PLOS NEGLECTED TROPICAL DISEASES

RESEARCH ARTICLE

The burden of T. solium cysticercosis and

selected neuropsychiatric disorders in
Mocuba district, Zambézia province,
Mozambique
Irene Langa1,2, Fernando Padama3, Noémia Nhancupe1,2, Alberto Pondja4,
Delfina Hlashwayo ID5*, Lidia Gouveia6, Dominik Stelzle7,8, Clarissa Prazeres da Costa9,
Veronika Schmidt7,10, Andrea S. Winkler7,10, Emı́lia Virgı́nia Noormahomed1,2,11
a1111111111
1 Microbiology Department, Parasitology Laboratory, Faculty of Medicine, Eduardo Mondlane University,
a1111111111
Maputo, Mozambique, 2 Mozambique Institute of Health Education and Research (MIHER), Maputo,
a1111111111 Mozambique, 3 Zambézia Operational Research Unit, Provincial Directorate of Health, Quelimane,
a1111111111 Mozambique, 4 Faculty of Veterinary, Eduardo Mondlane University, Maputo, Mozambique, 5 Faculty of
a1111111111 Sciences, Eduardo Mondlane University, Maputo, Mozambique, 6 Mental health Department; National Public
Health Directorate, Ministry of Health Maputo, Maputo, Mozambique, 7 Center for Global Health, Department
of Neurology, School of Medicine, Technical University of Munich, Munich, Germany, 8 Chair of
Epidemiology, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany,
9 Institute for Medical Microbiology, Immunology and Hygiene, Center for Global Health, School of Medicine,
Technical University of Munich, Munich, Germany, 10 Centre for Global Health, Institute of Health and
OPEN ACCESS Society, University of Oslo, Oslo, Norway, 11 Department of Medicine, Infectious Diseases Division,
Citation: Langa I, Padama F, Nhancupe N, Pondja University of California, San Diego, California, United States of America
A, Hlashwayo D, Gouveia L, et al. (2022) The
* [email protected]
burden of T. solium cysticercosis and selected
neuropsychiatric disorders in Mocuba district,
Zambézia province, Mozambique. PLoS Negl Trop
Dis 16(7): e0010606. https://doi.org/10.1371/ Abstract
journal.pntd.0010606

Editor: Eduardo Torres, Universidade do Rio de

Janeiro: Universidade do Estado do Rio de Janeiro, Background
BRAZIL
Taenia solium (neuro-)cysticercosis, a neglected tropical disease, can be associated with
Received: December 10, 2021 epileptic seizures and other neuropsychiatric (= neurological and psychiatric) disorders.
Accepted: June 24, 2022 This study aimed to evaluate the association of T. solium cysticercosis with selected neuro-
Published: July 14, 2022 psychiatric disorders and/or symptoms (chronic headache, epileptic seizures/epilepsy and
psychosis) in Mocuba district, Mozambique.
Peer Review History: PLOS recognizes the
benefits of transparency in the peer review
process; therefore, we enable the publication of Methodology
all of the content of peer review and author
responses alongside final, published articles. The
Between March and May 2018, a cross-sectional study was conducted among 1,086 partici-
editorial history of this article is available here: pants aged 2 years or above in Mocuba district, Zambézia province, central Mozambique, to
https://doi.org/10.1371/journal.pntd.0010606 assess the seroprevalence of human cysticercosis and risk factors for infection, as well as
Copyright: This is an open access article, free of all to explore its relation to selected neuropsychiatric disorders. Socio-demographic and clinical
copyright, and may be freely reproduced, data were collected from each participant using a modified questionnaire designed by the
distributed, transmitted, modified, built upon, or
Cysticercosis Working Group for Eastern and Southern Africa. Additionally, neuropsychiat-
otherwise used by anyone for any lawful purpose.
The work is made available under the Creative ric disorders, such as chronic headache, epileptic seizures/epilepsy and psychosis were
Commons CC0 public domain dedication. assessed using four vignettes. T. solium antigen and cysticercosis IgG in serum were
Data Availability Statement: The data set is detected using both T. solium antigen B158/B60 enzyme linked immunosorbent assay
deposited in Zenodo repository and can be (ELISA) and LDBIO Cysticercosis Western Blot, respectively.

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 1 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

accessed via the following link: https://doi.org/10. Principal findings

5281/zenodo.6815437.
Overall, 112/1,086 participants (10.3%) were sero-positive for T. solium antigen or antibod-
Funding: The main funder for this study was the
ies. Prevalence of antibodies (6.6%; n = 72) was higher than of antigens (4.9%; n = 54). In
German Federal Ministry of Education and
Research under CYSTINET-Africa project number the questionnaires, 530 (49.5%) of participants reported chronic headache, 293 (27%) had
01KA1618 (EVN and ASW). Further support was generalized epileptic seizures, 188 (18%) focal seizures and 183 (18.3%) psychosis. We
received from the Fogarty International Center (FIC) found a statistically significant association between seropositivity for T. solium and chronic
- National Institute of Health (NIH) grant
R25TW011216 (EVN) for training health
headache (p = 0.013). Additionally, increasing age (p = 0.03) was associated with Ag-ELISA
professionals on the diagnosis and treatment of seropositivity.
epilepsy. The funders had no role in study design,
data collection and analysis, decision to publish, or
preparation of the manuscript.
Conclusions
Competing interests: The authors have declared
Our study revealed that in Mocuba, T. solium cysticercosis is prevalent and associated with
that no competing interests exist.
self-reported chronic headache. Additionally, in the study setting, the seroprevalence of cys-
ticercosis increased with age. However, it is not associated with other neuropsychiatric dis-
orders such epileptic seizures/epilepsy and psychosis. Future studies are needed to confirm
the high burden of neuropsychiatric disorders and their possible etiology, including neuro-
cysticercosis, using additional serological, molecular biological and radiological diagnostic
tools, as well as in-depth clinical examinations.

Author summary
Taenia solium cysticercosis (TSC) is a neglected tropical disease caused by the larval stage
of T. solium. The disease is a serious threat to public health, especially in low-income
countries and is associated with poor pig husbandry practices, deficient hygiene and sani-
tation, close contact between humans and pigs, lack of slaughter facilities for pigs and
inadequate meat inspection. When the larva of T. solium lodges in the human central ner-
vous system, the disease is called neurocysticercosis (NCC). The most frequent neurologi-
cal manifestations of NCC are epileptic seizures and epilepsy. NCC diagnosis remains a
challenge in low-income countries and its relationship with neurological signs/symptoms
so far was not studied in Mocuba, located in Zambézia province, one of the districts with
the biggest pig populations in Mozambique. In this study we investigated the seropreva-
lence for TSC, risk factors for infection and the association with neuropsychiatric (= neu-
rological and psychiatric) disorders. Seroprevalence of TSC was 10.3%, and was associated
with chronic headache. Moreover, increasing age was associated with Ag-ELISA seroposi-
tivity. Future studies are needed applying in-depth clinical examination, and additional
serological, molecular biological and radiological diagnostic tools in order to confirm (or
not) the results of our study.

Introduction
Taenia solium cysticercosis (TSC) is a foodborne, zoonotic and neglected tropical disease
(NTD), caused by the larval stage (cysticercus) of T. solium. The disease is emerging as a seri-
ous threat to public health, inflicting significant economic losses and disabilities in low-income
countries of sub-Saharan Africa, Latin America and Asia where T. solium is endemic. It is also

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 2 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

of increasing concern in non-endemic countries due to globalization and the immigration of

tapeworm carriers [1–5].
Humans are the definitive host and thus carriers of the adult tapeworm which develops
after ingestion of measly raw or undercooked pork. However, humans may also become inter-
mediate hosts and develop TSC following direct or indirect ingestion of T. solium eggs which
develop into cystic larvae in various parts of the body [1,5–8]. When the larva lodges in the
central nervous system (CNS), the disease is called neurocysticercosis (NCC). The most fre-
quent neurological manifestations include epileptic seizures and epilepsy. In endemic areas,
up to 30% of people with epilepsy may suffer from NCC [1–5,9]. Other neurological signs and
symptoms include severe headache, intracranial hypertension, dementia, blindness, or chronic
meningitis. Also, different neuropsychiatric disorders have been associated with NCC
although there is only limited data available [1,5,7,8,10].
NCC prevails due to the maintenance of T. solium life cycle, associated with poor pig hus-
bandry practices, deficient hygiene and sanitation, close contact between humans and pigs, the
intermediate host, lack of slaughter facilities for pigs and inadequate meat inspection
[1,7,8,11,12]. However, the diagnosis of NCC remains a challenge because of the poor specific-
ity of clinical and neuroimaging findings, the latter including magnetic resonance imaging
(MRI) and computed tomography (CT scan), as well as suboptimal predictive values in immu-
nodiagnostic tests, particularly in endemic settings [1,2].
The few available cross-sectional serological studies from Mozambique found that the sero-
prevalence of either antibodies or antigens against T. solium cysticercerci varied between 15%
to 21% in apparently healthy children and adults, while in neurological patients the seropreva-
lence of cysticercosis can be as high as 51% [13–15]. Further, the only published community-
based study conducted in Angónia district, in the central western part of the country, found
that amongst 151(8.8%) people confirmed to be living with epilepsy, 107 (70.9%) were seropos-
itive to cysticercus antigens [14]. These data suggest that NCC might be potentially one of the
main causes of epileptic seizures/epilepsy and other neurological and/or psychiatric disorders
in Mozambique.
Therefore, this study investigated the seroprevalence for T. solium cysticercosis and its asso-
ciated risk factors as well as neuropsychiatric (= neurological and psychiatric) disorders with
an emphasis on chronic headache, epileptic seizures/epilepsy and psychosis in both children
and adults from Mocuba district, Zambézia province, Mozambique.

Methods
Ethics statement
The present study was approved by the Mozambique National Bioethical Committee of Health
(51/CNBS/2017) and by the administrative authorities from Zambézia province and commu-
nity leaders. The study also received approval from the ethics committee of the Klinikum
rechts der Isar, Technical University of Munich, Germany (537/18 S-KK).
Prior to the interviews and blood sampling, written consent were obtained from the enrolled
participants. Written consent from children aged below 12 years and illiterate participants were
obtained in the presence of a guardian or witness, who signed on their behalf. For participants
aged between 12 and 17 years a written assent was obtained in addition to their parents’ consent.
Each participant was assigned a unique identification study number and all data and samples
were handled confidentially using this study number from this point onward.
Participants who suffered from epileptic seizures/epilepsy or other neuropsychiatric disor-
ders were referred to the local health centre for diagnosis confirmation and follow-up accord-
ing to the Mozambique Ministry of Health guidelines [16].

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 3 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Study area and population

The study was conducted in seven villages of Mocuba district (Fig 1) located in Zambézia prov-
ince, central Mozambique (16˚50’ 13” S, 36˚59’ 14” E). The district has an area of 8,803 km2
and an altitude of 200–400 meters above sea level.
The total population is estimated at 422,681. There is an illiteracy rate of 62.5% with most
of the population (82.6%) living in rural areas. Moreover, the disease profile of Mocuba is
dominated by infectious diseases including many NTDs with higher prevalence estimates. As

Fig 1. Location of the study area. Created by Patricia Noormahomed based on EarthExplorer (https://earthexplorer.usgs.gov).
https://doi.org/10.1371/journal.pntd.0010606.g001

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 4 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

an example, the district has an HIV prevalence of 9% and 39% of children are infected by at
least one intestinal parasite [17–21].

Study design and sampling

A community-based cross-sectional study was conducted between March and May 2018. The
sampling frame was constructed using information of the National Institute of Statistics [22].
For the sample size calculation, it was estimated that 15% of households would have at least
one member with cysticercosis based on a study conducted in a northwestern district of
Mozambique [14]. Assuming a 95% confidence level and 20% precision, and correcting for a
finite population of households in the study area [22], a sample size of at least 543 households
was obtained by using the formula n = Z2p(1—p)/d2 [23], where n is the sample size required,
Z is the z–score for the desired confidence level, p is the expected proportion of households,
and d is the desired precision relative to the expected proportion of households. The sampling
procedure followed a two-stage household-based design, whereby Primary Sampling Units
(PSUs) consisted of villages, and households were chosen during the second stage. Prior to
selection of households, the village authorities were approached and the purpose of the study
was explained. Once the permission was granted, a systematic random sampling with proba-
bility proportional to size (PPS) technique was used to select households. Two eligible partici-
pants from each household were recruited randomly into the study (Fig 2). When only one

Fig 2. Data collection workflow of the study sample.

https://doi.org/10.1371/journal.pntd.0010606.g002

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 5 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

member was available in a selected household, either by absence or refusals of other members,
participants were recruited from the nearest household. Inclusion criteria were living in the
household and being at least 2 years old. People who had taken alcoholic beverages in the pre-
vious 24 hours were excluded. In total, 1,086 participants from 565 households were included
in the study.

Questionnaire survey and vignettes

A pre-designed questionnaire developed by the Cysticercosis Working Group for Eastern and
Southern Africa (CWGESA) was used, with some modifications, that included four vignettes
on neuropsychiatric disorders [24,25]. The four vignettes included chronic headache, epileptic
seizures/epilepsy (generalized and focal) and psychotic disorders, and were confirmed with a
neurologist (ASW). This was the major tool used to establish a diagnosis of neuropsychiatric
(= neurological and psychiatric) disorders in the study. The questionnaire also covered infor-
mation on socio-demographic and risk factors associated with cysticercosis such as age, gen-
der, education, sources of drinking water, use of latrines, rearing pigs and pig management
practices, consumption of pork, awareness about TSC transmission, risk-related habits and
practices.
Furthermore, direct observation to visualize the existence of latrines and usage and pig hus-
bandry system in the household was made by the enumerators. The questionnaire designed in
Portuguese language was used for the study, translated to the local language (Lomué) and back
translated to Portuguese.
The survey was carried out by locally selected enumerators with knowledge of the local lan-
guage, experience with community surveys, and basic training on TSC transmission, preven-
tion and clinical signs/symptoms of selected neuropsychiatric disorders. The training of the
enumerators was done via workshop sessions and pre-tested prior to commencement of the
study.

Vignette 1. Assessment of chronic headache

To assess chronic headache, participants were asked if they had a history of daily headache that
occurred for at least 15 consecutive days and for longer than three months. We did not ask for
severity or any specific characteristics of headaches in order to keep it more general and allow
for secondary causes of chronic headache such as NCC.

Vignette 2. Assessment of generalized tonic-clonic seizures

To assess generalized tonic-clonic seizures (GTCS), we asked the participant if he/she had ever
experienced a sudden loss of consciousness that caused him/her to fall to the ground or
whether he/she was told about such an event by someone else. We also asked if the eyes were
turned upwards, the body became rigid and/or involuntary violent movements of the arms
and legs were observed. In addition, we asked if they were told or noticed that they were drool-
ing and/or urinating and/or biting their tongue. We also asked if the person was asleep or slo-
wed down or even confused after the actual epileptic seizure and could not remember what
happened.

Vignette 3. Assessment of focal seizures

To assess focal seizures (FS), participants were asked whether they had ever noticed or been
told about uncontrolled movements in body parts such as an arm or leg without loss of

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 6 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

consciousness or before loss of consciousness. For the latter, we also asked about warning
signs such as a strange smell (aura) before the epileptic seizure.

Vignette 4. Assessment of psychotic disorders

To assess psychotic behaviour and/or hallucinations, we asked the participant if he/she was
informed of any changes in behaviour, such as becoming very unstable, appearing anxious
and/or doing inappropriate things, such as undressing or harming others for no reason. They
were also asked if they heard strange voices that no one else could hear, or if they saw things
that were not real to others. They were also asked if they had the impression of being followed.

Blood sampling
A 5 ml sample of venous blood was obtained by venepuncture from each of the recruited indi-
viduals after consenting [26]. The samples were immediately stored in cooling boxes at 4˚C
and transported to the Mocuba district Hospital Laboratory, where they were centrifuged for 5
min at 1500 r.p.m. to obtain serum. Serum was stored at -20˚C until shipment to the Parasitol-
ogy Laboratory at Faculty of Medicine, Eduardo Mondlane University (UEM) in Maputo
where samples were stored at -80˚C until further processing.

Serological testing
T. solium circulating antigens (Ag) were detected using the monoclonal antibody based
B158C11A10 Enzyme Linked Immunosorbent Assay (Cysticercosis Ag-ELISA, ApDia, Bel-
gium). Ag index was calculated as the mean of optical density (OD) of each serum sample
divided by the cut-off. In addition, IgG antibodies (Ab) against T. solium larva were deter-
mined via Western Blot (LDBIO Diagnostic, Lyon, France). A sample was considered positive
if at least 2 bands (6–8 kDa; 12 kDa; 23–26 kDa; 39 kDa; 50–55 kDa) were visible, according to
the manufacturer’s instructions.

Statistical analysis
Data were captured in EpiData Entry Client version 4.3 and analysed using STATA version
13.0 (Stata Corp., College Station, TX). Descriptive analyses were first performed by calculat-
ing frequencies and percentages for categorical variables. Age was categorized into age groups
(2–14, 15–24, 25–54 and >55 years) for the purpose of analysis. Using Chi-square test, bivari-
ate analysis was performed to assess associations between a positive Ag-ELISA and/or Western
Blot assay results and several factors. These factors included: socio-demographic and neuro-
psychiatric diseases; knowledge about T. solium; transmission risk-related variables and pig
management variables. Chi-square tests were also used to assess difference in seroprevalence
by district. Logistic regression models were performed to assess the association of seropreva-
lence of T. solium with the four vignettes. Models were run unadjusted and adjusted for age,
gender, education and occupation. The significance level was set at p<0.05.

Results
Among the 1,086 participants included in the study, the age ranged from 2 to 87 years, with a
median age of 25 years. A total of 656 participants (60.4%) were predominantly farmers, 640
(58.9%) were female, and the majority 763 (70.3%) attended primary school. A total of 237
(21.8%) participants reported outdoor defecation, 806 (74.2%) reported eating pork, 155
(14.3%) were pig keepers and 105 (9.7%) have heard about the pork tapeworm (Table 1).

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 7 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

The results of cysticercosis serological screening either for antigen or antibody detection or
both from each village are shown in Fig 3. Overall, out of the 1,086 samples tested, 112 (10.3%)
were positive in at least one serological test; 54 (4.9%) had circulating antigens and 72 (6.6%)
had circulating antibodies to T. solium larva. Moreover, 14 (1.3%) were positive in both tests.
A wide variation of seropositivity was observed across different villages ranging from 3.6% in
Alto Benfica village to 17.7% in Mocuba Municipality (p = 0.007).

Table 1. Socio-demographic characteristics of the study participants.

Variables Study participants
n (%)
Age group (years)
2–14 277 25.5
15–24 251 23.1
25–54 457 42.1
� 55 101 9.3
Gender
Male 446 41.1
Female 640 58.9
Level of education
No formal education 197 18.1
Primary 763 70.3
Secondary or higher 121 11.1
Other 5 0.5
Occupation
Farmer 656 60.4
Trading 28 2.6
Student 245 22.6
State employee 17 1.6
Other 140 12.9
Water source
River 82 7.6
Well 585 53.9
Borehole 405 37.3
Tap 14 1.2
Faecal disposal
Latrine 849 78.2
Outdoor defecation 237 21.8
Pork consumption
Yes 806 74.2
No 280 25.8
Pork preparation
Boiled 452 56.1
Grilled 345 42.8
Other 9 0.1
Pig keeping
Yes 155 14.3
No 931 85.7
Ever heard about tapeworm
Yes 105 9.7
No 981 90.3
https://doi.org/10.1371/journal.pntd.0010606.t001

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 8 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Fig 3. Prevalence of human cysticercosis according to each study village in Mocuba district.
https://doi.org/10.1371/journal.pntd.0010606.g003

In general, the seroprevalence of Ab tended to be higher (ranging from 3.6% in Alto Benfica
village to 9.5% in Mocuba Municipality) than that of Ag (ranging from 0% in Munhiba to
8.2% in Mocuba Municipality; p<0.005). The details about serological assay results from each
of the studied villages can be seen in Fig 3.
The analysis of socio-demographic variables in relation to the cysticercosis serological
assays are presented in Table 2. Seropositivity for antigen or antibody increased with age and
was lowest for children under the age of 15 years (p = 0.03). Seropositivity was not statistically
significantly different between males and females (11.7% versus 9.4%, p = 0.22), nor between
the levels of education (p = 0.12).
The findings concerning the assessment of clinical signs and symptoms related to neuro-
psychiatric disorders in relation to socio-demographic factors are presented in Table 3. A
total of 530 (49.5%) participants screened positive for vignette 1. More males screened posi-
tive than females (p = 0.02). Education was not associated with screening positive but farm-
ers more commonly screened positive than people with other occupations (p = 0.05).
Overall, 293 participants (27%) screened positive for vignette 2; positivity decreased with
increasing age and was similar for males and females. Vignette 3 was positive in 188 (18%)
of the participants and vignette 4 in 183 (18.3%). Vignette 4 was more commonly positive
among participants older than 14 years and was more commonly positive among farmers.
Of the total vignettes, chronic headache was associated with cysticercosis seropositivity
(p = 0.013) (Table 4).

Discussion
Our results indicate that T. solium antigens and antibodies were present in 10.3% of the study
participants from Mocuba district. Moreover, chronic headache presented a significant associ-
ation with cysticercosis seropositivity (p = 0.013), although neuropsychiatric disorders such as
epileptic seizures/epilepsy and psychosis presented no significant association. These findings
suggest that TSC is prevalent in Mocuba and chronic headache prevails as an important

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 9 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Table 2. Socio-demographic data and relation with serological assays to T. solium larva antigens and antibodies.
Variables Study participants n (%) Ag-Elisa + Western blot + Ag-Elisa + and Western blot + Ag-Elisa + or Western
blot +
n (%) n (%) n (%) n (%) p-value
Total 1086 54 (4.9) 72 (6.6) 14 (1.3) 112 (10.3)
Age group (years)
2–14 277 4 (1.4) 13 (4.7) 1 (0.4) 16 (5.8) 0.03
15–24 251 12 (4.8) 17 (6.8) 1 (0.4) 28 (11.2)
25–54 457 30 (6.6) 37 (8.1) 10 (2.2) 57 (12.5)
�55 101 8 (7.9) 5 (5.0) 2 (2) 11 (10.9)
Gender
Female 640 26 (4.1) 42 (6.6) 6 (1.3) 60 (9.4) 0.22
Male 446 28 (6.3) 30 (6.7) 8 (1.3) 52 (11.7)
Level of education
No formal education 197 5 (2.5) 7 (3.6) 0 (0) 12 (6.1) 0.12
Primary 763 40 (5.2) 55 (7.2) 14 (1.8) 81 (10.6)
Secondary or higher 121 9 (7.4) 10 (8.3) 0 (0) 19 (15.7)
Other 5 0 (0.0) 0 (0.0) 0 (0) 0 (0.0)
Occupation
Farmer 656 38 (5.8) 43 (6.6) 11 (1.7) 70 (10.7) 0.63
Other 430 16 (3.7) 29 (6.7) 3 (0.7) 42 (9.8)
Water source
River 82 7 (8.5) 5 (6.1) 3 (3.7) 9 (11.0) 0.67
Well 585 28 (4.8) 43 (7.4) 6 (1) 65 (11.1)
Borehole 405 19 (4.7) 22 (5.4) 5 (1.2) 36 (8.9)
Tap 14 0 (0.0) 2 (14.3) 0 (0) 2 (15.4)
Faecal disposal
Latrine 849 47 (5.5) 56 (6.6) 13 (1.5) 90 (10.6) 0.56
Outdoor defecation 237 7 (3.0) 16 (6.8) 1 (0.4) 22 (9.3)
Pork consumption
Yes 806 43 (5.3) 57 (7.1) 3 (1.1) 89 (11.0) 0.18
No 280 11 (3.9) 15 (5.4) 11 (1.4) 23 (8.2)
Pork preparation
Boiled 452 21 (4.6) 29 (6.4) 7 (1.5) 43 (9.5) 0.13
Grilled 345 22 (6.4) 28 (8.1) 4 (1.2) 46 (13.3)
Not specified 9 0 (0.0) 0 (0.0) 0 (0) 0 (0.0)
Source of pork
Informal market 747 41 (5.5) 52 (7.0) 10 (1.3) 83 (11.1) 0.88
Butchery 2 0 (0.0) 0 (0.0) 0 (0) 0 (0.0)
Other 56 2 (3.6) 5 (8.9) 1 (1.8) 6 (10.7)
Pig keeping
Yes 155 10 (6.5) 14 (9.3) 3 (1.9) 21 (13.5) 0.15
No 931 44 (4.7) 58 (6.2) 11 (1.2) 91 (9.8)
Pig husbandry system
Confinement 52 6 (11.5) 4 (7.7) 1 (1.9) 9 (17.3) 0.33
Free ranging 103 4 (3.9) 10 (9.7) 2 (1.9) 12 (11.7)
Ever heard about the tapeworm
Yes 105 2 (1.9) 6 (5.7) 1 (1) 7 (6.7) 0.20
No 981 52 (5.3) 66 (6.7) 13 (1.3) 105 (10.7)
https://doi.org/10.1371/journal.pntd.0010606.t002

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 10 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Table 3. Assessment of clinical signs and symptoms related to neuropsychiatric disorders in relation to socio-demographic factors.
Variables Study participants n (%) Vignette 1 (Chronic Vignette 2 (Tonic Vignette 3 (Focal Vignette 4 (Psychotic
headache) clonic seizure) seizure) disorder)
n (%) p-value n (%) p-value n (%) p-value n (%) p-value
Total 1086 530/1070 (49.5) 293/1086 (27) 188/1042 (18) 183/999 (18.3)
Age group (years)
2–14 277 123/268 (45.9) 0.47 89/277 (32.1) <0.01 45/251 (17.9) 0.55 23/219 (10.5) <0.01
15–24 251 125/247 (50.6) 73/251 (29.1) 48/247 (19.4) 49/242 (20.2)
25–54 457 227/454 (50) 116/457 (25.4) 82/444 (18.5) 92/441 (20.9)
�55 101 55/101 (54.5) 15/101 (14.9) 13/100 (13) 19/97 (19.6)
Gender
Female 446 197/438 (45) 0.02 128/446 (28.7) 0.32 72/424 (17) 0.51 84/407 (20.6) 0.14
Male 640 333/632 (52.7) 165/640 (25.8) 116/618 (18.8) 99/592 (16.7)
Level of education
No formal education 197 96/187 (51.3) 0.74 60/197 (30.5) 0.58 36/181 (19.9) 0.90 23/157 (14.6) 0.39
Primary 763 377/757 (49.8) 199/763 (26.1) 132/743 (17.8) 136/718 (18.9)
Secondary or higher 121 55/121 (45.5) 32/121 (26.4) 19/113 (16.8) 24/119 (20.2)
Other 5 2/5 (40) 2/5 (40) 1/5 (20) 0/5 (0)
Occupation
Farmer 656 338/650 (52) 0.05 162/656 (24.7) 0.04 113/646 (17.5) 0.61 130/635 (20.5) 0.03
Other 430 192/420 (45.7) 131/430 (30.5) 75/396 (18.9) 53/364 (14.6)
Water source
River 82 41/79 (51.9) 0.80 23/82 (28) 0.77 19/77 (24.7) 0.24 12/73 (16.4) 0.73
Well 585 292/582 (50.2) 165/585 (28.2) 102/560 (18.2) 104/531 (19.6)
Borehole 405 190/395 (48.1) 101/405 (24.9) 63/392 (16.1) 66/382 (17.3)
Tap 13 7/13 (53.8) 4/13 (30.8) 4/12 (33.3) 1/12 (8.3)
Other 1 0/1 (0) 0/1 (0) 0/1 (0) 0/1 (0)
Faecal disposal
Latrine 820 396/810 (48.9) 0.57 220/820 (26.8) 0.88 138/784 (17.6) 0.62 132/765 (17.3) 0.13
Outdoor defecation 237 121/231 (52.4) 64/237 (27) 46/230 (20) 43/208 (20.7)
Other 29 13/29 (44.8) 9/29 (31) 4/28 (14.3) 8/26 (30.8)
Pork consumption
Yes 280 127/276 (46) 0.20 64/280 (22.9) 0.08 40/269 (14.9) 0.14 43/260 (16.5) 0.44
No 806 403/794 (50.8) 229/806 (28.4) 148/773 (19.1) 140/739 (18.9)
Pork preparation
Boiled 452 192/446 (43) <0.001 113/452 (25) 0.04 72/431 (16.7) 0.15 62/411 (15.1) <0.01
Grilled 345 208/341 (61) 112/345 (32.5) 74/333 (22.2) 77/320 (24.1)
Not specified 9 3/7 (42.9) 4/9 (44.4) 2/9 (22.2) 1/8 (12.5)
Source of pork
Informal market 747 372/736 (50.5) 0.36 211/747 (28.2) 0.08 136/719 (18.9) 0.49 128/688 (18.6) 0.44
Butchery 2 2/2 (100) 2/2 (100) 1/2 (50) 0/2 (0)
Other 56 29/55 (52.7) 16/56 (28.6) 11/51 (21.6) 12/48 (25)
Pig keeping
Yes 155 66/153 (43.1) 0.11 44/155 (28.4) 0.74 27/146 (18.5) 0.97 31/146 (21.2) 0.39
No 931 464/917 (50.6) 249/931 (26.7) 161/896 (18) 152/853 (17.8)
Pig husbandry system
Confinement 52 21/52 (40.4) 0.75 15/52 (28.8) 1 9/49 (18.4) 1 9/50 (18) 0.63
Free ranging 103 45/101 (44.6) 29/103 (28.2) 18/97 (18.6) 22/96 (22.9)
Ever heard about the tapeworm
Yes 105 47/103 (45.6) 0.47 34/105 (32.4) 0.23 26/101 (25.7) 0.05 20/102 (19.6) 0.83
No 981 483/967 (49.9) 259/981 (26.4) 162/941 (17.2) 163/897 (18.2)
https://doi.org/10.1371/journal.pntd.0010606.t003

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 11 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Table 4. Analysis of statistical association between screening positive for vignettes and cysticercosis serology positivity.
Variables Study participants n Ag-ELISA+ or Western
(%) blot+
n (%) Unadjusted Odds Ratio (95% p-value Adjusted Odds Ratio (95% p-value
CI) CI)⸸
Total 1086 112 (10.3)
Vignette 1 (Chronic
headache)
No 540 69 (12.8) Reference 0.013 Reference 0.018
Yes 530 43 (8.1) 0.6 (0.4–0.9) 0.61 (0.41–0.91)
Vignette 2 (Tonic clonic
seizure)
No 793 85 (10.7) Reference 0.47 Reference 0.59
Yes 293 27 (9.2) 0.85 (0.53–1.32) 0.88 (0.55–1.38)
Vignette 3 (Focal seizure)
No 854 89 (10.4) Reference 0.93 Reference 0.90
Yes 188 20 (10.6) 1.02 (0.6–1.68) 1.04 (0.6–1.71)
Vignette 4 (Psychotic
disorder)
No 816 87 (10.7) Reference 0.91 Reference 0.62
Yes 183 19 (10.4) 0.97 (0.56–1.61) 0.88 (0.5–1.46)

Models were adjusted for age, gender, education and occupation

https://doi.org/10.1371/journal.pntd.0010606.t004

disorder in seropositive patients. To the best of our knowledge, this was the first pilot study
performed in the country, particularly in Mocuba district with the aim to generate baseline
information about seroprevalence and risk factors for human cysticercosis, and its possible
relationship with some selected neuropsychiatric disorders. There were several important find-
ings from our study.

Serology
Our findings revealed that human cysticercosis was prevalent in the setting of our study
(10.3%), although lower than previously reported in Angónia district and Beira city, Central
Mozambique [14,15]. The prevalence is still worrying as it demonstrates the potential for a
greater spread of the disease, which can be caused by several factors, including hygiene and
sanitation. The higher prevalence in some municipalities such as Mocuba (17.7%) in compari-
son with those with lower prevalences (e.g. Alto Benfica, 3.6%), may be explained by sociode-
mographic factors, which should be analysed in future studies.
Previous studies from Mozambique found in general higher prevalence of either antigens
(15%) or antibodies (10%) to T. solium larva than the ones reported in this study [14,15], and
were consistent with studies done in other settings such as Cameroon [27], Nigeria [28], Viet-
nam [29,30], Zambia [31] and Democratic Republic of Congo [5], which reported similar sero-
prevalence rates. In our study, only 12.5% of the screened sera tested simultaneously positive
to both serological assays. The differences in the prevalence of antigens (4.9%), that indicates a
current infection, and antibodies (6.2%), which indicates a previous or current exposure to
infection, may be influenced by the number, location of cysts and their larval stage. Further-
more, antibodies can persist longer, even after the clearance of the infection, while the presence
of antigens is only detected when viable parasites are present [1–3,10,32,33]. Moreover, the
western blot assay we used detected only three out of the seven glycoproteins described to be

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 12 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

specific for cysticercosis [1,32,34]. So, it is possible that the prevalence of antibodies found in
our study was underestimated.
In addition to that, the differences in study design, HIV serostatus characteristics of the
study participants (immunocompetent or immunocompromised), serological assays used for
each study, and parasite genetic diversity (which ultimately influenced the sensitivity and spec-
ificity of the serological assays) can explain the differences found within studies in the same
region and in other settings [5,9,10,35]. Of note, that to date, we do not have systematic studies
done in Mozambique accessing the existing genetic variants of T. solium, except for the one in
which phylogenetic studies of cysts from Central Mozambique revealed the existence of the
Latin variant [32]. As Mozambique has been exposed to migration from Europe and Asia, we
cannot exclude the possibility that Mozambique has both variants circulating in different
regions and further studies should be done in order to provide relevant information about this
subject.

Cysticercosis serology and neuropsychiatric disorders

Our study also demonstrated that chronic headache (49.5%), generalized epileptic seizures
(27%), focal epileptic seizures (18%), and psychosis (18.3%) affected a substantial proportion
of study participants irrespective of their cysticercosis serostatus. Our findings are consistent
with data from 2018 hospital records, indicating that Mocuba district had the highest number
of patients (7,416; 75.3%) in the entire province (9,844) with mental disorders. Out of these
7,416 mental health out-patients, 1,863 (25.1%) had epilepsy, 250 (3.4%) had mental retarda-
tion and 1,401 (18.9%) had psychosis [36].
In our study, epileptic seizures were significantly more prevalent in younger participants
(2–14 years) and decreased with age (p<0.001). This finding is consistent with recent mental
health data in Mozambique showing that among people living with epilepsy, 54% were chil-
dren aged up to 15 years, although the underlying causes of these conditions are not well
defined [21,37]. Similar studies in African countries also found that epileptic seizures and epi-
lepsy were the main leading causes of mental health diagnoses in out-patients’ consultations
and that the majority of people affected are children and adolescents [14,16,37,38]. Although
we did not find significant associations between serology and epileptic seizures, as with psy-
chosis, our findings therefore present a very high prevalence of epileptic seizures (both gener-
alized and focal) that occur independently of seropositivity to cysticercosis and thus could be
caused by other underlying diseases such as cerebral malaria, head trauma or perinatal hypoxia
in children, to name a few.
When compared with other similar studies, our findings here corroborate with results from
Bangoua, Cameroon [27], which did not find any statistically significant difference in the sero-
positivity to T. solium larva between people with epileptic seizures (1/61, 1.6%) and those with-
out (5/323, 1.5%). Similarly, another study in the Democratic Republic of Congo [5] revealed
that there was no difference in seropositivity between people with neurological disorders and
those without. In addition, there was no association between cysticercosis and epilepsy in a
study conducted in the Gambia [39]. To the contrary, it is well documented in the literature
from Latin America, Asia and Africa, including the study done in Angónia district, that sero-
positivity to circulating antigens or antibodies of cysticercosis were associated with epilepsy in
community-based studies [14,40,41,42]. Furthermore, the odds ratio from a study in Nigeria
revealed that people with epilepsy in the study area with a relatively high cysticercosis preva-
lence, were two times more likely to be seropositive than those without [28].
In our study, chronic headache was significantly associated with circulating antigens
(p = 0.013). In fact, other studies performed in Mozambique, Burkina Faso and Tanzania also

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 13 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

found that seropositivity to cysticercal antigens was associated with severe headache
[14,15,42,43]. Nevertheless, in other settings such as in Anzoátegui in Venezuela, Vietnam and
Nabo Village in Tiandong, China, no statistical association was found between these two vari-
ables [44–46]. Our findings may reflect the fact that headache may be correlated to the patho-
genesis of the disease in this study setting.
In addition to the high burden of epileptic seizures and chronic headache, we also found
that psychotic manifestations were highly prevalent in the setting of our study (18.3%), con-
firming the anecdotal reports from the Mocuba district community leaders of having a high
proportion of community residents with those conditions. As with the other two disorders,
psychotic disorders do not seem to be related to cysticercosis seropositivity either. Psychotic
disorders are understudied in Africa, as revealed by a recent scoping review [47], that found
only nine studies in which the prevalence of psychotic disorders was analysed in Africa from
1984 to 2020. The available reports describe a prevalence ranging from 1% to 4.4% in rural
regions. The only published population-based study done in 2003 in a rural (Cuamba) and
urban (Maputo) area of northern and southern Mozambique, respectively, found that seizure
disorders (4.4% vs 1.6%), psychosis (4.4% vs 1.9%) and mental retardation (1.9% vs 1.3%) were
higher in rural compared to urban areas [24] and well below the results of our study and recent
hospital data from Zambézia Provincial Directorate [36]. It is difficult to explain this high bur-
den. Apart from the possibility of other CNS pathogens causing epileptic seizures/epilepsy and/
or psychosis, such as Toxoplasma gondii, Toxocara spp. and Onchocerca volvulus (the latter was
recently identified in Zambézia province) [20,21,48,49], we think that the prolonged armed con-
flict that affected this region for decades in some of the study villages [50,51], combined with
the stress it provokes in the affected population, might be playing a role as causative agent for
this high prevalence of psychosis. Indeed, the effects of armed conflict on mental health within
the affected communities is well documented in the literature, as it causes disruption of socio-
economic and political infrastructure including the appropriate delivery of health care services,
which was the case in our study setting and other regions of Mozambique [50–53].

Risk factors and multivariate logistic regression

In our study, patients of older age were more likely to be seropositive for the parasite. Regard-
ing age, the results are important because they will allow us to understand the transmission
dynamics of TSC in the study region, and to identity the age groups at higher risk. It is likely
that infection events accumulate as people age [54], and that T. solium cysticercus antibodies
might persist for several years [55]. Similarly to our results, studies from Tanzania [43], Ecua-
dor [56], Zambia [31], Peru [57], Burkina Faso [58] and Vietnam [29], including a systematic
review [59], revealed an association between increasing age and seropositivity to cysticercosis,
except for a study conducted by Noormahomed et al. [15], in which age was not significantly
associated with the seroprevalence of the helminths studied, including cysticercosis.
Furthermore, in concordance with the present study, there was no statistically significant
difference between gender and seropositivity in Ecuador [56] and Zambia [31]. To the con-
trary, in Tanzania [43], females were more likely to be seropositive, while in Burkina Faso and
Vietnam this was true for males [29,58]. On the other hand, neither gender nor age presented
a statistically significant association with seropositivity to cysticercosis in other studies [30,
44,46, 60].
Analysing the knowledge of T. solium, although our results did not present a statistically
significant association with TSC seropositivity, in other countries such as Nigeria [28] poor
knowledge of cysticercosis and improper pork preparation were identified as main risk and
behavioural factors contributing to the high prevalence.

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 14 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Other potential risk factors such as consumption of pork [61], pig keeping, use of unsafe
water, faecal disposal and types of latrine were not statistically significant in our study, simi-
larly to the study done in Angónia district [14]. This was expected since the study participants
share the same environmental conditions, and are equally exposed to the same risk factors and
consequently equally exposed to the infection. Furthermore, although there is a fraction of
Muslim people amongst our study participants, we did not expect our findings to be affected
by the religion, since cysticercosis is acquired mainly through water or food contaminated
with T. solium eggs, and consequently anyone can acquire the infection regardless of the con-
sumption of pork meat or professed religion. In some studies, food, water and hygiene related
factors were significantly associated with cysticercosis seropositivity, including consumption
of undercooked pork [44], and using the same water source [43]; although in other studies, fac-
tors such as consumption of raw meat and/or vegetables [30] and hygiene (presence of latrine)
[57] were not associated with cysticercosis seropositivity.

Strengths and limitations

The strength of this study is reflected in the fact that, to the best of our knowledge, this is the
first assessment done in Mozambique aiming to define the seroprevalence of cysticercosis and
its possible association with some selected neuropsychiatric disorders. It is therefore the first
pilot community-based study representative of the Mocuba district population including rural
and urban settings and all age groups except those under 2 years old. This baseline information
will be useful to define strategies for control and mitigation of TSC in this district and to effec-
tively diagnose and treat neuropsychiatric disorders that might be associated with cysticerco-
sis. Additionally, further studies can be developed in other districts and provinces, taking into
account the population at risk.
One of the limitations was the lack of clinical examination and diagnostic tools required to
confirm the diagnosis of neuropsychiatric disorders. Also, patients with neuropsychiatric dis-
orders with positive or negative serology for cysticercosis did not undergo CT or MRI exami-
nation in order to confirm or not the diagnosis. Regarding the serological assays, these present
limitations in terms of sensitivity and specificity as well as on the discrimination of past or cur-
rent infection. Additionally, serological screening for malaria, toxoplasmosis, toxocariasis, and
onchocerciasis, that may cause neuropsychiatric disorders, was not done. Thus, it is not possi-
ble to draw firm conclusions about the fraction of participants whose neuropsychiatric signs/
symptoms could have been due to cysticercosis/NCC or its sequelae.

Conclusions and recommendations

In conclusion, our study found a seroprevalence of 10.3% of TSC and was associated with
chronic headache (p = 0.013). Nonetheless, the seroprevalence was not associated with epilep-
tic seizures/epilepsy, and/or psychosis. The lowest prevalence was found in Alto Benfica village
(3.6%) and the highest in Mocuba Municipality (17.7%). It was also shown that seropositivity
increased with age (p = 0.03). Our findings are important because there is a need to under-
stand the burden of mental illness and its causes in the region, and whether it is related to cys-
ticercosis/NCC.
Nevertheless, the role of TSC in the aetiology of neuropsychiatric disorders in cysticercosis
endemic areas should be further studied. In addition, other CNS pathogens should be investi-
gated to define their role in the burden of our targeted neuropsychiatric disorders as well as to
help in the differential diagnosis of cysticercosis/NCC. This should be done in combination
with studies of psychological, economic and societal impact of armed conflicts in the region
and in sub-Saharan Africa as a whole.

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 15 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

Given the limited value of serology for diagnosis of cysticercosis and NCC and the scarcity
and costliness of imaging techniques in endemic countries, research priorities should be given
to the development of a point-of-care diagnostic tool and/or a biomarker. This should be done
in combination with studies on parasite genetic diversity, and eco-epidemiological as well as
clinical features of cysticercosis/NCC to assess geographic distribution patterns to support sur-
veillance, diagnosis and control of cysticercosis and NCC.

Acknowledgments
We are indebted to the Zambézia Provincial Governor, Dr Abdul Razak Noormahomed, his
team and to the community leaders whose support and collaboration during the field work
was critical for the engagement of the study participants in this research. We also thank the
Mental health Department and the National Public Health Directorate of the Ministry of
Health in Maputo, Mozambique for providing clinical assistance to the participants. Finally,
we are thankful to the study participants who consented to participate in this study.

Author Contributions
Conceptualization: Alberto Pondja, Clarissa Prazeres da Costa, Veronika Schmidt, Andrea S.
Winkler, Emı́lia Virgı́nia Noormahomed.
Data curation: Irene Langa, Fernando Padama, Noémia Nhancupe, Alberto Pondja, Dominik
Stelzle, Emı́lia Virgı́nia Noormahomed.
Formal analysis: Alberto Pondja, Dominik Stelzle, Clarissa Prazeres da Costa, Veronika
Schmidt, Andrea S. Winkler, Emı́lia Virgı́nia Noormahomed.
Funding acquisition: Andrea S. Winkler, Emı́lia Virgı́nia Noormahomed.
Investigation: Irene Langa, Fernando Padama, Noémia Nhancupe, Alberto Pondja, Clarissa
Prazeres da Costa, Veronika Schmidt, Andrea S. Winkler, Emı́lia Virgı́nia Noormahomed.
Methodology: Irene Langa, Fernando Padama, Noémia Nhancupe, Emı́lia Virgı́nia
Noormahomed.
Project administration: Emı́lia Virgı́nia Noormahomed.
Supervision: Irene Langa, Fernando Padama, Noémia Nhancupe, Emı́lia Virgı́nia
Noormahomed.
Writing – original draft: Irene Langa, Fernando Padama, Noémia Nhancupe, Alberto Pondja,
Delfina Hlashwayo, Lidia Gouveia, Dominik Stelzle, Clarissa Prazeres da Costa, Veronika
Schmidt, Andrea S. Winkler, Emı́lia Virgı́nia Noormahomed.
Writing – review & editing: Irene Langa, Fernando Padama, Noémia Nhancupe, Alberto
Pondja, Delfina Hlashwayo, Lidia Gouveia, Dominik Stelzle, Clarissa Prazeres da Costa,
Veronika Schmidt, Andrea S. Winkler, Emı́lia Virgı́nia Noormahomed.

References
1. Carpio A, Fleury A, Romo ML, Abraham R. Neurocysticercosis: the good, the bad, and the missing.
Expert Rev Neurother. 2018; 18:289–301. https://doi.org/10.1080/14737175.2018.1451328 PMID:
29521117
2. Del Brutto OH. Neurocysticercosis in Western Europe: a re-emerging disease? Acta Neurol Belg. 2012;
112:335–343. https://doi.org/10.1007/s13760-012-0068-3 PMID: 22527788

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 16 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

3. Garcia HH, Nash TE, Del Brutto OH. Clinical symptoms, diagnosis, and treatment of neurocysticerco-
sis. Lancet Neurol. 2014; 13:1202–1215. https://doi.org/10.1016/S1474-4422(14)70094-8 PMID:
25453460
4. Nhancupe N, Noormahomed EV, Afonso S, Svard S, Lindh J. Further evaluation of recombinant Tsol-
p27 by enzyme-linked immunoelectrotransfer blot for the serodiagnosis of cysticercosis in pigs from
Mozambique. Parasit Vectors. 2019; 12:564. https://doi.org/10.1186/s13071-019-3816-x PMID:
31775845
5. Mukendi D, Kalo JL, Lutumba P, Barbé B, Jacobs J, Yansouni CP, et al. High frequency of Taenia
solium antigen positivity in patients admitted for neurological disorders in the Rural Hospital of
Mosango, Democratic Republic of Congo. BMC Infect Dis. 2021;17: 21(1):359. https://doi.org/10.1186/
s12879-021-06032-8 PMID: 33865327
6. Flisser A, Madrazo I, Plancarte A, Schantz P, Allan J, Craig P, et al. Neurological symptoms in occult
neurocysticercosis after single taeniacidal dose of praziquantel. Lancet. 1993; 342:748. https://doi.org/
10.1016/0140-6736(93)91743-6 PMID: 8103859
7. Winkler AS. Neurocysticercosis in sub-Saharan Africa: a review of prevalence, clinical characteristics,
diagnosis, and management. Pathog Glob Health. 2012; 106:261–274. https://doi.org/10.1179/
2047773212Y.0000000047 PMID: 23265550
8. Winkler AS, Willingham AL 3rd, Sikasunge CS, Schmutzhard E. Epilepsy and neurocysticercosis in
sub-Saharan Africa. Wien Klin Wochenschr. 2009; 121 Suppl 3:3–12. https://doi.org/10.1007/s00508-
009-1242-3 PMID: 19915809
9. Ndimubanzi PC, Carabin H, Budke CM, Nguyen H, Qian YJ, Rainwater E, et al. A systematic review of
the frequency of neurocyticercosis with a focus on people with epilepsy. PLoS Negl Trop Dis. 2010; 4:
e870. https://doi.org/10.1371/journal.pntd.0000870 PMID: 21072231
10. Garcia HH. Neurocysticercosis. Neurol Clin. 2018; 36:851–864; https://doi.org/10.1016/j.ncl.2018.07.
003 PMID: 30366559
11. Willingham AL 3rd,Engels D. Control of Taenia solium cysticercosis/taeniosis. Adv Parasitol. 2006;
61:509–566. https://doi.org/10.1016/S0065-308X(05)61012-3 PMID: 16735172
12. Winkler AS. Epilepsy and neurocysticercosis in sub-Saharan Africa. In: Foyaca-Sibat H, editor. Novel
aspects on cysticercosis and neurocysticercosis. InTech; 2013; p. 307–340.
13. Afonso SM, Vaz Y, Neves L, Pondja A, Dias G, Willingham AL, et al. Human and porcine Taenia solium
infections in Mozambique: identifying research priorities. Anim Health Res Rev. 2011; 12:123–129.
https://doi.org/10.1017/S1466252311000077 PMID: 21676344
14. Assane YA, Trevisan C, Schutte CM, Noormahomed EV, Johansen MV, Magnussen P. Neurocysticer-
cosis in a rural population with extensive pig production in Angonia district, Tete Province, Mozambique.
Acta Trop. 2017; 165:155–160. https://doi.org/10.1016/j.actatropica.2015.10.018 PMID: 26519884
15. Noormahomed EV, Nhacupe N, Mascaro-Lazcano C, Mauaie MN, Buene T, Funzamo CA, et al. A
cross-sectional serological study of cysticercosis, schistosomiasis, toxocariasis and echinococcosis in
HIV-1 infected people in Beira, Mozambique. PLoS Negl Trop Dis. 2014; 8:e3121. https://doi.org/10.
1371/journal.pntd.0003121 PMID: 25188395
16. Ministério da Saúde. Norma de tratamento da epilepsia. 2016; 24 p. República de Moçambique.
17. Noormahomed EV, Mandane A, Cuambe A, Rodrigues MA, Noormahomed S, Carrilho C, et al. Design
and Implementation of Postgraduate Programs in Health in a Resource-Limited Setting in Mozambique
(The Lurio University). Adv Med Educ Pract. 2021; 12:399–412. https://doi.org/10.2147/AMEP.
S291364 PMID: 33911914
18. Muadica AS, Balasegaram S, Beebeejaun K, Köster PC, Bailo B, Hernández-de-Mingo M, et al. (2021).
Risk associations for intestinal parasites in symptomatic and asymptomatic schoolchildren in central
Mozambique. Clin Microb Infect. 2021; 27(4):624–629. https://doi.org/10.1016/j.cmi.2020.05.031
PMID: 32505583
19. Grau-Pujol B, Massangaie M, Cano J, Maroto C, Ndeve A, Saute F, et al. Frequency and distribution of
neglected tropical diseases in Mozambique: a systematic review. Infect Dis Poverty. 2019; 8:103.
https://doi.org/10.1186/s40249-019-0613-x PMID: 31836025
20. Noormahomed EV, Akrami K, Mascaro-Lazcano C. Onchocerciasis, an undiagnosed disease in
Mozambique: identifying research opportunities. Parasit Vectors. 2016; 9:180. https://doi.org/10.1186/
s13071-016-1468-7 PMID: 27030247
21. Noormahomed EV, Mascaro-Lazcano C. Onchocerciasis in Mozambique: An unknown condition for
health professionals. EC Microbiol; 2019. 15;160–167. PMID: 30957099
22. INE. Folheto Estatistico Distrital Mocuba 2018; 2022. Available at: http://www.ine.gov.mz/estatisticas/
publicacoes/folheto-distrital/zambezia/411-folhetos-dpine-mocuba-2018.pdf/at_download/file.
Accessed: April 10, 2022.

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 17 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

23. Daniel WW. Biostatistics: A Foundation for Analysis in the Health Sciences. 1999. New York: John
Wiley & Sons.
24. Patel V, Simbine AP, Soares IC, Weiss HA, Wheeler E. Prevalence of severe mental and neurological
disorders in Mozambique: a population-based survey. Lancet. 2007; 370:1055–1060. https://doi.org/10.
1016/S0140-6736(07)61479-2 PMID: 17889244
25. Cysticercosis Working Group in Eastern and Southern Africa. Declaration on Taenia solium cysticerco-
sis/taeniosis. Acta Tropica. 2003; 87:1–2. https://doi.org/10.1016/S0001-706X(03)00049-4
26. Jane Shaw S. How to undertake venepuncture to obtain venous blood samples. Nurs Stand. 2018; 32
(29):41–47. https://doi.org/10.7748/ns.2018.e10531 PMID: 29537759
27. Nkouawa A, Dschanou AR, Moyou-Somo R, Sako Y, Ito A. Seroprevalence and risk factors of human
cysticercosis and taeniasis prevalence in a highly endemic area of epilepsy in Bangoua, west Camer-
oon. Acta tropica. 2017; 165:116–120. https://doi.org/10.1016/j.actatropica.2015.12.019 PMID:
26747010
28. Edia-Asuke AU, Inabo HI, Mukaratirwa S, Umoh VJ, Whong CM, Asuke S, et al. Seroprevalence of
human cysticercosis and its associated risk factors among humans in areas of Kaduna metropolis,
Nigeria. J Infect Dev Ctries. 2015; 9:799–805. https://doi.org/10.3855/jidc.5415 PMID: 26322870
29. Nguyen T, Cheong FW, Liew JW, Lau YL. Seroprevalence of fascioliasis, toxocariasis, strongyloidiasis
and cysticercosis in blood samples diagnosed in Medic Medical Center Laboratory, Ho Chi Minh City,
Vietnam in 2012. Parasit Vectors. 2016; 9(1):486. https://doi.org/10.1186/s13071-016-1780-2 PMID:
27595647
30. Binh VTL, Dung DT, Vinh HQ, Anke VH, Nicolas P, Pierre D, et al. Human Taeniasis and Cysticercosis
and Related Factors in Phu Tho Province, Northern Vietnam. Korean J Parasitol 2021; 59(4):369–376.
https://doi.org/10.3347/kjp.2021.59.4.369 PMID: 34470088
31. Mwape KE, Phiri IK, Praet N, Muma JB, Zulu G, Van den Bossche P, et al. Taenia solium Infections in a
rural area of Eastern Zambia-a community based study. PLoS Negl Trop Dis. 2012; 6(3):e1594. https://
doi.org/10.1371/journal.pntd.0001594 PMID: 22479664
32. Ito A, Yamasaki H, Nakao M, Sako Y, Okamoto M, Sato MO, et al. Multiple genotypes of Taenia solium
—ramifications for diagnosis, treatment and control. Acta Trop. 2003; 87:95–101. https://doi.org/10.
1016/s0001-706x(03)00024-x PMID: 12781383
33. Palafox-Fonseca H, Zuniga G, Bobes RJ, Govezensky T, Pinero D, Texco-Martinez L, et al. Genetic
variation in the Cytb gene of human cerebral Taenia solium cysticerci recovered from clinically and
radiologically heterogeneous patients with neurocysticercosis. Mem Inst Oswaldo Cruz. 2013;
108:914–920. https://doi.org/10.1590/0074-0276130308 PMID: 24271046
34. Tsang VC, Brand JA, Boyer AE. An enzyme-linked immunoelectrotransfer blot assay and glycoprotein
antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis. 1989; 159: 50–59. https://
doi.org/10.1093/infdis/159.1.50 PMID: 2909643
35. Rodriguez S, Wilkins P, Dorny P. Immunological and molecular diagnosis of cysticercosis. Pathog Glob
Health. 2012, 106:286–298. https://doi.org/10.1179/2047773212Y.0000000048 PMID: 23265553
36. Direcção Provincial de Saúde da Zambézia, Programa de Saúde Mental. 2019. Relatório annual de
Saúde Mental.
37. Wagenaar BH, Cumbe V, Raunig-Berho M, Rao D, Kohrt BA, Stergachis A, et al. Outpatient mental
health services in Mozambique: use and treatments. Psychiatr Serv. 2016; 67:588–590. https://doi.org/
10.1176/appi.ps.201500508 PMID: 26828400
38. Dos Santos PF, Cumbe V, Gouveia ML, de Fouchier C, Teuwen D, Dua T. Implementation of mhGAP
in Mozambique: integrating epilepsy care into the primary health care system. Int J Ment Health Syst.
2019; 13:36. https://doi.org/10.1186/s13033-019-0296-5 PMID: 31160920
39. Secka A, Marcotty T, De Deken R, Van Marck E, Geerts S. Porcine cysticercosis and risk factors in the
Gambia and Senegal. J Parasitol Res. 2010;823892. https://doi.org/10.1155/2010/823892 PMID:
20981349
40. Quet F, Guerchet M, Pion SD, Ngoungou EB, Nicoletti A, Preux PM. Meta-analysis of the association
between cysticercosis and epilepsy in Africa. Epilepsia. 2010; 51:830–837. https://doi.org/10.1111/j.
1528-1167.2009.02401.x PMID: 19919664
41. Debacq G, Moyano LM, Garcia HH, Boumediene F, Marin B, Ngoungou EB, et al. Systematic review
and meta-analysis estimating association of cysticercosis and neurocysticercosis with epilepsy. PLoS
Negl Trop Dis. 2017; 11:e0005153. https://doi.org/10.1371/journal.pntd.0005153 PMID: 28267746
42. Sahlu I, Carabin H, Ganaba R, Preux PM, Cisse AK, Tarnagda Z, et al. Estimating the association
between being seropositive for cysticercosis and the prevalence of epilepsy and severe chronic head-
aches in 60 villages of rural Burkina Faso. PLoS Negl Trop Dis. 2019; 13:e0007101. https://doi.org/10.
1371/journal.pntd.0007101 PMID: 30677038

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 18 / 19

PLOS NEGLECTED TROPICAL DISEASES T. solium cysticercosis and neuropsychiatric disorders in Mocuba

43. Mwanjali G, Kihamia C, Kakoko DV, Lekule F, Ngowi H, Johansen MV, et al. Prevalence and risk factors
associated with human Taenia solium infections in Mbozi District, Mbeya Region, Tanzania. PLoS Negl
Trop Dis. 2013; 7(3):e2102. https://doi.org/10.1371/journal.pntd.0002102 PMID: 23516650
44. Toquero M, Morocoima A, Ferrer E. [Seroprevalence and risk factors of cysticercosis in two rural com-
munities in Anzoátegui state, Venezuela]. Biomedica. 2017;1, 37(0):66–74. https://doi.org/10.7705/
biomedica.v37i2.2841 PMID: 28527268
45. Trung DD, Praet N, Cam TD, Lam BV, Manh HN, Gabriël S, et al. Assessing the burden of human cysti-
cercosis in Vietnam. Trop Med Int Health. 2013; 18(3):352–6. https://doi.org/10.1111/tmi.12043 PMID:
23279716
46. Chung JY, Eom KS, Yang Y, Li X, Feng Z, Rim HJ, et al. A seroepidemiological survey of Taenia solium
cysticercosis in Nabo, Guangxi Zhuang Autonomous Region, China. Korean J Parasitol. 2005; 43
(4):135–9. https://doi.org/10.3347/kjp.2005.43.4.135 PMID: 16340302
47. Greene MC, Yangchen T, Lehner T, Sullivan PF, Pato CN, McIntosh A, et al. The epidemiology of psy-
chiatric disorders in Africa: a scoping review. Lancet Psychiatry. 2021; 8(8):717–731. https://doi.org/10.
1016/S2215-0366(21)00009-2 PMID: 34115983
48. Forrester JV, McMenamin PG, Dando SJ. CNS infection and immune privilege. Nat Rev Neurosci.
2018; 19(11):655–671. https://doi.org/10.1038/s41583-018-0070-8 PMID: 30310148
49. Manuel L, Santos-Gomes G, Noormahomed EV. Human toxoplasmosis in Mozambique: gaps in knowl-
edge and research opportunities. Parasit Vectors. 2020; 13:571. https://doi.org/10.1186/s13071-020-
04441-3 PMID: 33176884
50. Noormahomed EV, Mocumbi AO, Ismail M, Carrilho C, Patel S, Nguenha A, et al. The medical educa-
tion partnership initiative effect on increasing health professions education and research capacity in
Mozambique. Ann Glob Health. 2018; 84:47–57. https://doi.org/10.29024/aogh.14 PMID: 30873790
51. Nachega JB, Grimwood A, Mahomed H, Fatti G, Preiser W, Kallay O, et al. From Easing Lockdowns to
Scaling Up Community-based Coronavirus Disease 2019 Screening, Testing, and Contact Tracing in
Africa-Shared Approaches, Innovations, and Challenges to Minimize Morbidity and Mortality. Clin Infect
Dis. 2021; 72:327–331. https://doi.org/10.1093/cid/ciaa695 PMID: 33501963
52. Cliff J, Noormahomed AR. Health as a target: South Africa’s destabilization of Mozambique. Soc Sci
Med. 1988; 27:717–722. https://doi.org/10.1016/0277-9536(87)90331-5 PMID: 3227373
53. Morina N, Akhtar A, Barth J, Schnyder U. Psychiatric Disorders in Refugees and Internally Displaced
Persons After Forced Displacement: A Systematic Review. Front Psychiatry. 2018; 9:433. https://doi.
org/10.3389/fpsyt.2018.00433 PMID: 30298022
54. Cavellani CL, Faleiros AC, Lino Rde S Jr, Dos Reis MA, Teixeira V. Cysticercosis in the elderly. Ann
Diagn Pathol. 2007: 11(5): 330–333. https://doi.org/10.1016/j.anndiagpath.2006.12.008 PMID:
17870018
55. Galipó E, Dixon MA, Fronterrè C, Cucunubá ZM, Basáñez MG, Stevens K, et al. Spatial distribution and
risk factors for human cysticercosis in Colombia. Parasites Vectors. 2021; 14:590. https://doi.org/10.
1186/s13071-021-05092-8 PMID: 34838117
56. Praet N, Speybroeck N, Rodriguez-Hidalgo R, Benitez-Ortiz W, Berkvens D, Brandt J, et al. Age-related
infection and transmission patterns of human cysticercosis. Int J Parasitol. 2010; 40(1):85–90. https://
doi.org/10.1016/j.ijpara.2009.07.007 PMID: 19683531
57. Moyano LM O’Neal SE, Ayvar V, Gonzalvez G, Gamboa R, Vilchez P, et al. High Prevalence of Asymp-
tomatic Neurocysticercosis in an Endemic Rural Community in Peru. PLoS Negl Trop Dis. 2016; 10
(12):e0005130. https://doi.org/10.1371/journal.pntd.0005130 PMID: 27992429
58. Carabin H, Millogo A, Cisse A, Gabriel S, Sahlu I, Dorny P, et al. Prevalence of and Factors Associated
with Human Cysticercosis in 60 Villages in Three Provinces of Burkina Faso. PLoS Negl Trop Dis.
2015; 9:e0004248. https://doi.org/10.1371/journal.pntd.0004248 PMID: 26588468
59. Coral-Almeida M, Gabriël S, Abatih EN, Praet N, Benitez W, Dorny P. Taenia solium Human Cysticer-
cosis: A Systematic Review of Sero-epidemiological Data from Endemic Zones around the World.
PLoS Negl Trop Dis. 2015; 9(7): e0003919. https://doi.org/10.1371/journal.pntd.0003919 PMID:
26147942
60. Goodman KA, Ballagh SA, Carpio A. Case-control study of seropositivity for cysticercosis in Cuenca,
Ecuador. Am J Trop Med Hyg. 1999; 60(1):70–4. https://doi.org/10.4269/ajtmh.1999.60.70 PMID:
9988326
61. Rebecca WP, Eugene II, Joshua K. Seroprevalence of antibodies (IgG) to Taenia solium among pig
rearers and associated risk factors in Jos metropolis, Nigeria. J Infect Dev Ctries. 2013; 7:67–72.
https://doi.org/10.3855/jidc.2309 PMID: 23416651

PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0010606 July 14, 2022 19 / 19