ArticlePDF Available

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

Authors:
  • Abrar University
  • Abrar University
  • Abrar University

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.
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 (13). 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 (1620). 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 (25C) until visible clot
formation, and then centrifuged at 1,500 ×g for 5 min and stored
at 20C 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 (14). 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
Article
Full-text available
Background and Objective: Toxoplasmosis is caused by Toxoplasma gondii and can result in foetal and neonatal death or various congenital defects in pregnancy. This study aimed to determine the prevalence and risk factors associated with Toxoplasma gondii infections in pregnant women attending antenatal clinics at the University of Uyo Health Center, Uyo, Nigeria. Materials and Methods: This was a cross-sectional study using 150 pregnant women after obtaining their informed consent. Detection of anti-T. gondii antibodies were conducted using Toxo IgG/IgM Rapid test kits. A structured questionnaire was administered to the participants to collect information on socio-demographic and risk factors associated with the infection. Results: The seroprevalence of T. gondii infection among the pregnant women was 77 (51.3%), which comprised 41.3% positivity for anti-T. gondii IgG (62/150), 6.7% for IgM (10/150) and 3.3% (5/150) for IgG plus IgM. A significant association was observed between seroprevalence and women residing area with an odd ratio of 0.186-1.36. Individuals having a cat as a pet was 55 (36.7%), while individuals with a cat in their neighbourhood were 62 (41.3%) with an odd ratio of 2.63. Pregnant women in their first trimester had the highest anti-T. gondii IgG of 30 (48:4%) and IgM was the lowest (6:60%). Conclusion: The seroprevalence of Toxoplasma gondii was relatively high in this study. Thus, health education and sensitisation on the disease and its transmission to women of childbearing age among pregnant women should be encouraged during antenatal follow-up, to reduce the risk of T. gondii infection during pregnancy.
Article
Full-text available
Background Toxoplasma gondii (T. gondii) is an intracellular pathogen that can lead to abortion in pregnant women infected with this parasite. Therefore, the present study aimed to estimate the global seroprevalence of anti-T. gondii antibodies in women who had spontaneous abortion based on the results of published articles and evaluate the relationship between seroprevalence of anti-T. gondii antibodies and abortion via a systematical review and meta-analysis. Methods Different databases were searched in order to gain access to all studies on the seroprevalence of anti- T. gondii antibodies in women who had spontaneous abortion and association between seroprevalence of anti-T. gondii antibodies and abortion published up to April 25th, 2019. Odds ratio (OR) and the pooled rate seroprevalence of T. gondii with a 95% confidence interval (CI) were calculated using the random effects model. Results In total, 8 cross-sectional studies conducted on 1275 women who had abortion in present pregnancy, 40 cross-sectional studies performed on 9122 women who had a history of abortion, and 60 articles (involving 35 cross-sectional studies including 4436 women who had spontaneous abortion as case and 10398 as control and 25 case-control studies entailing 4656 cases and 3178 controls) were included for the final analyses. The random-effects estimates of the prevalence of anti-T. gondii IgG antibody in women who had abortion in present pregnancy and women who had a history of abortion were 33% (95% CI: 17%-49%) and 43% (95% CI: 27%-60%), respectively. In addition, the pooled OR for anti-T. gondii IgG antibody in cross-sectional and case-control studies among women who had spontaneous abortion were 1.65 (95% CI: 1.31–2.09) and 2.26 (95% CI: 1.56–3.28), respectively. Also, statistical analysis showed that the pooled OR of the risk of anti-T. gondii IgM antibody 1.39 (95% CI: 0.61–3.15) in cross-sectional and 4.33 (95% CI: 2.42–7.76) in case-control studies. Conclusion Based on the results of the current study, T. gondii infection could be considered a potential risk factor for abortion. It is recommended to carry out further and more comprehensive investigations to determine the effect of T. gondii infection on abortion to prevent and control toxoplasmosis among pregnant women around the world.
Article
Full-text available
Background Brucellosis, coxiellosis, and toxoplasmosis can be transmitted from infected ruminants to pregnant women and may induce adverse pregnancy outcomes; however, there are to date few studies. This study aimed to examine the seropositivities of immunoglobulin G (IgG) against those three pathogens among pregnant women with adverse pregnancy outcomes, and to explore the associated factors. Methods A cross-sectional study was conducted in southern Thailand, where goat production is common. A total of 105 pregnant Thai women who had adverse pregnancy outcomes and serum samples collected at first antenatal care visit before their 28th gestational week from June 2015 to June 2016 were included. The seropositivities of IgG anti-Brucella abortus, Toxoplasma gondii, and Coxiella burnetii antibodies were tested by using commercial enzyme-linked immunosorbent assay (ELISA) kits. Associated factors with seropositivity were analyzed using multiple logistic regression. Results Most women were Muslim aged 20–34 years and 32.4% had a prior history of one or more adverse pregnancy outcomes. One-third of the women had been exposed to goats or raw goat products. Of the 105 serum samples, the seropositivity of anti-T. gondii IgG was highest (33/105, 31.4%), followed by anti-C. burnetii IgG (2/105, 1.9%), and anti-B. abortus IgG (1/105, 1.0%), respectively. None of the pregnant women were found to be co-seropositive for those three pathogens. Conclusions One-third of women with adverse pregnancy outcomes showed positive antibodies for toxoplasmosis, coxiellosis and brucellosis. A dose-response relationship between seropositivity of anti-T. gondii IgG and age was noticed.
Article
Full-text available
Background Brucellosis is a neglected debilitating zoonosis with a high prevalence in many developing countries. Bovine brucellosis is widespread in Cameroon but the epidemiological situation of human brucellosis is not known. A cross sectional study was carried to determine the seroprevalence and factors associated with bovine and human Brucellosis among abattoir personnel and pregnant women in Ngaoundéré, Cameroon. Methods Serum sample from 590 abattoir cattle and 816 plausible occupational risk and vulnerable humans to brucellosis (107 abattoir personnel and 709 pregnant women) were collected and screened for anti-brucella antibodies using Rose Bengal Plate Test (RBPT) and ELISA tests. Structured questionnaires were used to collect data on socio-demographics and risk-factors. The differences in proportions between seropositive and seronegative reactors were tested using odds-ratio and χ²tests. Results Bovine brucellosis seroprevalence was at 3.40% (n = 590; 3.4% for RBPT, 5.93% for i-ELISA). Human Brucella seroprevalence was at 5.6% among abattoir personnel (n = 107; 5.6% for RBPT, 12.15% for Brucella IgG ELISA) and 0.28% in pregnant women (n = 709; both tests). Breed (P < 0.00001) was associated with increased risk of brucellosis in cattle and the seroprevalence was highest among the Djafoun (OR = 16.67, 95%CI: 4.49–28.85) and Akou (OR = 16.96, 95% CI: 0.10–23.91) cattle compared to the other breeds. There was a moderate positive correlation (R² = 0.5025) of Brucella IgG concentrations (> 200 U/ml) and clinical data for Brucella IgG ELISA seropositive humans. Several potential factors were associated (P > 0.05) with increased risk of human brucellosis seroprevalence among the abattoir personnel. The abattoir personnel were essentially males; the seropositive respondents were male and did not use protective equipment at work. Handling of foetus and uterine contents (OR = 13.00, 95%CI: 1.51–111.88) was associated with increased risk of human brucellosis. Conclusions Antibrucella antibodies are prevalent in cattle (3.40%), among abattoir personnel (5.60%) and in pregnant women (0.28%) in Ngaoundéré, Cameroon. The study reports the first evidence of human brucellosis in Cameroon and therefore, an indication of a real public health problem. Public awareness campaigns and health education especially among livestock professional and in agropastoral communities should be highlighted to disseminate knowledge, associated risk factors and control measures of brucellosis.
Article
Full-text available
Background Relevant seroprevalence data for endemic pathogens in a given region provide insight not only into a population’s susceptibility to acute infection or risk for reactivation disease but also into the potential need for policy initiatives aimed at reducing these risks. Data from sub-Saharan Africa are sparse and since Aga Khan University Hospital Nairobi is an internationally accredited hospital equipped with a laboratory electronic medical record system, analysis of pertinent local seroprevalence data has been made possible. Methods We have analyzed serology data from laboratory electronic records at a 300 bed tertiary private teaching hospital in Kenya for the dates, 2008 to 2017 for Toxoplasma gondii, cytomegalovirus, and rubella, which were used primarily for antenatal screening. We also analyzed the data from hepatitis A and amebiasis serologies, which were used primarily for diagnostic purposes. Results For T. gondii, cytomegalovirus, and rubella, we used IgG serology to determine seroprevalence, finding rates of 32%, 86%, and 89%, respectively. There was no significant age-related difference in the 20 to 49 year old age range for any of these three pathogens. Of the Hepatitis A IgM tests that were ordered, 33% were positive with a peak positive rate of 70% in the five to nine year old age range. The seroprevalence of amebiasis was 4% and all cases of seropositivity were accompanied by compatible clinical illness (hepatic abscess). Conclusions These data provide insight into seroprevalence rates of selected pathogens that can be used to guide screening and diagnostic laboratory testing as well as private and public immunization practices.
Article
Full-text available
Primary Toxoplasma gondii infection in pregnant women may result in abortion, stillbirth, or lifelong disabilities of the unborn child. One of the main transmission routes to humans is consumption of raw or undercooked meat containing T. gondii tissue cysts. We aim to determine and compare the regional distribution of T. gondii seroprevalence in pregnant women and meat-producing livestock in China through a systematic literature review. A total of 272 eligible publications were identified from Medline, Scopus, Embase and China National Knowledge Infrastructure. Apparent and true seroprevalence were analysed by region using a novel Bayesian hierarchical model that allowed incorporating sensitivity and specificity of the applied serological assays. The true seroprevalence of T. gondii in pregnant women was 5.0% or less in seven regions of China. The median of the regional true seroprevalences in pigs (24%) was significantly higher than in cattle (9.5%), but it was not significantly higher than in chickens (20%) and small ruminants (20%). This study represents the first use of a Bayesian hierarchical model to obtain regional true seroprevalence. These results, in combination with meat consumption data, can be used to better understand the contribution of meat-producing animals to human T. gondii infection in China.
Article
Full-text available
Brucellosis is one of the most important zoonotic diseases worldwide. The disease was not fully assessed in Somalia particularly after the civil war of 1990s. The present study was conducted from December, 2015 to March, 2016 in order to determine the seroprevalence and possible risk factors associated with camel brucellosis in Mogadishu city of Somalia. Questionnaire survey was also used to evaluate the knowledge-attitude-practice (KAP) among camel owners. A total of 180 camel sera were randomly sampled and tested using Rose Bengal Plate Test (RBPT), Modified RBPT (mRBPT), Serum Agglutination Test (SAT) and Competitive Enzyme Linked Immunosorbent Assay (cELISA). The investigated camels were apparently healthy above two years of age with no history of vaccination against brucellosis. The overall seroprevalence of camel brucellosis was 4.4% at individual level and 31.3% at herd level. The Kappa statistics indicated that there was perfect agreement between mRBPT, SAT and cELISA (k=0.841) while the RBPT has a Kappa value of (0.589) which was found to be a moderate level of agreement when compared to the cELISA. Questionnaire survey among the camel owners determined that camels with proved reproductive problems were culled by 77% of the respondents which is a good practice that might have contributed to the low prevalence of brucellosis in the present study. Conversely, 100% of the respondents confirmed of consuming raw milk of camel as well as bare hand contact of abortion materials with abortion cases reported by 63% of them. Furthermore, 77% of the respondents did not know brucellosis and its zoonotic risk. Thus, these factors can play a vital role of transmission of this disease among Somali people. It was concluded that Brucella infection exists in camels in Mogadishu, Somalia, and mRBPT is as sensitive as SAT and cELISA techniques. Moreover RBPT is very sensitive test validated and its antigen standardized for bovine brucellosis. Therefore, the study recommends a wider epidemiological surveillance and further validation of diagnostic serological tests in camels and other ruminants as well as human with isolation and identification of the infective Brucella organism strains and further biovars which enables best options for selection of brucellosis control strategy suitable to Somalia context. Hence, improvement of the public awareness on zoonotic potential of the disease is also recommended.
Article
Full-text available
OBJECTIVE The objective of this study is to estimate the seroprevalence of human brucellosis in livestock professionals and analyze the factors associated with brucellosis focusing on sociodemographic variables and the variables of knowledge and practices related to the characteristics of the activities carried out in livestock. METHODS This is a cross-sectional seroepidemiological study with a population of 131 workers of butchers, slaughter rooms, and slaughterhouse and 192 breeders sampled randomly in Namibe province, Angola. The data were obtained from the collection of blood and use of questionnaires. The laboratory tests used were rose bengal and slow agglutination. The questionnaire allowed us to collect sociodemographic information and, specifically on brucellosis, it incorporated questions about knowledge, attitudes, and behaviors of livestock professionals. In addition to the descriptive statistical approach, we used the Chi-square test of independence, Fisher’s test, and logistic regression models, using a significance level of 10%. RESULTS The general weighted prevalence of brucellosis was 15.6% (95%CI 13.61–17.50), being it 5.3% in workers and 16.7% (95%CI 11.39–21.93) in breeders. The statistical significance was observed between human seroprevalence and category (worker and breeder) (p < 0.001) and education level (p = 0.032), start of activity (p = 0079), and service location (p = 0.055). In a multivariate context, the positive factor associated with brucellosis in professionals was the professional category (OR = 3.54; 95%CI 1.57–8.30, related to breeders in relation to workers). CONCLUSIONS Human brucellosis in livestock professionals is prevalent in Namibe province (15.6%), where the professional category was the most important factor. The seroprevalence levels detected are high when compared with those found in similar studies.
Article
Full-text available
Background: Toxoplasma gondii (T. gondii) is a ubiquitous, coccidian intracellular protozoan parasite that causes toxoplasmosis. T. gondii infection acquired during pregnancy may result in severe damage or death of the fetus and long-term sequelae in offspring. So far, no documented data concerning the seroprevalence of T. gondii infection among pregnant women is available in the study area. Therefore, this study was aimed at determining of T. gondii sero-prevalence and associated factors among pregnant women attending in ante natal clinic (ANC) of Arba Minch hospital, southern Ethiopia. Methods: A facility based cross sectional study design was employed. A total of 232 pregnant women visiting Arba Minch hospital ANC from February to April, 2015 were enrolled by using systematic sampling technique. Data regarding Socio-demographic and associated factors were gathered using pretest questionnaire. Approximately 2 milliliters of blood specimen was collected and serum samples were tested for anti-T. gondii IgG and IgM antibody using Enzyme Linked Immunosorbent Assay. Data were analyzed using SPSS version 20. Results: Out of the total 232 pregnant women tested, 184 were found to be seropositive, giving overall seroprevalence rate of T. gondii infection 79.3% (95%CI; 73.7-84.5). On multivariate analysis showed that consumption of raw meat (AOR=3.211; 95% CI: 1.592-6.477) and habit of eating raw vegetables or fruit (AOR=2.669; 95% CI: 1.264-5.639) were significantly associated with T. gondi infection. Conclusion: The overall seroprevalence of T. gondii infection among pregnant women was high and serological evidence of primary infection was observed. Therefore, screening of Toxoplasma infection should be considered during ANC follow up. Moreover, health information about ways to minimize exposure to the riskfactors should be provided with main focus on not eats raw meat and raw vegetables. Keywords: Seroprevalence; T. gondii; Pregnant women; Ethiopia
Article
Full-text available
Background: Brucella species occasionally cause spontaneous human abortion. Brucella can be transmitted commonly through the ingestion of raw milk or milk products. The objective of this study was to determine the sero-prevalence of and to identify potential risk factors for brucellosis in pregnant women from Rawalpindi, Pakistan. Methods: We conducted a cross-sectional study at the Gynecology Outdoor Patient department of the Benazir Bhutto Hospital, Rawalpindi, Pakistan from March to June 2013. Data related to potential risk factors and clinical history was collected by individual interviews on the blood sampling day. The 429 serum samples collected were initially screened by Rose Bengal Plate Agglutination test for the detection of Brucella antibodies. We applied standard descriptive statistics and logistic regression analyses. Results: Twenty five (5.8 %; 95 % confidence interval (CI): 3.8 % -8.5 %) serum samples were found to be seropositive. Brucellosis-related clinical symptoms were recorded in various seropositive cases. Animal contact, raw milk consumption, having an abortion history and the experience of an intrauterine fetal death were associated with seropositivity for brucellosis in univariate analyses (all p <0.05). In multiple logistic regression models only the contact with animals remained as independent and robust risk factor (odds ratio 5.21; 95 % CI: 1.88-13.75; p = 0.001) for seropositivity. Conclusion: Brucellosis is a serious threat for pregnant women and their unborn children in Pakistan. Pregnant women having brucellosis-related symptoms or previous history of abortions, miscarriages, intrauterine fetal death and other brucellosis-related manifestations should be screened for brucellosis - especially those exposed to animals given the increased risk - and medication should be administered according to state of the art.
Article
Full-text available
ntroduction Toxoplasmosis is a parasitary disease that presents high rates of gestational and congenital infection worldwide being therefore considered a public health problem and a neglected disease. Objective To determine the prevalence of toxoplasmosis amongst pregnant women and vertical transmission of Toxoplasma gondii in their newborns attended in the Basic Units of Health (BUH) from the city of Gurupi, state of Tocantins, Brazil. Methods A prevalence study was performed, including 487 pregnant women and their newborns attended in the BUH of the urban zone of the city of Gurupi, state of Tocantins, Brazil, during the period from February 2012 to February 2014. The selection of the pregnant women occurred by convenience. In the antenatal admission they were invited to participate in this study. Three samples of peripheral blood were collected for the detection of specific antiT. gondii IgG, IgM and IgA through ELISA, for the polimerase chain reaction (PCR) and IgG avidity during pregnancy. When IgM antibodies were detected the fetal and newborn infection investigation took place. The newborn was investigated right after birth and after one year of age through serology and PCR to confirm/exclude the vertical transmission. The analyses were performed in the Studies of the Host-Parasite Relationship Laboratory (LAERPH, IPTSP-UFG), Goiania, state of Goias, Brazil. The results were inserted in a data bank in Epi-Info 3.3.2 statistic software in which the analysis was performed with p�5%.Results The toxoplasmosis infection was detected in 68.37% (333/487, CI95%: 64.62–72.86). The toxoplasmosis chronic infection prevalence was of 63.03% (307/487, CI95%: 58.74–67.32). The prevalence of maternal acute infection was of 5.33% (26/487; CI95%: 3.3–7.3) suspected by IgM antibodies detection in the peripheral blood. The prevalence of confirmed vertical transmission was of 28% (7/25; CI95%: 10.4–45.6). Conclusions These results show an elevated prevalence of toxoplasmosis in pregnant women and vertical transmission of T. gondii in the city of Gurupi, state of Tocantins, Brazil.