Associations of mental disorders and neurotropic parasitic diseases: a meta-analysis in developing and emerging countries

doi:10.21203/rs.2.13886/v3

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Associations of mental disorders and neurotropic parasitic diseases: a meta-analysis in developing and emerging countries

https://doi.org/10.21203/rs.2.13886/v3

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Although they are declining worldwide, neurotropic parasitic diseases are still common in developing and emerging countries. The aim of this study was to estimate the pooled prevalence and pooled association measures of comorbidities between mental disorders (anxiety, depression, bipolar disorder, and schizophrenia) and neurotropic parasitic diseases (malaria, cysticercosis, toxoplasmosis, human African trypanosomiasis, Chagas disease, and human toxocariasis) in developing and emerging countries. As the first meta-analysis on this topic, this study was performed in accordance with PRISMA guidelines. The protocol was registered in PROSPERO (N°CRD42017056521). The Medline, Embase, Lilacs, and Institute of Epidemiology and Tropical Neurology databases were used to search for articles without any restriction in language or date. We evaluated the quality of studies independently by two investigators using the Downs and Black assessment grid and pooled estimates using the random-effects method from CMA (Comprehensive Meta Analysis) Version 3.0. In total, 18 studies published between 1997 and 2016 met our inclusion criteria. We found that the prevalence of anxiety and depression in people suffering from Chagas disease and/or neurocysticercosis was 44.9% (95% CI, 34.4 – 55.9). In 16 pooled studies that included 1,782 people with mental disorders and 1,776 controls, toxoplasmosis and/or toxocariasis were associated with increased risk of schizophrenia and/or bipolar disorders (odds ratio = 2.3; 95% CI, 1.7 – 3.2). Finally, toxocariasis and/or toxoplasmosis were associated with an increased risk of the onset of schizophrenia (odds ratio = 2.4; 95% CI, 1.7 – 3.4). Our pooled estimates show that the associations between diseases studied are relatively high in developing and emerging countries. This meta-analysis supports the hypothesis that toxoplasmosis could be the cause of schizophrenia. These findings could prove useful to researchers who want to further explore and understand the associations studied. Keywords: Meta-analysis, association, co-morbidities, mental disorders, neurotropic parasitic diseases.

Health Economics & Outcomes Research

Health Policy

Infectious Diseases

Meta-analysis

association

co-morbidities

mental disorders

neurotropic parasitic diseases.

Although parasitic diseases are declining, they are still common in developing and emerging countries. Among the public health issues typically faced by developing and emerging countries (all non high income countries according to World Bank rankings) [1], neurotropic parasitic diseases are very common [2]. Neurotropic parasitic diseases such as malaria, cysticercosis, toxoplasmosis, human African trypanosomiasis (HAT), Chagas disease, and human toxocariasis have a predilection for infesting the central nervous system, which can lead to neurological disorders. Similarly, mental disorders are frequent with pooled 12-month period prevalence estimates of 17.6% (15.5% – 20.0%) in low and middle-income countries [3]. However, there are few studies regarding the association of mental disorders with neurological parasitoses in these countries.

To date, epidemiological studies have identified several risk factors for the different disease groups studied [4-9]. The table below (Table 1) provides a summary of the main risk factors of interest diseases in this meta-analysis. We have focused our attention on parasitic diseases due to the ever-present burden of these diseases in developing and emerging countries, and we selected the diseases according to their overall burden [10-13]. Mental disorders rank third among the foremost frequent diseases in the world after cancer and cardiovascular diseases [14].

In line with surveys conducted in developing and emerging countries, over 25% of individuals develop one or more mental or behavioural disorders throughout their lifetime [15]. Among the general population, severe depression affects 3% of people, generalised anxiety disorder affect 2%, and schizophrenia affects nearly 1% [16]. Parasitic diseases remain a major burden to developing and emerging countries, although this type of disease has declined globally. In 2015, out of 95 countries and territories in the world where malaria transmission remains high, it is estimated that the number of malaria cases was 214 million (95% CI, 149 - 303) and that malaria is responsible for 438,000 deaths per year (95% CI, 236 000 - 635 000) mainly in Africa (88%) [17]. In 2012, eight million individuals were already infected with Trypanosoma cruzi, the parasite that causes Chagas disease, in endemic areas of 21 Latin American countries. In addition, the chronic infection caused by this parasite is incurable, can be disabling, and causes more than 10,000 deaths per year [18]. The seroprevalence of toxocariasis varies from 2.4% to 30.0% in Europe [19], but in tropical countries, higher prevalences have been reported: 7.5% to 92.8% in Africa [20, 21], 6.4% to 52.0% in South America [22, 23], and 5.0% to 84.6% in Asia [24, 25]. Human African trypanosomiasis (HAT) affects 60 million inhabitants mainly living in rural areas of 36 endemic sub-Saharan countries in East, West and Central Africa [26]. Toxoplasmosis remains frequent in these countries and even in developed countries [27]. Finally, the agent responsible for cysticercosis, Taenia solium, is found mainly in Latin America, Asia, sub-Saharan Africa, and the Indian Ocean region. According to the World Health Organization (WHO), cysticercosis is responsible for 50,000 deaths per year with 2.5 to 5 million adult worm carriers and 50 million cysticercal larvae carriers [28, 29]. Neurocysticercosis, a type of brain damage resulting from cysticercosis, is thought to be a factor responsible for more than 50% of late onset epileptic seizures in developing countries [28].

In recent years, there has been an increasing number of studies on co-morbidities between mental disorders and parasitic diseases, particularly those with neurological tropism such as toxoplasmosis [9], human toxocariasis [30, 31], and cysticercosis [32-35]. However, these have produced heterogenous data and to date, no meta-analysis has been published on the association of mental disorders and parasitic diseases in developing and emerging countries; hence the reason why we decided to perform this study.

PURPOSE OF THE STUDY

The purpose of this study was to estimate the pooled prevalence and pooled association measures of comorbidities between mental disorders and neurotropic parasitic diseases in developing and emerging countries.

Implementation procedure

To perform this meta-analysis, the diseases of interest are neutropic parasitic diseases: malaria, cysticercosis, toxoplasmosis, HAT, Chagas disease, and human toxocariasis [9, 13]. These are forms of parasitoses that have a predilection for infesting the central nervous system and which can result in neurological disorders. Mental disorders of interest included: anxiety, depression, bipolar disorder, and schizophrenia [10, 11]. Mental disorders are outlined as medical conditions that interfere with thinking, feeling, mood, communication, and daily functioning, which typically lead to a reduced ability to address routine daily activities, such as working or raising a family [36].

Since this meta-analysis is the continuation of a previously published study on the association of mental disorders and chronic physical diseases in developing and emerging countries, its shares the same methods and research strategy [37]. Its protocol was recorded in PROSPERO, accessible via the following link: http://www.crd.york.ac.uk/PROSPERO and registered under CRD42017056521. It follows the recommended methodology for the meta-analysis of observational studies [38] and was performed in accordance with Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines [39].

Research strategy

The search for articles was conducted through four databases: Medline, Embase, Lilacs, and IENT (database of the Institute of Epidemiology and Tropical Neurology of the University of Limoges in France: http://www-ient.unilim.fr/). LOD, the principal investigator, conducted article searches on these databases from February to May 2017 without linguistic or date restrictions, using the same research equation built on Medline [37].

(“Depressive Disorder”[Mesh] OR “Depression” [Mesh] OR “Anxiety Disorders”[Mesh] OR “Anxiety” [Mesh] OR “Bipolar Disorder”[Mesh] OR “Schizophrenia”[Mesh]) AND (“Diabetes metillus”[Mesh] OR “Obesity”[Mesh] OR “Neoplasms”[Mesh] OR “Cardiovascular Diseases”[Mesh] OR “Pulmonary Disease, Chronic Obstructive”[Mesh] OR “Malaria”[Mesh] OR “Cysticercosis”[Mesh] OR “Toxoplasmosis”[Mesh] OR “Toxocariasis”[Mesh] OR “Trypanosomiasis”[Mesh] OR “Chagas Disease”[Mesh]) AND (“Name of a country”[Mesh]).

This equation, initially built for both studies, allowed us to search articles on: associations of mental disorders and chronic physical diseases, which have been published in another meta-analysis; and associations of mental disorders and neurotropic parasitic diseases, that we discuss in this article.

In Lilacs and Embase, the keywords employed to build the research equation were identical. In total, 139 different equations corresponding to the 139 developing and emerging countries studied were used to search for articles on three databases (Medline, Embase, and Lilacs). When searching on the IENT database, articles were searched using the additional terms “comorbidity” or “comorbidity in mental health.” This methodology was adopted for the latter database because it is specifically dedicated to research on neurotropic parasitoses in developing and emerging countries. Finally, the registration and selection of articles throughout this work was done through the Zotéro bibliographical management software package.

Inclusion criteria and selection of articles

Every article included in this meta-analysis had to be: an article with full text available; a cross-sectional or analytical study; conducted among adults, male and female, of all ages (age ≥ fifteen years); and a study involving either only hospitalised subjects or only non-hospitalised subjects (but not hospitalised subjects and non-hospitalised subjects at the same time). Every article also had to specify the method used to diagnose the diseases. In this study, by non-hospitalised, we mean patients who reside in the community or who attended a health centre (clinic or hospital) for care but did not remain at the health centre for one or more nights. On the other hand, hospitalised patients are those who have stayed in a health care centre for one or more nights. The cross-sectional studies included in this meta-analysis had to each present the prevalence, or the data from which it might be calculated. Analytical studies had to offer the association measures, or the data from which they might be calculated.

Data extraction and assessment of article quality

The data were extracted from each article by LOD (the principal investigator). This included: reference, title, country and continent, the study type and study population, the original disease, the associated disease searched for and its method of diagnosis, the prevalence or measures of association of the disease searched for (or the data needed to calculate them), as well as the sample size, sex ratio, and mean subjects age.

The assessment of the studies quality was performed independently by two investigators (LOD and PEB) using the revised Downs and Black assessment grid. Every article was assigned a score by each investigator [40, 41] and, therefore, the final score was set by mutual agreement after examination of the ratings. In the event of a disagreement, the expert opinion of a third investigator (PMP) was requested, without this investigator knowing the scores given by the first two investigators. The final score was given by mutual agreement between the three investigators.

Statistical analyses

The software system Comprehensive Meta-Analysis (CMA) Version 3.0 [42] was used for the analyses. The heterogeneity of the selected studies was assessed using Q and I² statistical tests [43, 44]. The value of I² was considered such that I² = 0 showed a lack of heterogeneity, I² < 0.25 showed low heterogeneity, I² between 0.25 and 0.5 showed moderate heterogeneity, and I² > 0.5 showed significant heterogeneity. Pooled estimates were then calculated using the DerSimonian-Laird random-effects technique [45], with the results obtained displayed on a forest plot [46] with a significance threshold of 5%. Afterwards, the investigation for publication bias was performed by constructing a funnel plot, a Duval and Tweedie trim and fill test check [45], and an Egger’s regression [47]. To assess the robustness of the principal results of our meta-analysis, we carried out a sensitivity analysis by removing the study with the greatest weighting as well as the studies of lower quality within the pooled studies. The study variables “original disease,” “associated disease,” “subjects type,” and “continent” were used to perform subgroup analyses.

General results

Through the built research equation, we identified 2,604 articles in several languages (English, French, Spanish, Portuguese, Chinese, and Russian). Among the articles meeting our inclusion criteria, there were 18 co-morbidity studies on mental disorders and neurotropic parasitic diseases [48-65] (Figure 1) with two of those being prevalence studies in individuals with neurotropic parasitic diseases who were screened for mental disorders, and sixteen analytical studies in individuals with mental disorders who were screened for neurotropic parasitic diseases (Table 2 and Table 3). These studies were conducted between 1997 and 2016.

In the prevalence studies examined in this meta-analysis, the female to male sex ratio was 1.1 and the mean age was 43.9 ± 7.5 years. In the analytical case-control studies, the female to male sex ratio was 0.7, while the mean age was 36.0 ± 11.0 years for cases, and 37.6 ± 10.5 years for controls. In the 18 analytical studies conducted, 11 were hospitalised patients. Non-hospitalised patients were studied in two prevalence studies and in the 7 remaining analytical studies. With the Downs and Black assessment grid, the mean quality score for the prevalence studies was found to be 18.5 ± 2 (maximum score of 22), while the mean for the case-control studies was found to be 16.4 ± 3.1 (maximum score of 25) (Table S1 and Table S2).

Main findings

In the prevalence studies, the diseases found were anxiety and/or depression for mental disorders, and Chagas disease and neurocysticercosis for neurotropic parasitic diseases. There were 16,610 subjects enrolled in these studies. The prevalence of depression in the 148 individuals with Chagas disease and neurocysticercosis was 44.9% (95% CI, 34.4 – 55.9) (Figure 2). With regard to neuotropic parasitic diseases, toxoplasmosis and toxocariasis were found. In the 16 pooled studies that included 1,782 people with schizophrenia and/or bipolar disorders, and 1,776 controls, mental disorders (schizophrenia and/or bipolar disorders) were associated with an increased risk of toxoplasmosis and/or toxocariasis (odds ratio = 2.3; 95% CI, 1.7 – 3.2) (Figure 3).

The distribution of the pooled studies was illustrated using a funnel plot. Based on Duval and Tweedie's "trim and fill" visual method, we found that 2 analytical studies were missing (Figures 4). Afterwards, we found that the intercept result obtained by the Egger test was 2.4 (95% CI, -0.5 - 5.3 / p = 0.09), which confirms the existence of publication bias.

From the included analytical studies, we found that the pooled odds ratio of the association of schizophrenia and/or bipolar disorders and toxoplasmosis and/or toxocariasis in cases (people with mental disorders) versus controls after sensivity analyses did not changes. It varied from 2.3 (95% CI, 1.7 – 3.2) to 2.3 (95% CI, 1.7 – 3.3) when the study with the greatest weight, Esshili et al. [54], was withdrawn. And it became 2.2 (95% CI, 1.6 – 3.1) when Cetinkaya et al. [51] and Hamidinejat et al. [56], the studies with the lowest quality scores, were withdrawn.

Analysis of the selected subgroups by type of disease investigated, type of associated disease, type of subjects included, and continent allowed us to show the following findings: the odds ratio of the association between schizophrenia and toxocariasis was 2.7 (95% CI, 1.1 – 7.0) in people with schizophrenia compared to the control group. And the association between mental disorders (schizophrenia and/or bipolar disorders) with toxoplasmosis was 2.3 (95% CI, 1.7 – 3.2) in people with schizophrenia and/or bipolar disorders compared to the control group. For the association between schizophrenia and neurotropic parasitic diseases (toxocariasis and/or toxoplasmosis) the odd ratio was 2.4 (95% CI, 1.7 – 3.4). Co-morbidities between mental disorders (schizophrenia and/or bipolar disorders) and neurotropic parasitic diseases (toxoplasmosis and/or toxocariasis) had closely similar odds ratios in both hospitalised and non-hospitalised people. The odds ratio was 2.3 (95% CI, 1.5 – 3.3) for the association between mental disorders (schizophrenia and/or bipolar disorders) and neurotropic parasitic diseases (toxoplasmosis and/or toxocariasis) when comparing cases with schizophrenia and/or bipolar disorders and controls. It was 2.5 (95% CI, 1.4 – 4.4) for the association between mental disorders (schizophrenia and/or bipolar disorders) and toxoplasmosis when comparing cases with schizophrenia and/or bipolar disorders and controls (Figure 5). Finally, the subgroup analysis by continent showed that in Asia, the odds ratio of co-morbidities between mental disorders (schizophrenia and/or bipolar disorders) and neurotropic parasitic diseases (toxoplasmosis and/or toxocariasis) was 2.3 (95% CI, 1.6 – 3.3).

We focused on developing and emerging countries studied due to their high burden in the selected diseases. For mental disorders, these were anxiety, depression, bipolar disorder, and schizophrenia [10, 11] and for parasitic diseases with neurological tropism, these were malaria, cysticercosis, toxoplasmosis, HAT, Chagas disease, and human toxocariasis [9, 13].

In general, the diagnosis of diseases in the studies selected in this meta-analysis was performed using acceptable diagnostic techniques. Indeed, the quality of diagnostic techniques used to screen for mental disorders has been developed in accordance with DSM-5 and ICD-10 [66]. Nevertheless, it has been shown, as in the study of Kirkil et al., that the questionnaire used can also influence the results in terms of diagnosis [67]. The variety of questionnaires used in the studies included in this meta-analysis can be explained by the need to adapt the questionnaire to the population studied [68-76], as is usually recommended. Regarding laboratory diagnostic techniques, it is recommended to use two complementary diagnostic tests (one very sensitive and therefore very specific) and to have the samples handed by two different technicians who do not know the clinical condition of the subject [77]. However, most of the studies included in this meta-analysis generally use only one fairly sensitive and specific diagnostic method at a time, which is not the best practice. This can be partly explained by financial constraints related to the cost of diagnostic tests, which are often quite expensive in low-income countries, and by the nature of the sample size, which increases the burden of work. This may be acceptable for this type of disease, since parasitic diseases are very commonly found in these countries.

The quality scores of the studies included in this meta-analysis are in line with those found by other authors [78]. There was publication bias and great heterogeneity in our estimates. In both the prevalence studies and the analytical studies, the quality scores were all largely above the average score (i.e. above half the maximum score: 11 for prevalence studies and 12.5 for case-control studies). But since our estimates did not change after we performed the sensitivity analysis. In our pooled estimates after withdrawing the study with the highest weight on the one hand, and the study with the lowest quality score on the other, using the two recommended methods, the sensitivity test had almost no impact on our results and the results remained robust. However, the different levels of heterogeneity found in the pooled estimates after analysis of the selected subgroups (type of original disease, type of associated disease, type of subjects included, and continent) implied that there were other covariates in play and that the latter could be the source of these heterogeneities.

This meta-analysis revealed that, despite the small number of studies included, the prevalence of anxiety and/or depression was almost 50% in people with Chagas disease and/or neurocysticercosis. " In addition, toxocariasis and/or toxoplasmosis was associated with an increased risk of schizophrenia and/or bipolar disorders (odds ratio = 2.3). More specifically, through subgroup analysis, we were able to show that toxocariasis (odds ratio = 2.7) and toxocariasis and/or toxoplasmosis (odds ratio = 2.4) were associated with increased risk of schizophrenia. In hospitalised subjects, the results of the subgroup analysis showed that in the presence toxocariasis and/or toxoplasmosis, the increased risk of mental disorders (schizophrenia and/or bipolar disorders) was 130%, and, in non-hospitalised subjects the increased risk of mental disorders (schizophrenia and/or bipolar disorders) in presence of toxoplasmosis was 150%. This similarity of results in the two types of subjects might reflect the difficulties of access to mental and neurological health care in developing and emerging countries, with mental and neurological diseases being grossly under-diagnosed, and suffering both from a low ranking in terms of public health priority.

Due to the well-known neurotropic characteristics of Toxoplasma gondii, it is commonly accepted that many psychiatric symptoms, like mental retardation, may be due to Toxoplasma gondii infections [79]. Much interest exists in determining a causative relationship between this parasite and some mental disorders, in particular schizophrenia [80] and bipolar disorders [81]. Our investigation into the presence of IgG antibodies in people with mental disorders produced results that are similar to those obtained by other authors. People living with schizophrenia were found to have a risk ratio of 1.43 to 2.73 for toxoplasmosis and/or toxocariasis [80, 82], while people with bipolar disorders were found to have a risk ratio of 1.26 to 1.52 [81, 82].

The analytical studies on the association of mental disorders with neurotropic parasitic diseases (mostly conducted in Asia) didn’t allow statistical analyses, such as subgroup analysis. Only Asia, which accounted for most of the studies, made it possible to estimate that there was a 130% increased risk of toxoplasmosis and/or toxocariasis for a person living with schizophrenia and/or bipolar disorders. This lack of data on mental disorders in some developing and emerging countries may well be explained by the dearth of medical consultations for individuals with mental disorders and, additionally, by the rather limited number of health centres which, when they exist, do not seem to be accessible or to have healthcare providers trained to manage mental disorders. Additionally, faith and religion can have a significant impact on the diagnosis of mental disorders and neurotropic parasitic diseases in developing and emerging countries. Often wrongly attributing mental illness to a spiritual effect, 80% of people with mental disorders and their families prefer to consult religious leaders, healers, or exorcist-priests [83], and between 76% and 85% of people with severe mental disorders receive no treatment for their disorder in these countries [84]. Poverty and the lack of national and international funding for mental health often further exacerbate the situation. The results from this meta-analysis would suggest that further studies on comorbidities of mental disorders and neurotropic parasitic diseases in developing and emerging countries might be required.

Despite efforts made to reduce bias in this study, it still had some limitations. These limitations primarily involve: the size of the various samples, which were often relatively small; the identification of mental disorders which were not confirmed by a specialist in some studies; and the focus on Asia, which may well be an obstacle towards generalizing the results to other continents. Additionally, some estimates could not be determined due to the lack of studies meeting our inclusion criteria.

Nonetheless, our meta-analysis on the co-morbidities between mental disorders and neurotropic parasitic diseases is the first to involve primarily developing and emerging countries. It has been performed following the PRISMA 2015 guidelines and the protocol was registered in the PROSPERO database. Finally, we performed our sensitivity tests by withdrawing the studies with the greatest weight and the studies with the lowest quality as it is it is receommended.

In this meta-analysis, the results show that the pooled estimates of co-morbidities between mental disorders and neurotropic parasitic diseases in developing and emerging countries are relatively high. Most of the included studies were conducted in Asia. In conclusion, our findings support the hypothesis that toxoplasmosis could be the cause of schizophrenia and/or bipolar disorders. We hope that this meta-analysis, the first of its kind to focus on developing and emerging countries, can provide some guidance to researchers to further explore and understand the associations between mental disorders and neurotropic parasitic diesases in developing and emerging countries.

BDI: Beck Depression Inventory

CMA: Comprehensive Meta Analysis

DSM–5: Diagnostic and Statistical Manual of Mental Disorders

EIA: Enzyme Immuno Assay Enzyme Immuno Assay

ELISA: Immunosorbant Enzyme-Linked Assay

GHQ: General Health Questionnaire

HAT: Human African Trypanosomiasis

ICD–10: International Classification of Diseases

IENT: Institute of Epidemiology and Tropical Neurology

IFA: Immunofluorescent Assay

MMSE: Mini Mental State Examination

MSE: Mental Status Examination

PCR: Polymerase Chain Reaction

PRISMA: Preferred Reporting Items for Systematic Review and Meta-Analysis

PSE: Present State Examination

qPCR: quantitave Polymerase Chain Reaction

SADS-L: Schedule for Affective Disorders and Schizophrenia-Lifetime

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

All information generated or analyzed during this meta-analysis is available in the additional data provided by the first author.

Competing interests

VL and PEB are Sanofi employees and own Sanofi stocks. DG is a former employee of Sanofi. All other authors declare that there is no conflict of interest related to the writing and publication of this article.

Funding

The first author (LOB) was an intern at SANOFI for 6 months during which he received a grant. SANOFI has also provided access to its electronic databases.

Authors' contributions

PMP contributed to writing funding applications, the design of the research protocol, the validation of the studies’ quality scores, the interpretation of the data, and the preparation of the manuscript. BM and FB contributed to finalizing the research protocol, data analysis, and preparation of the manuscript. VL contributed to finalizing the research protocol and preparation of the manuscript. PEB contributed to finalizing the research protocol, the evaluation of the studies’ quality scores, the interpretation of the data, and the preparation of the manuscript. DG contributed to finalizing the research protocol and the preparation of the manuscript. He also contributed to writing funding applications. Finally, LOD contributed to the drafting of the research protocol, its registration in PROSPERO, the selection of articles, the evaluation of the studies’ quality scores, the data analysis, the interpretation of the data, and the preparation of the manuscript.

This manuscript has been read and approved by all authors.

Acknowledgements

Not applicable.

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Table 1: Risk factors of interest diseases

Disease

Risk factor

Mental disorders

· Family history

· Stressful living conditions

· Existence of a chronic disease

· Traumatisms

· Drug use

· Child abuse or neglect and/or

lack of social support [4, 5]

Neurotropic parasitic diseases

Human African Trypanosomiasis (HAT)

Chagas disease

Cysticercosis

Toxoplasmosis

Human Toxocariasis

· Family history of HAT, living near a wetland [6]

· Economic, cultural, and human behaviour [7]

· Age, home, consumption of undercooked meat, and unwashed fruit or raw vegetables [8]

· Bare hand contact with the ground or injury to animals, consumption of poorly washed vegetables [27]

Table 2: Characteristics of prevalence studies of associations of mental disorders and neurotropic parasitic diseases

Reference

Continent

Subjects type

Original disease

Associated disease

Positive

(n)

Total

(N)

Diagnostic method

F/M

Average age

Ozaki et al. [64]

Qual Life Res, 2011

Asia

Non-hospitalised

Chagas disease

Anxiety and Depression

110

BDI

56/54

51±13

Forlenza et al. [55]

J Neurol Neurosurg Psychiatry, 1997

America

Non-hospitalised

Neurocysticer- cosis

Depression

PSE ; MMSE ; SADS-L ; MSE

20/18

36.7

Description of data:

BDI: Beck Depression Inventory, PSE: Present State Examination, MMSE: Mini Mental State Examination, SADS-L: Schedule for Affective Disorders and Schizophrenia-Lifetime, MSE: Mental Status Examination, F: Female, M: male, Age in years.

Table 3: Characteristics of analytical studies of associations of mental disorders and neurotropic parasitic diseases

Reference	Continent	Subjects type	Original disease	Associated disease	Positive (n)	Total (N)	OR	Diagnostic method	F/M	Age (case / control)
Daryani et al. [52] Trop Biomed, 2010	Asia	Non-hospitalised	Schizophrenia	T. gondii infection	28 25	80 99	–	ELISA “IgG & IgM” (Germany) ELISA reader (USA)	–	32.95±10.05 33.76±10.50
Alipour et al. [48] Iran J Parasitol, 2011	Asia	Hospitalised	Schizophrenia	T. gondii infection	42 23	62 62	–	IFA and ELISA “ IgG” (Denmark) ELISA reader (BioTek, USA)	59/65	37.54± 9.75 37.24 ±10.24
Karabulut et al. [59] J Chin Med Assoc, 2015	Asia	Hospitalised	Schizophrenia	T. gondii infection	–	85 60	1,008	ELISA Kits (Spain) Triturus system (Spain)	60/85	41.73 ± 12.07 40.45 ± 9.49
Khademvatan et al. [61] Jundishapur J Microbiol, 2014	Asia	Non-hospitalised	Schizophrenia	T. gondii infection	34 53	100 200	–	ELISA “IgG (USA)	139/161	36.39±10.28 25.04
Hamidinejat et al. [56] Int J Infect Dis, 2010	Asia	Hospitalised	Schizophrenia	T. gondii infection	–	98 94	2,99	ELISA kits “IgG and M” (USA)	–	33 (Case & Control)
Tamer et al. [65] Adv Ther, 2008	Asia	Hospitalised	Schizophrenia	T. gondii infection	16 5	40 37	–	ELISA (Germany)	–	Cas : 33 Control : –
Alvarado-Esquivel et al. [50] Parasitol Int, 2011	America	Hospitalised	Schizophrenia	T. gondii infection	–	50 150	4,44	EIA kit “Ig G & M” (USA)	–	45.12±11.5 45.1±11.4
Cetinkaya et al. [51] Schizophr Bull, 2007	Asia	Non-hospitalised	Schizophrenia	T. gondii infection	66 33	100 100	–	ELISA kit “Ig G” (France)	103/97	37.25 ± 11.51 37.3 ± 5.78
Omar et al. [63] Korean J Parasitol, 2015	Asia	Non-hospitalised	Schizophrenia	T. gondii infection	52 10	101 55	–	ELISA PCR (Qpcr) (Germany)	74/82	41.1±10.9 45.3±14.5
Esshili et al. [54] Psychiatry Res, 2016	Africa	Non-hospitalised	Schizophrenia	T. gondii infection	–	246 117	2,54	ELISA kit “IgG” (France) ELISA reader	89/274	40.5±10.2 38.6±10.4
Juanah et al. [57] Am J Infect Dis, 2013	Asia	Hospitalised	Schizophrenia	T. gondii infection	–	88 88	2,01	EIA “IgG & M” (Italy) Microtiter plate reader (DYNEX, MRX)	66/110	39.42 (Case & Control)
Kheirandish et al. [62] Arch Clin Infect Dis, 2016	Asia	Hospitalised	Schizophrenia and bipolar disorders	Toxoplasmosis	49 and 54 65 and 65	85 170		EIA “IgG” Microplate reader (USA)	85/150	37.2 (Case & Control)
Emelia et al. [53] Trop Biomed, 2012	Asia	Hospitalised	Schizophrenia	Toxocariasis	54 49	144 144		ELISA “Ig G” (USA) ELISA reader (SKANIT Software)	–	–
Alvarado-Esquivel et al. [49] Int Int J Biomed Sci, 2014	America	Hospitalised	Schizophrenia	Toxocariasis	50 100			EIA “IgG” (U.S.A.)	–	45.12 ± 11.5 45.5 ± 13.1

Reference

Continent

Subjects type

Original disease

Associated disease

Positive

(n)

Total

(N)

Diagnostic method

F/M

Age (case / control)

Kaplan et al. [58]

Yonsei Yonsei Med J, 2008

Asia

Hospitalised

Schizophrenia

Toxocariasis

100

–

ELISA kit “IgG & M” (Germany)

ELISA microtiter plate reader

95/103

38 ± 11

35 ± 8

Khademvatan et al. [60]

J Med Sci Faisalabad, 2013

Asia

Hospitalised

Bipolar disorders (I)

Toxoplasma

–

117

200

0,78

ELISA “IgG & M” (USA)

162/155

33.93±11.87 33.88±11.45

Description of data:

Kheirandish et al., 2016: Cases = 49 patients with schizophrenia and 54 patients with bipolar disorders, Controls = 85 for schizophrenia cases and 85 for bipolar disorder cases.

T. gondii: Toxoplasma gondii, GHQ: General Health Questionnaire, ELISA: Immunosorbant Enzyme-Linked Assay, IFA: Immunofluorescent Assay, EIA: Enzyme Immuno Assay Enzyme Immuno Assay, PCR: Polymerase Chain Reaction, qPCR: quantitave Polymerase Chain Reaction, F: Female, M: male, Age in years.

Additional file 1

Table S1: Characteristics of quality scores of prevalence studies

Description of data: Global quality (Items: 1-2-3-5-6-7-9-10); External validity (Items :11-12-13); Results bias (Items: 15-16-18-20); Confusion and selection bias (Item: 25); Power (Item: 27) and S: Quality score.

Additional file 2

Table S2: Characteristics of quality scores of analytical studies

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Associations of mental disorders and neurotropic parasitic diseases: a meta-analysis in developing and emerging countries

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