Global prevalence and risk factors associated with Toxoplasma gondii infection in wild birds: A systematic review and meta-analysis

Abstract

A systematic review and meta-analysis were performed to identify the global prevalence and factors associated with Toxoplasma gondii infection in wild birds. Six bibliographic databases (Chinese National Knowledge Infrastructure, VIP Chinese Journal Database, Wanfang Data, PubMed, Web of science and ScienceDirect) were searched from inception to February 2023. The search yielded 1220 records of which 659 articles underwent full- text evaluation, which identified 49 eligible articles and 16,030 wild bird samples that were included in the meta-analysis. The estimated pooled global prevalence of T. gondii infection in wild birds was 16.6%. Out of the variables tested, publication year after 2020 and climate type were significantly associated with T. gondii infection (P<0.01). Our data indicate that the prevalence of T. gondii in wild birds can be influenced by epidemiological variables. Further research is needed to identify the biological, environmental, anthropogenic, and geographical risk factors which impact the ecology and prevalence of T. gondii in wild birds.

Full text

Preventive Veterinary Medicine 226 (2024) 106187
Available online 20 March 2024
0167-5877/© 2024 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Global prevalence and risk factors associated with Toxoplasma gondii
infection in wild birds: A systematic review and meta-analysis
Chao Chen
a
,
b
,
1
, Si-Yuan Qin
c
,
1
, Xing Yang
d
,
1
, Xiao-Man Li
e
, Yanan Cai
a
, Cong-Cong Lei
c
,
Quan Zhao
a
,
*
, Hany M. Elsheikha
f
,
*
, Hongwei Cao
b
,
*
a
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin 130118, PR China
b
School of Pharmacy, Yancheng Teachers University, Yancheng, Jiangsu 224002, PR China
c
Center of Prevention and Control Biological Disaster, State Forestry and Grassland Administration, Shenyang, Liaoning 110034, PR China
d
Department of Medical Microbiology and Immunology, School of Basic Medicine, Dali University, Dali, Yunnan 671000, PR China
e
College of Veterinary Medicine, Qingdao Agricultural University, Qingdao, Shandong 266109, PR China
f
Faculty of Medicine and Health Sciences, School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, Loughborough, United
Kingdom
ARTICLE INFO
Keywords:
Meta-analysis
Systematic review
Toxoplasma gondii
Wild birds
Zoonotic diseases
ABSTRACT
A systematic review and meta-analysis were performed to identify the global prevalence and factors associated
with Toxoplasma gondii infection in wild birds. Six bibliographic databases (Chinese National Knowledge
Infrastructure, VIP Chinese Journal Database, Wanfang Data, PubMed, Web of science and ScienceDirect) were
searched from inception to February 2023. The search yielded 1220 records of which 659 articles underwent full-
text evaluation, which identied 49 eligible articles and 16,030 wild bird samples that were included in the
meta-analysis. The estimated pooled global prevalence of T. gondii infection in wild birds was 16.6%. Out of the
variables tested, publication year after 2020 and climate type were signicantly associated with T. gondii
infection (P<0.01). Our data indicate that the prevalence of T. gondii in wild birds can be inuenced by
epidemiological variables. Further research is needed to identify the biological, environmental, anthropogenic,
and geographical risk factors which impact the ecology and prevalence of T. gondii in wild birds.
1. Introduction
Toxoplasmosis is a zoonotic disease caused by the opportunistic
protozoan Toxoplasma gondii, which has a worldwide distribution
(Crozier and Schulte-Hostedde, 2014; Jenkins et al., 2015). Approxi-
mately one-third of the world’s human population are chronically
infected by T. gondii, which can remain dormant in the host for many
years (Zhang et al., 2016). Although T. gondii infection is generally
asymptomatic in immunocompetent individuals, the parasite can have
an adverse impact on the health of the fetus due to congenital trans-
mission during pregnancy and the immunodecient individuals (Cortes
et al., 2019; Dubey, 2010; Elsheikha, 2008; Elsheikha et al., 2020).
Many bird species can be infected by T. gondii, however canaries and
pigeons can experience severe disease (Dubey, 2002).
T. gondii is considered a generalist parasite, with a heteroxenous life
cycle involving a broad range of mammalian and avian intermediate
hosts and a feline denitive host (Aguirre et al., 2019). T. gondii may
have originated from South American cats and spread around the world
through migratory birds (Lehmann et al., 2006). The migratory behavior
of wild birds and ability to travel long distances make them an efcient
source and vector for cross-species dispersal of zoonotic pathogens
(Rahman et al., 2021).
Birds play an important role in the epidemiology and transmission of
T. gondii to other hosts (Dubey and Jones, 2008). Birds acquire infection
by consuming cysts in the muscle and brain of T. gondii-infected animals
through hunting or scavenging. They can also consume food or water
contaminated with oocysts. When infected birds are preyed on by cats
(Abdoli et al., 2018), the parasite undergoes sexual reproduction in the
feline intestine, culminating in formation and excretion of many oocysts
in the cat feces (Dubey et al., 2020). Infected cats shed oocysts for a short
duration and adult cats contribute far less to the environmental
contamination with oocysts compared to young cats (Dubey, 1976).
* Corresponding authors.
E-mail addresses: zhaoquan0825@163.com (Q. Zhao), Hany.Elsheikha@nottingham.ac.uk (H.M. Elsheikha), caohw@yctu.edu.cn (H. Cao).
1
These authors contributed equally to this work.
Contents lists available at ScienceDirect
Preventive Veterinary Medicine
journal homepage: www.elsevier.com/locate/prevetmed
https://doi.org/10.1016/j.prevetmed.2024.106187
Received 13 August 2023; Received in revised form 13 March 2024; Accepted 14 March 2024

Preventive Veterinary Medicine 226 (2024) 106187
2
The use of wild birds as sentinels for multiple zoonotic pathogens
(Hamer et al., 2012) has elicited a growing interest in investigating the
prevalence of T. gondii infection in wild and domestic birds. However,
disparities exist in T. gondii prevalence between countries (Costa et al.,
2022; Dubey et al., 2020; Wang et al., 2021) and the global prevalence in
wild birds remains unknown. To comprehensively examine this topic,
we conducted a systematic literature review and meta-analysis to esti-
mate the global prevalence of T. gondii in wild birds and identify po-
tential factors associated with T. gondii infection in wild birds. The study
results highlight the need for more surveillance of T. gondii infection in
wild birds to improve understanding of the ecology and transmission
pathways of T. gondii genotypes in wild birds and their relationships to
animal and human disease.
2. Materials and methods
2.1. Literature search strategy
The present systematic review and meta-analysis followed the
Preferred Reporting Items for Systematic Reviews and Meta-Analyses
Protocols (PRISMA). To estimate the global prevalence of T. gondii
infection in wild birds, a comprehensive review of the English and
Chinese literature was performed. We searched six online bibliographic
databases for articles related to T. gondii infection in wild birds,
including the China National Knowledge Infrastructure (CNKI), VIP
Chinese Journal Database, Wanfang Data, PubMed, ScienceDirect, and
Web of Science from inception to February 2023. The advanced search
was carried out using “Wild birds (in Chinese)” and “Toxoplasma gondii
(in Chinese)” as keywords in the three Chinese databases. We used a
combination of Medical Subject Headings (MeSH) terms and keywords
(“Toxoplasma gondii”, “Wild birds”) in the search strategy. We used
Boolean operators “AND” to link MeSH terms and “OR” to link the entry
terms. Finally, the search formula was (“Birds”[Mesh]) OR (Bird[Title/
Abstract]) OR (Aves[Title/Abstract]) OR (Wild bird[Title/Abstract]) OR
(Waterfowl[Title/Abstract]) OR (Migratory bird[Title/Abstract])) AND
(“Toxoplasma”[Mesh]) OR (Toxoplasmas[Title/Abstract]) OR (Toxo-
plasma gondii[Title/Abstract]). In ScienceDirect, the keywords "Wild
birds", "Toxoplasma gondii" and "Prevalence OR Seroprevalence" were
used in the search. In Web of Science, the search formula was (AB=
(Birds) OR AB=(Bird) OR AB=(Aves) OR AB=(Wild bird) OR AB=
(Waterfowl) OR AB=(Migratory bird)) AND (AB=(Toxoplasma) OR AB=
(Toxoplasmas) OR AB=(Toxoplasma gondii)). Bibliographies of the
included articles and relevant reviews were scrutinized for more refer-
ences. The search was not restricted by the publication year and
geographic origin of the published articles. However, the literature
search was limited to articles published in Chinese or English language.
2.2. Study selection and quality assessment
This study focused on wild birds and T. gondii for literature search to
identify all qualied articles. The quality of studies was graded using the
Grading of Recommendations, Assessment, Development and Evalua-
tions (GRADE) framework (Guyatt et al., 2008). The eligible articles
were assessed for quality of design and methodology based on ve
criteria: random sampling, number of samples analyzed (≥100), clear
sampling location(s), reporting ≥6 epidemiological variables and clear
description of the detection method. The studies that fullled all 5
criteria received a score of 5. Studies were rated as low (1–2 points),
medium (3 points), or high quality (4–5 points). Articles that did not
meet these criteria were excluded. Review papers, case reports, reprints,
and unpublished reports were also excluded.
Table 1
Normal distribution test for the normal rate and the different conversions of the
normal rate.
Conversion form W P
PRAW 0.89191 P<0.001
PLN 0.95676 0.069
PLOGIT 0.98979 0.944
PAS 0.96173 0.111
PFT 0.95874 0.084
“PRAW”: original rate; “PLN”: logarithmic transformation; “PLOGIT”: logit
transformation; “PAS”: arcsine transformation; “PFT”: double−arcsine
transformation.
Fig. 1. PRISMA ow chart shows the steps used for article screening and selection.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
3
2.3. Data extraction
Two independent reviewers reviewed the abstracts of the selected
references to determine whether the studies met the inclusion criteria, in
which case a full review of the article was conducted. The information
extracted for this study included the detection method, year of publi-
cation of the study, continent, sample type, country, order of the wild
birds, hemisphere, and climate. The meteorological data were obtained
from the National Centers for Environmental Information (https://www
.ncei.noaa.gov/maps/monthly/). The data about the geographic loca-
tion (latitude and longitude) and altitude were obtained by searching for
information about the sampling site or neighboring sites at the respec-
tive location. The climate of the areas in the included studies was
categorized by using the K¨
oppen-Geiger classication (KGC) (Peel et al.,
2007). Because of the many different wild bird species worldwide, we
presented all bird species at the order level to facilitate data analysis. All
wild bird species were classied by https://avibase.bsc-eoc.org/. Data
from each of eligible study were extracted and recorded independently.
2.4. Statistical analyses
The quantitative meta-analysis was performed with the R software
(4.3.2 version) using the meta package 7.0.0 version (https://cran.r-p
roject.org/web/packages/meta/index.html). We used the random-
effects model to determine the pooled prevalence of T. gondii and sub-
group analysis at 95% condence interval (CI). To t the data to
Gaussian distribution, ve transformation methods were implemented
(Table 1). These included logit transformation (PLOGIT), arcsine
transformation (PAS), double-arcsine transformation (PFT), logarithmic
transformation (PLN), and original rate (PRAW). The normality of the
data was checked by Shapiro-Wilk test. The closer the ‘W’was to the
value 1 (maximum value of this statistic) with a P value ≥0.05, the
closer the t to Gaussian normal distribution. The PLOGIT with the
largest p-value was chosen to analyze the data.
Publication bias was assessed by visual inspection of the inverted
funnel plot asymmetry and by using Egger test to assess the small-study
effects. To further examine and adjust for publication bias, we imputed
Table 2
Summary of studies included in the meta-analysis of T. gondii prevalence in wild birds.
Study reference Sampling time Country Method No. positive/ No. tested Quality score
Tsai et al. (2006) 2004–2004 China LAT 31/665 High
Murao et al. (2008) 2003–2005 Russia and Japan ELISA 81/418 High
Dubey et al. (2010) 2008–2010 USA MAT 38/382 High
Gondim et al. (2010) 2007–2008 Brazil MAT 3/293 High
Alvarado-Esquivel et al. (2011) 2009–2010 USA MAT 17/653 High
Cabezon et al. (2011) 1996–2010 Spain MAT 282/1079 Medium
Darwich et al. (2012) N/D Spain PCR 12/201 High
Huang et al. (2012) N/D China PCR 4/178 Medium
Molina-Lopez et al. (2012) 2006–2010 Spain MAT 91/113 High
Tian et al. (2012) 2011–2012 China MAT 35/277 High
Cong et al. (2013) 2011–2011 China MAT 39/313 High
Khademvatan et al. (2013) 2011 Iran PCR 25/146 High
Mancianti et al. (2013) 2011–2012 Italy MAT 9/103 High
Salant et al. (2013) 2010–2011 Israel MAT 92/223 Medium
Sandstrom et al. (2013) 2006–2010 Russia, Netherlands, Denmark MAT 247/2675 High
Hu et al. (2014) 2010–2013 China MAT 36/131 High
Barros et al. (2014) 2010–2011 Brazil MAT 46/206 High
Gennari et al. (2014) 2010–2011 Brazil MAT 73/202 High
Miao et al. (2014) 2012–2013 China MAT 131/659 High
Muz et al., (2015) 2007–2014 Turkey PCR 7/103 High
Chen et al. (2015) 2013–2014 China MAT 92/394 High
Zhang et al. (2015) 2013 China PCR 18/249 High
Andrade et al. (2016) 2011–2013 Brazil MAT 3/222 High
Cabez´
on et al. (2016) 2009–2011 Spain MAT 110/525 High
Gennari et al., (2016a) N/D Brazil MAT 28/100 Medium
Gennari et al. (2016b) 2013 Brazil MAT 24/69 High
Love et al. (2016) 2012–2014 United States MAT 97/281 High
Wu et al. (2017) 2016–2016 China MAT 20/179 High
Tidy et al. (2017) 2014–2015 Portugal MAT 17/77 High
Luo et al. (2017) 2010–2016 China IHT 72/751 High
Mirza et al. (2017) 1990–2014 Netherlands PCR 9/117 High
Amouei et al., (2018) 2014–2015 Iran MAT 26/50 High
Abdoli et al. (2018) N/D Iran PCR 9/55 Medium
Lukasova et al. (2018) 2014–2015 South Africa PCR 3/110 High
Nazir et al. (2018) N/D Pakistan PCR 19/54 Medium
Acosta et al. (2019) 2011–2015 Chile MAT 57/132 High
Huang et al. (2019) 2014–2015 China MAT 120/350 High
Liu et al. (2019) 2017 China PCR 13/239 High
Naveed et al. (2019) 2016–2017 Pakistan LAT 25/200 High
Lohr et al. (2020) 2012–2013 Italy PCR 45/771 High
Iemmi et al. (2020) 2016–2017 Italy MAT 91/147 High
Ammar et al. (2021) 2016–2018 USA MAT 32/155 High
Bata et al. (2021) 2018–2019 Nigeria ELISA 13/92 High
Gazzonis et al. (2021) 2018–2019 Italy PCR 35/56 High
Lopes et al. (2021) N/D Portugal MAT 96/263 Medium
Poulle et al., (2021) 2011–2015 Western Indian Ocean MAT 170/1014 High
Sato et al. (2021) 2014–2015 Brazil IFAT 6/72 Low
Tayyub et al. (2022) 2018–2018 Pakistan PCR 46/120 High
Karadjian et al. (2022) 2017–2018 France MAT 65/166 High
Abbreviation: N/D; data not available; LAT: Latex agglutination test; ELISA: Enzyme linked immunosorbent assay; MAT: Modied agglutination test; PCR: Polymerase
chain reaction; IHT: Indirect hemagglutination test; IFAT: Indirect immunouorescent antibody test.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
4
potentially missing studies using the trim-and-ll method (Duval and
Tweedie, 2000). To evaluate the heterogeneity between studies,
Cochran Q test, I
2
statistics and
χ
2
test were used (Chen and Benedetti,
2017; Higgins and Thompson, 2002). Subgroup analysis was performed
to investigate the differences in the prevalence and potential sources of
heterogeneities due to categorical variables, including detection
method, sample type, continent, hemisphere, economic status, latitude,
altitude, climate type, publication year, and level of study quality.
3. Results
3.1. Study selection and characteristics
The search of the databases yielded 1220 records. After removal of
125 duplicates, 1095 were screened at the title and abstract level, and
659 studies underwent full-text evaluation. Of those, 610 articles were
excluded for various reasons listed in the PRISMA owchart for study
selection. Finally, 49 studies met the inclusion criteria and were
Fig. 2. Forest plot of the global prevalence of T. gondii infection in wild birds. Gray squares and their corresponding lines are the point estimates and 95% CI. The
diamond represents the pooled estimate (width denotes 95% CI). Heterogeneity was considered high (I
2
=97%).
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
5
included in the meta-analysis (Fig. 1). Table 2 summarizes the main
characteristics of the 49 articles included in this meta-analysis. Of the 49
eligible studies, 41 (83.67%), seven (14.28%), and one (2.04%) were
considered of high, medium, and low quality, respectively.
3.2. Publication heterogeneity, bias and sensitivity analysis
The heterogeneity test showed I
2
=97% (
χ
2
=1.41, P <0.01),
suggesting high heterogeneity in T. gondii infection prevalence in wild
birds (Fig. 2). The publication bias was statistically signicant
(P<0.0001) as revealed by the Egger’s regression test (Fig. 3). Visual
inspection of the funnel plot revealed asymmetry, suggesting that the
results may have been inuenced by publication bias or small sample
bias (Fig. 4). The trim and ll analysis identied six studies with nega-
tive results (shown as white circles in Fig. 5), indicating potential pub-
lication bias. Sensitivity analysis revealed that the reorganized data had
no impact on the outcome of the analysis (Fig. 6).
3.3. Global prevalence and study-level covariates of T. gondii prevalence
in wild birds
The univariate analysis was conducted on 49 eligible studies with
16,030 samples, of which 2660 samples were positive for T. gondii. The
highest prevalence was detected in Europe (Fig. 7). The estimated
pooled global prevalence of T. gondii infection in wild birds was 16.6%
(95% CI: 12.40–21.87). Strigiformes (33.5%, 95% CI: 21.46–48.16) had
the highest prevalence followed by Falconiformes, which had a preva-
lence close to 30%. Charadriiformes also had a high prevalence
(Table 3). However, the order of birds did not have any signicant effect
on T. gondii prevalence (P=0.08).
The results of sub-group and meta-regression analysis considered the
following variables: detection method, sample type, continent, hemi-
sphere, economic status, latitude, altitude, climate type, publication
year, and level of study quality (Table 4). T. gondii detection methods
reported in the meta-analysis included enzyme-linked immunosorbent
test (ELISA), indirect hemagglutination test (IHT), indirect immunou-
orescent antibody test (IFAT), latex agglutination test (LAT), modied
agglutination test (MAT), and polymerase chain reaction (PCR).
Regarding the detection method subgroup, the highest prevalence
21.3% (95% CI: 14.95–29.44) correlated with the use of MAT. However,
there were no signicant differences in T. gondii prevalence between the
detection methods (P=0.44). In the sampling type subgroup (P=0.46),
the highest prevalence was associated with blood samples 18.1% (95%
CI: 13.05–24.45).
While no signicant effect was detected in the continent subgroup
(P=0.15), Europe had the highest pooled prevalence 14.2% (95% CI:
13.45–15.05). This was followed by Asia 14.1% (95% CI: 13.21–15.10),
South America 11.8% (95% CI: 9.98–13.68), North America 10.2%
(95% CI: 8.70–11.79), and Africa 6.9% (95% CI: 3.83–10.80). Only one
study was reported in Oceania with a prevalence of 7.7% (95% CI:
3.58–13.19). Analysis of the hemisphere (P=0.30) showed that the
highest prevalence was detected in northern hemisphere (16.8%; 95%
CI: 12.49–22.26) and eastern hemisphere (16.8%; 95% CI:
12.28–22.57). Regarding the economic status (P=0.13), the prevalence
was higher in countries with developing economy (14.7%, 95% CI:
12.22–13.81) than in countries with developed economy.
Analysis of the latitude (P=0.13) and altitude (P=0.53) showed that
the highest prevalence was detected in the latitude category 30◦–60◦
(19.5%; 95% CI: 13.78–26.90) and altitude category 100–1000 m
(16.6%; 95% CI: 9.33–27.89). Of all climate types (P<0.01), tropical
monsoon climate had the highest prevalence of T. gondii infection
(34.8%; 95% CI:24.53–46.67), followed by dry winter subtropical
climate (26.3%;95% CI:13.54–44.96) and dry summer, Mediterranean,
climate (24.2%;95% CI:9.34–49.67).
Fig. 3. Egger’s test for the assessment of publication bias.
Fig. 4. Funnel plot with pseudo 95% CI for examination of the publication bias.
Each dot represents one study.
Fig. 5. Funnel plot shows evidence of publication bias in the meta-analysis of
T. gondii prevalence in wild birds, with missing studies imputed via the trim and
ll method. Shaded circles represent the original study estimates, and the un-
shaded circles represent the missing estimates.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
6
Regarding the year of publication subgroup, the prevalence reported
in articles published after 2020 was 26.9% (95% CI: 16.96–39.81;
P<0.01), the highest prevalence among all articles combined. The
highest T. gondii prevalence in wild birds correlated with medium
quality studies 22.6% (95% CI: 12.03–38.37). However, T. gondii prev-
alence was not inuenced by the quality of studies (P =0.32).
4. Discussion
We conducted the rst comprehensive evaluation of the global
prevalence of T. gondii in wild birds. This systematic review and meta-
analysis estimated a pooled global prevalence of T. gondii in wild birds
of 16.6%, suggesting the widespread distribution of T. gondii in wild
birds. Our results along with others (Dubey, 2002), corroborate the
variation in the susceptibility to T. gondii among different bird species. In
our study, Strigiformes had the highest prevalence followed by Falco-
niformes. Most species in the Strigiformes and Falconiformes are
nocturnal predators that feed primarily on small rodents (Andrle, 2011;
Bertolino et al., 2001), the natural intermediate host of T. gondii (Krijger
et al., 2020), making Strigiformes and Falconiformes more likely to
acquire T. gondii infection.
By comparing methods used for detection of T. gondii infection in
wild birds, MAT was found associated with the highest prevalence,
followed by ELISA. This result is consistent with a previous study
showing MAT as the most appropriate serological test for detection of
T. gondii in birds (Dubey, 2002). MAT is the gold standard assay for
detection of T. gondii (Fernandes et al., 2019) and has good sensitivity
for measurement of anti-T. gondii antibodies (Dubey et al., 2016; Lan-
goni‚ et al., 2007; Macrì et al., 2009). MAT is also simple to use, requires
no special equipment or species-specic reagents, antigens are stable for
Fig. 6. Sensitivity analysis of T. gondii prevalence in wild birds.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
7
months, and reagents are commercially available (Fernandes et al.,
2019). The prevalence detected by ELISA, although was lower than that
obtained by MAT, it was much higher than the prevalence obtained by
the other diagnostic methods. Although ELISA is one of the most reliable
methods for detecting anti-T. gondii specic antibodies, only two of the
articles included in this review used ELISA, presumably because it is
time-consuming, laborious, and relatively expensive (Dard et al., 2016).
The prevalence was higher in blood samples compared with the brain
tissue and muscle samples collected from wild birds. This result may be
attributed to the increased number of studies utilizing serological
analysis because blood analysis can provide valuable information
without the need for constraining or euthanasia of the bird (Angelier
et al., 2011).
Subgroup analysis by continent showed that the highest and lowest
prevalence was detected in Europe and Africa, respectively. The inter-
continental differences may have a plausible explanation. Migrant
birds can contribute to the spread and diversity of parasites by hosting
more parasites than resident birds and by facilitating long-distance
parasite dispersal (Bauer and Hoye, 2014; Jourdain et al., 2007). In
Europe, most of the bird habitats are wetlands and marshes, and with the
predicted changes in climate, wetter areas can become more humid
(Soultan et al., 2022), favoring more spread of T. gondii. Warm and
humid environments are conducive to the survival T. gondii oocysts
(Robert-Gangneux and Dard´
e, 2012). The lowest prevalence detected in
Africa may be attributed to the dry and hot climatic conditions, which do
not support the survival of T. gondii oocysts, and thus may not favor the
transmission of T. gondii. The modest number of studies reported from
Africa is perhaps related to the limited resources which may impede
investment in research.
The prevalence was higher in the eastern hemisphere compared with
the western hemisphere and higher in the northern hemisphere than the
southern hemisphere. Most of the continents are in the northern hemi-
sphere and most of the bird migration occurs in the northern hemi-
sphere. The life cycle of T. gondii is closely affected by climatic
conditions such as temperature and humidity, which are common fea-
tures of the northeastern hemisphere’s climate. These results are
consistent with the results of the continent subgroup analysis which
detected the highest prevalence in Europe and Asia.
Fig. 7. Worldwide map showing the continent-wise prevalence of T. gondii infection in wild birds.
Table 3
Pooled prevalence of T. gondii in various wild birds.
Order No. studies No. examined No. positive % (95% CI) Heterogeneity Univariate meta−regression
χ
2 P−value I
2
(%) P−value Coefcient (95% CI)
Accipitriformes 11 789 180 16.27 (7.49–31.81) 61.2 <0.01 83.7 0.08 0.9094 (−0.1230 to 1.9418)
Anseriformes 11 3507 395 20.09 (11.49–32.75) 116.9 <0.01 91.4
Charadriiformes 7 1938 415 26.43 (18.48–36.29) 28.9 <0.01 79.3
Columbiformes 12 1833 130 8.97 (4.76–16.26) 123.9 <0.01 91.1
Falconiformes 10 916 278 29.67 (17.54–45.56) 96.1 <0.01 90.6
Gruiformes 7 93 10 9.02 (3.04–23.85) 11.0 0.09 45.8
Passeriformes 21 3120 588 16.28 (9.96–25.48) 411.9 <0.01 95.1
Pelecaniformes 6 224 48 21.79 (4.53−62.08) 15.7 <0.01 68.3
Strigiformes 12 698 254 33.50 (21.46–48.16) 49.2 <0.01 77.7
Others 41 1711 239 9.71 (5.73–15.98) 137.4 <0.01 70.9
Abbreviations: CI: Condence interval; P-value: P ≤0.05 is statistically signicant.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
8
Table 4
Sub−group analysis of the prevalence of T. gondii in wild birds.
Variable Category No.
studies
No.
examined
No.
positive
% (95% CI) Heterogeneity Univariate meta−regression
χ
2 P−value I
2
(%)
P−value Coefcient (95% CI)
Detection
method
ELISA 2 510 94 18.4
(15.30–22.04)
1.3 0.24 26.9 0.44 0.8740 (−3.0919 to
1.3440)
IHT 1 751 72 9.6 (7.68–11.91) 0.0 NA NA
IFAT 1 72 6 8.3 (3.79–17.33) 0.0 NA NA
LAT 2 865 56 7.5 (3.72–14.60) 14.4 <0.01 93.1
MAT 30 11,433 2187 21.3
(14.95–29.44)
973.6 <0.01 97.0
PCR 13 2399 245 11.0 (5.93–19.41) 244.4 <0.01 95.1
Sample type Blood 36 14,236 2395 18.1
(13.05–24.45)
1191.4 <0.01 97.1 0.46 −0.3547 (−1.3006 to
0.5913)
Brain 8 1030 150 13.3 (5.90–27.41) 143.5 <0.01 95.1
Muscles 3 398 88 17.0 (3.47–53.70) 39.6 <0.01 95.0
Continent Africa 2 202 16 6.9 (3.83–10.80) 9.6 <0.01 89.6 0.15 0.2368 (−0.0851 to
0.5586)
Asia 22 5197 811 14.1
(13.21–15.10)
462.2 <0.01 95.5
Europe 17 7332 1161 14.2
(13.45–15.05)
896.0 <0.01 98.2
North
America
4 471 184 10.2 (8.70–11.79) 185.9 <0.01 98.4
Oceania 1 117 9 7.7 (3.58–13.19) 0.0 NA NA
South
America
7 1164 183 11.8 (9.98–13.68) 247.7 <0.01 97.6
Hemisphere West 11 2764 373 11.40
(5.52–23.00)
261.3 <0.01 96.2 0.30 −0.4302 (−1.2380 to
0.3776)
East 36 10,827 1494 16.80
(12.28–22.57)
953.4 <0.01 96.3
South 8 1319 189 9.36 (3.32–23.73) 117.0 <0.01 94.0
North 39 12,272 1678 16.82
(12.49–22.26)
1093.0 <0.01 96.5
Economic status Developed 22 8688 1365 13.8
(13.08–14.53)
1186.8 <0.01 98.2 0.13 −0.0900 (−0.2067 to
0.0267)
Developing 31 6795 999 14.70
(12.22–13.81)
650.5 <0.01 95.4
Latitude −60◦− − 30◦1 117 9 7.96 (4.05–14.13) 0.0 NA NA 0.13 0.7514 (−0.2111 to
1.7140)
−30◦−0◦7 1202 180 9.59 (2.92–27.26) 101.5 <0.01 94.1
0◦−30◦7 2979 332 9.44 (5.23–16.45) 156.7 <0.01 96.2
30◦−60◦29 6394 1062 19.52
(13.78–26.90)
794.8 <0.01 96.5
60◦−90◦3 2899 284 13.15
(8.38–20.03)
13.8 <0.01 85.6
Altitude <100 m 20 8704 1054 15.46
(11.51–20.44)
403.1 <0.01 95.3 0.53 0.3037 (−0.6451 to
1.2525)
100–1000 m 17 2939 566 16.63
(9.33–27.89)
367.7 <0.01 95.6
>1000 m 10 1948 247 12.69
(5.15–28.00)
304.8 <0.01 97.0
Climate type Am 1 69 24 34.78
(24.53–46.67)
0.0 NA NA 0.01 −2.9073 (−5.2372 to
−0.5775)
Aw 3 715 31 2.68 (0.63–10.68) 28.9 <0.01 93.1
Bs 4 1458 97 5.80 (2.77–11.74) 36.9 <0.01 91.9
Bw 1 146 25 17.12
(11.84–24.12)
0.0 NA NA
Cf 16 5245 771 17.08
(11.08–25.40)
393.1 <0.01 96.2
Cs 6 1208 207 24.18
(9.34–49.67)
244.2 <0.01 98.0
Cw 6 796 236 26.34
(13.54–44.96)
111.7 <0.01 95.5
Df 2 298 51 8.75 (1.68–34.98) 10.4 <0.01 90.4
Dw 4 722 136 17.96
(8.79–33.21)
64.7 <0.01 95.4
ET 4 2934 289 13.10
(8.84–18.98)
14.6 <0.01 79.5
Publication year 2000−2010 4 1758 153 6.0 (2.07–16.19) 72.8 <0.01 95.9 0.01 −1.7430 (−3.1244 to
−0.3616
)
2011−2020 37 12,334 2044 16.5
(11.82–22.57)
1138.2 <0.01 96.8
(continued on next page)
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
9
In the latitude subgroup analysis, we found that mid-latitude had the
highest prevalence, followed by high latitude, whereas low latitudes had
the lowest prevalence. Climatic conditions in mid-latitudes are often
more humid and warm, which favor the survival of T. gondii oocysts
(Rostami et al., 2017) and maintain their infectivity (Pereira et al.,
2020). In the subgroup analysis of altitude, the highest prevalence was
found in the range of 100–1000 m. The prevalence of low altitude
(<100 m) was very close to that of 100–1000 m. The low prevalence at
the high altitude (>1000 m) is perhaps related to the low air pressure,
oxygen deprivation, low temperature, high solar radiation and unpre-
dictable climate (Zhang and Li, 2015), which are not supportive to the
survival and transmission of T. gondii.
In terms of climate type (P<0.05), the present study showed that
tropical monsoon climate had the highest prevalence, however this
result was based on a single article and cannot reect the actual effect of
climate on T. gondii prevalence. The second highest prevalence was
correlated with dry-summer, Mediterranean, climate and dry-winter
subtropical climate. Temperature, rainfall, and geographic location
can inuence the occurrence of T. gondii infection (Oliveira et al., 2019).
T. gondii is more prevalent in regions with high humidity and warm
climates (Webster, 2010). Tropical monsoon climate is characterized by
high temperature and humidity, which favor the maturation and sur-
vival oof T. gondii oocysts (Hung et al., 2007). Tropical climates are also
richer in biodiversity and forests (Sloan et al., 2019), providing a suit-
able habitat for T. gondii transmission. These results highlight the need
for more surveillance of T. gondii infection in wild birds in humid and
warm regions.
Subgroup analysis by publication year (P<0.01) revealed an increase
in the prevalence from 6.0% in 2000–2010 to 16.5% in 2011–2020 and
26.9% after 2020. This temporal progressive increase in the prevalence
of T. gondii infection in wild birds may be attributed to increased
anthropological activities (Loiselle et al., 2010; Szabo et al., 2012),
changes in the agricultural landscapes (Green et al., 2005) or advances
in the development of methods that enable better detection and moni-
toring of pathogens (Suminda et al., 2022). A high attention given to
health and environmental issues in recent years may also play a role in
increasing the awareness of and reporting T. gondii infection in wild
birds.
4.1. Limitations and perspectives
Some aspects need to be considered when interpreting the ndings of
our study. First, our meta-analysis showed high heterogeneity, which is
common in meta-analyses of prevalence estimates owing to the meth-
odological variability between studies and residual confounding that are
difcult to control. Second, some of the tested variables lack sufcient
epidemiological data due to the low number of included studies, with
analysis of some categories based on only one article. Therefore, the
results should be interpreted with some caution because of the marked
differences in the number of studies between the analyzed categories.
Future systematic reviews should consider studies published in other
languages to increase the number of studies included in the analysis.
Future investigations should also consider more surveillance of wild bird
migration routes because migratory birds can spread T. gondii to a wide
range of warm-blooded animals, particularly outdoor reared mammals.
The detection and genotyping of T. gondii isolates from wild birds can
help identify the likely source of infection and trace potential trans-
mission routes. Future research should also assess additional risk factors
such as age and gender of the birds.
5. Conclusions
Results from the systematic review and meta-analysis of 49 studies
revealed 16.6% pooled global prevalence of T. gondii infection in wild
birds. Meta-regression analysis showed that two variables, publication
year and climate type, can have a signicant inuence on T. gondii
prevalence. The inclusion of more studies reporting on the prevalence of
T. gondii in wild birds may assist in distinguishing actual differences
among other variables such as the geographical location, and method of
detection. More investigations can improve understanding of T. gondii
infection epidemiology in wild birds and contribute to the development
of measures to prevent the transmission of infection to mammalian hosts
and humans.
Funding
This work was supported by National Key R&D Program of China
(2021YFC2300903).
CRediT authorship contribution statement
Cong-Cong Lei: Software, Investigation, Formal analysis. Quan
Zhao: Writing – review & editing, Supervision, Project administration,
Conceptualization. Hany Elsheikha: Writing – review & editing, Visu-
alization, Validation, Resources, Conceptualization. Hongwei Cao:
Writing – review & editing, Supervision, Project administration, Fund-
ing acquisition, Conceptualization. Si-Yuan Qin: Resources, Investiga-
tion, Formal analysis. Xing Yang: Writing – original draft, Visualization,
Validation, Data curation. Xiao-Man Li: Visualization, Software, Re-
sources, Methodology, Data curation. Yanan Cai: Methodology,
Table 4 (continued )
Variable Category No.
studies
No.
examined
No.
positive
% (95% CI) Heterogeneity Univariate meta−regression
χ
2 P−value I
2
(%)
P−value Coefcient (95% CI)
After 2020 8 1938 463 26.9
(16.96–39.81)
132.4 <0.01 94.7
Quality level 5 29 11,105 1640 14.8
(10.04–21.20)
982.1 <0.01 97.1 0.32 −0.3432 (−1.0304 to
0.3441)
4 12 2901 484 19.4
(10.38–33.28)
259.3 <0.01 95.8
3 7 1952 530 22.6
(12.03–38.37)
64.6 <0.01 90.7
2 1 72 6 8.3 (3.79–17.33) 0.0 NA NA
Total 49 16,030 2660 16.6
(12.40–21.87)
Abbreviations: CI: Condence interval; NA: not applicable; P−value: P ≤0.05 was set at the statistical signicance threshold; LAT: Latex agglutination test; ELISA:
Enzyme linked immunosorbent assay; MAT: Modied agglutination test; PCR: Polymerase chain reaction; IHT: Indirect hemagglutination test; IFAT: Indirect
immunouorescent antibody test; Am: Tropical monsoon climate; Aw: Tropical savannah climate; Bs: Arid steppe climate; Bw: Arid desert climate; Cf: Temperate
without dry season climate; Cs: Temperate dry summer climate; Cw: Temperate dry winter climate; Df: Cold without dry season climate; Dw: Cold dry winter climate;
ET: Polar tund.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
10
Investigation, Formal analysis, Data curation. Chao Chen: Writing –
original draft, Software, Methodology, Investigation, Formal analysis,
Data curation.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
References
Abdoli, A., Arbabi, M., Pirestani, M., Mirzaghavami, M., Ghaffarifar, F., Dalimi, A.,
Sadraei, J., 2018. Molecular assessment of Neospora caninum and Toxoplasma gondii
in hooded crows (Corvus cornix) in Tehran, Iran. Comp. Immunol. Microbiol. Infect.
Dis. 57, 69–73. https://doi.org/10.1016/j.cimid.2018.06.008.
Acosta, I.C.L., Souza-Filho, A.F., Mu˜
noz-Leal, S., Soares, H.S., Heinemann, M.B.,
Moreno, L., Gonz´
alez-Acu˜
na, D., Gennari, S.M., 2019. Evaluation of antibodies
against Toxoplasma gondii and Leptospira spp. in Magellanic penguins (Spheniscus
magellanicus) on Magdalena Island, Chile. Vet. Parasitol. Reg. Stud. Rep. 16, 100282
https://doi.org/10.1016/j.vprsr.2019.100282.
Aguirre, A.A., Longcore, T., Barbieri, M., Dabritz, H., Hill, D., Klein, P.N., Lepczyk, C.,
Lilly, E.L., McLeod, R., Milcarsky, J., Murphy, C.E., Su, C., VanWormer, E.,
Yolken, R., Sizemore, G.C., 2019. The one health approach to toxoplasmosis:
epidemiology, control, and prevention strategies. Ecohealth 16, 378–390. https://
doi.org/10.1007/s10393-019-01405-7.
Alvarado-Esquivel, C., Rajendran, C., Ferreira, L.R., Kwok, O.C., Choudhary, S.,
Alvarado-Esquivel, D., Rodriguez-Pena, S., Villena, I., Dubey, J.P., 2011. Prevalence
of Toxoplasma gondii infection in wild birds in Durango, Mexico. J. Parasitol. 97,
809–812. https://doi.org/10.1645/GE-2844.1.
Ammar, S., Wood, L., Su, C., Spriggs, M., Brown, J., Van Why, K., Gerhold, R., 2021.
Toxoplasma gondii prevalence in carnivorous wild birds in the eastern United States.
Int. J. Parasitol. Parasites Wildl. 15, 153–157. https://doi.org/10.1016/j.
ijppaw.2021.04.010.
Amouei, A., Sharif, M., Hosseini, S.A., Sarvi, S., Mizani, A., Salehi, S., Gholami, S., Jafar-
Ramaji, T., Daryani, A., 2018. Prevalence of Toxoplasma gondii infection in domestic
and migrating birds from Mazandaran Province, Northern Iran. Avian Biol. Res. 11,
12–15. https://doi.org/10.3184/175815617×15105842200.
Andrade, L.H.M., Lugarini, C., Oliveira, R.A.S., Silva, L.T.R., Marvulo, M.F.V., Garcia, J.
E., Dubey, J.P., Silva, J.C.R., 2016. Ocorrˆ
encia de anticorpos anti-Toxoplasma gondii
em aves silvestres de trˆ
es Unidades de Conservaç˜
ao Federais da Paraíba e da Bahia.
Pesq. Vet. Bras. 36, 103–107. https://doi.org/10.1590/S0100-
736×2016000200007.
Andrle, K., 2011. The implications of diet composition and declining vole supply on
populations of vole eating raptors. Examensarbete I ¨
amnet biologi, 2011:3, Swedish
University of Agricultural Sciences, Umeå, Sweden. 〈http://urn.kb.se/resolve?urn
=urn:nbn:se:slu:epsilon-s-251〉.
Angelier, F., Weimerskirch, H., Chastel, O., 2011. Capture and blood sampling do not
affect foraging behaviour, breeding success and return rate of a large seabird: the
black-browed albatross. Polar Biol. 34, 353–361. https://doi.org/10.1007/s00300-
010-0888-7.
Barros, L.D., Taroda, A., Zulpo, D.L., Cunha, I.A., Sammi, A.S., Cardim, S.T., Miura, A.C.,
Su, C., Machado, R.Z., Vidotto, O., Garcia, J.L., 2014. Genetic characterization of
Toxoplasma gondii isolates from eared doves (Zenaida auriculata) in Brazil. Rev. Bras.
Parasitol. Vet. 23, 443–448. https://doi.org/10.1590/S1984-29612014073.
Bata, S.I., Maikai, B.V., Kwaga, J.K.P., Okubanjo, O.O., Pam, L., Wungak, Y.S.,
Kamani, J., Elisha, C., Ogbu, K., Dike, M., Ringyl, C.S., Makama, S., 2021. Serological
evidence of exposure to Toxoplasma gondii infection in wild birds and local chickens
(Gallus gallus domesticus) in Plateau State, North Central Nigeria. Vet. Parasitol. Reg.
Stud. Rep. 25, 100601 https://doi.org/10.1016/j.vprsr.2021.100601.
Bauer, S., Hoye, B.J., 2014. Migratory animals couple biodiversity and ecosystem
functioning worldwide. Science 344, 1242552. https://doi.org/10.1126/
science.1242552.
Bertolino, S., Ghiberti, E., Perrone, A., 2001. Feeding ecology of the long-eared owl (Asio
otus) in northern Italy: is it a dietary specialist? Can. J. Zool. 79 (12), 2192–2198.
https://doi.org/10.1139/z01-182.
Cabezon, O., Garcia-Bocanegra, I., Molina-Lopez, R., Marco, I., Blanco, J.M., Hoe, U.,
Margalida, A., Bach-Raich, E., Darwich, L., Echeverria, I., Obon, E., Hernandez, M.,
Lavin, S., Dubey, J.P., Almeria, S., 2011. Seropositivity and risk factors associated
with Toxoplasma gondii infection in wild birds from Spain. PLoS One 6, e29549.
https://doi.org/10.1371/journal.pone.0029549.
Cabez´
on, O., Cerd`
a-Cu´
ellar, M., Morera, V., García-Bocanegra, I., Gonz´
alez-Solís, J.,
Napp, S., Ribas, M.P., Blanch-L´
azaro, B., Fern´
andez-Aguilar, X., Antilles, N., L´
opez-
Soria, S., Lorca-Or´
o, C., Dubey, J.P., Almería, S., 2016. Toxoplasma gondii infection in
Seagull chicks is related to the consumption of freshwater food resources. PLoS One
11, e0150249. https://doi.org/10.1371/journal.pone.0150249.
Chen, B., Benedetti, A., 2017. Quantifying heterogeneity in individual participant data
meta-analysis with binary outcomes. Syst. Rev. 6, 243. https://doi.org/10.1186/
s13643-017-0630-4.
Chen, J.C., Tsai, Y.J., Wu, Y.L., 2015. Seroprevalence of Toxoplasma gondii antibodies in
wild birds in Taiwan. Res. Vet. Sci. 102, 184–188. https://doi.org/10.1016/j.
rvsc.2015.08.010.
Cong, W., Huang, S.Y., Zhou, D.H., Zhang, X.X., Zhang, N.Z., Zhao, Q., Zhu, X.Q., 2013.
Prevalence and genetic characterization of Toxoplasma gondii in house sparrows
(Passer domesticus) in Lanzhou, China. Korean J. Parasitol. 51, 363–367. https://doi.
org/10.3347/kjp.2013.51.3.363.
Cortes, J.A., Roncancio, A., Uribe, L.G., Cortes-Luna, C.F., Montoya, J.G., 2019.
Approach to ocular toxoplasmosis including pregnant women. Curr. Opin. Infect.
Dis. 32, 426–434. https://doi.org/10.1097/QCO.0000000000000577.
Costa, W., Barbosa, I., Prado, D., Domann, N., Rezende, H.H.A., 2022. A systematic
review of Toxoplasma gondii genotypes in Gallus gallus domesticus worldwide: The
focus is Brazil. Transbound. Emerg. Dis. 69, 2440–2450. https://doi.org/10.1111/
tbed.14221.
Crozier, G., Schulte-Hostedde, A.I., 2014. The ethical dimensions of wildlife disease
management in an evolutionary context. Evol. Appl. 7, 788–798. https://doi.org/
10.1111/eva.12171.
Dard, C., Fricker-Hidalgo, H., Brenier-Pinchart, M.P., Pelloux, H., 2016. Relevance of and
new developments in serology for toxoplasmosis. Trends Parasitol. 32, 492–506.
https://doi.org/10.1016/j.pt.2016.04.001.
Darwich, L., Cabezon, O., Echeverria, I., Pabon, M., Marco, I., Molina-Lopez, R., Alarcia-
Alejos, O., Lopez-Gatius, F., Lavin, S., Almeria, S., 2012. Presence of Toxoplasma
gondii and Neospora caninum DNA in the brain of wild birds. Vet. Parasitol. 183,
377–381. https://doi.org/10.1016/j.vetpar.2011.07.024.
Dubey, J.P., 1976. Reshedding of Toxoplasma oocysts by chronically infected cats. Nature
262, 213–214. https://doi.org/10.1038/262213a0.
Dubey, J.P., 2002. A review of toxoplasmosis in wild birds. Vet. Parasitol. 106, 121–153.
https://doi.org/10.1016/s0304-4017(02)00034-1.
Dubey, J.P., 2010. Toxoplasma gondii infections in chickens (Gallus domesticus):
prevalence, clinical disease, diagnosis and public health signicance. Zoonoses
Public Health 57, 60–73. https://doi.org/10.1111/j.1863-2378.2009.01274.x.
Dubey, J.P., Felix, T.A., Kwok, O.C., 2010. Serological and parasitological prevalence of
Toxoplasma gondii in wild birds from Colorado. J. Parasitol. 96, 937–939. https://
doi.org/10.1645/GE-2501.1.
Dubey, J.P., Jones, J.L., 2008. Toxoplasma gondii infection in humans and animals in the
United States. Int. J. Parasitol. 38, 1257–1278. https://doi.org/10.1016/j.
ijpara.2008.03.007.
Dubey, J.P., Laurin, E., Kwowk, O.C., 2016. Validation of the modied agglutination test
for the detection of Toxoplasma gondii in free-range chickens by using cat and mouse
bioassay. Parasitology 143, 314–319. https://doi.org/10.1017/
S0031182015001316.
Dubey, J.P., Pena, H.F.J., Cerqueira-Cezar, C.K., Murata, F.H.A., Kwok, O.C.H., Yang, Y.
R., Gennari, S.M., Su, C., 2020. Epidemiologic signicance of Toxoplasma gondii
infections in chickens (Gallus domesticus): the past decade. Parasitology 147,
1263–1289. https://doi.org/10.1017/S0031182020001134.
Elsheikha, H.M., 2008. Congenital toxoplasmosis: priorities for further health promotion
action. Public Health 122 (4), 335–353. https://doi.org/10.1016/j.
puhe.2007.08.009.
Elsheikha, H.M., Marra, C.M., Zhu, X.Q., 2020. Epidemiology, pathophysiology,
diagnosis, and management of cerebral toxoplasmosis. Clin. Microbiol. Rev. 34 (1),
e00115–e00119. https://doi.org/10.1128/CMR.00115-19.
Fernandes, S., Brilhante-Simoes, P., Coutinho, T., Cardoso, L., Dubey, J.P., Lopes, A.P.,
2019. Comparison of indirect and modied agglutination tests for detection of
antibodies to Toxoplasma gondii in domestic cats. J. Vet. Diagn. Invest. 31, 774–777.
https://doi.org/10.1177/1040638719868753.
Gazzonis, A.L., Villa, L., Lubian, E., Ressegotti, S., Grilli, G., Raimondi, S., Zanzani, S.A.,
Manfredi, M.T., 2021. Molecular survey on Toxoplasma gondii and Neospora caninum
infection in wild birds of prey admitted to recovery centers in northern Italy.
Microorganisms 9, 736. https://doi.org/10.3390/microorganisms9040736.
Gennari, S.M., Ogrzewalska, M., Soares, H.S., Saraiva, D.G., Pinter, A., Labruna, M.B.,
Dubey, J.P., 2014. Occurrence of Toxoplasma gondii antibodies in birds from the
Atlantic Forest, state of Sao Paulo, Brazil. Vet. Parasitol. 200, 193–197. https://doi.
org/10.1016/j.vetpar.2013.10.003.
Gennari, S.M., Niemeyer, C., Catao-Dias, J.L., Soares, H.S., Acosta, I.C., Dias, R.A.,
Ribeiro, J.D., Lassalvia, C., Maracini, P., Kolesnikovas, C.K., Mayorga, L.F., Dubey, J.
P., 2016a. Survey of Toxoplasma gondii antibodies in Magellanic Penguins (Spheniscus
magellanicus Forster, 1781). J. Zoo. Wildl. Med. 47, 364–366. https://doi.org/
10.1638/2015-0103.1.
Gennari, S.M., Niemeyer, C., Soares, H.S., Musso, C.M., Siqueira, G.C., Catao-Dias, J.L.,
Dias, R.A., Dubey, J.P., 2016b. Seroprevalence of Toxoplasma gondii in seabirds from
Abrolhos Archipelago, Brazil. Vet. Parasitol. 226, 50–52. https://doi.org/10.1016/j.
vetpar.2016.06.016.
Gondim, L.S.Q., Abe-Sandes, K., Uzˆ
eda, R.S., Silva, M.S.A., Santos, S.L., Mota, R.A.,
Vilela, S.M.O., Gondim, L.F.P., 2010. Toxoplasma gondii and Neospora caninum in
sparrows (Passer domesticus) in the Northeast of Brazil. Vet. Parasitol. 168, 121–124.
https://doi.org/10.1016/j.vetpar.2009.09.055.
Guyatt, G.H., Oxman, A.D., Vist, G.E., Kunz, R., Falck-Ytter, Y., Alonso-Coello, P.,
Schünemann, H.J., 2008. GRADE: an emerging consensus on rating quality of
evidence and strength of recommendations. BMJ 336, 924–926. https://doi.org/
10.1136/bmj.39489.470347.AD.
Hamer, S.A., Lehrer, E., Magle, S.B., 2012. Wild birds as sentinels for multiple zoonotic
pathogens along an urban to rural gradient in greater Chicago, Illinois. Zoonoses
Public Health 59 (5), 355–364. https://doi.org/10.1111/j.1863-2378.2012.01462.x.
Higgins, J.P., Thompson, S.G., 2002. Quantifying heterogeneity in a meta-analysis. Stat.
Med 21, 1539–1558. https://doi.org/10.1002/sim.1186.
Huang, S.Y., Cong, W., Zhou, P., Zhou, D.H., Wu, S.M., Xu, M.J., Zou, F.C., Song, H.Q.,
Zhu, X.Q., 2012. First report of genotyping of Toxoplasma gondii isolates from wild
birds in China. J. Parasitol. 98, 681–682. https://doi.org/10.1645/GE-3038.1.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
11
Huang, S.-Y., Fan, Y.-M., Chen, K., Yao, Q.-X., Yang, B., 2019. Seroprevalence and risk
assessment of Toxoplasma gondii in Java sparrows (Lonchura oryzivora) in China.
BMC Vet. Res. 15 (1), 129. https://doi.org/10.1186/s12917-019-1888-7.
Hung, C.C., Fan, C.K., Su, K.E., Sung, F.C., Chiou, H.Y., Gil, V., da Conceicao, dR.F.M., de
Carvalho, J.M., Cruz, C., Lin, Y.K., Tseng, L.F., Sao, K.Y., Chang, W.C., Lan, H.S.,
Chou, S.H., 2007. Serological screening and toxoplasmosis exposure factors among
pregnant women in the Democratic Republic of Sao Tome and Principe. Trans. R.
Soc. Trop. Med. Hyg. 101, 134–139. https://doi.org/10.1016/j.trstmh.2006.04.012.
Iemmi, T., Vismarra, A., Mangia, C., Zanin, R., Genchi, M., Lanfranchi, P., Kramer, L.H.,
Formenti, N., Ferrari, N., 2020. Toxoplasma gondii in the Eurasian kestrel (Falco
tinnunculus) in northern Italy. Parasit. Vectors 13, 262. https://doi.org/10.1186/
s13071-020-04134-x.
Jenkins, E.J., Simon, A., Bachand, N., Stephen, C., 2015. Wildlife parasites in a one
health world. Trends Parasitol. 31, 174–180. https://doi.org/10.1016/j.
pt.2015.01.002.
Jourdain, E., Gauthier-Clerc, M., Bicout, D.J., Sabatier, P., 2007. Bird migration routes
and risk for pathogen dispersion into western Mediterranean wetlands. Emerg.
Infect. Dis. 13 (3), 365–372. https://doi.org/10.3201/eid1303.060301.
Karadjian, G., Laboutiere, L., Chevillot, A., Voisinot, A., Blaizot, A., Puech, M.P.,
Aubert, D., Risco-Castillo, V., Blaga, R., Vallee, I., 2022. Toxocara cati and
Toxoplasma gondii in French Birds of Prey. J. Wildl. Dis. 58, 373–379. https://doi.
org/10.7589/JWD-D-21-00034.
Khademvatan, S., Saki, J., Youse, E., Abdizadeh, R., 2013. Detection and genotyping of
Toxoplasma gondii strains isolated from birds in the southwest of Iran. Br. Poult. Sci.
54, 76–80. https://doi.org/10.1080/00071668.2013.763899.
Krijger, I.M., Ahmed, A.A.A., Goris, M.G.A., Cornelissen, J.B.W.J., Meerburg, B.G., 2020.
Wild rodents and insectivores as carriers of pathogenic Leptospira and Toxoplasma
gondii in The Netherlands. Vet. Med. Sci. 6 (3), 623–630. https://doi.org/10.1002/
vms3.255.
Langoni, H., Silva, A., Pezerico, S., Lima, V., 2007. Utilization of modied agglutination
test and indirect immunouorescent antibody test for the detection of Toxoplasma
gondii antibodies in naturally exposed horses. Braz. J. Vet. Res. Anim. Sci. 44 (1),
27–32.
Lehmann, T., Marcet, P.L., Graham, D.H., Dahl, E.R., Dubey, J.P., 2006. Globalization
and the population structure of Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 103
(30), 11423–11428. https://doi.org/10.1073/pnas.0601438103.
Liu, M.T., Jiang, W.X., Gui, B.Z., Jin, Y.C., Yi, J.N., Li, F., Zheng, W.B., Liu, G.H., 2019.
Molecular prevalence and genetic characterization of Toxoplasma gondii in wild birds
in Hunan province, China. Vector Borne Zoonotic Dis. 19 (5), 378–383. https://doi.
org/10.1089/vbz.2018.2371.
Lohr, M.T., Lohr, C.A., Burbidge, A.H., Davis, R.A., 2020. Toxoplasma gondii
seropositivity across urban and agricultural landscapes in an Australian owl. Emu -
Austral Ornithol. 120, 275–285. https://doi.org/10.1080/01584197.2020.1831393.
Loiselle, B.A., Graham, C.H., Goerck, J.M., Ribeiro, M.C., 2010. Assessing the impact of
deforestation and climate change on the range size and environmental niche of bird
species in the Atlantic forests, Brazil. J. Biogeogr. 37 (7), 1288–1301. https://doi.
org/10.1111/j.1365-2699.2010.02285.x.
Lopes, C., Brandao, R., Lopes, A.F., Sargo, R., Casero, M., Nunes, C., Silva, F., Dubey, J.P.,
Cardoso, L., Lopes, A.P., 2021. Prevalence of antibodies to Toxoplasma gondii in
different wild bird species admitted to rehabilitation centres in Portugal. Pathogens
10 (9), 1144. https://doi.org/10.3390/pathogens10091144.
Love, D., Kwok, O.C., Verma, S.K., Dubey, J.P., Bellah, J., 2016. Antibody prevalence and
isolation of viable Toxoplasma gondii from raptors in the Southeastern USA. J. Wildl.
Dis. 52, 653–656. https://doi.org/10.7589/2015-10-269.
Lukasova, R., Kobedova, K., Halajian, A., Bartova, E., Murat, J.B., Rampedi, K.M., Luus-
Powell, W.J., 2018. Molecular detection of Toxoplasma gondii and Neospora caninum
in birds from South Africa. Acta Trop. 178, 93–96. https://doi.org/10.1016/j.
actatropica.2017.10.029.
Luo, H., Li, K., Shahzad, M., Zhang, H., Lan, Y., Xiong, X., 2017. Seroprevalence of
Toxoplasma gondii Infection in wild boars, wild rabbits, and wild chickens in Hubei
Province, China. Korean J. Parasitol. 55, 85–88. https://doi.org/10.3347/
kjp.2017.55.1.85.
Macrì, G., Sala, M., Linder, A.M., Pettirossi, N., Scarpulla, M., 2009. Comparison of
indirect uorescent antibody test and modied agglutination test for detecting
Toxoplasma gondii immunoglobulin G antibodies in dog and cat. Parasitol. Res. 105,
35. https://doi.org/10.1007/s00436-009-1358-4.
Mancianti, F., Nardoni, S., Mugnaini, L., Poli, A., 2013. Toxoplasma gondii in waterfowl:
the rst detection of this parasite in Anas crecca and Anas clypeata from Italy.
J. Parasitol. 99, 561–563. https://doi.org/10.1645/12-34.1.
Miao, Q., Han, J.Q., Xiang, X., Yuan, F.Z., Liu, Y.Z., Duan, G., Zhu, X.Q., Zou, F.C., 2014.
Prevalence of antibody to Toxoplasma gondii in black-headed gulls (Chroicocephalus
ridibundus), Dianchi Lake, China. J. Wildl. Dis. 50, 717–719. https://doi.org/
10.7589/2014-01-016.
Mirza, V., Burrows, E.B., Gils, S., Hunter, S., Gartrell, B.D., Howe, L., 2017.
A retrospective survey into the presence of Plasmodium spp. and Toxoplasma gondii in
archived tissue samples from New Zealand raptors: New Zealand falcons (Falco
novaeseelandiae), Australasian harriers (Circus approximans) and moreporks (Ninox
novaeseelandiae). Parasitol. Res. 116, 2283–2289. https://doi.org/10.1007/s00436-
017-5536-5.
Molina-Lopez, R., Cabezon, O., Pabon, M., Darwich, L., Obon, E., Lopez-Gatius, F.,
Dubey, J.P., Almeria, S., 2012. High seroprevalence of Toxoplasma gondii and
Neospora caninum in the Common raven (Corvus corax) in the Northeast of Spain.
Res. Vet. Sci. 93, 300–302. https://doi.org/10.1016/j.rvsc.2011.05.011.
Murao, T., Omata, Y., Kano, R., Murata, S., Okada, T., Konnai, S., Asakawa, M.,
Ohashi, K., Onuma, M., 2008. Serological survey of Toxoplasma gondii in wild
waterfowl in Chukotka, Kamchatka, Russia and Hokkaido, Japan. J. Parasitol. 94 (4),
830–833. https://doi.org/10.1645/GE-1434.1.
Muz, M.N., Kılınç, ¨
O.O., ˙
Ișler, C.T., Altu˘
g, E., Karakavuk, M., 2015. Molecular diagnosis
of Toxoplasma gondii and Neospora caninum in brain tissues of some wild birds.
Kafkas Üniv. Vet. Fak. Ültesi Derg. 21 (2), 173–178.
Naveed, A., Ali, S., Ahmed, H., Simsek, S., Rizwan, M., Kaleem, I., Gondal, M.A.,
Shabbir, A., Pervaiz, F., Khan, M.A., Nadeem, M.S., Afzaal, M.S., Umar, S., 2019.
Seroprevalence and risk factors of Toxoplasma gondii in wild birds of Punjab
Province, Pakistan. J. Wildl. Dis. 55 (1), 129–135. https://doi.org/10.7589/2017-
09-228.
Nazir, M.M., Ayaz, M.M., Ahmed, A.N., Maqbool, A., Ashraf, K., Oneeb, M., Yasin, G.,
Subhani, A., Ali, M.A., Nazir, N., Sajid, M.A., 2018. Prevalence of Toxoplasma gondii,
Neospora caninum, and Sarcocystis species DNA in the heart and breast muscles of
rock pigeons (Columbia livia), 62640422018 J. Parasitol. Res. 2018. https://doi.org/
10.1155/2018/6264042.
Oliveira, J., Casseb, A., Ramos, A., Filho, S., Pereira, W., 2019. Risk factors associated
with the epidemiology of Toxoplasma gondii in cattle and buffaloes in the state of
Par´
a, Brazil. Semin.: Ciˆ
encias Agr. ´
arias 39 (5), 2029–2037. https://doi.org/
10.5433/1679-0359.2018v39n5p2029.
Peel, M.C., Finlayson, B.L., McMahon, T.A., 2007. Updated world map of the Kppen-
Geiger climate classication. Hydrol. Earth Syst. Sci. 11 (5), 1633–1644. https://doi.
org/10.5194/hess-11-1633-2007.
Pereira, D.C., Dubey, J.P., Mata, A.D., Neto, H., Lopes, A.P., 2020. Seroepidemiology of
Toxoplasma gondii in domestic cattle, sheep, goats and pigs from So Tom´
e and
Príncipe. Rev. Bras. Parasitol. Vet. 29 (1), e014819 https://doi.org/10.1590/
S1984–29612019101.
Poulle, M.L., Le Corre, M., Bastien, M., Gedda, E., Feare, C., Jaeger, A., Larose, C.,
Shah, N., Voogt, N., Gopper, B., Lagadec, E., Rocamora, G., Geers, R., Aubert, D.,
Villena, I., Lebarbenchon, C., 2021. Exposure of pelagic seabirds to Toxoplasma
gondii in the Western Indian Ocean points to an open sea dispersal of this terrestrial
parasite. PLoS One 16, e0255664. https://doi.org/10.1371/journal.pone.0255664.
Rahman, M.M., Talukder, A., Chowdhury, M.M.H., Talukder, R., Akter, R., 2021.
Coronaviruses in wild birds - A potential and suitable vector for global distribution.
Vet. Med. Sci. 7, 264–272. https://doi.org/10.1002/vms3.360.
Robert-Gangneux, F., Dard´
e, M.L., 2012. Epidemiology of and diagnostic strategies for
toxoplasmosis. Clin. Microbiol. Rev. 25, 264–296. https://doi.org/10.1128/
CMR.05013-11.
Rostami, A., Riahi, S.M., Fakhri, Y., Saber, V., Hanifehpour, H., Valizadeh, S.,
Gholizadeh, M., Pouya, R.H., Gamble, H.R., 2017. The global seroprevalence of
Toxoplasma gondii among wild boars: a systematic review and meta-analysis. Vet.
Parasitol. 244, 12–20. https://doi.org/10.1016/j.vetpar.2017.07.013.
Salant, H., Hamburger, J., King, R., Baneth, G., 2013. Toxoplasma gondii prevalence in
Israeli crows and Griffon vultures. Vet. Parasitol. 191, 23–28. https://doi.org/
10.1016/j.vetpar.2012.07.029.
Sandstrom, C.A., Buma, A.G., Hoye, B.J., Prop, J., van der Jeugd, H., Voslamber, B.,
Madsen, J., Loonen, M.J., 2013. Latitudinal variability in the seroprevalence of
antibodies against Toxoplasma gondii in non-migrant and Arctic migratory geese. Vet.
Parasitol. 194, 9–15. https://doi.org/10.1016/j.vetpar.2012.12.027.
Sato, A.P., Goulart, M.A., Konell, A.L., de Oliveira Koch, M., da Fonseca, F.M., Morel, A.
P., Locatelli-Dittrich, R., 2021. Serosurvey of Toxoplasma gondii, Neospora caninum
and Sarcocystis neurona in raptors and risk factor analysis. Parasitol. Int. 82, 102312
https://doi.org/10.1016/j.parint.2021.102312.
Sloan, S., Meyfroidt, P., Rudel, T.K., Bongers, F., Chazdon, R., 2019. The forest
transformation: Planted tree cover and regional dynamics of tree gains and losses.
Glob. Environ. Change 59, 101988. https://doi.org/10.1016/j.
gloenvcha.2019.101988.
Soultan, A., Pav´
on-Jord´
an, D., Bradter, U., Sandercock, B.K., Hochachka, W.M.,
Johnston, A., Brommer, J., Gaget, E., Keller, V., Knaus, P., Aghababyan, K.,
Maxhuni, Q., Vintchevski, A., Nagy, K., Raudonikis, L., et al., 2022. The future
distribution of wetland birds breeding in Europe validated against observed changes
in distribution. Environ. Res. Lett. 17, 024025 https://doi.org/10.1088/1748-9326/
ac4ebe.
Suminda, G.G.D., Bhandari, S., Won, Y., Goutam, U., Kanth Pulicherla, K., Son, Y.O.,
Ghosh, M., 2022. High-throughput sequencing technologies in the detection of
livestock pathogens, diagnosis, and zoonotic surveillance. Comput. Struct.
Biotechnol. J. 20, 5378–5392. https://doi.org/10.1016/j.csbj.2022.09.028.
Szabo, J.K., Khwaja, N., Garnett, S.T., Butchart, S.H.M., 2012. Global patterns and
drivers of avian extinctions at the species and subspecies level. Plos One 7, e47080.
https://doi.org/10.1371/journal.pone.0047080.
Tayyub, M., Ali, S., Javid, A., Imran, M., 2022. Molecular detection of Toxoplasma gondii
and Neospora caninum in rock pigeons (Columba livia) in Punjab, Pakistan. Parasitol.
Res. 121, 1499–1505. https://doi.org/10.1007/s00436-022-07494-8.
Tian, Y.M., Dai, F.Y., Huang, S.Y., Deng, Z.H., Duan, G., Zhou, D.H., Yang, J.F., Weng, Y.
B., Zhu, X.Q., Zou, F.C., 2012. First report of Toxoplasma gondii seroprevalence in
peafowls in Yunnan Province, Southwestern China. Parasit. Vectors 5, 205. https://
doi.org/10.1186/1756-3305-5-205.
Tidy, A., Fangueiro, S., Dubey, J.P., Cardoso, L., Lopes, A.P., 2017. Seroepidemiology
and risk assessment of Toxoplasma gondii infection in captive wild birds and
mammals in two zoos in the North of Portugal. Vet. Parasitol. 235, 47–52. https://
doi.org/10.1016/j.vetpar.2017.01.004.
Tsai, Y.J., Chung, W.C., Lei, H.H., Wu, Y.I., 2006. Prevalence of antibodies to Toxoplasma
gondii in pigeons (Columba livia) in Taiwan. J. Parasitol. 92, 871. https://doi.org/
10.1645/GE-716R2.1.
Wang, X., Talbot, C.T., Yin, J.H., Kalalah, A.A., Wang, C., Newton, J.C., 2021.
Disseminated Toxoplasma gondii infection in an adult osprey (Pandion haliaetus). Vet.
Sci. 9, 5. https://doi.org/10.3390/vetsci9010005.
C. Chen et al.

Preventive Veterinary Medicine 226 (2024) 106187
12
Webster, J.P., 2010. Dubey, J.P. Toxoplasmosis of animals and humans. Parasit. Vectors
3 (1), 2.
Zhang, F.K., Wang, H.J., Qin, S.Y., Wang, Z.D., Lou, Z.L., Zhu, X.Q., Liu, Q., 2015.
Molecular detection and genotypic characterization of Toxoplasma gondii in wild
waterfowls in Jilin Province, Northeastern China. Parasitol. Int. 64, 576–578.
https://doi.org/10.1016/j.parint.2015.08.008.
Zhang, J.L., Li, X.Y., 2015. A review of drug metabolism under hypoxia environment at
high altitude. Yao Xue Xue Bao 50, 1073–1079. PMID: 26757541.
Zhang, N., Wang, S., Wang, D., Li, C., Zhang, Z., Yao, Z., Li, T., Xie, Q., Liu, S., Zhang, H.,
2016. Seroprevalence of Toxoplasma gondii infection and risk factors in domestic
sheep in Henan province, central China (do). Parasite 23, 53. https://doi.org/
10.1051/parasite/2016064.
C. Chen et al.