphilis; and environmental variables such as water sources and the presence and confinement levels of backyard farm animals, and pets. The study participants attending antenatal care were conveniently sampled at all the selected health facilities.
Data collection procedure
After obtaining informed consent, face-to-face interviews and observational methods were used to gather data from participants using a structured questionnaire. Information on socio-demographic characteristics, environmental exposures, and obstetric history was collected. In addition, routine screening test results recorded in the participants’ antenatal care (ANC) record books were reviewed and extracted.
All 201 participants were screened for T. gondii using the TOXO IgG/IgM Rapid Test Cassette. However, only 178, 156, and 163 participants had been tested for hepatitis B virus (HBV), HIV, and syphilis, respectively, at the time of data collection. These tests are part of the routine ANC screening; however, some participants reported that they were unable to complete all required tests due to financial constraints. This limitation was considered during data analysis, and missing values were handled appropriately.
Blood sample collection and laboratory methods
A 2 ml of each participant’s blood was collected using venipuncture and into EDTA tubes. This was centrifuged at 1780 x g for 10 minutes at 40C to separate plasma for subsequent serological analysis. The plasma was promptly assayed for anti-T. gondii IgG and IgM antibodies using the immunochromatography Test (ICT) technique. The specific ICT used was the TOXO IgG/IgM One-Step Rapid Test Cassette (WB/S/P) produced by Evancare Medical (Nantong) Co., Ltd. (China). This assay employs a lateral flow chromatographic immunoassay for the simultaneous detection and differentiation of IgG and IgM anti-T. gondii in human serum, plasma, or whole blood. Testing procedures were strictly followed according to the manufacturer’s instructions [27].
Statistical analysis
Data were entered into Microsoft Excel (version 2016) and exported into IBM SPSS version 27.0 for statistical analysis. All variables used in the analysis were categorical in nature. Some variables, such as T. gondii, HBV, HIV, syphilis test results and other risk factors were binary (e.g., positive/negative), while others like age group, education level, and other variables had more than two levels.
Descriptive statistics were applied to determine the frequencies and percentages of T. gondii, HBV, HIV, syphilis, and other socio-demographic and environmental characteristics. The co-infection rate was calculated by dividing the number of individuals positive for both T. gondii and any of the ANC-related infections (HBV, HIV, or syphilis) by the total number of T. gondii-positive individuals, and expressed as a percentage:
Chi-square test of independence and binary logistic regression were used to assess the association between T. gondii infection and other variables. Prior to conducting logistic regression, model fitness was evaluated using the Hosmer-Lemeshow goodness-of-fit test (p > 0.05 indicating good fit). Additionally, the Nagelkerke R² statistic and the model’s classification accuracy were examined to assess the model’s explanatory power and predictive ability.
For the multivariate logistic regression analysis, all variables with a p-value less than 0.2 in the univariate analysis were considered for inclusion. Variables with more than two levels were included as categorical factors using dummy coding in SPSS. Variables of known epidemiological importance were also retained in the final model regardless of statistical significance. A p-value < 0.05 and a 95% confidence interval were used to determine statistical significance.
Ethical review and clearance
The study received ethical approval from the Committee on Human Research, Publications, and Ethics (CHRPE) of the Kwame Nkrumah University of Science and Technology, under reference number CHRPE/AP/717/23. Following ethical clearance, official permissions were obtained from the Ashanti Regional and Asante Mampong Municipal Health Directorates, as well as from the respective health facilities where the research was conducted.
Before data collection began, each participant was given a detailed verbal explanation of the study’s objectives, procedures, potential risks, and benefits. They were also informed of their right to voluntary participation and their freedom to withdraw from the study at any time without any consequences. After this briefing, participants who agreed to take part signed a written informed consent form, confirming their voluntary participation.
3. Results
Seroprevalence of T. gondii
The prevalence of T. gondii infection among the participants was 49.75% (100/201), of which 40.30% (81/201), 2.49% (5/201), and 6.97% (14/201) tested positive for IgG, IgM, and IgG/IgM, respectively (Fig 1).
Prevalence of Hepatitis B, HIV and syphilis among pregnant women in Asante Mampong Municipal of Ghana
In Table 1, the prevalence of HBV, HIV, and syphilis among pregnant women screened during ANC was 14.61%, 0.61% and 3.07%, respectively. There were variations in the sample sizes occasioned by the non-availability of routine screening tests at the ANC clinics for these routine ANC tests.
Toxoplasmosis concurrence with HBV, HIV, and syphilis screened among participants
Table 2 shows the prevalence of co-infection of toxoplasmosis with HBV, HIV, and syphilis were 15%, 1%, and 4%, respectively. T. gondii infection was not associated with the HBV, HIV, and Syphilis screened at ANC (P-value > 0.05).
Association of T. gondii infection with sociodemographic characteristics of participants
In Table 3, the level of education and residential area were significantly associated with T. gondii infection (χ2 = 6.56, p = 0.04) and (χ2 = 10.97, p = 0.004), respectively. Participants with tertiary education were less likely to be infected with T. gondii infections than those with lower levels of education [AOR = 0.39 (0.13–0.99) p = 0.049]. Expectant mothers who reside in the peri-urban and urban areas were less likely to be infected with T. gondii as compared with rural residents [AOR = 0.13 (0.02–0.70) p = 0.02; AOR = 0.10 (0.02–0.78) p = 0.03]. Age, religion, gestational period, and gravida were not associated with toxoplasmosis (P-value > 0.05).
Risks factors of T. gondii infection among pregnant women
Table 4 shows that participants with backyard animals, with the extensive and semi-intensive system, without veterinary care, and contact with animal faeces had significant odds of being infected with T. gondii [AOR = 3.90 (1.60–9.48) p = 0.003], [AOR = 31.7 (20.90–8921.3) p < 0.001]; AOR = 5.2 (3.37–367.70) p = 0.003], [AOR = 2.90 (1.10–7.46) p = 0.031], and [AOR = 3.90 (1.81–8.35) p = 0.001], respectively, whereas the use of disposable gloves to hand animals’ faeces significantly reduced the odds [AOR = 0.05 (0.002–0.91) p = 0.043]. Table 4 further shows that participants using river, stream, or well water had 2.91 times the odds of being infected with T. gondii infections [AOR = 2.91 (1.07–7.92) p = 0.037], whereas participants who treated their water before drinking had less risk of the infection [AOR = 0.26 (0.10–0.70) p = 0.008]. There was no association between eating undercooked animal meat and drinking unpasteurized milk with T. gondii infections (P-value > 0.05). It should be noted that response totals for certain variables may be less than 100 due to skip logic in the questionnaire design, where only applicable participants responded to follow-up questions.
Association between toxoplasmosis and obstetric factors
Table 5 shows that pregnant women with T. gondii infection were associated with miscarriage (χ2 = 6.1, p = 0.014). Participants who had ever had a miscarriage were 2.93 times more likely to be infected with T. gondii [AOR = 2.93 (1.20–7.04), p = 0.016]. It should be noted that response totals for certain variables may be less than 100 due to skip logic in the questionnaire design, where only applicable participants responded to follow-up questions.
4. Discussion
Seroprevalence of T. gondii
The seroprevalence of T. gondii infection in this study was 49.75% among pregnant women. This finding is consistent with previous studies conducted in Ghana, which reported seroprevalence rates ranging from 50% to 56% among pregnant women attending health facilities [20,28,29]. However, some studies conducted in other regions of Ghana have reported significantly higher prevalence rates, exceeding 76% [30–32]. These within-country variations may be attributed to differences in geographic settings, urban–rural residency, levels of sanitation, pet ownership, access to veterinary services, and socioeconomic conditions. The relatively lower prevalence in the current study could reflect better hygienic practices or improved awareness in the study area compared to regions with higher reported prevalence.
In contrast, when comparing with studies from other countries, the seroprevalence reported in this study was higher than findings from Ethiopia (35.6%) in different settings [33], but relatively lower than rates reported in Western Romania (55.8%) and Brazil (71%) [34,35]. These international disparities may result from differences in climate, dietary habits (such as consumption of undercooked meat), environmental exposures, and public health infrastructure. Additionally, methodological differences such as serological testing tools, sample sizes, and study designs can influence prevalence rates across countries [36,37].
The current study also found that participants residing in rural areas and those with lower socioeconomic status were more vulnerable to T. gondii infection, likely due to poorer sanitation, limited access to clean water, and close contact with animals. Key risk factors included poor management of pets and backyard livestock, lack of veterinary care, and exposure to contaminated water sources, all of which are more common in rural settings [38,39].
Importantly, approximately 10% of participants had acute infection, with about 3% being seronegative (naïve), suggesting a high potential risk of mother-to-child transmission of T. gondii, which can have serious implications for fetal development and pregnancy outcomes [20,40,41].
Prevalence of HBV, syphilis and HIV Screened at ANC among the participants
Ghana, over the years, has formulated policies for screening expectant mothers for viral hepatitis, HIV/AIDS, syphilis, and malaria to improve pregnancy outcomes and neonatal health [15,16]. Nevertheless, this study reported a high prevalence of 14.61%. 3.07% and 0.61% for hepatitis B, syphilis, and HIV infections, respectively, among the participants.
The rate of viral hepatitis B (HBV) infection was much higher than in previous studies in Ghana which reported between 2.4% and 10.6% among pregnant women [42–50]. These disparities in HBV prevalence among pregnant women in Ghana could be attributed to the different settings and cultural and behavioural characteristics of the participants [51]. In 2002, Ghana initiated a national expanded program for hepatitis B immunization [52] in response to the WHO target to eliminate HBV infection by 2030 [53,54]. However, this current rate of HBV infection suggests a low vaccine uptake, and the 2030 target may not be achieved. This current rate presents a high risk for mother-to-child transmission, which is the main route of HBV infection, including sexual and other behavioural characteristics [52,55].
The seroprevalence of syphilis was 3.07% among the participants, well aligned with the 3.7% and 4.1% reported among pregnant women at the Cape Coast Metropolitan Hospital [56] and gold miners in Konongo [57] in Ghana. This rate is, however, higher than 0.4%, previously reported in the general population [58]. Several studies have also reported syphilis among pregnant women: 2.5% in Tanzania [59], 1.9% in Ethiopia [60] and 4.4% in Brazil [61]. These prevalence rates somewhat differ from value reported in our study. The variations in these rates may be associated with several factors, including sexual behaviours, lifestyle factors, availability and access to screening services, and cultural and geographical settings [62].
This current study reported a 0.61% HIV infection rate, much lower than the 1.89%, 1.91%, and 1.66% among the adult population, in the Asante Mampong municipal, Ashanti region and the nation, respectively [63]. The current study result is at variance with 2.8% reported among pregnant women in the Asante Municipality in an HIV Sentinel survey [58]. The low HIV prevalence in this current study could be due to several causes, including the small number of participants screened, the sample size, and the data collection duration. This study observed a very low screening rate for HIV among the participants, and this can be a drawback for the zero-prevalence expected among mothers.
Toxoplasmosis concurrence with HBV, HIV, and syphilis screened at ANC
This study reported 15%, 1%, and 4% T. gondii concurrence with HBV, HIV, and syphilis, respectively, among the population. Although these co-infections were observed, no statistically significant association was established between T. gondii infection and any of HBV, HIV, and syphilis screened [64]. This suggests that the observed co-occurrences may be incidental rather than indicative of synergistic interactions or shared transmission pathways.
Nonetheless, the clinical implications of co-infections, particularly during pregnancy, warrant further attention. For instance, co-infection with HIV has been shown in other studies to impair immune responses, potentially increasing the susceptibility to opportunistic infections such as toxoplasmosis and worsening pregnancy outcomes [65–67]. A study in Tanzania reported that toxoplasmosis co-infection could increase mortality among people living with HIV [68]. Although our study did not find such an association, the low HIV prevalence in our sample may have limited the statistical power to detect this relationship.
Given the potential implications of co-infections on maternal and neonatal health, this finding reinforces the need for independent and comprehensive screening protocols for T. gondii, HBV, HIV, and syphilis as part of routine antenatal care. Preventive strategies should be tailored to address each condition separately while also considering their possible interactions in immunocompromised individuals.
It is important to note that this study was conducted exclusively within the Asante Mampong Municipality, which may limit the generalizability of the findings to other regions of Ghana or populations with differing socio-economic or epidemiological profiles. Future studies with broader geographic coverage and larger sample sizes are recommended to explore regional variations and more comprehensively assess the dynamics of co-infections in pregnancy.
Association of T. gondii infection with socio-demographic characteristics of participants
Although the prevalence of T. gondii decreases with increasing age in consonance, as in previous studies in Italy [69] and Pakistan [70], there was no association. However, this finding contradicts earlier reports in Nigeria [71], the USA [72], and the UK [73], which associated increasing age with T. gondii infection. The sharp difference could be attributable to our study’s generally younger population of women in their reproductive age.
The findings in this study demonstrated that respondents’ educational status and residential area were associated with T. gondii infection, as earlier reported [74]. Participants with primary or informal education had an increased risk of T. gondii infection in consonance with a report from Ethiopia [75]. Rural dwellers had an increased risk of infection than urban residents, probably due to the inadequate and deplorable social amenities and environmental factors [76]. The plausible reasons for the increased risk of T. gondii infection among participants with low education and rural residents may be due to their generally low socio-economic status, limited knowledge of the disease transmission, exposure to backyard animals and pets, and limited access to health facilities, and screening and treatment [77–79].
Transmission dynamics of T. gondii infection among pregnant women
This study has shown that the presence of backyard farm animals in households, their levels of confinement, exposure to faecal droppings, and veterinary care services were significant risk factors for T. gondii transmission. Cat is the primary host of T. gondii, with several other domestic animals as secondary and mechanical hosts [80], and their interaction with humans can transmit the parasites through their fur, saliva, or faeces [81]. This assertion is affirmed by previous studies that implicated the interaction of domesticated cats and dogs as a risk of T. gondii transmission to humans [82,83]. This study also revealed that backyard animal husbandry practices increase the risk of T. gondii infection. The free-range backyard animal-rearing practice is more associated with rural households with little or no veterinary care, increasing the risk of T. gondii transmission. These animals could contaminate the environment with their faeces, which contain parasites and pose a risk to humans. In this study, contact with animal faeces increased the risk of T. gondii infection four-fold. This implies that droppings and litter from animals in the environment and poor hygiene practices can facilitate the transmission of T. gondii to humans [84]. However, using personal protective equipment to handle animals’ faeces highly reduced the risks of T. gondii infection.
In this study, the consumption of animal products was not associated with T. gondii infection, contrary to an earlier report [64] that linked eating meat and other animal products to the infection [85]. This study has shown that there is a three-fold increased risk of T. gondii infection in drinking water from rivers, streams, or wells, akin to a study in Brazil [86]. Livestock often share rivers and streams with humans and are most likely contaminated with faecal droppings containing T. gondii oocysts. The tachyzoite and bradyzoite forms of the parasite can persist in water and be accidentally ingested. However, treating water before drinking decreases the risk of T. gondii infection.
Effect of toxoplasmosis on pregnancy outcomes
This study has indicated that T. gondii infection was significantly associated with a higher risk of miscarriage among participants. Participants who were seropositive for toxoplasmosis had a threefold increased risk of miscarriages. T. gondii infection increases the risk of miscarriage due to its invasion of the placenta, causing inflammation and damage and leading to spontaneous expulsion of the fetuses [12]. This assertion aligns with several studies that linked T. gondii infection with spontaneous abortion [87–89]. The study findings highlight the public health significance and call for concerted efforts to integrate T. gondii screening with other co-infections to improve pregnancy outcomes.
Limitation of the study
The sample size of this study was relatively small compared to the study population and may fail to capture the diversity of the population. The serological method was only used to determine the status of T. gondii infection without confirmatory tests, such as PCR or avidity tests, with its inherent limitations. The study participants’ responses may suffer from recall bias, compromising their reports. This was a health facility-based study and could influence participants’ responses. The test results of the co-infections were based on those reported by the facility and were subject to inaccuracies. Notwithstanding these limitations, the outcomes of this study are relevant for public health policy consideration that could improve maternal and neonatal healthcare services.
5. Conclusion
The burden of toxoplasmosis and concurrence with HBV and syphilis was high among pregnant women, but they were not at risk for its transmission. Low levels of education, living in rural areas, animals in households, little or no veterinary services, and drinking water from rivers significantly influenced the transmission of T. gondii. An infection with T. gondii in pregnancy significantly increases the risk of miscarriage. Toxoplasmosis was associated with miscarriage; thus, integrating it into routine antenatal screening could improve pregnancy outcomes. Health promotion interventions such as education on zoonotic risks, improved sanitation, safe water practices, and veterinary care for domestic animals are recommended to reduce infection risk among pregnant women.
Acknowledgments
We sincerely acknowledge the invaluable contributions of Olivia Ndele, Uginabor Jonathan Matani, Lambon Isaac, Tikpinja Moses, Bright Bindink Kididisil, Beatrice Ellen, and Adam Kofi Jamiru, former Public Health students of the Akenten Appiah-Menka University of Skills Training and Entrepreneurial Development (AAMUSTED), Asante Mampong Campus. Their dedication to data collection and entry of responses into Google Forms during their voluntary attachment at the health facilities was instrumental to this study. We are also deeply grateful to Mr. Richard Sombeley Assoah and Madam Ndaayaa Margaret Kweasi, the brother and mother of the lead author (Ebenezer Assoah), respectively, for their support throughout the course of this study.
References
- 1. Algabbani Q. Nanotechnology: a promising strategy for the control of parasitic infections. Exp Parasitol. 2023;250:108548.
- 2. Hossain MS, Hatta T, Labony SS, Kwofie KD, Kawada H, et al. Food- and vector-borne parasitic zoonoses: global burden and impacts. Adv Parasitol. 2023;120:87–136. pmid:36948728
- 3. Bekele D. A review on the relationship between nutrition and health condition in humans. Arch Nutr Public Health. 2020;3.
- 4. Augusto L, Martynowicz J, Amin PH, Carlson KR, Wek RC, Sullivan WJ Jr. TgIF2K-B is an eIF2α kinase in Toxoplasma gondii that responds to oxidative stress and optimizes pathogenicity. mBio. 2021;12(1):e03160-20. pmid:33500345
- 5. Yan C, Liang L-J, Zheng K-Y, Zhu X-Q. Impact of environmental factors on the emergence, transmission and distribution of Toxoplasma gondii. Parasit Vectors. 2016;9:137. pmid:26965989
- 6. Molan A. Global status of Toxoplasma gondii infection: systematic review and prevalence snapshots. Trop Biomed. 2019;36(4):898–925.
- 7. Rostami A, Riahi SM, Gamble HR, Fakhri Y, Nourollahpour Shiadeh M, Danesh M, et al. Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis. Clin Microbiol Infect. 2020;26(6):673–83. pmid:31972316
- 8. Tarekegn ZS, Dejene H, Addisu A, Dagnachew S. Potential risk factors associated with seropositivity for Toxoplasma gondii among pregnant women and HIV infected individuals in Ethiopia: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2020;14(12):e0008944. pmid:33320848
- 9. Montazeri M, et al. The global serological prevalence of Toxoplasma gondii in felids during the last five decades (1967–2017): a systematic review and meta-analysis. BMC Infect Dis. 2020;13:1–10.
- 10. Bigna JJ, Tochie JN, Tounouga DN, Bekolo AO, Ymele NS, Youda EL, et al. Global, regional, and country seroprevalence of Toxoplasma gondii in pregnant women: a systematic review, modelling and meta-analysis. Sci Rep. 2020;10(1):12102. pmid:32694844
- 11. Gómez-Chávez F, Cañedo-Solares I, Ortiz-Alegría LB, Flores-García Y, Figueroa-Damián R, Luna-Pastén H, et al. A Proinflammatory immune response might determine Toxoplasma gondii vertical transmission and severity of clinical features in congenitally infected newborns. Front Immunol. 2020;11:390. pmid:32231666
- 12. Borges M, Magalhães Silva T, Brito C, Teixeira N, Roberts CW. How does toxoplasmosis affect the maternal-foetal immune interface and pregnancy? Parasite Immunol. 2019;41(3):e12606. pmid:30471137
- 13. Bollani L, Auriti C, Achille C, Garofoli F, De Rose DU, Meroni V, et al. Congenital toxoplasmosis: the state of the art. Front Pediatr. 2022;10:894573.
- 14. Curcio AM, Shekhawat P, Reynolds AS, Thakur KT. Neurologic infections during pregnancy. Handb Clin Neurol. 2020;172:79–104.
- 15.
Bamgbose T. Analysis of malaria-induced anemia and gender differences among children in Nigeria. Walden University; 2021.
- 16. Kipo-Sunyehzi DD. Quality healthcare services under National Health Insurance Scheme in Ghana: perspectives from health policy implementers and beneficiaries. PAP. 2021;24(3):320–32.
- 17. Amissah-Reynolds P. Toxoplasmosis in humans and animals in Ghana (1962–2020): a review. Int J Trop Dis Health. 2020;41(14).
- 18. Bobić B, Villena I, Stillwaggon E. Prevention and mitigation of congenital toxoplasmosis. Economic costs and benefits in diverse settings. Food Waterborne Parasitol. 2019;16:e00058. pmid:32095628
- 19. Stabnick A, Yeboah M, Arthur-Komeh J, Ankobea F, Moyer CA, Lawrence ER. “Once you get one maternal death, it’s like the whole world is dropping on you”: experiences of managing maternal mortality amongst obstetric care providers in Ghana. BMC Pregnancy Childbirth. 2022;22(1):206. pmid:35287601
- 20. Agordzo SK. Seroprevalence, risk factors and impact of Toxoplasma gondii infection on haematological parameters in the Ashanti region of Ghana: a cross-sectional study. AAS Open Res. 2019;2:166.
- 21.
Mampong-Municipal-Health-Directorate. 2014-2023 ANC Data from the Mampong Municipal Health Directorat, Ghana, GHS, Retrieved on Appril 2024 uppong request by Assoah Ebenezer Mphil Biology Final Year student. 2024.
- 22. Amoah LAO, Oppong M, Amoah SK, Bimi L. Toxocariasis in Ghanaian neighbourhoods: a need for action. Sci One Health. 2023;2:100018. pmid:39077038
- 23.
GSS. 2021 Population and housing census. Ghana Statisrical Service. 2021.
- 24. Yar DD, Kwenin WKJ, Balali GI, Assoah E, Addy R, Francis G. Food milling machines are hosts to pathogenic bacteria: a cross-sectional study in the Asante Mampong Municipal, Ghana. Sci Afr. 2023;20:e01673.
- 25.
Sarmah H, et al. An investigation on effect of bias on determination of sample size on the basis of data related to the students of schools of Guwahati. 2013;2(1):33–48.
- 26. Amissah-Reynolds PKJI, Health T. Toxoplasmosis in humans and animals in Ghana (1962–2020): a review. J Toxicol Dis. 2020;41(14):20–31.
- 27. Evancare. Evancar IVD Professor: TOXO Toxoplasma Ab IgM/IgG Rapid Test Cassette (WB/S/P):Specification:Test Procedure. 2024 [cited 2024 Jul 24. ]; Available from: https://evancaremed.com/TOXO-Toxoplasma-Ab-IgM-IgG-Rapid-Test-Cassette-WB-S-P-PG7238081
- 28.
Addo SO, et al. Toxoplasma gondii among pregnant women attending antenatal care in a district hospital in Ghana. 2023;2(2):e82.
- 29. Ayi I, et al., Toxoplasma gondii infections among pregnant women, children and HIV-seropositive persons in Accra, Ghana. Trop Med Health. 2016;44:1–8.
- 30. Ayi I. Sero-epidemiology of toxoplasmosis amongst pregnant women in the greater Accra region of Ghana. Ghana Med J. 2009;43(3).
- 31. Blay EA, Ghansah A, Otchere J, Koku R, Kwofie KD, Bimi L, et al. Congenital toxoplasmosis and pregnancy malaria detection post-partum: effective diagnosis and its implication for efficient management of congenital infection. Parasitol Int. 2015;64(6):603–8. pmid:26264261
- 32.
Sefah-Boakye J. Seroprevalence of Toxoplasma gondii infection among pregnant women in the Ashanti region of Ghana. 2016;4(1):70–4.
- 33. Teweldemedhin M. Seroprevalence and risk factors of Toxoplasma gondii among pregnant women in Adwa district, northern Ethiopia. Ethiop J Health Sci. 2019;19:1–9.
- 34. Olariu TR, Ursoniu S, Hotea I, Dumitrascu V, Anastasiu D, Lupu MA. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Western Romania. Vector Borne Zoonotic Dis. 2020;20(10):763–7. pmid:32589521
- 35. Rocha ÉMD, Lopes CWG, Ramos RAN, Alves LC. Risk factors for Toxoplasma gondii infection among pregnant women from the State of Tocantins, Northern Brazil. Rev Soc Bras Med Trop. 2015;48(6):773–5. pmid:26676506
- 36. Vueba AN, Faria CP, Almendra R, Santana P, Sousa M do C. Serological prevalence of toxoplasmosis in pregnant women in Luanda (Angola): geospatial distribution and its association with socio-demographic and clinical-obstetric determinants. PLoS One. 2020;15(11):e0241908. pmid:33156846
- 37. Blaga R. Toxoplasma gondii in beef consumed in France: regional variation in seroprevalence and parasite isolation. Vet Parasitol. 2019;26.
- 38. Stelzer S, Basso W, Benavides Silván J, Ortega-Mora LM, Maksimov P, Gethmann J, et al. Toxoplasma gondii infection and toxoplasmosis in farm animals: risk factors and economic impact. Food Waterborne Parasitol. 2019;15:e00037. pmid:32095611
- 39. Gebremedhin EZ. Prevalence and risk factors of Toxoplasma gondii and Leishmania spp. infections in apparently healthy dogs in west Shewa zone, Oromia, Ethiopia. BMC Vet Res. 2021;17:1–10.
- 40. Kwofie KD. Risk of mother-to-child transmission of Toxoplasma gondii infection among pregnant women in the Greater Accra region. Matern Child Health J. 2012;20(12):2581–8.
- 41.
Mensah, et al., Seroprevalence and the associated risk factors of Toxoplasma gondii infection among pregnant women in the middle belt of Ghana. 2019.
- 42. Cho Y, Bonsu G, Akoto-Ampaw A, Nkrumah-Mills G, Nimo JJA, Park JK, et al. The prevalence and risk factors for hepatitis B surface ag positivity in pregnant women in eastern region of ghana. Gut Liver. 2012;6(2):235–40. pmid:22570754
- 43. Ephraim R, Donko I, Sakyi SA, Ampong J, Agbodjakey H. Seroprevalence and risk factors of hepatitis B and hepatitis C infections among pregnant women in the Asante Akim North Municipality of the Ashanti region, Ghana; a cross sectional study. Afr Health Sci. 2015;15(3):709–13. pmid:26957956
- 44. Luuse A, et al. Sero-prevalence of hepatitis B surface antigen amongst pregnant women attending an antenatal clinic, Volta region, Ghana. J Public Health Afr. 2016;7(2):584.
- 45. Helegbe GK, et al., Seroprevalence of malaria and hepatitis B coinfection among pregnant women in tamale metropolis of Ghana: a cross-sectional study. Can J Infect Dis Med Microbiol. 2018;2018:5610981.
- 46. Anabire NG, Aryee PA, Abdul-Karim A, Abdulai IB, Quaye O, Awandare GA, et al. Prevalence of malaria and hepatitis B among pregnant women in Northern Ghana: comparing RDTs with PCR. PLoS One. 2019;14(2):e0210365. pmid:30726218
- 47. Bobie SA, Afakorzi SH, Manortey S. Prevalence of hepatitis B infections and associated risk factors among pregnant women at Hawa Memorial Saviour Hospital in the Abuakwa North Municipality, Ghana. World J Adv Res Rev. 2022;16(1):904–14.
- 48. Antuamwine BB, Herchel ED, Bawa EM. Comparative prevalence of hepatitis B virus infection among pregnant women accessing free maternal care in a tertiary hospital in Ghana. PLoS One. 2022;17(3):e0263651. pmid:35245287
- 49. Dortey BA, Anaba EA, Lassey AT, Damale NKR, Maya ET. Seroprevalence of Hepatitis B virus infection and associated factors among pregnant women at Korle-Bu Teaching Hospital, Ghana. PLoS One. 2020;15(4):e0232208. pmid:32320459
- 50. Kwadzokpui PK. Prevalence and knowledge of hepatitis B virus infection among pregnant women in the Ningo-Prampram district, Ghana. J Med Res. 2020.
- 51. Wakjira M, Darega J, Oljira H, Tura MR. Prevalence of hepatitis B virus and its associated factors among pregnant women attending antenatal care in Ambo town, Central Ethiopia: a cross-sectional study. Clin Epidemiol Global Health. 2022;15:101054.
- 52. Abesig J, Chen Y, Wang H, Sompo FM, Wu IXY. Prevalence of viral hepatitis B in Ghana between 2015 and 2019: a systematic review and meta-analysis. PLoS One. 2020;15(6):e0234348. pmid:32530945
- 53.
Dun-Dery F, et al. Assessing the knowledge of expectant mothers on mother–to-child transmission of viral hepatitis B in Upper West region of Ghana. 2017;17:1–10.
- 54. Abdulai MA, Baiden F, Adjei G, Owusu-Agyei S. Low level of Hepatitis B knowledge and awareness among pregnant women in the Kintampo North Municipality: implications for effective disease control. Ghana Med J. 2016;50(3):157–62. pmid:27752190
- 55. Nartey Y. A nationwide cross-sectional review of in-hospital hepatitis B virus testing and disease burden estimation in Ghana, 2016-2021. BMC Infect Dis. 2022;22(1):2149.
- 56.
Kwamena A. A retrospective assessment of syphilis seroprevalence among pregnant women, Cape Coast, Ghana. 2019;6(2):54–60.
- 57. Adjei AA, et al. Human immunodeficiency virus, syphilis prevalence and risk factors among migrant workers in Konongo, Ghana. BMC Infect Dis. 2014.
- 58.
Ghana-Health-Service. Ghana National AIDS Commussion. 2019.
- 59. Manyahi J, et al. Prevalence of HIV and syphilis infections among pregnant women attending antenatal clinics in Tanzania. Tanzan J Health Res. 2015;15(1):1–9.
- 60. Yitbarek Y, Ayele BAJ. Prevalence of syphilis among pregnant women attending antenatal care clinic, Sede Muja District, South Gondar, Northwest Ethiopia. J Pregnancy. 2019;2019:1584527.
- 61. Benedetti KCSV, Ribeiro AD da C, Queiroz JHF de S, Melo ABD, Batista RB, Delgado FM, et al. High prevalence of syphilis and inadequate prenatal care in Brazilian pregnant women: a cross-sectional study. Am J Trop Med Hyg. 2019;101(4):761–6. pmid:31407659
- 62. Pereira Nogueira W. Syphilis in riverine communities: prevalence and associated factors. Revista Brasileira de Epidemiologia. 2022;56:e20210258.
- 63.
Ghana-HIV-Fact-Sheeet, National HIV Estimates and Projection Dissemination. 2022.
- 64. Safarpour H, Cevik M, Zarean M, Barac A, Hatam-Nahavandi K, Rahimi MT, et al. Global status of Toxoplasma gondii infection and associated risk factors in people living with HIV. AIDS. 2020;34(3):469–74. pmid:31714356
- 65. Obase BN, Bigoga JD, Nsagha DS. Malaria and HIV co-infection among pregnant women in africa: prevalence, effect on immunity and clinical management: review. IJTM. 2023;3(2):187–202.
- 66. Mabbott NA. The influence of parasite infections on host immunity to co-infection with other pathogens. Front Immunol. 2018;9:2579. pmid:30467504
- 67. Singer MJID. Development, coinfection, and the syndemics of pregnancy in sub-Saharan Africa. Infect Dis Poverty. 2013;2:1–10.
- 68. Mboera LEG, Kishamawe C, Kimario E, Rumisha SF. Mortality patterns of toxoplasmosis and its comorbidities in Tanzania: a 10-year retrospective hospital-based survey. Front Public Health. 2019;7:25. pmid:30838195
- 69. Mosti M, Pinto B, Giromella A, Fabiani S, Cristofani R, Panichi M, et al. A 4-year evaluation of toxoplasmosis seroprevalence in the general population and in women of reproductive age in central Italy. Epidemiol Infect. 2013;141(10):2192–5. pmid:23228486
- 70. Sadiqui S. Distribution of Toxoplasma gondii IgM and IgG antibody seropositivity among age groups and gestational periods in pregnant women. F1000Res. 2018;7:1823.
- 71. Olarinde O, Sowemimo OA, Chuang T-W, Chou C-M, Olasanmi SO, Ikotun K, et al. Toxoplasma gondii infection: seroprevalence and associated risk factors for women of childbearing age in Osun State, Nigeria. Pathog Glob Health. 2022;116(1):59–65. pmid:34254567
- 72. Wyman CP, Gale SD, Hedges-Muncy A, Erickson LD, Wilson E, Hedges DW. Association between Toxoplasma gondii seropositivity and memory function in nondemented older adults. Neurobiol Aging. 2017;53:76–82. pmid:28235681
- 73. Nash JQ, Chissel S, Jones J, Warburton F, Verlander NQ. Risk factors for toxoplasmosis in pregnant women in Kent, United Kingdom. Epidemiol Infect. 2005;133(3):475–83. pmid:15962554
- 74. Dambrun M, Dechavanne C, Guigue N, Briand V, Candau T, Fievet N, et al. Retrospective study of toxoplasmosis prevalence in pregnant women in Benin and its relation with malaria. PLoS One. 2022;17(1):e0262018. pmid:34995295
- 75. Negero J, Yohannes M, Woldemichael K, Tegegne D. Seroprevalence and potential risk factors of T. gondii infection in pregnant women attending antenatal care at Bonga Hospital, Southwestern Ethiopia. Int J Infect Dis. 2017;57:44–9. pmid:28167254
- 76.
Ngakane L. Health concerns related to housing, sanitation, water access and waste disposal in a poor mixed urban community, Mbekweni in Paarl. Stellenbosch: Stellenbosch University; 2021.
- 77. Shapiro K, Bahia-Oliveira L, Dixon B, Dumètre A, de Wit LA, VanWormer E, et al. Environmental transmission of Toxoplasma gondii: Oocysts in water, soil and food. Food Waterborne Parasitol. 2019;15:e00049. pmid:32095620
- 78. Marín-García P-J, Planas N, Llobat L. Toxoplasma gondii in foods: prevalence, control, and safety. Foods. 2022;11(16):2542. pmid:36010541
- 79. Thebault A, Kooh P, Cadavez V, Gonzales-Barron U, Villena I. Risk factors for sporadic toxoplasmosis: a systematic review and meta-analysis. Microbial Risk Analysis. 2021;17:100133.
- 80. Abdel-Rahman M. Toxoplasmosis in man and animals. J Toxoplasmosis. 2017;3(2):54–73.
- 81.
Udainiya S. Zoonotic diseases of dogs and cats. Introduction to diseases, diagnosis, and management of dogs and cats. Elsevier; 2024. pp. 559–72.
- 82. Iddawela D, Vithana SMP, Ratnayake CJBPH. Seroprevalence of toxoplasmosis and risk factors of Toxoplasma gondii infection among pregnant women in Sri Lanka: a cross sectional study. Sri Lanka J Infect Dis. 2017;17(1):1–6.
- 83. Opsteegh M, Swart A, Mensink-Beerepoot M, Hofhuis A, Langelaar M, Van der Giessen HR. Seroprevalence and risk factors for Toxoplasma gondii infection in domestic cats in the Netherlands. Vet Parasitol. 2012;104(3-4):317–26.
- 84. Deshmukh AS, Hebbar BK, Mitra P, Shinde S, Chaudhari S, Barbuddhe SB. Seroprevalence and risk factors of Toxoplasma gondii infection among veterinary personnel and abattoir workers in Central India. Parasitol Int. 2021;84:102402. pmid:34119685
- 85. Ertug S. Seroprevalence and risk factors for toxoplasma infection among pregnant women in Aydin Province, Turkey. J Infect Dev Ctries. 2005;5(1):1–6.
- 86. Doline FR, Farinhas JH, Biondo LM, de Oliveira PRF, Rodrigues NJL, Patrício KP, et al. Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals. One Health. 2023;16:100567. pmid:37363212
- 87. Kalantari N, Gorgani-Firouzjaee T, Moulana Z, Chehrazi M, Ghaffari S. Toxoplasma gondii infection and spontaneous abortion: a systematic review and meta-analysis. Microb Pathog. 2021;158:105070. pmid:34186117
- 88. Zeinali S, Khademvatan S, Jafari R, Vazifekhah S, Yousefi E, Behroozi-Lak T. Prevalence and risk factors of Toxoplasma gondii infection among women with miscarriage and their aborted fetuses in the northwest of Iran. PLoS One. 2023;18(10):e0283493. pmid:37883415
- 89. Shojaee S, et al. The relation of secondary sex ratio and miscarriage history with Toxoplasma gondii infection. J Infect Public Health. 2018;18:1–6.