Prevalence of Anti-Toxoplasma gondii and Anti-Brucella Spp. Antibodies in Pregnant Women From Mogadishu, Somalia

Abstract

Toxoplasmosis and brucellosis are zoonotic diseases of worldwide distribution. They
both cause abortion and infertility in human and animals. Limited data are available
about these pathogens in Somali people and their animals. Hence, this study has
evaluated the prevalence of anti-Toxoplasma gondii and anti-Brucella spp. antibodies
in pregnant women in Mogadishu, Somalia. Serum samples from 307 pregnant women
from Mogadishu, Somalia were tested for anti-T. gondii antibodies by Latex Agglutination
Test (LAT) and anti-Brucella spp. antibodies by Rose Bengal Plate Test (RBPT) and a
commercial competitive-ELISA (cELISA). A total of 119/307 (38.76%) pregnant women
had a prior history of abortion. A total of 159/307 (51.79%; 95% CI: 46.2–57.35%)
pregnant women were seroreactive for T. gondii by LAT at different stages of pregnancy.
For Brucella spp., when RBPT and cELISA were combined 4/307 (1.30%; 95% CI:
0.36–3.30%) pregnant women were seroreactive to anti-Brucella spp. antibodies, being
2/307 (0.65%; 95% CI: 0.18–2.34%) by RBPT and 3/307 (0.98%; 95% CI: 0.33–2.83%)
by cELISA. Two women were seroreactive for both agents. A high seropositivity to T.
gondii and low seropositivity to Brucella spp. have been found in pregnant women from
Mogadishu, Somalia. Considering the high number of abortions in the country associated
to the fact that awareness on other zoonotic abortifacient pathogens in Somalis is very
low, further studies should be conducted to evaluate the potential causes of abortions.

Full text

ORIGINAL RESEARCH
published: 04 August 2021
doi: 10.3389/frph.2021.672885
Frontiers in Reproductive Health | www.frontiersin.org 1August 2021 | Volume 3 | Article 672885
Edited by:
Renu Bharadwaj,
B. J. Medical College and Sassoon
Hospital, India
Reviewed by:
Theocharis Koufakis,
University General Hospital of
Thessaloniki AHEPA, Greece
Bahador Sarkari,
Shiraz University of Medical
Sciences, Iran
*Correspondence:
Abdulkarim A. Yusuf
karimvet@abrar.edu.so
Rafael F. C. Vieira
rvieira@ufpr.br
Specialty section:
This article was submitted to
Reproductive Epidemiology,
a section of the journal
Frontiers in Reproductive Health
Received: 10 March 2021
Accepted: 06 July 2021
Published: 04 August 2021
Citation:
Yusuf AA, Hassan-Kadle AA,
Ibrahim AM, Hassan-Kadle MA,
Yasin AM, Khojaly M, Garcia JL and
Vieira RFC (2021) Prevalence of
Anti-Toxoplasma gondii and
Anti-Brucella Spp. Antibodies in
Pregnant Women From Mogadishu,
Somalia.
Front. Reprod. Health 3:672885.
doi: 10.3389/frph.2021.672885
Prevalence of Anti-Toxoplasma
gondii and Anti-Brucella Spp.
Antibodies in Pregnant Women From
Mogadishu, Somalia
Abdulkarim A. Yusuf1, 2
*, Ahmed A. Hassan-Kadle 1,2 , Abdalla M. Ibrahim 1,2,3 ,
Mohamed A. Hassan-Kadle 3, Abdullahi M. Yasin3, Maha Khojaly 4, João L. Garcia 5and
Rafael F. C. Vieira 1,6
*
1Vector-Borne Diseases Laboratory, Department of Veterinary Medicine, Universidade Federal Do Paraná, Curitiba, Brazil,
2Abrar Research and Training Centre, Abrar University, Mogadishu, Somalia, 3College of Medicine and Health Science, Abrar
University, Mogadishu, Somalia, 4Central Veterinary Research Laboratory, Khartoum, Sudan, 5Department of Veterinary
Preventive Medicine, Londrina State University, Londrina, Brazil, 6Global One Health Initiative, The Ohio State University,
Columbus, OH, United States
Toxoplasmosis and brucellosis are zoonotic diseases of worldwide distribution. They
both cause abortion and infertility in human and animals. Limited data are available
about these pathogens in Somali people and their animals. Hence, this study has
evaluated the prevalence of anti-Toxoplasma gondii and anti-Brucella spp. antibodies
in pregnant women in Mogadishu, Somalia. Serum samples from 307 pregnant women
from Mogadishu, Somalia were tested for anti-T. gondii antibodies by Latex Agglutination
Test (LAT) and anti-Brucella spp. antibodies by Rose Bengal Plate Test (RBPT) and a
commercial competitive-ELISA (cELISA). A total of 119/307 (38.76%) pregnant women
had a prior history of abortion. A total of 159/307 (51.79%; 95% CI: 46.2–57.35%)
pregnant women were seroreactive for T. gondii by LAT at different stages of pregnancy.
For Brucella spp., when RBPT and cELISA were combined 4/307 (1.30%; 95% CI:
0.36–3.30%) pregnant women were seroreactive to anti-Brucella spp. antibodies, being
2/307 (0.65%; 95% CI: 0.18–2.34%) by RBPT and 3/307 (0.98%; 95% CI: 0.33–2.83%)
by cELISA. Two women were seroreactive for both agents. A high seropositivity to T.
gondii and low seropositivity to Brucella spp. have been found in pregnant women from
Mogadishu, Somalia. Considering the high number of abortions in the country associated
to the fact that awareness on other zoonotic abortifacient pathogens in Somalis is very
low, further studies should be conducted to evaluate the potential causes of abortions.
Keywords: foodborne pathogens, toxoplasmosis, brucellosis, abortion, One Health, Somalia
INTRODUCTION
Toxoplasmosis, caused by Toxoplasma gondii, and brucellosis, caused by Brucella spp., are
important zoonotic diseases with worldwide occurrence (1–3). These zoonotic pathogens may
be transmitted from animals to human beings and lead to negative health consequences such as
abortion and complete sterility (4).

Yusuf et al. Toxoplasmosis and Brucellosis in Somalia
Brucellosis in humans is commonly caused by Brucella
melitensis and/or Brucella abortus, and is characterized by
inflammation of the genitals and fetal membranes, abortions,
sterility and lesions in the lymphatic system and joints
(4,5). Endocarditis and neurological outcomes including
motor deficits, cranial nerve deficits, sciatica, confusion and/or
psychological disturbances, meningitis and seizures are severe
clinical presentations of the disease (6). Spontaneous miscarriage
and intrauterine fetal death during the first trimesters have
also been reported among pregnant women (5,7). The most
common causes of human infection were linked to consumption
of unpasteurized dairy products and labor conditions (e.g.,
veterinarians, slaughterhouse workers, and animal breeders) (4,
8).
Toxoplasma gondii is an important food and waterborne
opportunistic pathogen that causes severe disease in
immunocompromised individuals including pregnant women
which may result in abortion, fetal anomaly, stillbirth, fetal
growth restriction, and preterm birth (4,9,10). Acute phase of the
disease during pregnancy also causes congenital toxoplasmosis
(11). Several risk factors have been associated with human
toxoplasmosis, particularly cat contact and a history of raw
or undercooked meat consumption (4). Somali people do not
usually keep pets, but stray cats sometimes let into the houses and
some households perform their house activities on the ground
with a possibility of high risk of contamination (12). Hygienic
conditions, socio-economic structure, food and environment can
collectively have a notable influence on the diffusion of T. gondii
(13). Moreover, a previous study has reported the presence of T.
gondii (3.12%) in raw milk of camel from Iran (14).
Somalia is a tropical developing country in which climatic and
living conditions favors the dissemination of zoonotic pathogens.
Despite public and economic importance of toxoplasmosis and
brucellosis, few data are available in Somali people (12,13,
15) and their animals (16–20). In addition, there are little
or no concerted medical and veterinary efforts to maximize
toxoplasmosis and brucellosis detection rates. Therefore, the
present study aimed to assess the prevalence of anti-T. gondii
and anti-Brucella spp. antibodies in pregnant women in
Mogadishu, Somalia.
MATERIALS AND METHODS
Ethics Statement
This study was approved by the Ethics Committee on Human
Research at Abrar University, Somalia (Reference Number
AU/ARTC/EC/04/02/2017). The directors of the involved Health
Offices gave their permission to conduct the research in their
respective facility. All pregnant women that accepted being part
of this study provided a written consent to participate.
Study Design
A cross-sectional study design was conducted from August 2017
and November 2018 to determine the prevalence of anti-T.gondii
and anti-Brucella spp. antibodies in pregnant women referred
to the Banadir Maternity and Children Hospital or Maternal
and Child Health (MCH) clinics in Mogadishu city, Somalia.
Facilities were selected based on their specialty in this sector,
while the pregnant women were selected on their willingness to
cooperate for this study. Participants were informed about the
study and a written consent was signed. The age of pregnant
women was stratified into groups of 15–30, 31–40, and >40
years old for statistical analysis. All study participants were
interviewed using a questionnaire which included demographics
and obstetric information comprising age, gestational age and
history of abortion.
Sampling
A total of 307 blood samples including first trimester (gestational
age of <14 weeks; n=44), second trimester (gestational age
between 14 and 28 weeks; n=53) and third trimester (gestational
age >28 weeks; n=210) pregnant women were evaluated. Blood
samples (3 mL) were collected by nurses by venipuncture of
brachial vein using plain sterile vacutainer tubes and labeled.
Samples were kept at room temperature (25◦C) until visible clot
formation, and then centrifuged at 1,500 ×g for 5 min and stored
at −20◦C until laboratory analysis.
Serological Diagnosis of Anti-T. gondii and
Anti-Brucella Spp. Antibodies
For the detection of anti-T. gondii antibodies, serum samples
were screened by a commercial latex agglutination test (LAT)
(SPINREACT, S.A/S.A.U Ctra, Santa Coloma, Spain), according
to the manufacturers’ instructions. The positive reactors were
then diluted; two-fold dilution, 1:2 up to 1:128. Sera showing titer
of ≥1:2 were considered positive for T.gondii.
For anti-Brucella spp. antibodies detection, serum samples
were initially screened by the Rose Bengal Plate Test (RBPT)
(CVRL, Khartoum, Sudan) and retested by a commercial
competitive-ELISA (cELISA) (Svanova Biotech AB, Uppsala,
Sweden), according to the manufacturers’ instructions. The
optical density (OD) was measured using a wavelength of
450 nm, and samples with a percentage of inhibition (% I) ≥30%
were considered positive by cELISA. Samples were considered
seropositive for anti-Brucella spp. antibodies when the serum
tested positive to RBPT and/or cELISA.
Data Analysis
Data were compiled and analyzed by Statistical Package for
Social Sciences (SPSS) version 25 (IBM Corp., Armonk, NY,
USA). Either Chi-square or Fisher’s exact-test was used to assess
association of the age, gestational age and history of abortion with
seropositivity of anti-T.gondii and anti-Brucella spp. antibodies.
Odds ratio (OR), 95% confidence intervals (95% CI) and P-values
were calculated, and results were considered significant when
P<0.05.
RESULTS
The majority of pregnant women were found within the age
group 15–30 years (85.34%) and two-thirds were presented in
the third trimester of gestational age (68.40%). A total of 119/307
(38.76%) pregnant women had a prior history of abortion
(Table 1).
Frontiers in Reproductive Health | www.frontiersin.org 2August 2021 | Volume 3 | Article 672885

Yusuf et al. Toxoplasmosis and Brucellosis in Somalia
TABLE 1 | Prevalence of anti-Toxoplasma gondii and anti-Brucella spp. antibodies in pregnant women from Mogadishu, Somalia.
Variable LAT RBPT cELISA
+/nPrevalence (%) (95% CI) P-value OR (95% CI) +/nPrevalence (%) (95% CI) +/nPrevalence (%) (95% CI)
Age 15–30* 132/262 50.38 (44.37–56.39) 1/262 0.38 (0.00–2.35) 2/262 0.76 (0.03–2.9)
31–40 25/42 59.52 (44.47–72.98) 0.272 (χ2=1.2) 1.4 (0.7–2.8) 1/42 2.38 (0.00–13.44) 1/42 2.38 (0.00–13.44)
>40 2/3 66.67 (20.25–94.37) 0.575 (χ2=0.3) 2 (0.2–22) 0/3 0.00 0/3 0.00
Gestational age 1st trimester 24/44 54.55 (40.06–68.3) 0.507 (χ2=0.4) 1.2 (0.6–2.4) 0/44 0.00 0/44 0.00
2nd trimester 32/53 60.38 (46.92–72.43) 0.140 (χ2=2.2) 1.6 (0.9–2.9) 0/53 0.00 0/53 0.00
3rd trimester* 103/210 49.05 (42.36–55.76) 2/210 0.95 (0.03–3.59) 3/210 1.43 (0.29–4.25)
History of abortion Yes 64/119 53.78 (44.85–62.48) 0.579 (χ2=0.3) 1.1 (0.7–1.8) 2/119 1.68 (0.08–6.2) 3/119 2.52 (0.52–7.29)
No* 95/188 50.53 (43.45–57.6) 0/188 0.00 0/188 0.00
*Reference, +, number of positive samples; n, number of samples; 95% CI, 95% confidence interval; OR, odds ratio.
A total of 161/307 (52.44%; 95% CI: 46.85–57.99%) pregnant
women were seroreactive for at least one pathogen. Anti-T. gondii
antibodies were detected in 159/307 (51.79%; 95% CI: 46.2–
57.35%) pregnant women by LAT. The antibody titers to T.
gondii positive sera were 5 (3.14%), 55 (34.59%), 50 (31.45%),
26 (16.35%), 16 (10.06%), 7 (4.40%), and 0 (0%) by dilution of
1:2, 1:4, 1:8, 1:16, 1:32, 1:64, and 1:128, respectively. Most of
pregnant women (34.59%) had antibody titer of 1:4 while higher
antibody titers, 1:64, were detected in seven pregnant women
serum sample.
Anti-Brucella spp. antibodies were detected in two out of
307 (0.65%; 95% CI: 0.18–2.34%) and three out of 307 (0.98%;
95% CI: 0.33–2.83%) pregnant women by RBPT and cELISA,
respectively. Only one out of 307 (0.33%; 95% CI: 0.06–1.82%)
pregnant woman was seroreactive for Brucella spp. by both
methods. All pregnant women seroreactive for Brucella spp. were
in the third trimester of gestational age and had a history of
abortion (Table 1).
Two out of 307 (0.65%; 95% CI: 0.18–2.34%) pregnant women
were seropositive for both T. gondii and Brucella spp. The
seroprevalence of Brucella spp. and T. gondii for each variable
evaluated is summarized in Table 1.
DISCUSSION
Toxoplasmosis and brucellosis are zoonotic diseases that may
lead to negative health consequences worldwide (1–4). Hence,
determining the prevalence of these pathogens among pregnant
women is paramount for prophylactic measures toward the
susceptible women and reducing the adverse health events
toward the seropositive women (21). Since the Somali civil war
of the 1990s, no studies have been conducted on the prevalence
and importance of toxoplasmosis and brucellosis in human
beings from Somalia, a livestock dependent country in East
Africa with a population of around 12.3 million (22). Previous
studies conducted in the 1980s in the country have showed
toxoplasmosis prevalence ranging from 10 to 61.2% in the general
human population (12,13,23) and 0% in pregnant women
(12), while prevalence of brucellosis ranged between 0 and 0.6%
(15,24).
Herein, the overall seroprevalence of brucellosis in pregnant
women was low (1.30%), in agreement with the prevalence
of brucellosis in animals (1.7%) from Somalia (16). This may
be due to the traditional prevention of diseases in livestock
farms through culling of animals with proven reproductive
problems. A strong association between human and animal
seropositivity of brucellosis has been reported in a linked study
in Kenya (25). However, the public health associated risk factors
of zoonotic pathogens like prevailing tradition of unheated milk
consumption and handling of aborted materials and reproductive
excretions with bare hands are commonly practiced in Somalia
(16), and this should be considered as a potential risk factor
for brucellosis and other abortifacients zoonotic pathogens.
Moreover, in the present study, all pregnant women seroreactive
for Brucella spp. were in the third trimester of gestational
age and had a prior history of abortion. However, pregnancy
Frontiers in Reproductive Health | www.frontiersin.org 3August 2021 | Volume 3 | Article 672885

Yusuf et al. Toxoplasmosis and Brucellosis in Somalia
complications associated with brucellosis in the country needs
further investigation.
The current finding on the prevalence of toxoplasmosis
(51.79%) is slightly higher than the previous reports of 43.6%
(13) and 40% (12) in Mogadishu, Somalia. However, the
present study is similar with previous reports from Kisumu,
Kenya (52%) (26), but lower than the findings from Arba
Minch, Ethiopia (79.3%) (27). The high seroprevalence of
toxoplasmosis found herein may be related to risk factors
described previously for the same location (12). Moreover, the
differences in the prevalence of toxoplasmosis between studies
may also be due to the antigen used (recombinant protein vs.
crude antigens).
In the present study, the seroreactivity rates to toxoplasmosis
were higher with the age, in agreement with previous studies
(4,27). This may be explained by the longer period of exposure
to risk factors (28). Moreover, association between seroreactivity
to T. gondii and history of abortion was not found (p=0.579).
Although the cause of abortion is multi-factorial, previous studies
have associated spontaneous abortion in pregnant women and
seroreactivity to T. gondii (2,29).
Previous studies have reported the majority of human beings
infected by T. gondii after birth are asymptomatic, however, some
may develop a mild disease or in rare cases, a more severe
systemic illness (2). Nonetheless, transplacental transmission of
T. gondii occurs if women acquire primary infection during
pregnancy (30). However, the risk of vertical transmission to
the fetus increases from the first trimester (10–24%) to the
third trimester (60–90%), but the potential of congenital defect
on fetus is more serious with earlier infections (27,31). In
the present study, we found higher rates of seroreactivity to
T. gondii in the first and second trimesters of gestational age,
indicating more serious effects on the fetus if fetal transmission
is developed. Unfortunately, no follow-up was conducted to
trace congenital transmission of toxoplasmosis and health
consequences of seroreactive pregnant women. Screening for T.
gondii infection during pregnancy is not regularly performed at
all maternity hospitals and clinics in Somalia, and most facilities
neglect this screening (data not shown). Prompt diagnosis
and treatment is essential for the prevention of a possible
vertical transmission of T. gondii and may minimize the fetal
sequelae (21).
There were some limitations in the present study; the
serological tests used were for the detection of anti-IgG
antibodies to T. gondii and Brucella spp. Thus, pregnant
women seroreactive for T. gondii and Brucella spp. may
have been previously exposed to the agents. Further studies
should use diagnostic methods to detect acute infection (IgM
serology and/or qPCR) on pregnant women, in order to guide
physicians for administering or not the properly therapy.
Moreover, Mogadishu city harbors fewer animal populations
when compared to other regions of Somalia, and thus, our
findings may not represent pregnant women from other regions.
However, our findings may still be useful as baseline information
for antenatal care in regions where animal rearing is common,
and also help to increase awareness of zoonotic diseases affecting
maternal and neonatal health.
CONCLUSION
A high seropositivity to T. gondii and low seropositivity to
Brucella spp. have been found in pregnant women from
Mogadishu, Somalia. Considering the high number of abortions
in the country associated to the fact that awareness on other
zoonotic abortifacient pathogens in Somalis is very low, further
studies should be conducted to evaluate the potential causes
of abortions.
DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
ETHICS STATEMENT
The studies involving human participants were reviewed
and approved by the Ethics Committee on Human
Research at Abrar University, Somalia (Reference Number
AU/ARTC/EC/04/02/2017). The patients/participants provided
their written informed consent to participate in this study.
AUTHOR CONTRIBUTIONS
AAY, AH-K, AI, and MH-K designed the study. AAY, AH-K,
MH-K, and AMY collected the data. AAY, AH-K, and MH-K
curated the data. AAY, AH-K, AI, MH-K, AMY, MK, JG, and RV
carried out the methodology. AAY, AH-K, and RV performed the
data analysis. AAY, AH-K, JG, and RV drafted the manuscript.
All authors edited and approved the final manuscript.
FUNDING
This study was financially supported by Abrar University,
Somalia, with Grant Number AURG04022017. The funder had
no role in the study design, collection, analysis and interpretation
of data, preparation of the manuscript or decision to publish.
ACKNOWLEDGMENTS
The authors would like to thank staff members of Banadir
Maternity and Children Hospital and Maternal and Child Health
(MCH) clinics in Mogadishu, Somalia for their kind assistance
in the collection of blood samples and questionnaires. We also
thank pregnant women who participated in this study. This study
is part of a master’s degree for AAY at the Universidade Federal
do Parana. AAY was sponsored by a fellowship from the Brazilian
National Council of Scientific and Technological Development
(CNPq). AH-K acknowledges The World Academy of Sciences
(TWAS), UNESCO and Islamic Development Bank (IsDB) for
their support through IsDB-TWAS post-doctoral fellowship
program in Sustainability Sciences (Grant No. 15/2020) at the
Universidade Federal do Paraná, Brazil. CNPq also provided a
Research Productivity (PQ) fellowship of to JG and RV (CNPq
- 313161/2020-8).
Frontiers in Reproductive Health | www.frontiersin.org 4August 2021 | Volume 3 | Article 672885

Yusuf et al. Toxoplasmosis and Brucellosis in Somalia
REFERENCES
1. Corbel MJ, Food and Agriculture Organization of the United Nations, World
Health Organization & World Organisation for Animal Health?. Brucellosis in
Humans and Animals. Geneva: World Health Organization (2006).
2. Dubey J, Jones J. Toxoplasma gondii infection in humans and
animals in the United States. Int J Parasitol. (2008) 38:1257–78.
doi: 10.1016/j.ijpara.2008.03.007
3. Tenter, Astrid M. Toxoplasma gondii in animals used for human
consumption. Memórias do Instituto Oswaldo Cruz. (2009) 104:364–9.
doi: 10.1590/S0074-02762009000200033
4. Kledmanee K, Liabsuetrakul T, Sretrirutchai S. Seropositivities against
brucellosis, coxiellosis, and toxoplasmosis and associated factors in pregnant
women with adverse pregnancy outcomes: a cross-sectional study. PLoS ONE.
(2019) 14:e0216652. doi: 10.1371/journal.pone.0216652
5. Awah-Ndukum J, Mouiche MMM, Kouonmo-Ngnoyum L, Bayang HN,
Manchang TK, Poueme RSN, et al. Seroprevalence and risk factors of
brucellosis among slaughtered indigenous cattle, abattoir personnel and
pregnant women in Ngaoundéré, Cameroon. BMC Infect Dis. (2018) 18:611.
doi: 10.1186/s12879-018-3522-x
6. Dean AS, Crump L, Greter H, Hattendorf J, Schelling E, Zinsstag J. Clinical
manifestations of human brucellosis: a systematic review and meta-analysis.
PLoS Negl Trop Dis. (2012) 6:e1929. doi: 10.1371/journal.pntd.0001929
7. Ali S, Akhter S, Neubauer H, Scherag A, Kesselmeier M, Melzer F, et al.
Brucellosis in pregnant women from Pakistan: an observational study. BMC
Infect Dis. (2016) 16:468. doi: 10.1186/s12879-016-1799-1
8. Mufinda FC, Boinas F, Nunes C. Prevalence and factors associated with
human brucellosis in livestock professionals. Rev Saude Publica. (2017) 51–7.
doi: 10.1590/s1518-8787.2017051006051
9. Robert-Gangneux F, Dardé M-L. Epidemiology of and diagnostic
strategies for toxoplasmosis. Clin Microbiol Rev. (2012) 25:264–96.
doi: 10.1128/CMR.05013-11
10. Deng H, Devleesschauwer B, Liu M, Li J, Wu Y, van der Giessen JWB, et al.
Seroprevalence of Toxoplasma gondii in pregnant women and livestock in the
mainland of China: a systematic review and hierarchical meta-analysis. Sci
Rep. (2018) 8:6218. doi: 10.1038/s41598-018-24361-8
11. Yamada H, Nishikawa A, Yamamoto T, Mizue Y, Yamada T, Morizane M, et
al. Prospective study of congenital toxoplasmosis screening with use of IgG
avidity and multiplex nested PCR methods. J Clin Microbiol. (2011) 49:2552–6.
doi: 10.1128/JCM.02092-10
12. Hinda JA, Hassan HM, Marian WY, Said FA, Gunnel H. Human
toxoplasmosis in Somalia, prevalence of Toxoplasma antibodies in a village
in the Lower Scebelli region and in Mogadishu. Trans R Soc Trop Med Hyg.
(1988) 82:330–2. doi: 10.1016/0035-9203(88)90465-8
13. Zardi O, Adorisio E, Harare O, Nuti M. Serological survey of
toxoplasmosis in Somalia. Trans R Soc Trop Med Hyg. (1980) 74:577–81.
doi: 10.1016/0035-9203(80)90143-1
14. Dehkordi FS, Borujeni MRH, Rahimi E, Abdizadeh R. Detection of
Toxoplasma gondii in raw caprine, ovine, buffalo, bovine, and camel milk
using cell cultivation, cat bioassay, capture ELISA, and PCR methods in Iran.
Foodb Pathog Dis. (2013) 10:120–5. doi: 10.1089/fpd.2012.1311
15. Hussein AS, Singh SS, Haji H. A survey of bovine brucellosis in the Southern
parts of Somalia a comparative study of prevalence of the disease in farm
animals and animals from nomadic herds. Bull Anim Health Prod Africa.
(1978) 26:150–3.
16. Kadle AAH, Shadia AM, Ibrahim AM, Alawad MF. Sero-epidemiological
study on camel brucellosis in Somalia. Eur Acad Res. (2017) 5:2925–42.
17. Andreani E, Prosperi S, Salim AH, Arush AM. Serological and bacteriological
investigation on brucellosis in domestic ruminants of the Somali democratic
republic. Revue d’Elevage et de Med Vet des pays Tropicaux. (1982) 35:329–33.
18. Amina H. Hussein. Prevalence of Brucella antibodies in Somali camels
(Camelus dromadarius). Sci Bull Facul Anim Husb Vet Med Somali Natl Univ.
(1987) 7:13–6.
19. Baumann MP, Zessin KH. Productivity and health of camels (Camelus
dromedarius) in Somalia: associations with trypanosomosis and brucellosis.
Trop Anim Health Prod. (1992) 24:145–6. doi: 10.1007/BF02359606
20. Ghanem YM, El-khodery SA, Saad AA, Abdelkader AH, Heybe A, Musse YA.
Seroprevalence of camel brucellosis (Camelus dromedarius) in Somaliland.
Trop Anim Health Prod. (2009) 41:1779–86. doi: 10.1007/s11250-009-9377-9
21. Gontijo da Silva M, Clare Vinaud M, de Castro AM. Prevalence
of toxoplasmosis in pregnant women and vertical transmission of
Toxoplasma gondii in patients from basic units of health from Gurupi,
Tocantins, Brazil, from 2012 to 2014. PLoS ONE. (2015) 10:e0141700.
doi: 10.1371/journal.pone.0141700
22. UNFPA. Population Estimation Survey 2014 for the 18 pre-war Regions of
Somalia. United Nations Population Fund, Somalia Country Office (2014).
23. Kagan IG, Cahill KM. Parasitic serologic studies in Somaliland. Am J Trop
Med Hyg. (1968) 17:392–6. doi: 10.4269/ajtmh.1968.17.392
24. Wiegand D, Marx W. Serological investigations into antibodies against
brucella, coxiella and chlamydia in serum of domestic animals in the lower
Juba Region. In: Proceedings of the 2nd International Congress of Somalia
Studies (“Studies in Humanities and Natural Sciences”),University of Hamburg,
1-6 August 1983. p. 231–48.
25. Osoro EM, Munyua P, Omulo S, Ogola E, Ade F, Mbatha P, et al.
Strong Association Between human and animal Brucella seropositivity in a
linked study in Kenya, 2012-2013. Am J Trop Med Hyg. (2015) 93:224–31.
doi: 10.4269/ajtmh.15-0113
26. Nisbet AI, Omuse G, Revathi G, Adam RD. Seroprevalence data at a
private teaching hospital in Kenya: an examination of Toxoplasma gondii,
cytomegalovirus, rubella, hepatitis A, and Entamoeba histolytica.PLoS ONE.
(2018) 13:e0204867. doi: 10.1371/journal.pone.0204867
27. Yohanes T, Zerdo Z, Chufamo N, Ashenafi Abossie A. Seroprevalence
and associated factors of Toxoplasma gondii infection among pregnant
women attending in antenatal Clinic of Arba Minch Hospital,
South Ethiopia: cross sectional study. Transl Biomed. (2017) 8:105.
doi: 10.21767/2172-0479.1000105
28. da Silva MG, Câmara JT, Vinaud MC, de Castro AM. Epidemiological factors
associated with seropositivity for toxoplasmosis in pregnant women from
Gurupi, State of Tocantins, Brazil. Revista da Soc Brasileira de Med Trop.
(2014) 47:469–75. doi: 10.1590/0037-8682-0127-2014
29. Nayeri T, Sarvi S, Moosazadeh M, Amouei A, Hosseininejad Z, Daryani A.
The global seroprevalence of anti-Toxoplasma gondii antibodies in women
who had spontaneous abortion: A systematic review and meta-analysis. PLoS
Negl Trop Dis. (2020) 14:e0008103. doi: 10.1371/journal.pntd.0008103
30. Kieffer F, Wallon M. Congenital toxoplasmosis. Handb Clin Neurol. (2013)
112:1099–101. doi: 10.1016/B978-0-444-52910-7.00028-3
31. Uttah E, Ogban E, Okonofua C. Toxoplasmosis: a global infection, so
widespread, so neglected. Int J Sci Res. (2013) 3:1–6.
Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
Publisher’s Note: All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated organizations, or those of
the publisher, the editors and the reviewers. Any product that may be evaluated in
this article, or claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Copyright © 2021 Yusuf, Hassan-Kadle, Ibrahim, Hassan-Kadle, Yasin, Khojaly,
Garcia and Vieira. This is an open-access article distributed under the terms
of the Creative Commons Attribution License (CC BY). The use, distribution or
reproduction in other forums is permitted, provided the original author(s) and the
copyright owner(s) are credited and that the original publication in this journal
is cited, in accordance with accepted academic practice. No use, distribution or
reproduction is permitted which does not comply with these terms.
Frontiers in Reproductive Health | www.frontiersin.org 5August 2021 | Volume 3 | Article 672885