Seroprevalence of human toxoplasmosis in Sudan from 1990 to 2022: A systematic review and meta-analysis

doi:10.21203/rs.3.rs-5180231/v1

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Systematic Review

Seroprevalence of human toxoplasmosis in Sudan from 1990 to 2022: A systematic review and meta-analysis

https://doi.org/10.21203/rs.3.rs-5180231/v1

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Human toxoplasmosis is a prevalent zoonotic infection with significant public health implications. Sudan has a high burden of toxoplasmosis, but the overall prevalence of the infection is unknown. This meta-analysis was conducted to estimate the pooled seroprevalence of human toxoplasmosis in Sudan and identify its risk factors. This meta-analysis study adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. It included all studies conducted in both English and Arabic before March 31, 2023, from different databases. The results were analyzed using STATA software version 16.0.

Fifty-six studies with 10,006 participants were included in the analysis. The pooled seroprevalence of human toxoplasmosis in Sudan was 36% (95% confidence interval (CI): 31%–41%). Males had a higher pooled seroprevalence than females (56% vs. 44%). Other risk factors for toxoplasmosis infection included hemodialysis, being of childbearing age, HIV infection, and occupational exposure to animals. People living in southern Sudan had the highest pooled seroprevalence of toxoplasmosis (47%).

The findings of this meta-analysis suggest that human toxoplasmosis is a highly endemic infection in Sudan, with a higher prevalence in the southern region. Males, hemodialysis patients, women of childbearing age, HIV patients, and workers occupationally exposed to animals are at an increased risk of infection.

Epidemiology

Preventive Medicine

Human toxoplasmosis

Sudan

seroprevalence

systematic review

meta-analysis

Toxoplasmosis is a parasitic infection caused by the protozoan T. gondii (1). It is one of the most common parasitic infections in humans, with an estimated one-third of the world's population infected (2). The prevalence of toxoplasmosis varies widely across different regions and populations (3). In general, countries with poor sanitation and hygiene practices and areas with high rates of meat consumption have the highest rates of infection. Toxoplasmosis can have serious health consequences for individuals with weakened immune systems, such as pregnant women(3), HIV patients(4), cancer patients(5), hemodialysis patients(6), and tuberculosis patients (7). These individuals are at a higher risk of developing severe complications from toxoplasmosis.

Toxoplasmosis was first reported in Sudan in 1966(8), but since then, only a few studies have been conducted to assess its prevalence and risk factors (9). The available data suggest that human toxoplasmosis is widespread in Sudan (9). This is likely due to a number of factors, including the hot and humid climate, which is favorable for the survival of T. gondii oocysts, and the large population of livestock, which can serve as reservoirs for the parasite (10, 11).

A comprehensive study conducted on domestic animals in Sudan found that the pooled prevalence of overall T. gondii infections was 38% (12). The high prevalence of T. gondii among domestic animals in Sudan suggests that the disease is also common among the Sudanese population. Despite the high prevalence of toxoplasmosis in Sudan, there is a need for more comprehensive and up-to-date data to account for the temporal and spatial variability of parasite prevalence, which can be influenced by factors such as climate conditions, war, and other socioeconomic determinants.

To date, there have been a number of studies conducted on the seroprevalence of toxoplasmosis in Sudan. However, these studies have been conducted in different regions of the country and have used different methodologies. This has made it difficult to compare the results and get an accurate estimate of the overall seroprevalence of toxoplasmosis in Sudan. However, by employing robust statistical techniques, meta-analysis allows for a more accurate and reliable estimate of the prevalence of toxoplasmosis in the Sudanese population than would be possible based on individual studies alone.

The aim of this meta-analysis is to systematically review and analyze the existing studies published between 1990 and 2022 on the seroprevalence of toxoplasmosis in Sudan and to identify the population groups that are most at risk of infection. This will provide a more accurate and comprehensive estimate of the seroprevalence of toxoplasmosis in the country and identify potential risk factors for infection. The findings of this meta-analysis will be of interest to public health officials, researchers, and clinicians. The information can be used to develop and implement effective prevention and control strategies for toxoplasmosis in Sudan.

2.1. Design and protocol registration

This meta-analysis adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines(13). The study protocol was prospectively registered in the International Prospective Register of Systematic Reviews (No. CRD42023389388).

2.2. Data items, information sources, and search strategy

The primary objective of this study was to determine the seroprevalence of human toxoplasmosis in Sudan. This was achieved by collating and analyzing direct reports from individual studies and interpreting the results by comparing the percentages of humans who tested positive for toxoplasmosis to the total human population studied. Two independent investigators, AM and MA, searched relevant research databases (Table 1) from their inception to March 30, 2023, for studies on human toxoplasmosis in Sudan published in English and/or Arabic. In addition to the electronic databases and grey literature sources, the authors also searched the reference lists of relevant studies for additional eligible studies. The research strategy employed Boolean search terms (AND, OR, NOT) to identify relevant literature on the topic of human toxoplasmosis in Sudan. The search terms were focused on titles and abstracts and were translated into Arabic to ensure a comprehensive search of both English and Arabic literature. The following Boolean search string was used: ((toxoplasmosis) OR (Toxoplasma) OR (Toxoplasma gondii) OR (T. gondii)) AND ((prevalence) OR (seroprevalence) OR (epidemiology) OR (frequency) OR (risk factors)) AND ((humans)) AND (Sudan). This search string ensured that all retrieved studies were relevant to the research question, which was to investigate the prevalence, seroprevalence, epidemiology, frequency, and risk factors of toxoplasmosis in humans in Sudan.

2.3. Inclusion and exclusion criteria

The following criteria were used to determine inclusion for the current study: (1) all observational studies; (2) published in Arabic or English; (3) conducted on the Sudanese population; (4) reported the prevalence of toxoplasmosis; and (5) positive cases of toxoplasmosis must be detected using standard serological diagnostic methods. Studies were excluded if they did not provide sufficient information on sample size, sampling location, or sampling period, as these factors may affect the representativeness and quality of the data. Additionally, reviews, letters, editorials, and studies without full-text availability or that did not report the information needed to meet the above-mentioned eligibility criteria were excluded. In cases where the primary investigator (AM) encountered studies with missing information, they contacted the corresponding author(s) via email to obtain the original data. If the primary investigator failed to obtain the missing information within 4 weeks, or if it was not obtained at all, the study or studies with the missing information were excluded.

2.4. Study selection process and risk of bias assessment

The selection process of studies was based on inclusion and exclusion criteria. It began with the primary screening of all electronic databases to identify eligible studies and retrieve them. The identified studies were then exported to version X9.3.3 of the EndNote citation manager to identify and remove duplicates. Subsequently, the remaining articles underwent independent screening and evaluation by AM and MA. They thoroughly read each article’s title, abstract, and full text to eliminate studies that did not meet the previously defined objectives. The remaining articles were also subjected to additional quality checks using the Joanna Briggs Institute quality assessment tools checklist (14). The inter-rater agreement between the two investigators was measured using Cohen’s Kappa statistic (15). The two searched authors achieved a kappa value of 0.99, which is considered almost perfect agreement. Any discrepancies in the study findings were resolved through discussion between the study authors. The entire selection process was depicted using the PRISMA statement flow diagram (Fig. 1).

Table 1

Databases searched and number of hits
Database	Website	No. hits
Scopus	https://www.scopus.com/	13
Web of Science	https://www.webofscience.com/wos/	19
PubMed	https://pubmed.ncbi.nlm.nih.gov/	24
PMC	https://www.ncbi.nlm.nih.gov/pmc/	159
Google Scholar	https://scholar.google.com/schhp?hl=ar&as_sdt=0,5	74
ResearchGate	https://www.researchgate.net/	34
Semantic Scholar	https://www.semanticscholar.org/	37
African Journals Online (AJOL)	https://www.ajol.info/index.php/ajol	92
University of Khartoum Repository	http://khartoumspace.uofk.edu/home	48
Sudan University of Science and Technology Repository	https://repository.sustech.edu/	17
University of Gezira Repository	http://repo.uofg.edu.sd/	24
Al-Neelain University Repository	http://repository.neelain.edu.sd:8080/xmlui/	14
Omdurman Islamic University Repository	http://repository.oiu.edu.sd:8080/xmlui/	3
Shendi University Repository	http://repository.ush.sd:8080/xmlui/	1

2.5. Data extraction process

After completing the study selection process, we used a Microsoft Word 2016 data extraction template to extract the relevant data. The extraction template includes various information such as the author’s name and publication year, study period, diagnostic method, geographical location (based on state names), type of immune globulins targeted in the diagnostic test, study group, age in year, sample size, and the prevalence of human toxoplasmosis (overall and in males and females) (Table 2). To ensure accuracy, we compared the extraction results of two authors, AM and MA. They independently extracted data from a randomly selected set of papers, which accounted for 30% of the total.

2.6. Synthesis methods

The data from the current study were analyzed using STATA software version 16.0, with a statistical significance level set at p < 0.05. The study results were calculated using two statistical measurements: effect size (ES) with a 95% confidence interval (CI) and standard error (SE). The ES was calculated using the binomial distribution and the prevalence of toxoplasmosis (proportion). The SE was calculated using the following formula:

SE = sqrt (p (1-p) / n).

where:

p is the proportion of toxoplasmosis-positive cases in the overall population.

n is the sample size.

The heterogeneity among the included studies was assessed using the degree of inconsistency (I²), which is expressed as a percentage ranging from 0–100%. To quantify the I² result, the current study followed the recommendation of Higgins et al. (2003) (16), which defined heterogeneity as low, medium, and high for I2 values of 25%, 50%, and 75%, respectively.

To further investigate the potential heterogeneity among the included studies and identify potential sources of bias and sensitivity, subgroup analyses were conducted. Sensitivity analyses were conducted by excluding studies with low-quality scores or studies that were outliers. Subgroup analyses were conducted by stratifying the studies by study variables such as study region, study population, and study methodology, as described by Ahmed et al. (2022)(17) and Mohammed et al. (2023)(18).

The results of the final meta-analysis model were presented as forest plots, which included the results of each individual study as well as the pooled results of all included studies. The effect size (prevalence) with a 95% confidence interval (CI) was reported. Moreover, to check for potential publication bias, the visual symmetry of the funnel plot and the result of the regression-based Egger test were used. The Egger test was considered significant if the P values were less than 0.10. To investigate the possible relationship between study variables and the prevalence of human toxoplasmosis, a meta-regression test (univariate and multivariate regression) was performed. Finally, the results of this study were presented using a narrative synthesis, followed by the full meta-analysis chart.

3.1. Study identification and selection

The study authors conducted an extensive search of major electronic databases (Table 1) and other relevant sources to identify all relevant studies. The initial search results yielded 559 scientific articles (538 from database searching and 21 from citation searching). After removing 172 duplicate articles, 387 studies were retained for further critical appraisal. Following a meticulous screening of titles and abstracts, 291 studies were excluded. Additionally, four articles could not be retrieved. Of the remaining 92 articles, 36 were rejected for various reasons, including insufficient data (8), poor quality (20), and duplicate data (8). Ultimately, 56 studies met the eligibility criteria and were included in the systematic review and meta-analysis. The entire study selection process is depicted in Fig. 1.

3.2. The main characteristics of the included studies

The main characteristics of the 56 studies included in this comprehensive meta-analysis are summarized in Table 2. All of the included studies were published in English between 1990 and 2022, and most (30/56, 53.6%) were university theses (28 master's theses and 2 PhD dissertations). The remaining 26/56 (46.4%) studies were peer-reviewed articles. Of the 56 studies, 12 (21.4%) were case-control studies, 42 (75%) were cross-sectional studies, 1 (1.8%) was a retrospective study, and 1 (1.8%) was a prospective study. A total of 10,006 human subjects were included in the qualitative and quantitative analyses.

All of the included studies reported on the overall prevalence of human toxoplasmosis in Sudan in the following groups: General population: 7 studies (12.5%), blood donors: 9 studies (16.1%), workers occupationally exposed to animals: 6 studies (10.7%), childbearing-age women: 6 studies (10.7%), pregnant women: 17 studies (30.4%), aborted women: 4 studies (7.1%), immunocompromised women: 1 study (1.8%), HIV patients: 2 studies (3.6%), hemodialysis patients: 2 studies (3.6%), retinitis patients: 1 study (1.8%), and Tuberculosis patients: 1 study (1.8%). Additionally, 17/56 (30.4%) studies demonstrated an association between gender and human toxoplasmosis. Meanwhile, of all the available serological diagnostic tests for human toxoplasmosis, only the following four were mentioned in the included studies: Immunochromatography test (ICT): 4 times (7.1%), latex agglutination test (LAT): 32 times (57.1%), enzyme-linked immunosorbent assay test (ELISA): 18 times (32.1%), and rapid diagnostic testing (RDT): 2 times (3.6%).

The current study found that human toxoplasmosis was distributed throughout Sudan, with the exception of the western region. The geographic distribution of the included studies revealed that central Sudan was the most frequently studied region, accounting for 87.5% (49 studies) of all studies. Northern Sudan, eastern Sudan, and southern Sudan were the next most frequently studied regions, accounting for 5.4% (3 studies), 3.6% (2 studies), and 3.6% (2 studies), respectively.

3.3. Results of synthesis

The prevalence of human toxoplasmosis in Sudan varied widely across the 56 included studies, with the lowest prevalence (2%) reported in blood donors from a study conducted in Wad Madani City, Gezira State (19), and the highest prevalence (82.2%) reported in women of reproductive age from a study conducted in Ruffa City, Gezira State(20) (Table 2). The substantial heterogeneity across studies (P < 0.0001; I^2 = 97.39%) necessitated the use of the random-effects model (REML) for the final analysis, which yielded a pooled prevalence of human toxoplasmosis in Sudan of 36% (95% CI: 31–41%) (Fig. 2).

3.4. Subgroup analysis

To identify the source of high heterogeneity in the current study, a subgroup analysis was conducted to explore how the following variables (gender, study group, study region, study years, diagnostic method, and diagnostic target) may contribute to the observed heterogeneity in the prevalence of human toxoplasmosis. The results of the subgroup analysis are presented in Table 3. The subgroup analysis revealed that the pooled prevalence of human toxoplasmosis in Sudan was higher in males compared with females (56% vs. 44%) (see Fig. 3).

Additionally, the study found that hemodialysis patients had the highest prevalence of human toxoplasmosis (56%), followed by childbearing-age women (48%), HIV patients (42%), workers occupationally exposed to animals (40%), aborted women (32%), pregnant women (32%), blood donors (31%), immunocompromised women (27%), retinitis patients (24%), and tuberculosis patients (17%). Furthermore, despite the small number of studies conducted in the southern region of the country, people living in southern Sudan had the highest pooled prevalence of T. gondii (47%) compared to other regions of Sudan.

Finally, it is important to note that there has been a noted change in the prevalence of human toxoplasmosis in Sudan over time, with the prevalence decreasing slightly in recent years.

Table 2

Main characteristics of studies included in the meta-analysis
No	Study author	Study duration/years	City (region)	Study design	Diagnostic method	Diagnostic target	Study group	Age in years	Sample size			Seroprevalence, n (%)
No	Study author	Study duration/years	City (region)	Study design	Diagnostic method	Diagnostic target	Study group	Age in years	Overall	Male	Female	Overall	Male	Female
1.	NaserAldeen, N 2012(21)	June 2011- March 2012	Khartoum (central)	CS	ELISA	IgG & IgM	General population	20–70	40	2	38	17 (42.5)	1 (5.9)	16 (94.1)
2.	Mohammed 2022(22)	2019–2020	Khartoum (central)	CS	ELISA	IgG & IgM	Renal transplant recipients	12–80	58	36	22	22 (37.9)	14 (63.6)	8 (36.4)
							HIV/AIDS patients	22–62	50	25	25	10 (20)	4 (40)	6 (60)
							Overall	12–80	108	61	47	32 (29.6)	18 (56.3)	14 (43.7)
5.	Alhidai et al.2018 (23)	October-December 2010	Al-Gezira (Central)	CS	LAT	IgG & IgM	Hemodialysis patients	20–80	150	101	49	110 (73.3)	74 (67.3)	36 (32.7)
6.	Mohamed et al 2012(24)	2011	Al-Gezira (Central)	CS	ELISA	IgG	Childbearing age women	18–45	253	NA	NA	183 (72.3)	NA	NA
7.	Munsoor & Ahmed, 2012(25)	2011–2013	Khartoum (central)	CS	LAT	IgG & IgM	Blood donors	18–56	534	NR	NR	235 (44)	NR	NR
8.	Ali 2012(26)	2011–2012	Khartoum (central)	CS	ELISA	IgG & IgM	General population	10–51	350	200	150	91 (26)	61 (67)	30 (33)
							Pregnant women	18–45	150	NA	NA	44 (29.3)	NA	NA
							Overall	10–51	500	NA	NA	135 (27)	NA	NA
11.	Mohammed et al 2021(27)	2019–2020	Khartoum (central)	CS	ELISA	IgG & IgM	Blood donors	18–58	50	NR	NR	16 (32)	NR	NR
12.	Ibrahim et al 2019(28)	October 2015-January 2016	Khartoum (central)	CS	ELISA	IgG	Retinitis patients	NR	90	49	41	22 (24.4)	9 (40.9)	13 (59.1)
13.	Elamin et al 2012(29)	March 2002-May 2004	Al-Gezira (Central)	CC	ELISA	IgG & IgM	Pregnant women	20–39	188	NA	NA	70 (37.2)	NA	NA
14.	Abdelmola et al 2021(30)	April 2015- October 2016	Khartoum (central)	CS	ELISA	IgG & IgM	Pregnant women	18–45	200	NA	NA	26 (13)	NA	NA
15.	Khalil et al 2013 (31)	NR	Khartoum (central)	CS	LAT	IgG & IgM	General population	18–62	282	NR	NR	127 (45)	NR	NR
							Pregnant Women	16–45	245	NA	NA	88 (35.9)	NA	NA
							Aborted women	18–50	209	NA	NA	122 (58.4)	NA	NA
							Neonates	1–28 days	150	NR	NR	75 (50)	NR	NR
							Children	< 18	147	NR	NR	20 (13.6)	NR	NR
							HIV Patients	14–75	44	NR	NR	33 (75)	NR	NR
							Cancer Patients	4–85	59	NR	NR	25 (42.4)	NR	NR
							WOEA	12–85	10	NA	NA	10 (100)	NA	NA
							Overall	1 day-85 years	1146	NR	NR	500 (43.6)	NR	NR
24.	Musa 2021 (32)	2020–2021	Al-Gezira (Central)	CS	LAT	IgG & IgM	WOEA	16–68	120	66	54	47 (39.2)	32 (68.1)	15 (31.9)
25.	Idris 2021 (33)	February 2020-July 2021	Al-Gezira (Central)	CS	LAT	IgG & IgM	WOEA	6–80	120	78	42	54 (45)	38 (70.4)	16 (29.6)
26.	Mohamed 2021 (34)	February 2020-July 2021	Al-Gezira (Central)	CS	LAT	IgG & IgM	WOEA	1-100	120	56	64	51 (42.5)	27 (52.9)	24 (47.1)
27.	Ahmed 2021(35)	February 2020- September 2021	Al-Gezira (Central)	CS	LAT	IgG & IgM	WOEA	1–80	120	30	90	96 (80)	27 (28.1)	69 (71.9)
28.	Moustafa & Kheiry 2019(36)	August-December 2016	Khartoum (central)	CS	LAT	IgG & IgM	WOEA	15–69	60	30	2	12 (20)	12 (100)	0 (0)
29.	Alshaeb 2017(37)	November 2017	Al-Gezira (Central)	CC	LAT	IgG & IgM	WOEA	NR	70	NA	NA	8 (11.4)	NA	NA
30.	Mustafa et al 2019(38)	January- November 2018	Khartoum (central)	CS	RDT	IgG & IgM	Immunocompromised women	15–50	100	NA	NA	27 (27)	NA	NA
31.	Salih 2014(39)	May-September 2013	Gadarif (Eastern)	CS	LAT	IgG & IgM	Blood donors	18–47	100	NR	NR	14 (14)	NR	NR
32.	Yassin 2015(40)	NR	Khartoum (central)	CC	LAT	IgG & IgM	Tuberclosis patients	20–72	64	48	16	11 (17.2)	8 (72.7)	3 (27.3)
33.	Tamomh et al 2016(41)	2015–2016	White Nile (Southern)	CC	LAT	IgG & IgM	Pregnant Women	16–45	104	NA	NA	40 (38.5)	NA	NA
34.	Hamad 2018(42)	NR	Khartoum (central)	CC	LAT	IgG & IgM	Childbearing age women	18–49	45	NA	NA	15 (33.3)	NA	NA
35.	Elmubarak 2016(43)	November-December 2015	Al-Gezira (Central)	CS	LAT	IgG	Aborted women	15–45	100	NA	NA	16 (16)	NA	NA
36.	Elshiekh 2015(44)	November-December 2014	Al-Gezira (Central)	CS	LAT	IgG	Pregnant women	15–45	100	NA	NA	69 (69)	NA	NA
37.	Shabo 2015(45)	January- Jane 2015	Al-Gezira (Central)	CS	LAT	IgG & IgM	Aborted women	15–45	96	NA	NA	42 (43.8)	NA	NA
38.	Ali 2022(46)	NR	Al-Gezira (Central)	CC	LAT	IgG & IgM	Pregnant women	15–45	90	NA	NA	53 (58.9)	NA	NA
39.	Abbas 2019(47)	January-March 2019	Al-Gezira (Central)	CS	ICT	IgG	Blood donors male	20–40	100	NA	NA	17 (17)	NA	NA
40.	Ata Alfadeel 2019(19)	January-March 2019	Al-Gezira (Central)	CS	ICT	IgM	Blood donors male	20–40	100	NA	NA	2 (2)	NA	NA
41.	Mohammed 2017(48)	May 2015-April 2017	River Nile (Northern)	CS	LAT	IgG & IgM	Pregnant women	15–40	300	NA	NA	90 (30)	NA	NA
42.	Abdel-Hameed 1991(49)	NR	Al-Gezira (Central)	CC	LAT	IgG	General population	9–54	386	212	174	161 (41.7)	83 (51.6)	78 (48.4)
43.	Satti et al 2011(50)	June 2006-July 2008	Khartoum (central)	CC	LAT	IgG & IgM	Pregnant women	25–35	455	NA	NA	80 (17.6)	NA	NA
44.	Ibrahim et al 2015(51)	September 2014-February 2015	Khartoum (central)	CC	LAT	IgG & IgM	HIV Patients	18–63	82	40	42	36 (43.9)	20 (55.6)	16 (44.4)
45.	Mohammed et al 2018 (52)	April 2015- May 2017	Khartoum (central)	CS	ELISA	IgG & IgM	Pregnant women	18–45	300	NA	NA	68 (22.7)	NA	NA
46.	Bashir et al 2017(53)	March-August 2016	Khartoum (central)	CS	ELISA	IgG & IgM	Blood donors	10–50	100	NA	NA	35 (35)	NA	NA
47.	Eljack et al 2018 (54)	March-June 2015	Khartoum (central)	CS	LAT	IgG & IgM	General population	10–60	157	56	101	37 (23.6)	29 (78.4)	8 (21.6)
48.	Ahmed 2018(55)	January 2017-April 2018	Khartoum (central)	CC	ELISA	IgG & IgM	Pregnant women	17–45	100	NA	NA	19 (19)	NA	NA
49.	Alamin 2021(56)	May 2021- September 2021	Khartoum (central)	CS	RDT	IgG & IgM	Hemodialysis patients	20–60	75	17	58	29 (38.7)	6 (20.7)	23 (79.3)
50.	Abd Ewahid et al 2020 (57)	January 2009-December 2010	River Nile (Northern)	RS	LAT	IgG & IgM	Pregnant women	16–45	383	NA	NA	285 (74.4)	NA	NA
51.	Ahmed 2016(58)	May-August 2016	Al-Gezira (Central)	CS	ICT	IgG	Pregnant women	20–38	80	NA	NA	2 (2.5)	NA	NA
52.	Taha 2017(59)	February-November 2017	River Nile (Northern)	CS	LAT	IgG & IgM	Aborted women	25–49	152	NA	NA	51 (33.6)	NA	NA
53.	Idres 2022(60)	2021-August 2022	Al-Gezira (Central)	CS	ICT	IgG & IgM	Blood donors	18–50	54	NA	NA	24 (44.4)	NA	NA
54.	Abdel-Raouff, &Elbasheir 2014(61)	June-August 2013	Khartoum (central)	CS	ELISA	IgG	Pregnant women	18–49	163	NA	NA	33 (20.3)	NA	NA
55.	Abubakar 2020(62)	December 2018-October 2019	Al-Gezira (Central)	CS	LAT	IgG & IgM	Blood donors	20–35	100	NR	NR	64 (64)	NR	NR
56.	Elhag & Elturabi, 2015(63)	January 2012-January 2013	Khartoum (central)	CS	ELISA	IgG & IgM	Aborted women	18–45	95	NA	NA	32 (33.7)	NA	NA
57.	Abdalla 2016(64)	March -August 2016	Khartoum (central)	CS	ELISA	IgG & IgM	Blood donors	10–50	100	NR	NR	32 (32)	NR	NR
58.	Mahjoub 2014(65)	January- April 2014	Al-Gezira (Central)	CS	LAT	IgG & IgM	Childbearing age women	15–45	100	NR	NR	49 (49)	NR	NR
59.	Suleiman & Afifi, 2020(66)	NR	Kassala (Eastern)	CS	LAT	IgG & IgM	General population	18–40	300	121	179	170 (56.7)	60 (35.3)	110 (64.7)
60.	Abdelrahim 2019 (67)	October 2018-February 2019	Al-Gezira (Central)	CS	LAT	IgG & IgM	Pregnant women	15–40	100	NR	NR	16 (16)	NR	NR
61.	Abbas & Saad 2011(68)	NR	Khartoum (central)	CC	LAT	IgG & IgM	Childbearing age women	14–45	200	NR	NR	45 (22.5)	NR	NR
62.	Mohamed 2008(69)	NR	Khartoum (central)	PS	LAT	IgG & IgM	HIV Patients	3–65	144	116	28	59 (41)	49 (83)	10 (17)
63.	Elnahas et al 2003(70)	June-December 2000	Khartoum (central)	CS	ELISA	IgG	Pregnant women	18–49	487	NR	NR	166 (34.1)	NR	NR
64.	Saeed 2008(71)	June 2007- October 2007	Khartoum (central)	CS	ELISA	IgG & IgM	Pregnant women	15–55	100	NR	NR	10 (10)	NR	NR
65.	Elamin 2017(20)	June 2012- March 2014	Al-Gezira (Central)	CS	LAT	IgG & IgM	Childbearing age women	12–47	180	NR	NR	148 (82.2)	NR	NR
66.	Hajtaha 2015(72)	January-April 2015	Khartoum (central)	CS	LAT	IgG & IgM	Childbearing age women	15–45	100	NR	NR	28 (28)	NR	NR
67.	Mizo 2015(73)	August- November 2013	Sinnar (Southern)	CS	ELISA	IgG	Pregnant women	15–45	165	NR	NR	89 (53.9)	NR	NR
68.	Alshareef et al 2018(74)	NR	Khartoum (central)	CC	ELISA	IgG	Pre-eclampsia women	18–49	90	NR	NR	29 (32.2)	NR	NR
							Pregnant women	18–49	90	NR	NR	4 (4.4)	NR	NR
							Overall	18–49	180	NR	NR	33 (18.3)	NR	NR

Abbreviations: CC; Case control study, CS; Cross- sectional study, ELISA; enzyme linked immunosorbent assay, ICT; Immuochromatography test, LAT; latex agglutination test, NA; Not applicable, NR; Not reported, PS; Prospective study, RS; Retrospective study, RDT; Rapid diagnostic testing, WOEA; Workers occupationally exposed to animals. Notes: Workers occupationally exposed to animals included animal breeders, butchers, livestock workers, meatpacking workers, slaughterhouse workers, and veterinary personnel.

3.5. Meta-regression, sensitivity analysis, and publication bias

A meta-regression analysis was conducted to investigate the possible relationship between study variables (study year(s), study group, study region, diagnostic method, and diagnostic target) and the prevalence of human toxoplasmosis (Figure 4). None of these variables showed a statistically significant association with the prevalence of toxoplasmosis (Table 3), suggesting that they did not account for the observed heterogeneity between studies.

Additionally, to further clarify these findings, a sensitivity analysis was performed by sequentially excluding studies from the meta-analysis model. This analysis did not reveal any significant differences in the pooled prevalence of toxoplasmosis, indicating that the meta-analysis findings were robust.

Finally, two methods were used to assess publication bias: a funnel plot (Figure 5) and the regression-based Egger test (Egger's test). The funnel plot was symmetrical, and the Egger's test was not statistically significant (P = 0.261), suggesting that there is a low likelihood of publication bias in this study.

Table 3

Pooled prevalence of human toxoplasmosis in Sudan based of the findings of sub-groups and meta-regression analysis
Analysis of human toxoplasmosis		Pooled Estimates				Heterogeneity				Meta-regression
Analysis of human toxoplasmosis		No of studies	Pooled sample size	Cases	Pooled prevalence % (95% CI)	Q-value	I²%	H²	Q-p value	P- value	OR (95% CI)
Gender	Male	17	1035	554	56 (44–68)	1390.60	97.23	36.14	< 0.001	0.14	(-0.042-0.289)
Gender	Female	17	1035	481	44 (32–56)	1390.55	97.23	36.14	< 0.001	0.14	(-0.042-0.289)
Study group	Aborted women	4	443	141	32 (20–43)	23.43	86.48	7.39	0.81	0.45	(-0.024-0.011)
	Blood donors	9	1238	439	31 (19–44)	410.08	96.95	32.82	< 0.001
	Childbearing age women	6	878	468	48 (28–68)	297.02	97.80	45.53	< 0.001
	General population	7	2637	1052	38 (29–47)	111.26	94.96	19.85	< 0.001
	HIV patients	2	226	95	42 (36–49)	0.18	0.00	1.00	0.672
	Hemodialysis Patients	2	225	139	56 (22–90)	26.80	96.27	26.80	< 0.001
	Immunocompromised women	1	100	27	27 (18–36)	0.00	NE	NE	NE
	Livestock workers& veterinarians	6	610	268	40 (21–59)	192.17	96.81	31.32	< 0.001
	Pregnant women	17	3495	1145	32 (22–42)	961.11	98.22	56.14	< 0.001
	Retinitis patients	1	90	22	24 (16–33)	0.00	NE	NE	NE
	Tuberculosis patients	1	64	11	17 (1–26)	0.00	NE	NE	NE
Study region	Central Sudan	49	8502	3068	35 (30–40)	2182.06	97.34	37.63	< 0.001	0.3	(-0.034-0.112)
	Eastern Sudan	2	400	184	35 (10–77)	90.16	98.89	90.16	< 0.001
	Northern Sudan	3	835	426	46 (18–74)	193.08	98.71	77.43	< 0.001
	Southern Sudan	2	269	129	47 (31–62)	6.27	84.05	6.27	0.012
Study year/s	Before 2000	1	386	161	42 (37–47)	0.00	NE	NE	NE	0.7	(-0.109-0.073)
	Between 2000 to 2010	5	1374	385	28 (16–40)	87.34	96.01	25.06	< 0.001
	After 2010	50	8246	3261	37 (31–42)	2562.55	97.38	38.18	< 0.001
Diagnostic method	ELISA	18	3219	1014	32 (25–39)	402.52	95.04	20.15	< 0.001	0.11	(-0.01-0.101)
	ICT	4	334	45	16 (3–34)	50.37	98.40	62.67	< 0.001
	LAT	32	6278	2692	41 (34–48)	1262.49	97.44	39.13	< 0.001
	RDT	2	175	56	32 (21–44)	2.67	62.49	2.67	0.102
Diagnostic target	IgG	11	2104	787	35 (22–48)	646.39	98.25	57.23	< 0.001	0.36	(-0.184-0.066)
	IgG & IgM	44	7802	3018	37 (32–42)	1511.10	96.64	29.76	< 0.001
	IgM	1	100	2	2 (1–5)	0.00	NE	NE	NE
Overall		56	10006	3807	36 (31–41)	2707.10	97.39	38.33	< 0.001

Toxoplasmosis is a neglected zoonotic parasitic infection that affects humans and animals worldwide. One-third of the world's population is infected with T. gondii, but the highest burden of the disease is in developing countries. The prevalence of human toxoplasmosis in Sudan has been a topic of interest for researchers for several years, but there is no comprehensive overview of the available data. This systematic review and meta-analysis of studies published between 1990 and 2022 aims to fill this gap in the literature. Although many studies have investigated the prevalence of human toxoplasmosis in Sudan, the overall epidemiology of the disease is still not clear in many parts of the country. Our study showed that 36% of the overall population in Sudan is infected with human toxoplasmosis, which is similar to the pooled prevalence of toxoplasmosis in domestic animals in Sudan (38%) (12).

Compared to other countries, the prevalence of human toxoplasmosis in Sudan is higher than those reported in previous studies of the disease among the general population in many African countries, namely Angola, Swaziland, Zambia, Zimbabwe, Mozambique, South Africa, Namibia (75), and Nigeria (76) (4%, 4%, 7%, 10%, 13%, 18%, 25%, and 32.9%, respectively), as well as in China (8.2%)(77), Pakistan (23.9%)(78), and Mexico (27.97%)(79). However, the prevalence of human toxoplasmosis in Sudan is lower than the highest pooled prevalence observed in Ethiopia (74.73%)(80), Iran (39.5% and 43%)(81, 82), Malaysia (59.7%)(83), and Botswana (92%)(75).

From the information presented above, it can be concluded that Sudan has the third-highest pooled prevalence of human toxoplasmosis in Africa, the second-highest in the East Africa region, and the highest in Arabic countries. The reasons behind the high prevalence of human toxoplasmosis in Sudan are not entirely clear. However, it has been suggested that the hot and humid climate in Sudan may contribute to the high prevalence of the disease, as the oocysts of T. gondii survive better in these types of environments (84, 85). Furthermore, people in Sudan have some unique feeding habits, such as consuming raw meat like camel liver and sheep offal "Elmaraara" and raw milk (86). This can increase the risk of exposure to T. gondii oocysts. In addition, there is a large population of stray cats in Sudan, which may contribute to the high prevalence of toxoplasmosis in humans.

Sudan is a country with a long history of conflicts that have led to the displacement and dislocation of people, which can lead to poor sanitation and hygiene practices(87). This can increase the risk of exposure to T. gondii oocysts. Additionally, limited information on the prevalence, distribution, and magnitude of the disease among both humans and animals in Sudan may have contributed to the high prevalence of human toxoplasmosis. It is important to note that the prevalence of toxoplasmosis can vary widely within a country, depending on several factors such as climate, sanitation and hygiene practices, diet, and contact with animals. Therefore, it is possible that the prevalence of toxoplasmosis in Sudan is higher in some regions than others.

More research is needed to identify the risk factors for toxoplasmosis infection in Sudan, particularly in light of the COVID-19 pandemic and the ongoing armed conflict. This research should inform the development of effective prevention and control strategies.

The pooled seroprevalence of human toxoplasmosis in Sudan was 37% for IgG and IgM antibodies, followed by 35% and 2% for IgG and IgM antibodies alone, respectively. This is consistent with a similar finding of human toxoplasmosis reported by Rahmanian et al. (2020) in Iran (36%)(2). In addition, the prevalence of human toxoplasmosis in Sudan appears to have decreased over time. This could be due to a combination of factors, such as improved sanitation and hygiene practices and increased use of antiparasitic drugs. The study also found that human toxoplasmosis is more prevalent in Southern Sudan and Northern Sudan (47% and 46%, respectively) than in Central and Eastern Sudan (35% and 35%, respectively).

In this comprehensive study, we found that the pooled prevalence of T. gondii was slightly higher in males than in females. Several studies have reported similar findings in Iran (81), and Nigeria (76). One possible explanation for this difference is that males may be more likely to be employed in occupations that involve exposure to infected animals or their feces, such as farming, ranching, and veterinary medicine (88). Additionally, males are more likely to engage in behaviors that increase the risk of exposure to toxoplasmosis, such as hunting, fishing, and eating raw or undercooked meat. However, more research is needed to identify the reasons behind this difference.

In contrast to these findings, a study conducted in Pakistan (78), reported that the human toxoplasmosis seropositivity rate is higher in women than in men. The reasons behind this difference are also not entirely clear and require further investigation.

Moreover, the results of this study indicate that the prevalence of human toxoplasmosis varies among different risk groups. Hemodialysis patients had the highest prevalence of human toxoplasmosis (56%), followed by childbearing-age women (48%), HIV patients (42%), workers occupationally exposed to animals (40%), aborted women (32%), pregnant women (32%), blood donors (31%), immunocompromised women (27%), retinitis patients (24%), and tuberculosis patients (17%). These findings are consistent with previous studies that have identified these groups as being at higher risk of infection (4, 6, 89).

The high prevalence of human toxoplasmosis among hemodialysis patients, HIV patients, tuberculosis patients, and immunocompromised women may be due to their weakened immune systems, which make them more susceptible to infections and make it more difficult for the body to fight off infections.

Hemodialysis patients have weakened immune systems due to the dialysis process itself. Hemodialysis is a procedure that filters the blood through a machine to remove waste products and excess fluids. This process can damage the white blood cells, which are responsible for fighting infection (6). HIV patients have weakened immune systems due to the HIV virus. HIV attacks the white blood cells, making it difficult for the body to fight off infection. Therefore, toxoplasmosis is one of the leading opportunistic infections in HIV patients(69, 90). Immunocompromised women are those with weakened immune systems due to factors such as cancer, or the use of immunosuppressive drugs. These factors can make it difficult for the body to fight off infection, increasing the risk of developing toxoplasmosis(89). Tuberculosis patients are at increased risk of toxoplasmosis infection because of their weakened immune systems. Tuberculosis is a bacterial infection that typically affects the lungs. Tuberculosis can weaken the immune system and make people more susceptible to other infections, such as toxoplasmosis (7). Overall, the high prevalence of toxoplasmosis in these populations is a serious public health concern. It is important to identify and treat toxoplasmosis infections in these populations promptly to avoid serious complications.

Occupationally exposed animal workers (WOEA) in Sudan are at an increased risk of toxoplasmosis infection, as demonstrated in this study. This is due to their exposure to infected animals and their bodily fluids, which can contain Toxoplasma gondii cysts (12). WOEA who handle these animals or their bodily fluids are at risk of becoming infected.

The seroprevalence of toxoplasmosis in WOEA varies widely among countries, ranging from 4.8% in the United States (91) to 84% in Kenya (92). The current study found that the seroprevalence of T. gondii among WOEA in Sudan is 40%. This prevalence is within the global range of toxoplasmosis infection among WOEA.

The results of this meta-analytical study suggest that the probability of pregnant women, aborted women, and women of childbearing age getting infected with T. gondii in Sudan is very high, with more than 30% of these women at increased risk of toxoplasmosis infection.

This is a significant public health concern, as toxoplasmosis can cause serious birth defects or miscarriage if infection occurs during pregnancy, where studies showed that T. gondii is the most abortifacient human protozoan infection and can cause spontaneous abortion in women with a latent or recent infection.

The current study’s findings are consistent with previous reports from Africa and around the world (93-98). The high prevalence of toxoplasmosis infection in pregnant women, aborted women, and women of childbearing age in Sudan is a major public health concern. Therefore, it is essential to raise awareness about the risks of toxoplasmosis infection among this population and to take measures to reduce its spread. This includes educating women about how to protect themselves and their children, as well as conducting further research to understand the risk factors for toxoplasmosis infection in Sudan and to develop more effective prevention and control strategies.

The results of the present study suggest that Sudanese blood donors have a high risk of toxoplasmosis infection, with a prevalence of 31%. This is slightly lower than the global prevalence of toxoplasmosis of 33%, as reported in 2016 (99). Studies showed that T. gondii parasites can survive in blood for several weeks, and blood banks screen donated blood for T. gondii antibodies(2, 100, 101). However, this test is not perfect and does not detect all infections.

The high prevalence of toxoplasmosis infection among blood donors in Sudan is a significant public health concern, as it can lead to the transmission of the parasite to recipients through transfusion. Therefore, it is important to take steps to reduce the risk of toxoplasmosis infection in blood donors. This could include educating blood donors about the risks of toxoplasmosis infection and how to protect themselves, as well as adopting more sensitive and accurate tests for detecting T. gondii infection in blood, such as PCR in the blood bank tests (102).

Finally, the present study is the first national or regional survey of human toxoplasmosis in Sudan. Its findings contribute to our understanding of the burden of human toxoplasmosis in Sudan and help identify high-risk groups and areas. This information can guide public health interventions, such as educational campaigns, screening programs, and targeted treatment strategies.

The serious public health issues reported in the current study warrant collaborative effort and immediate action from policymakers and governments to adopt a nationwide epidemiological program to clarify the design of regional strategies and guide the development of prevention and eradication programs in the spirit of the One Health concept.

This study has several limitations. First, it is based on observational data, which cannot establish a causal relationship between the risk factors identified and the development of toxoplasmosis infection. Second, the study included studies from different regions of Sudan, which may have different prevalence rates of toxoplasmosis infection. Third, the study included studies with different methodologies, which may have introduced some bias to the findings. Fourth, the study included studies that did not address the potential for cross-reactivity, which can lead to diagnostic bias. Therefore, it is important to keep in mind the limitations of this study when interpreting the findings. More research is needed to identify specific risk factors for toxoplasmosis infection in Sudan and to address the potential for cross-reactivity.

In conclusion, the meta-analytical study provides valuable insights into the epidemiology of human toxoplasmosis in Sudan, with an overall prevalence of 36%. The study highlights the high prevalence of toxoplasmosis infection among hemodialysis patients, childbearing-age women, HIV patients, WOEA, aborted women, pregnant women, and blood donors in Sudan. The study also found that males and people from southern and northern Sudan have a higher prevalence of toxoplasmosis infection than females and people from central and eastern Sudan. The high prevalence of toxoplasmosis infection in these regions is a significant public health concern. It is essential to take measures to reduce its spread by educating people about how to protect themselves, conducting further research to understand the risk factors for toxoplasmosis infection in Sudan, and developing more effective prevention and control strategies. However, the interpretation of these findings should take into consideration the presence of substantial heterogeneity among the included studies.

Author contributions

Abdullah Mohammed: conceptualized the study, designed the search strategy, conducted the literature search, screened and selected studies, extracted data, performed the meta-analysis, interpreted the results, drafted the manuscript, and revised the manuscript.

Musa Ahmed: assisted with the design of the search strategy, conducted the literature search, screened and selected studies, extracted data, and reviewed the manuscript.

Nasir IBRAHIM: assisted with the design of the search strategy, conducted the literature search, screened and selected studies, extracted data, and reviewed the manuscript.

All authors approved the final version of the manuscript.

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The authors declare no competing interests.

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Seroprevalence of human toxoplasmosis in Sudan from 1990 to 2022: A systematic review and meta-analysis

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Abstract

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1. Introduction

2. Materials and methods

2.1. Design and protocol registration

2.2. Data items, information sources, and search strategy

2.3. Inclusion and exclusion criteria

2.4. Study selection process and risk of bias assessment

2.5. Data extraction process

2.6. Synthesis methods

3. Results

3.1. Study identification and selection

3.2. The main characteristics of the included studies

3.3. Results of synthesis

3.4. Subgroup analysis

4. Discussion

5. Conclusion

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References

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