Prevalence of Toxoplasmosis among the Human Population in Indonesia: A Systematic Review and Meta-Analysis

doi:10.21203/rs.3.rs-4954271/v1

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Systematic Review

Prevalence of Toxoplasmosis among the Human Population in Indonesia: A Systematic Review and Meta-Analysis

https://doi.org/10.21203/rs.3.rs-4954271/v1

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Background

Toxoplasma gondii is a ubiquitous parasite that can cause significant complications when it infects pregnant women and immunocompromised patients. These complications include miscarriage, fetal abnormalities, and fatal cerebral toxoplasmosis. Despite its significance, the true burden of toxoplasmosis in Indonesia remains underexplored. Therefore, we aim to assess the prevalence of toxoplasmosis among the human population in Indonesia using serological, molecular, and histopathological examinations. In addition, we assessed whether the prevalence differed across geographical regions, populations, or population risk levels.

Methods

Following Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines, we conducted a systematic review and meta-analysis of data retrieved from PubMed, Google Scholar, and Portal Garuda. We pooled prevalence data using the inverse-variance method and a random effects model. Heterogeneity was assessed using I² statistics and Cochran’s Q test. Study quality was evaluated using a checklist for prevalence studies developed by the Joanna Briggs Institute. Publication bias was assessed using Doi plots and Luis Furuya-Kanamori (LFK) index. We performed subgroup analysis, meta-regression, and sensitivity analysis to explore sources heterogeneity and the robustness of the pooled estimates.

Result

In total, 52 studies were included in this study. The adjusted pooled seroprevalence was 58.13% (95% CI: 49.56–66.24%). We observed no subgroup differences based on study location, study population, population risk level, sample size, detection method, or study quality. The range of toxoplasmosis prevalence as measured via polymerase chain reaction and histopathological examination was 0–32.81% and 0%, respectively. Meta-analysis was not performed for molecular or histopathological data.

Conclusion

Toxoplasmosis is highly prevalent among the human population in Indonesia; however, our study mainly relied on studies with small-sample sizes. Furthermore, most of the studies were performed in Java; therefore, some high-quality population-based studies must be conducted in other regions of Indonesia to better estimate the prevalence of toxoplasmosis across the country.

Toxoplasma gondii

Systematic Review

Meta-analysis

Prevalence

Toxoplasma gondii is an apicomplexan parasite that infects most warm-blooded animals, including humans. In otherwise healthy adults, Toxoplasma infection, known as toxoplasmosis, typically results in asymptomatic chronic infection. However, in several particular populations, toxoplasmosis may lead to debilitating or even fatal illness. For example, acute toxoplasmosis in pregnant women can lead to miscarriage, preterm birth, low birth weight, and fetal abnormalities [1, 2]. In patients with HIV, acute or reactivated toxoplasmosis may result in cerebral or disseminated toxoplasmosis, with cerebral toxoplasmosis having an estimated mortality rate of approximately 30% [3–5]. Survivors may face persistent neurological deficits [6].

The prevalence of Toxoplasma infection in humans varies between regions and communities, depending on social, economic, and cultural factors [7, 8]. For example, Jones et al. reported an adjusted seroprevalence of 22.5% among people over 12 years of age in the United States [9]. A study in Germany estimated that 55% of adults in the country are seropositive for Toxoplasma [10]. However, much lower Toxoplasma seroprevalence was observed in China, with only 12.3% of the examined samples being positive [11].

A recent meta-analysis [12] estimated that the seroprevalence of Toxoplasma infection in Indonesia is at least 60%, but this estimate was based on a single study [13]; the authors’ search strategy did not include Indonesian journal databases such as Portal Garuda, in which several articles on this subject are indexed. To address this gap, we conducted a systematic review and meta-analysis to assess the prevalence of Toxoplasma infection in the human population in Indonesia as measured via serological, molecular, and histopathological examination. In addition, we assessed whether the prevalence differs across geographical regions, populations, or population risk levels.

This systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 guidelines [14] and is registered with PROSPERO (ID CRD42023466909). The PRISMA 2020 checklist is available in Additional file 1.

Eligibility Criteria

We included studies that met the following criteria:

Reported the prevalence of Toxoplasma gondii infection in the human population in Indonesia or presented data to estimate prevalence

Detailed the diagnostic methods used to estimate the prevalence of Toxoplasma gondii infection in the human population in Indonesia

Were published before July 2024

We excluded studies that met the following criteria:

Did not contain primary data (e.g., reviews)

Were case reports

Had limited access and failed to respond to follow-up emails twice

Search Strategy

We searched PubMed, Google Scholar, and Portal Garuda for eligible records using a combination of identified keywords (Additional file 2). Boolean operators and truncation were used to increase the sensitivity of the search strategy. No language or study type restrictions were applied. We retrieved all the records identified through searches in both PubMed and Portal Garuda. However, as Google Scholar has a limited filtering capability, only records that were present in the first 10 pages of the search results were retrieved. The identified records were then uploaded to Rayyan [15] for review.

Selection Process

After deduplication, two reviewers (SK and AHD) independently selected records that satisfied the eligibility criteria. Any disagreements between the reviewers were resolved through discussion. Afterward, a third reviewer (TMP) confirmed the eligibility of the records included. The reviewers were not blinded to the journal titles, study authors, or institutions.

Data Extraction

In this review, Toxoplasma infection is defined as the detection of signs of Toxoplasma infection through serological, histopathological, or molecular testing of the human population. The primary outcome of this review is the pooled prevalence of Toxoplasma infection in the human population in Indonesia. Prevalence is defined as the ratio of positive samples to the total number of samples. The results obtained from different examination strategies were pooled separately. Moreover, the additional outcomes of this study were the prevalence of Toxoplasma infection across different geographical regions, study populations, and population risk levels. The study locations were grouped based on the major geographical regions to which they belong, which were Java, Sumatera, Kalimantan, Sulawesi and Maluku, Lesser Sunda Island, and Papua. The population risk level was stratified into high- and low-risk groups [16]. Populations that belonged to the high-risk group included women with a history of miscarriage and/or stillbirth, people who routinely have close contact with animals (e.g., animal market workers, pet shop workers), cat owners, immunocompromised patients, and psychiatric patients. Populations that did not belong to any of these groups were classified as low risk.

We extracted the following data from the studies: first author’s last name, year of publication, study location, population studied, diagnostic method, sample size, and total number of cases. If the number of cases was not presented directly, we inferred it based on the reported prevalence. These data were extracted into a Google Sheets spreadsheet by the two reviewers (SK and AHD). A third author (TMP) referred to the original studies to confirm whether these data had been extracted correctly.

Quality Assessment

The quality of the records that were included was assessed independently by two authors (SK and AHD), using a checklist for prevalence studies developed by the Joanna Briggs Institute [17]. When assessing the question, “Was the sample size adequate?”, we estimated the minimum sample size via the formula [n = z^2 * (p * (1-p))/e^2], where z was set at 95%, e was set at 5%, and p was set at 16.4% following the estimated prevalence of toxoplasmosis in Asia [12]. Based on these findings, we set the minimum sample size at 211 participants and used this value as our evaluation standard. A score was calculated based on the proportion of “yes” answers. Afterward, the records were classified as “low risk of bias,” “moderate risk of bias,” or “high risk of bias” if their scores were ≥ 70%, 50–69%, or ≤ 49%, respectively [18, 19]. Studies were included regardless of their risk of bias (RoB) assessment results.

Data Analysis

To synthesize systematic review data, a combination of narrative and quantitative approaches was used. Unless otherwise stated, all data processing and analysis were conducted via R (version 4.4.1). Meta-analysis was performed via the Meta (version 7.0–0) and MetaSens (version 1.5-2) packages in R [20]. The prevalence estimate was calculated for each study and we then pooled the prevalence data via the inverse-variance method and a random effects model. We also calculated the 95% confidence interval (95% CI). A summary of the results and the heterogeneity among the studies was presented via a forest plot. I² statistics were used to determine heterogeneity, with a value of > 75% considered substantial heterogeneity [19]. Cochran’s Q test was used to test the significance of heterogeneity. Subgroup analysis and meta-regression were performed to explore potential sources of heterogeneity. Moderators that were assessed in this analysis included geographical region, study population, population risk level, sample size, detection method, and RoB assessment results. In addition, sensitivity analysis was performed to assess any study that might impact the pooled prevalence estimate. Doi plots and the Luis Furuya-Kanamori (LFK) index were used to assess the presence of publication bias [21]. A p-value was considered significant if it was < 0.01.

Our search identified 489 publications (Fig. 1), 85 of which passed the initial screening and were retrieved for further assessment. Among these, 52 met our inclusion criteria and were, therefore, included in the subsequent analysis.

In general, Toxoplasma infections are diagnosed via either serologic investigation or polymerase chain reaction (PCR). Two studies used multiple approaches to detect toxoplasmosis—Halleyantoro used PCR in addition to serology to detect Toxoplasma infection [22], and Sardjono used a histopathological approach as well as the other two methods to detect toxoplasmosis [23]. Forty-seven studies used IgG and/or IgM detection [8, 13, 22–66]. Among these, three studies used only IgM [35, 45, 62]. One study [58] re-analyzed HIV + serum samples collected between 2009 and 2011. This group of samples overlapped with the one analyzed in two other studies [53, 59]. Therefore, we included only the data retrieved from the HIV patients in these two studies. Moreover, seven studies detected Toxoplasma infections through the PCR of blood (two studies), cerebrospinal fluid (CSF; two studies), ocular fluid (one study), pregnancy products (one study), and urine samples (one study) [22, 23, 67–71]. All these studies used the B1 gene as their PCR target.

Quality Assessment

The RoB for the included studies was assessed via a checklist for prevalence studies developed by the Joanna Briggs Institute [17]. Overall, 14 studies (26.92%) had a low RoB, 23 studies (44.23%) had a moderate RoB, and 15 studies (28.85%) had a high RoB (Additional file 3). Most studies (n = 40) had sample sizes of fewer than 211 participants. All studies, regardless of the RoB, were included in our analysis, as they may still represent the status of toxoplasmosis in a real-world setting.

Pooled Seroprevalence of Toxoplasmosis

The data from the 47 studies (Table 1) that assessed the seroprevalence of toxoplasmosis were derived from 10,295 participants [8, 13, 22–66]. Among them, 5540 cases were identified. According to the random effects model (Fig. 2), the pooled seroprevalence of toxoplasmosis in Indonesia was 46.27% (95% CI: 39.58–53.09%). As expected, the pooling result was substantially heterogeneous (I² = 94.1% (95% CI: 92.9–95.1%); Q < 0.0001).

Table 1

List and characteristics of studies that assessed the *Toxoplasma* seroprevalence in Indonesia.
Author	Location	Region	Method	Population	Risk Group	Case	Sample	ROB Score	Ref
Afrianti (2023)	Semarang City	Java	ELFA	Cat Owner	High	6	25	67	[41]
Afrianti (2023)	Semarang City	Java	ELFA	General population	Low	2	25	67	[41]
Afrianti (2024)	Semarang Regency	Java	ELFA	General Population	Low	47	177	67	[42]
Agustin (2015)	Surabaya City	Java	ELISA	Cat Owner	High	13	25	78	[43]
Agustin (2015)	Surabaya City	Java	ELISA	General population	Low	12	25	78	[43]
Arwie (2019)	Makassar City	Sulawesi and Maluku	AT	People with Close Contact with Animals	High	4	10	44	[40]
Darmawan (2019)	Jambi City	Sumatera	LFA	General population	Low	17	41	56	[39]
Dwinata (2016)	Badung Regency	Lesser Sunda Islands	ELISA	Pregnant women	Low	36	330	67	[38]
Dzikriana (2020)	Surabaya City	Java	LFA	People with Close Contact with Animals	High	26	30	56	[34]
Fatmawati (2021)	Batu City	Java	ELISA	People with Close Contact with Animals	High	4	25	33	[35]
Febianingsih (2017)	Gianyar Regency	Lesser Sunda Islands	ELISA	General population	Low	136	240	78	[37]
Fihiruddin (2020)	Sleman Regency	Java	ELISA	General population	Low	224	385	78	[36]
Halleyantoro (2019)	Jakarta	Java	ELISA	Immunocompromised Patients	High	34	88	56	[22]
Hanina (2023)	Jambi City	Sumatera	ELFA	Women with History of Miscarriage and/or Stillbirth	High	22	52	56	[32]
Harianja (2021)	Samarinda City	Kalimantan	ECLIA	Cat Owner	High	10	23	56	[31]
Humaryanto (2020)	Jambi City	Sumatera	AT	General Population	Low	36	60	56	[30]
Iskandar (2017)	Malang City	Java	ELISA	General Population	Low	50	57	44	[33]
Jayawardhana (2023)	Sidoarjo Regency	Java	AT	Immunocompromised Patients	High	4	30	33	[29]
Konishi (2000)	Surabaya City	Java	ELISA	General Population	Low	1021	1761	67	[28]
Krihariyani (2015)	Surabaya City	Java	ELISA	Pregnant Women	Low	26	40	33	[27]
Laksemi (2013)	Denpasar City	Lesser Sunda Islands	ELISA	General Population	Low	391	790	44	[26]
Laksmi (2016)	Karangasem Regency	Lesser Sunda Islands	ELISA	General Population	Low	14	106	78	[25]
Lestari (2016)	Minahasa Regency	Sulawesi and Maluku	AT	General Population	Low	15	22	44	[24]
Marthalia (2020)	Surabaya City	Java	ELFA	Cat Owner	High	11	19	44	[66]
Meirawan (2023)	Jakarta	Java	ELISA	Immunocompromised Patients	High	38	56	56	[65]
Muflikhah (2018)	Sleman Regency	Java	ELISA	Psychiatric Patients	High	65	94	56	[64]
Muflikhah (2018)	Sleman Regency	Java	ELISA	General Population	Low	42	64	56	[64]
Murkati (2004)	Surakarta Regency	Java	ELISA	Women with History of Miscarriage and/or Stillbirth	High	33	100	56	[63]
Nadayang (2020)	Jakarta	Java	ELISA	Pregnant Women	Low	2	33	33	[62]
Polanunu (2022)	Makassar City	Sulawesi and Maluku	ELISA	Pregnant Women	Low	60	184	89	[60]
Prasetyo (2014)	Surakarta Regency	Java	ELISA	General Population	Low	39	130	67	[59]
Prasetyo (2015)	Central Java Province	Java	ELISA	Immunocompromised Patients	High	260	597	78	[58]
Pratama (2023)	South Tangerang City	Java	LFA	People with Close Contact with Animals	High	11	25	78	[61]
Rahman (2024)	Yogyakarta City	Java	LFA	General Population	Low	14	25	33	[55]
Reshnaleksmana (2014)	West Nusa Tenggara Province	Lesser Sunda Islands	ELISA	Psychiatric Patients	High	23	42	56	[57]
Retmanasari (2017)	Central Java Province	Java	ELISA	General Population	Low	394	630	78	[8]
Riansari (2023)	Semarang City	Java	ELISA	General Population	Low	43	88	56	[56]
Sanjaya (2009)	Manado City	Sulawesi and Maluku	AT	General Population	Low	22	50	56	[54]
Sardjono (2002)	Malang City	Java	ELISA	Pregnant women	Low	14	23	78	[23]
Sardjono (2002)	Malang City	Java	ELISA	Women with History of Miscarriage and/or Stillbirth	High	22	43	78	[23]
Sari (2015)	Central Java	Java	ELISA	General Population	Low	150	357	78	[53]
Sari (2014)	Bantul Regency	Java	ELISA	Cat Owner	High	7	11	56	[52]
Sari (2014)	Bantul Regency	Java	ELISA	General Population	Low	43	79	56	[52]
Seran (2016)	Minahasa Regency	Sulawesi and Maluku	AT	General Population	Low	11	22	78	[50]
Setia (2023)	Malang City	Java	ECLIA	Immunocompromised Patients	High	87	87	56	[51]
Terazawa (2003)	Jakarta	Java	ELISA	General Population	Low	1185	1693	78	[13]
Tuda (2016)	Manado City	Sulawesi and Maluku	AT	General Population	Low	72	135	67	[49]
Tuda (2016)	Manado City	Sulawesi and Maluku	AT	Pregnant Women	Low	47	109	67	[49]
Tuda (2017)	North Sulawesi, Gorontalo, and North Maluku Province	Sulawesi and Maluku	AT	General Population	Low	501	856	78	[48]
Uga (1993)	Sidoarjo Regency	Java	ELISA	General Population	Low	156	244	56	[47]
Widyaswara (2024)	Magelang Regency	Java	LFA	General Population	Low	0	25	44	[44]
Wikandari (2024)	Semarang City	Java	ELISA	General Population	Low	31	87	56	[46]
Wulandari (2019)	Sleman Regency	Java	ELISA	General Population	Low	1	20	33	[45]
ELFA: Enzyme-linked fluorescence assay; ELISA: Enzyme-linked immunosorbent assay; AT: Agglutination Test; LFA: Lateral-flow Immunoassay; ECLIA: Enhanced chemiluminescence immunoassay; ROB: Risk-of-Bias.

To determine the pooling result, we performed a sensitivity analysis using two scenarios and a leave-one-out analysis. In the first scenario, we included five studies that assessed the seroprevalence of toxoplasmosis but did not specify their detection methods, therefore, these studies did not meet our inclusion criteria [72–76]. In the second scenario, we excluded three studies in which only IgM was detected [35, 45, 62]. The results of the two scenarios were 45.87% (95% CI: 39.35–52.53%) and 48.70% (95% CI: 42.37–55.07%), respectively. Furthermore, when we performed a leave-one-out analysis, the meta-analysis results remained stable after re-evaluation. Detailed sensitivity analysis results can be seen in Additional file 4.

Subgroup analysis was then performed based on the region in which the study took place, the study population, the population risk level, the sample size, the detection method, and the RoB assessment result. Some of the studies derived their data from different populations, therefore, the number of data sources for the subgroup analysis differed from the number of studies included.

Table 2

Subgroup analysis results.
Sub-Group Name	Number of data source	Pooled Prevalence	95%CI	I²	Subgroup Differences
By Region
Java	31	47,38%	37,96% − 57,00%	93,8%	P = 0,7709
Sumatera	3	48,37%	36,36% − 60,57%	57,5%
Kalimantan	1	43,48%	25,22% − 63,69%	-
Lesser Sunda Islands	5	33,10%	15,00% − 58,11%	97,7%
Sulawesi and Maluku	7	50,24%	40,91% − 59,55%	86,4%
Papua	0	-	-	-
By Study Population
General Population	28	48,52%	40,98% − 56,12%	93,4%	P = 0,2697
Cat Owner	5	46,79%	33,66% − 60,38%	45,1%
People with routine close contacts with animals	4	47,39%	17,72% − 79,03%	86,4%
Pregnant women	6	32,20%	14,57% − 56,96%	94,7%
Women with history of miscarriage and/or stillbirth	3	40,96%	30,92% − 51,81%	53,8%
Immunocompromised patients	5	59,88%	17,46% − 91,33%	89,1%
Psychiatric patients	2	63,10%	48,44% − 75,69%	61,5%
By Population Risk Level
Low risk	34	45,22%	37,49% − 53,19%	94,9%	P = 0,5942
High risk	19	48,74%	38,68% − 58,90%	80,9%
By Sample Size
< 211 Samples	35	44,20%	35,68% − 53,07%	87,7%	P = 0,3206
≥ 211 Samples	12	51,12%	40,80% − 61,34%	97,3%
By Detection Method
ELFA	4	33,26%	18,65% − 52,01%	80,5%	P = 0,4828
ELISA	28	45,33%	36,78% − 54,16%	95,8%
AT	8	50,83%	40,38% − 61,22%	72,9%
LFA	5	45,91%	17,37% − 77,40%	81,5%
ECLIA	2	90,74%	4,63% − 99,95%	92,6%
By ROB Assessment Result
Low risk of bias	13	53,53%	47,70% − 59,27%	94,7%	P = 0,1443
Moderate risk of bias	23	45,34%	35,81% − 55,23%	94,6%
High risk of bias	11	33,69%	15,49–58,47%	87,9%
ELFA: Enzyme-linked fluorescence assay; ELISA: Enzyme-linked immunosorbent assay; AT: Agglutination Test; LFA: Lateral-flow Immunoassay; ECLIA: Enhanced chemiluminescence immunoassay; ROB: Risk-of-Bias.

Pooled seroprevalence by region

In total, 31 studies were performed in Java, three in Sumatera, one in Kalimantan, five in the Lesser Sunda Islands, and seven in Sulawesi and Maluku (Table 2; Additional file 5). No study has been performed in Papua. The pooled seroprevalence rates of toxoplasmosis in Java, Sumatera, Kalimantan, Lesser Sunda Island, and Sulawesi and Maluku were 47.38% (95% CI: 37.96–57.00%), 48.37% (95% CI: 36.36–60.57%), 43.48% (25.22–63.69%), 33.10% (95% CI: 15.00–58.11%), and 50.24% (95% CI: 40.91–59.55%), respectively. No differences between subgroups were observed (p = 0.7709).

Pooled seroprevalence by study population

The data from the studies were derived from eight groups of study populations (Table 2; Additional file 5). These include the general population (n = 28), cat owners (n = 5), people who routinely had close contact with animals (n = 4), pregnant women (n = 6), women with a history of miscarriage and/or stillbirth (n = 3), immunocompromised patients (n = 5), and psychiatric patients (n = 2). Unintentionally, the immunocompromised group comprised only HIV-infected individuals. The pooled prevalence rates for each of these population groups were 48.52% (95% CI: 40.98–56.12%) for the general population, 46.79% (95% CI: 33.66–60.38%) for cat owners, 47.39% (95% CI: 17.72–79.03%) for people who routinely had close contact with animals, 32.20% (95% CI: 14.57–56.96%) for pregnant women, 40.96% (95% CI: 30.92–51.81%) for women with a history of miscarriage and/or stillbirth, 59.88% (95% CI: 17.46–91.33%) for immunocompromised patients, and 63.10% (95% CI: 48.44–75.69%) for psychiatric patients. No differences between the subgroups were observed (p = 0.2697).

Pooled seroprevalence by population risk level

In total, we found 19 data points from the high-risk group and 34 data points from the low-risk group (Table 2; Additional file 5). The pooled seroprevalence of toxoplasmosis in the high-risk group was 48.74% (95% CI: 38.68–58.90%), whereas that in the low-risk group was 45.22% (37.49–53.19%). We observed no differences between the subgroups (p = 0.5942).

Pooled seroprevalence by sample size

We separated the studies by whether they passed our minimum sample size (211 samples) or not. As a result, 12 studies passed the threshold, whereas 35 did not (Table 2; Additional file 5). The pooled seroprevalence of studies that passed the threshold was 51.12% (95% CI: 40.80–61.34%), whereas studies that did not pass the threshold had a seroprevalence of 44.20% (95% CI: 35.68–53.07%). We observed no statistically significant differences between the subgroups (p = 0.3206).

Pooled seroprevalence by detection method

The studies assessed the seroprevalence of toxoplasmosis using an enzyme-linked fluorescence assay (ELFA; four studies), an enzyme-linked immunosorbent assay (ELISA; 28 studies), an agglutination test (AT; eight studies), a lateral flow assay (LFA; five studies), and an enhanced chemiluminescence immunoassay (ECLIA; two studies). The pooled seroprevalence rates based on ELFA, ELISA, AT, LFA, and ECLIA were 33.26% (95% CI: 18.65–52.01%), 45.33% (95% CI: 36.78–54.16%), 50.83% (95% CI: 40.38–61.22%), 45.91% (95% CI: 17.37–77.40%), and 90.74% (4.63–99.95%), respectively (Table 2; Additional file 5). No substantial differences between the subgroups were observed (p = 0.4828).

Pooled seroprevalence by RoB assessment results

Most of the studies had a medium RoB (23 studies), followed in descending order by a low RoB (13 studies) and a high RoB (11 studies). The pooled seroprevalence rate based on the RoB assessment results was 53.53% (95% CI: 47.70–59.27%) for studies with a low RoB, 45.34% (95% CI: 35.81–55.23%) for studies with a medium RoB, and 33.69% (95% CI: 15.49–58.47%) for studies with a high RoB (Table 2; Additional file 5). No significant differences between the subgroups were observed (p = 0.1443).

Meta-regression for seroprevalence studies

As assessed by meta-regression, the seroprevalence of toxoplasmosis was not affected by the study region (p = 0.7247), study population (p = 0.7351), population risk level (p = 0.5984), sample size (p = 0.3781), detection method (p = 0.4424), or RoB assessment result (p = 0.3339).

Toxoplasmosis Prevalence by PCR

Seven studies assessed the number of Toxoplasma infections via PCR (Table 3), three studies assessed the prevalence of toxoplasmosis in patients with HIV, two assessed toxoplasmosis in pregnant women, one assessed toxoplasmosis in patients with ophthalmological and/or neurological problems, and one evaluated toxoplasmosis in women who had recently experienced miscarriage [22, 23, 67–71]. However, these studies used different sample types including urine, CSF, ocular fluid, blood, and pregnancy tissue. Therefore, we deemed it inappropriate to perform a meta-analysis on these studies.

Table 3

List and characteristics of studies that assessed the *Toxoplasma* prevalence in Indonesia via PCR
Author	Location	Region	PCR Sample	Target Gene	Population	Risk Group	Case	Sample	ROB Score	Ref
Naully (2020)	West Bandung Regency	Java	Blood PCR	B1 Gene	Pregnant Women	Low	7	50	44	[67]
Naully (2022)	Bandung Regency	Java	Blood PCR	B1 Gene	Pregnant Women	Low	3	42	44	[68]
Ganiem (2013)	Bandung City	Java	CSF PCR	B1 Gene	Immunocompromised Patients	High	21	64	78	[70]
Halleyantoro (2019)	Jakarta	Java	CSF PCR	B1 Gene	Immunocompromised Patients	High	23	88	56	[22]
Kurniawan (2020)	Jakarta	Java	Ocular Fluid PCR	B1 Gene	Patients with ophthalmological and/or neurological complaints	High	8	64	44	[69]
Sardjono (2002)	Malang City	Java	Pregnancy product PCR	B1 Gene	Women with History of Miscarriage and/or Stillbirth	High	0	43	78	[23]
Fitriana (2021)	Jakarta	Java	Urine PCR	B1 Gene	Immunocompromised Patients	High	7	30	33	[71]
CSF: Cerebrospinal Fluid

Toxoplasmosis prevalence by PCR from blood samples

In two separate publications, Naully examined the prevalence of toxoplasmosis in two different regions in West Java via PCR of blood samples [67, 68]. In West Bandung Regency, Naully recruited 50 pregnant women and reported that 14.00% of their number had toxoplasmosis. On the other hand, Naully found that 7.14% of 42 participants in Bandung Regency tested positive for toxoplasmosis.

Toxoplasmosis prevalence by PCR from CSF samples

Both Ganiem (2013) and Halleyantoro (2019) assessed the prevalence of toxoplasmosis in HIV + patients who presented with neurological symptoms [22, 70]. Both studies used patients’ CSF samples as material for their PCR examination. Ganiem (2013), who conducted a study in West Java, reported that 32.81% of 64 patients tested positive for toxoplasmosis, while among the 88 patients recruited by Halleyantoro (2019) in Jakarta, 26.14% were found to be positive for toxoplasmosis.

Toxoplasmosis prevalence by PCR from ocular fluid samples

Only one study by Kurniawan (2020) used PCR from ocular fluid samples. This study was performed in Jakarta and included 64 patients with atypical uveitis. The prevalence of toxoplasmosis was 12.5%.

Toxoplasmosis prevalence by PCR from pregnancy clinical samples

The study by Sardjono (2002) performed in East Java Province is the only one that performed PCR on pregnancy tissue samples [23]. The study examined tissue samples from spontaneous abortion cases (n = 43) for the Toxoplasma B1 gene. None of the tissues examined tested positive for Toxoplasma.

Toxoplasmosis prevalence by PCR from urine samples

Fitriana (2021) examined urine samples from 30 HIV + patients who were hospitalized at Pengayoman Hospital, Jakarta, for the Toxoplasma B1 gene [71]. Seven of the samples tested positive for the target gene, giving a 23.33% prevalence of toxoplasmosis in this study.

Table 4

List and characteristics of studies that assessed the *Toxoplasma* prevalence in Indonesia via histopathological examination
Author	Location	Region	Staining Method	Population	Risk Group	Case	Sample	ROB Score	Ref
Sardjono (2002)	Malang City	Java	hematoxylin-eosin	Women with History of Miscarriage and/or Stillbirth	High	0	43	78	[23]

Toxoplasmosis Prevalence by Histopathology

Only one study—done by Sardjono—examined toxoplasmosis histopathologically (Table 4). The sample consisted of 43 women who had experienced spontaneous abortion, and 1 cm³ of tissue sample was collected from the expelled pregnancy product to be stained using hematoxylin‒eosin and examined via light microscopy. These tissue samples included decidua (n = 35), chorionic villi (n = 19), and trophoblasts (n = 17). They did not find any parasites or Toxoplasma-associated inflammatory reactions. Instead, they found necrotic tissue with nonspecific inflammation and mononuclear and polymorphonuclear cell infiltration.

Publication Bias Analysis

We performed publication bias analysis on studies that used serological tests with the LFK index and Doi plot. Unfortunately, since the number of extant studies was insufficient, we could not perform publication bias analysis on studies that used PCR and histopathological examination. We detected publication bias in favor of studies with lower seroprevalence rates (LFK index = − 2.35; Fig. 3). We then performed a trim-and-fill analysis, which assigned 13 studies (Fig. 4). This resulted in a pooled seroprevalence of 58.13% (95% CI: 49.56–66.24%; τ²: 1.6924; I²: 95.6%).

This systematic review and meta-analysis were conducted to approximate the true prevalence of toxoplasmosis in Indonesia based on the available literature. Unlike other systematic reviews on similar topics, we included Portal Garuda, a database that indexes literature published in Indonesian journals. Given that many of these studies were published in the Indonesian language, our attempt allowed us to minimize the occurrence of language bias in our work. In addition, we examined the RoB of the studies rigorously using a critical appraisal tool for prevalence studies developed by the Joanna Briggs Institute [77]. Based on the results of the RoB assessment, only 14 out of 52 studies were classified as having a low risk of bias. Compared with studies that have a high RoB, these studies tend to recruit a higher number of samples and have a higher prevalence with narrower confidence intervals. In addition, when we pooled only the seroprevalence of studies with a low RoB, the result was close to the adjusted seroprevalence.

Serological examination is the most prevalent approach used by clinicians and researchers to detect Toxoplasma infection. In our study, 47 out of 52 studies used this approach. The adjusted seroprevalence of toxoplasmosis in Indonesia that we found was 58.13%. This result was comparable to those of other systematic reviews conducted in Thailand and Malaysia, which reported seroprevalence rates of between 2.6% and 53.7% in Thailand and between 10.6% and 59.7% in Malaysia [78, 79]. However, other neighboring countries, namely, Cambodia, Singapore, Myanmar, Laos, and Vietnam, had much lower estimated seroprevalence rates of between 5.8% and 31.7% [79]. In addition, our estimated seroprevalence was higher than the overall estimated seroprevalence in Asia, which ranges from 16.4–29% [12, 80, 81]. However, as noted by Fuchs et al., many of these studies derived their data from limited regions within the country and particular cohorts only [79]. This makes it difficult to extrapolate these data to a country-wide level. Our review encountered a similar problem in that while our region-based subgroup analysis indicated that these regions have similar toxoplasmosis seroprevalence rates (p = 0.1913), most of the studies were conducted in Java (n = 31). The regions with the second highest number of studies were Sulawesi and Maluku with only seven studies. Moreover, no study has been conducted in Papua. Given this context, the results of our region-specific toxoplasmosis seroprevalence must be interpreted with care.

We estimated that the seroprevalence of toxoplasmosis among women with a history of miscarriage and/or stillbirth was 40.96%. These data were derived from three studies that reported 195 cases in total. Our findings are similar to those of several other meta-analyses that investigated similar conditions. The reported seroprevalence ranged from 32–43% [16, 82, 83]. Indeed, toxoplasmosis has long been reported as one of the risk factors for miscarriage, with IgM seropositivity resulting in a higher chance of miscarriage than IgG seropositivity alone [1, 83]. Moreover, our PCR-based estimate for this cohort returned zero detected cases. This rate is much lower than the estimate provided by Kalantari et al., who reported 10% positive PCR results among women with recent and spontaneous abortions [1]. Notably, our estimate was based on one study and thus, difficult to extrapolate.

Cats are the definitive hosts of Toxoplasma. As such, they are believed to be a significant risk factor for toxoplasmosis through close contact with them [84, 85]. In addition, given that Toxoplasma can infect virtually all warm-blooded animals, people with occupations that put them in close contact with animals are also thought to be at increased risk of contracting the disease [84]. However, in our study, the estimated seroprevalence of toxoplasmosis among cat owners, people who routinely have close contact with animals, and the general population did not differ substantially (46.79%, 47.39%, and 48.52%, respectively). There are several possible explanations for this. First, the studies that assess the toxoplasmosis seroprevalence specifically among cat owners and people who routinely have close contact with animals in the current review only included a small number of participants. This potentially makes them unable to assess the true prevalence accurately in the population. In addition, unlike feral cats, domestic cats may have a controlled food source, making toxoplasmosis less prevalent among their population and thus, reducing the possibility of them transmitting Toxoplasma [86, 87]. Regardless, a large population-based study assessing this issue might be needed to estimate more accurately the seroprevalence of toxoplasmosis among cat owners in Indonesia.

Our study revealed an alarmingly high seroprevalence of toxoplasmosis among HIV-infected individuals (59.88%). This prevalence is much higher than the estimated seroprevalence in the Asia–Pacific region, which is only 25.1% [88]. People infected with HIV are at increased risk of suffering from severe forms of toxoplasmosis, such as cerebral toxoplasmosis. This condition has approximately a 30% mortality rate and may even leave surviving patients with lingering sequelae [3–6]. The Indonesian government recommends Toxoplasma screening for all patients newly diagnosed with HIV [89]. In addition, HIV-infected individuals with CD4 + T cells of fewer than 100 cells/µl and seropositive for Toxoplasma are required to receive primary prophylaxis via cotrimoxazole.

The connection between toxoplasmosis and psychiatric disorders in humans has been studied extensively. For example, Toxoplasma IgG seropositivity was associated with schizophrenia and bipolar disorder [90, 91]. Hence, psychiatric patients are among the populations of interest when studying toxoplasmosis. In our analysis, the estimated seroprevalence of toxoplasmosis among psychiatric patients was 63.10%. This result was higher than the estimated seroprevalence in Asia as a whole, which was 43.0% [92].

The included studies assessed the seroprevalence of toxoplasmosis using different diagnostic methods, namely, ELFA, ELISA, AT, LFA, and ECLIA. Based on a systematic review conducted by Robert-Gangneux and Guegan, these tests have comparable sensitivity and specificity [93]. In parallel with this, we observed no statistically significant difference in the seroprevalence measured by any of the detection methods. In our study, ELISA was the most commonly used method. Indeed, ELISA is a relatively inexpensive, simple, and accessible test. This technique is readily accessible across academic, hospital, and even commercial laboratories in Indonesia. This explains at least partially why the overwhelming majority of the studies employed it.

The prevalence rates determined via PCR from blood, CSF, ocular fluid, pregnancy clinical samples, and urine samples were 7.14–14.00%, 26.14–32.81%, 12.5%, 0%, and 23.33%, respectively. Other studies reported that the prevalence of toxoplasmosis according to PCR ranges from 6–17.9%, depending on the type of sample [94–96]. This low prevalence was likely due to the progression of acute toxoplasmosis, which in an otherwise healthy individual only lasts for several days to weeks. Primarily, PCR examinations are employed to detect acute Toxoplasma infection, which narrows the detection window. In our study, higher rates of PCR positivity were detected in the CSF samples of patients with suspected cerebral toxoplasmosis, which unquestionably increased their pretest probability compared with those of other cohorts. Additionally, the central nervous system is one of the primary targets of Toxoplasma in humans, which makes it more likely to be detected in the CSF than in, for example, the peripheral blood [97, 98].

Histopathology is a technique rarely used to detect toxoplasmosis. When it is employed, its role is mostly to confirm other diagnostic results. For example, Mederle et al. examined the placenta of women who had experienced miscarriage and had positive IgM results [99]. The study failed to find any tachyzoites. Instead, they found signs of nonspecific immune activities. These findings align with the results of the histopathological assessment of our included studies. Sardjono et al. examined 43 pregnancy products expelled during miscarriage and found necrotic tissue with nonspecific inflammation and no tachyzoites [23].

Regardless, although we observed a high prevalence of toxoplasmosis among the human population in Indonesia, most of the studies had a small-sample size. Even when we set the standard to the modest 16.4% estimated prevalence in Asia overall [12], most of the studies did not meet our minimum sample size criteria. Studies with small-sample sizes tend to have wider margins of error, i.e., their observed prevalence is more likely to deviate from the true population prevalence [100]. In addition, most of the studies were conducted in Java. Therefore, although we attempted to ensure the robustness of our findings, care should be taken when extrapolating the data.

Overall, toxoplasmosis is highly prevalent among the human population in Indonesia. We observed an estimated 58.13% prevalence based on serological studies. However, our data were primarily derived from small-sample studies, most of which were conducted only in Java. Therefore, we recommend conducting large-scale, population-based studies in other regions of Indonesia to obtain a more accurate assessment of the true prevalence of toxoplasmosis.

PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses

RoB: Risk-of-Bias

CI: Confidence Interval

LFK Index: Luis Furuya-Kanamori Index

PCR: Polymerase Chain Reaction

CSF: Cerebrospinal Fluid

ELFA: Enzyme-linked fluorescence assay

ELISA: Enzyme-linked immunosorbent assay

AT: Agglutination Test

LFA: Lateral-flow Immunoassay

ECLIA: Enhanced chemiluminescence immunoassay

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

All data that were analyzed for this study are included in both the main manuscript and the additional files.

Competing interest

The authors declare that they have no competing interests.

Funding

This study received no funding.

Authors’ contributions

TMP wrote the the systematic review protocol, confirmed the eligibility of the included studies, cross-checked the validity of data extraction, analyzed the extracted data using R, and drafted the main manuscript text. AHD screened the eligibility of identified records, assessed the quality of the included studies, extracted the data of the included studies, and prepared the figures. SK screened the eligibility of identified records, assessed the quality of the included studies, extracted the data of the included studies, and prepared the tables. All authors reviewed the manuscript.

Acknowledgements

The authors would like to express their gratitude to Ahmad Watsiq Maula from the Department of Biostatistics, Epidemiology and Population Health, Universitas Gadjah Mada for his advice during the data analysis process. We thank Enago for providing their professional English language editing service.

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Prevalence of Toxoplasmosis among the Human Population in Indonesia: A Systematic Review and Meta-Analysis

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Abstract

Background

Methods

Result

Conclusion

Figures

Background

Methods

Eligibility Criteria

Search Strategy

Selection Process

Data Extraction

Quality Assessment

Data Analysis

Results

Quality Assessment

Pooled Seroprevalence of Toxoplasmosis

Pooled seroprevalence by region

Pooled seroprevalence by study population

Pooled seroprevalence by population risk level

Pooled seroprevalence by sample size

Pooled seroprevalence by detection method

Pooled seroprevalence by RoB assessment results

Meta-regression for seroprevalence studies

Toxoplasmosis Prevalence by PCR

Toxoplasmosis prevalence by PCR from blood samples

Toxoplasmosis prevalence by PCR from CSF samples

Toxoplasmosis prevalence by PCR from ocular fluid samples

Toxoplasmosis prevalence by PCR from pregnancy clinical samples

Toxoplasmosis prevalence by PCR from urine samples

Toxoplasmosis Prevalence by Histopathology

Publication Bias Analysis

Discussion

Conclusion

Abbreviations

Declarations

Ethics approval and consent to participate

Consent for publication

Availability of data and materials

Competing interest

Funding

Authors’ contributions

Acknowledgements

References

Additional Declarations

Supplementary Files

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