Relationship Between Cat Contact and Infection by Toxoplasma

gondii in Humans: A Meta-Analysis

Author(s): Hai-Xia Wei, Cheng He, Pei-Liang Yang, David S. Lindsay, and
Hong-Juan Peng,
Source: Comparative Parasitology, 83(1):11-19.
Published By: The Helminthological Society of Washington
https://doi.org/10.1654/1525-2647-83.1.11
URL: http://www.bioone.org/doi/full/10.1654/1525-2647-83.1.11

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Comp. Parasitol.
83(1), 2016, pp. 1119

Relationship Between Cat Contact and Infection by Toxoplasma gondii in

Humans: A Meta-Analysis

HAI-XIA WEI,1,5 CHENG HE,1,4 PEI-LIANG YANG,2 DAVID S. LINDSAY,3 AND HONG-JUAN PENG1,5
1
Department of Pathogen Biology, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public
Health and Tropical Medicine, Southern Medical University, Guangzhou, Guangdong, the Peoples Republic of China
(e-mail: hongjuan@smu.edu.cn),
2
Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong, the Peoples Republic of China (e-mail:
723488559@qq.com), and
3
Department of Biomedical Sciences & Pathobiology, VA-MD Regional College of Veterinary Medicine, Virginia Tech,
Duck Pond Drive, Blacksburg, Virginia 24061, U.S.A. (e-mail: lindsayd@vt.edu)

ABSTRACT: Domestic cats are well known to play an important role in the transmission of infective stages of Toxoplasma
gondii to humans and other warm-blooded animals, and it is therefore logical to assume that individuals who own cats would
have a higher prevalence of antibodies to T. gondii than would individuals from a normal age-matched population. However,
a review of the literature indicates that cat ownership is of variable importance and that it is not always a significant risk
factor. The present study was conducted using a meta-analysis to evaluate the relationship between infection by T. gondii and
cat ownership. The related literature was searched in multiple literature databases, regardless of language. Odds ratios (ORs)
and 95% confidence intervals (CIs) were used to evaluate the risks of infection by T. gondii. In total, 46 of the 1,813 detected
articles were included in our analysis. The risk of infection by T. gondii had a significant association with cat contact
(P , 0.05) in the general population, as well as with immunocompromised people, people with special occupations, and cat
owners, with ORs (95% CI) of 1.413 (1.1631.717), 1.558 (1.1732.069), 1.493 (1.0882.049), and 1.421 (1.1741.721),
respectively. Interestingly, the risk of infection by T. gondii had no significant association with neighborhood cat contact
versus no contact (P 5 0.104), with an OR of 1.544 (95% CI: 0.9142.606), and the proportions of cat ownership in
individuals infected and uninfected by T. gondii were not significantly different (P 5 0.389), with an OR of 1.375 (95% CI:
0.6662.840). These data indicate that cat contact can increase the risk of infection by T. gondii in various populations,
including the general population, immune-suppressed/pregnant individuals, those with special occupations, and cat(s)
owners. Interestingly, the risk of infection by T. gondii has no significant association with neighborhood cat contact versus no
contact, and the analysis of the data extracted from a case-control study shows that there is no significant difference in the
rate of cat ownership between those infected by T. gondii and those uninfected. Therefore, while significant, cat contact may
not be the most important risk factor for infection by T. gondii in cat owners.
KEY WORDS: Toxoplasma gondii, infection, toxoplasmosis, cat contact, meta-analysis.

Toxoplasma gondii has been found to be capable of
infecting all warm-blooded animals, including hu-
mans, and it is estimated that one third of the worlds
population is infected with T. gondii (Montoya and
Liesenfeld, 2004). Primary infection with T. gondii
in pregnant women can result in vertical transmission
of the parasite and may result in miscarriage, stillbirth,
premature birth, malformation, or other adverse
pregnancy outcomes (Li et al., 2014). The annual
number of global cases of congenital toxoplasmosis
was estimated to be 190,100 (95% confidence interval
[CI]: 179,300206,300) in 2013, and the global burden
of congenital toxoplasmosis was estimated at 1.20
million disability-adjusted life years (DALYs; 95%
CI: 0.761.90; Torgerson and Mastroiacovo, 2013).
Additionally, toxoplasmosis can be life-threatening in
4
These authors contributed equally to this work.
5
Corresponding author.
immunocompromised patients and can result in
toxoplasmic encephalitis (Montoya and Liesenfeld,
2004). The life cycle of T. gondii was not discovered
until 1970, when felids were found to be its definitive
hosts, and the importance of oocysts excreted in the
feces of cats was recognized as an important public
health concern (Dubey et al., 1970a, 1970b, 1970c;
Frenkel et al., 1970; Elmore et al., 2010). Felids,
particularly domestic cats, are the definitive hosts of
T. gondii, because sexual reproduction of the parasite
occurs in the gastrointestinal tract, with the result being
that infected cats pass environmentally resistant
oocysts in their feces (Lappin, 2010). These oocysts
undergo sporogony in the environment and become
infectious within 1 or 2 d, depending on temperature
and humidity (Dubey, 1998, 2010; Dubey and Frenkel,
1972). Additionally, oocysts are very robust and can
survive in the environment, depending on the envi-
ronmental conditions, for up to 1218 mo (Innes,

11
12 COMPARATIVE PARASITOLOGY, 83(1), JANUARY 2016
2010). The oocysts of T. gondii are an important source
of infection for intermediate hosts (Innes, 2010; Dattoli
et al., 2011; Bangoura et al., 2013; Lilly and Wortham,
2013), many of which are herbivores. There are several
potential sources of T. gondii infection for humans.
Non-oocyst-induced infections can occur after the
ingestion of infective tissue cysts in infected raw or
undercooked meat, from drinking tachyzoites in
unpasteurized milk (usually goat milk), by maternal
transmission, and by blood transfusion or organ
transplantation. Oocyst-induced infections occur after
drinking oocyst-contaminated water, from eating un-
washed and contaminated raw vegetables or fruits,
from eating insect and bivalve transport hosts
harboring infective oocysts, from contaminated soil
left under finger nails, or from infective oocysts
aerosoled when cleaning contaminated cat litter boxes.
Toxoplasma gondii oocysts do not stick to cat fur;
therefore, petting a cat is not a likely source of oocyst
transfer to humans. Cats do not transmit infection by
bites or scratches.
Several studies have investigated the relationship
between infection by T. gondii and cat contact, but
their conclusions differ. For example, it has been
reported that cat ownership had no significant influence
on the risk of infection, as confirmed by antibody tests
for T. gondii (Rai et al., 1999; Elmore et al., 2010;
Minbaeva et al., 2013), while other studies have
reported that people with a history of raising cats
showed a significantly higher seroprevalence for
T. gondii than did those who had no such history
(Seuri and Koskela, 1992; Liu et al., 2009; Fan et al.,
2012). A meta-analysis was applied in this study to
evaluate the association between infection by T. gondii
and cat contact because of the extremely high numbers
of domestic and feral cats in developed countries and
their potentially important role in transmitting the
parasite to humans.
MATERIALS AND METHODS
Search strategy
We searched the Wanfang database, China National
Knowledge Infrastructure (CNKI), Weipu, PubMed, and
ScienceDirect for papers published up to June 2014. Studies
were identified using combinations of the following search
terms regardless of language: cat or cats or felis or feline or
felines and Toxoplasma gondii or toxoplasmosis and
infection.
Literature citation inclusion and exclusion criteria
Citations were screened according to the following
inclusion criteria: (i) a cohort or case-control study that
was related to our theme; (ii) the included subjects were
human beings and not animals; and (iii) the diagnosis of
infection by T. gondii was based on the detection of parasite-
specific immunoglobulin G/immunoglobulin M (IgG/IgM)
in an enzyme-linked immunosorbent assay (ELISA),
western blot, or indirect fluorescent antibody test; the
detection of positive reactions in hemagglutination assays,
the latex agglutination test, modified direct agglutination
test, complement fixation test, Sabin-Feldman dye test, or
indirect hemagglutination; a positive polymerase chain
reaction (PCR) test of parasite DNA; or observation of
parasites following inoculation of placenta and cord blood
into mice. When more than one article was based on a study
of the same population, the one with the highest quality (i.e.,
the Science Citation Index [SCI] was highest or the citations
of the article were highest) was chosen.
Articles were excluded from this study if (i) the paper was
a review or a descriptive study; (ii) the data were duplicates
or the study only presented the final results without the raw
data; or (iii) the study included pet cats and other animals
but the data related to cat contact were not provided
separately.
Data extraction
The following information was extracted from each
study: first author, publication year, location of the
study, the number of cases and controls, and diagnostic
methods. Two reviewers independently collected the data
and reached a consensus after discussing any controver-
sial literature.
Statistical analysis
The risk of infection by T. gondii was estimated using the
odds ratio (OR) with 95% confidence intervals (95% CI).
It was considered significant if the P value was less than
0.05 (P , 0.05). In the forest plots (see below), an OR . 1
represented a risk effect, and an OR , 1 represented
a protective effect. The statistical heterogeneity of the results
was appraised using a x2-based Q test and I2 statistic
(Higgins and Thompson, 2002). 2
Q was calculated as
follows: Q~Ski~1 wi Ti 2 { SwSwi Ti i , where wi means the weight
value of the i of all of the studies and is defined as the
2
inverse of the variance (1/Si ), and Ti represents the effect
size (OR) introduced in the article. Q obeys a x2 distribution
with a degree of freedom k 2 1, and if the value of Q is
larger, the corresponding value of P is smaller. If the P value
is less than 0.05, heterogeneity exists among the studies.
A random-effects model was adopted to analyze the data.
I2 5 100% 3 (Q 2 df)/Q, where Q represents the Q
statistic, and df equals k 2 1. If the I2 is larger, the
heterogeneity among studies is larger, and if the I2 is larger
than 50%, the random-effects model was adopted. The
Q-test is easily affected by a change in the sample size, and
compared with I2, the power of the Q-test was lower. If the
sample size is small, a false negative result may occur. The
I2 statistic is not affected by a change in the included
articles, and the result of the heterogeneity test is more
robust after correcting for the degrees of freedom. In our
study, the heterogeneity was considered not significant if
P . 0.05 and I2 , 50%, and the fixed-effects model was
used; otherwise, the random-effects model was employed.
All analyses were conducted using the Stata software,
version 11.0 (Stata Corporation, College Station, Texas,
U.S.A.), and publication bias was considered significant
WEI ET AL.META-ANALYSIS ON RELATIONSHIP BETWEEN CAT AND INFECTION BY TOXOPLASMA GONDII 13

Table 1. Studies involving infection rate by Toxoplasma gondii in immune-competent people with cat contact.

First author Year Area Diagnosis of infection by T. gondii Contact yes/no

Santos, TR 2009 Jauru microregion, southwest of Mato Grosso, Brazil IFAT* 96/20
Jafari, R 2012 Tabriz, Iran Positive IgG 42/128
Rey, LC 1999 Fortaleza, Brazil Positive IgG 256/741
Negash, T 2008 Nazaret, Ethiopia Positive IgG 30/35
Lopes, AP 2012 North Portugal Positive IgG and IgM 110/291
Bobic, B 1998 Belgrade, Yugoslavia Positive IgG 320/837
Gebremedhin, EZ 2013 Central Ethiopia Positive IgG 255/170
Kolbekova, P 2007 Czech Republic Positive IgG and IgM 1,157/2,091
Fan, CK 2001 Two offshore islands near Taiwan, China Latex agglutination (LA) test 132/834
Hofhuis, A 2011 Netherlands Positive IgG 1,625/5,320
Tizard, IR 1977 Ontario, Canada Positive IgG 68/72
Minbaeva, G 2013 The Kyrgyz Republic Positive IgG 303/759
Jones, JL 2001 U.S.A. Positive IgG 2,473/15,170
Pereira, LH 1992 Nova Scotia, Canada Antibodies 337/649
Alvarado-Esquivel, C 2012 Durango, Mexico Positive IgG and IgM 80/76
Fu, B 2004 Jining, Zhaozhuang and Linyi, China Positive IgG 94/221
Su, CK 2002 Nanning, China Test antibodies with IHA{ 216/182
DiGiacomo, RF 1990 University of Washington, U.S.A. Antibodies 80/36

* Antibodies detected by indirect fluorescent antibody test (IFAT).

{ IHA, indirect hemagglutination assay.

if P , 0.05 according to either Beggs test or Eggers
test (Egger et al., 1997).
Sensitivity analysis
A sensitivity analysis indicates the degree to which
a single study affected the result of the meta-analysis. In
our study, the overlap of 95% CI was observed in a forest
map, and if the 95% CI of one study had a slight overlap
with other studies, a reanalysis excluding this study was
performed to evaluate the robustness of the combined result.
If the combined result changed significantly, we excluded
the study and analyzed the reason for the change. If
the combined result did not change substantially, the study
was included. In a meta-analysis, a funnel plot can be
used both to investigate whether all studies come from
a single population and to search for publication bias. In our
study, the x-axis of the funnel plot represents the standard
error of the log10 OR, and the y-axis represents the log OR.
care specialists) and cat contact; 21 papers concerned
people identified as cat owners; 3 papers were about
people contacting cats in their neighborhoods; and
4 papers were on the rate of contacting cats and the
development of antibodies to T. gondii versus cases that
remained negative for T. gondii. Among these 46
included articles, some were repeatedly categorized
because they met more than 1 category criteria. Details
of the first author, publishing year, area, diagnostic
methods, and number of subjects contacting cat(s) are
shown in Table 1. A flow diagram of the selection and
nature of the studies is shown in Figure 1.

RESULTS
Study characteristics
Of the 1,813 articles initially detected using our
criteria, 46 were included. The results from these studies
were weighted according to the category and available
data in each paper. Eighteen studies were about
infection rate by T. gondii in the general population
contacting cats; 17 studies were about immune-
weakened people contacting cats, including pregnant
women, children, those infected by human immunode-
ficiency virus (HIV) the elderly, and individuals
with severe mental illness; 5 studies examined people
with special occupations (veterinary personnel, farmers,
produce pickers, waste workers, swine farmers, and cat Figure 1. Flow diagram of the selection of the studies.
14 COMPARATIVE PARASITOLOGY, 83(1), JANUARY 2016

Figure 2. Forest plot of the relationship between infection by Toxoplasma gondii and cat contact. a. In immune-competent
individuals. b. In pregnant women and immunosuppressed individuals. c. In people with special occupations. The dots and
whiskers represent the odds ratios (ORs) and 95% confidence intervals (CIs) of individual studies. The gray box reflects the
sample size of each study, and the diamond describes the pooled OR value and the confidence interval of all the studies.

Quantitative synthesis and heterogeneity In pregnant women and immune-suppressed peo-

analysis
Comparison of chances of infection by T. gondii
between people contacting and not contacting cats
classified by health status (immune competent or
immune suppressed/pregnant) and occupation: In
healthy individuals, the chances of contracting an
infection by T. gondii had a significant association with
cat contact (P 5 0.001, P , 0.05), with an OR of 1.413
(95% CI: 1.1631.717), which was analyzed with
a random-effects model (Fig. 2a; Table 1). The rate of
infection by T. gondii in people in the general
population contacting cats was 1.413 times higher
than that in people in the general population who
reported not contacting cats.
ple, such as children, HIV-infected individuals, the
elderly, and individuals with severe mental illness,
the results were interesting. In a sensitivity analysis
including one study (Fan et al., 2012), the infection
rate by T. gondii had a significant association with
contacting cats (P 5 0.002), with an OR of 1.558
(95% CI: 1.1732.069) when analyzed with the
random-effects model. However, when excluding
this study from the sensitive analysis, the pooled
OR was not significantly affected (OR 5 1.443;
95% CI 5 1.1341.837; P 5 0.003) according to the
random-effects model (Fig. 2b; Table 2). This result
indicates that the rate of infection by T. gondii in the
group of people contacting cats was higher than that

Table 2. Studies involving infection rate by T. gondii in pregnant women and immune-suppressed people with
cat contact.

First author Year Area Diagnosis of infection by T. gondii Contact yes/no

Sharif, M 2010 Sari, Iran Positive IgG 664/539

Lopes-Mori, FM 2013 Parana, Brazil Positive IgG 1,376/774
Messerer, L 2014 Pasteur Institute, Algeria Positive IgG, IgM, and parasite detection* 86/404
Fallah, M 2008 Hamadan, Iran IFA{ 110/466
Souza, WJ 1987 Rio de Janeiro Positive IgG 96/144
Zemene, E 2012 Jimma, Ethiopia Positive IgG and IgM 59/142
Walle, F 2013 Bahir Dar, Ethiopia Positive IgG and IgM 72/31
Doudou, Y 2014 Kinshasa, Democratic Republic of Congo Positive IgG and IgM 113/567
Dattoli, VC 2011 Salvador, Brazil Positive IgG 215/1,002
Jones, JL 2005 Guatemala Positive IgG 253/681
Ertug, S 2005 Aydin, Turkey Positive IgG 8/345
Flatt, A 2013 Central London, U.K. Positive IgG 358/2,252
Etheredge, GD 2004 Eastern Republic of Panama Positive IgG 254/505
Fakhfakh, N 2013 Tunisia Positive IgG and IgM 455/1896
Huang, MC 1996 Tianyang, China IHA{ 229/1518
Chintapalli, S 2013 Andhra Pradesh, India Positive IgG 20/32
Fan, CK 2012 Capital areas of Democratic Republic Test antibodies by latex 126/115
of Sao Tome and Prncipe agglutination (LA) test

* Search for the parasite was made by inoculation of the placenta and cord blood into mice.
{ Test antibodies by indirect fluorescent antibody (IFA) test.
{ IHA, indirect hemagglutination assay.
WEI ET AL.META-ANALYSIS ON RELATIONSHIP BETWEEN CAT AND INFECTION BY TOXOPLASMA GONDII 15

Table 3. Studies involving infection rate by T. gondii in people with special occupations and cat contact.

First author Year Area Diagnosis of infection by T. gondii Contact yes/no

Seuri, M 1992 Central and northern Finland Positive IgG 153/254

Alvarado-Esquivel, C 2008 Durango, Mexico Positive IgG and IgM 71/102
Weigel RM 1999 Illinois, U.S.A. Modified direct agglutination test 128/46
DiGiacomo, RF 1990 University of Washington, U.S.A. Antibodies 30/86
Sengbusch, HG 1976 12 western New York State small IFA and IHA 60/60
animal hospitals and State
University College at Buffalo, U.S.A.

of people not contacting cats, and that the meta-
analysis results were robust.
In people with special occupations, which included
1 study (Sengbush and Sengbush, 1976), the infection
rates by T. gondii between people contacting cats
and those not contacting cats were not significantly
different (P 5 0.135). After further analysis, we
determined that the publication year of the Sengbush
and Sengbush (1976) article was too early and that the
control population (volunteers from college summer
session students) was inappropriate for our research
aim (whether cat contact was the risk factor for the
people with special occupations), resulting in exclu-
sion of the article. After this exclusion, the infection
prevalence of T. gondii had a significant association
with cat contact (P 5 0.013), with an OR of 1.493
(95% CI: 1.0882.049) according to the fixed-effects
model (Fig. 2c; Table 3).
Comparison of chances of infection by T. gondii
between contacting and not contacting cats according
to type of contact: For cat owners, including 1 study
(Fan et al., 2012), the chances of infection by T. gondii
had a significant association with cat contact
(P 5 0.000), with an OR of 1.421 (95% CI: 1.174
1.721) according to the random-effects model. As
shown in Figure 2b, the overlap between the 95% CI
of the data extracted from the study performed by Fan
et al. (2012) and that of the other studies is very small,
which suggests that heterogeneity may exist among
studies. Therefore, a further analysis excluding this
study was performed. After excluding this study in the
analysis, the pooled OR was not significantly affected
(OR 5 1.386, 95% CI: 1.1601.614; P , 0.000)
according to the random-effects model (Fig. 3a;
Table 4). This result showed that the rate of infection
by T. gondii in the group of cat owners was higher than
that of people not contacting cats, and the results were
not significantly changed by 1 papers results.
Relative to people contacting cats in their neigh-
borhood, the infection rates by T. gondii between
people contacting cats and not contacting cats were
not significantly different (P 5 0.104), and the OR
was 1.544 (95% CI: 0.9142.606) according to the
random-effects model (Fig. 3b; Table 5).
Analysis of the relationship between cat ownership
and infection by T. gondii indicated that there was no
significant difference (P 5 0.389) in the proportions

Figure 3. Forest plot of the relationship between infection by T. gondii and cat contact according to type of contact. a.
Cat owners. b. Cats in the neighborhood. Please refer to Figure 2 about the symbols in this figure.
16 COMPARATIVE PARASITOLOGY, 83(1), JANUARY 2016

Table 4. Studies involving infection rate by T. gondii in populations of people that own cat(s).

First author Year Area Diagnosis of infection by T. gondii Contact yes/no

Gebremedhin, EZ 2013 Central Ethiopia Positive IgG 258/167

Dattoli, VC 2011 Salvador, Brazil Positive IgG 215/1,002
Kolbekova, P 2007 Czech Republic Positive IgG and IgM 1,157/2,091
Jones, JL 2005 Guatemala Positive IgG 253/681
Fan, CK 2001 Two offshore islands from Taiwan, China Latex agglutination (LA) test 132/834
Hofhuis, A 2011 Netherlands Positive IgG 1,625/5,320
Tizard, IR 1977 Ontario, Canada Positive IgG 68/72
Seuri, M 1992 Central and northern Finland Positive IgG 153/254
Ertug, S 2005 Aydin, Turkey Positive IgG 8/345
Flatt, A 2013 Central London, U.K. Positive IgG 358/2,252
Etheredge, GD 2004 Eastern Republic of Panama Positive IgG 254/505
Minbaeva, G 2013 The Kyrgyz Republic Positive IgG 303/759
Jones, JL 2001 U.S.A. Positive IgG 2,473/15,170
Pereira, LH 1992 Nova Scotia, Canada Antibodies 337/649
Alvarado-Esquivel, C 2012 Durango, Mexico Positive IgG and IgM 80/76
Chiang, TY 2012 Taiwan, China Enzyme immunoassays and real-time PCR 187/1593
Alvarado-Esquivel, C 2008 Durango, Mexico Positive IgG and IgM 71/102
Alvarado-Esquivel, C 2012 Durango, Mexico Positive IgG and IgM 202/280
Alvarado-Esquivel, C 2007 Durango, Mexico Positive IgG and IgM 116/314
DiGiacomo, RF 1990 University of Washington, U.S.A. Antibodies 80/36
Fan, CK 2012 Capital areas of Democratic Test antibodies by latex 126/115
Republic of Sao Tome and Prncipe agglutination (LA) test

Table 5. Studies involving infection rate by T. gondii in people and the presence of cat(s) in the neighborhood.

First author Year Area Diagnosis of infection by T. gondii Contact yes/no

Chiang, TY 2012 Taiwan Immunoassays and real-time PCR* 451/1,313

Alvarado-Esquivel, C 2012 Durango, Mexico Positive IgG and IgM 323/158
Alvarado-Esquivel, C 2007 Durango, Mexico Positive IgG and IgM 155/273

* PCR, polymerase chain reaction.

of cat ownership between infected and uninfected DISCUSSION

individuals, with an OR of 1.375 (95% CI: 0.666 In our study, the association of infection by
2.840) according to the random-effects model (Fig. 4; T. gondii and cat contact was evaluated with a meta-
Table 6). A summary of the meta-analysis results is analysis. The results confirmed that contacting cats
shown in Table 7. was a risk factor for infection by T. gondii in humans.
The risk of infection was relatively higher in the
Publication bias
In the analysis of the association between chances
of infection by T. gondii and contacting cats in cat
owners, the publication bias was significant (Eggers
test 5 0.013; Fig. 5a). To evaluate the effect of
publication bias on the result, the trim-and-fill
method was adopted. After the analysis, the results
showed that there was no trimming performed or data
change (Fig. 5b). This result suggested that a partic-
ular degree of publication bias existed but that the
analytic result of the association between chances of
infection by T. gondii and owning cat(s) was reliable. Figure 4. Comparison of the proportions of cat owner-
No publication bias was found in the other analyses ship between people infected and uninfected by T. gondii.
(data not shown). Please refer to Figure 2 for the symbols in this figure.
WEI ET AL.META-ANALYSIS ON RELATIONSHIP BETWEEN CAT AND INFECTION BY TOXOPLASMA GONDII 17

Table 6. Studies involving the rate of contact with cat(s) between patients with diagnosed toxoplasmosis
and controls.

First author Year Area Diagnosis of infection by T. gondii Cases/controls

Chiang, TY 2014 Taiwan, China Positive IgG and IgM and Real-time PCR* 30/224
Baril, L 1999 France Positive IgG and IgM 80/80
Cook, AJ 2000 Naples, Lausanne, Copenhagen, Oslo, Positive IgM 252/852
Brussels, Milan, Italy
James, BO 2013 Nigeria Positive IgG and IgM 140/140

* PCR, polymerase chain reaction.

contact group than in the control group (the general
population), as well as in people with weakened
immune systems, in people with special occupations,
and in cat owners, with ORs of 1.396, 1.627, 1.493,
and 1.421, respectively. According to previous
studies, the ORs with 95% CI for infection by T.
gondii transmitted through various routes were the
following: having cats in the household resulted in
an OR of 2.9 (95% CI: 1.17.9) or an adjusted OR
of 2.0 (95% CI: 1.23.2; Chiang et al., 2012, 2014);
undercooked pork consumption resulted in an OR of
2.9 (95% CI: 1.36.5), raw clam consumption had an
OR of 3.7 (95% CI: 1.49.9; Chiang et al., 2012),
and raw mussel consumption had an OR of 5.3
(95% CI: 1.519.1; Chiang et al., 2014). Based on
our analysis and these other reported results in-
volving differing infection routes in humans, cat
contact may not be the most important risk factor
associated with infection by T. gondii. This result
may be due to the following: (i) It is possible that
the persons who were interviewed had difficulties
recalling events in their childhood pertaining to
these risk factors (James et al., 2013); (ii) most cats
contacted by people were domestic cats, for which
their living environment and source of food were
highly variable; (iii) it is difficult to confine cats
when they are outside in neighborhoods, and such
cats may excrete oocysts and contaminate the
environment where there were no cat owners and
where people who were not a cat owner then
became infected; and (iv) oocysts survive a long
time in the environment and are distributed by water
runoff after storms, thereby potentially infected
people far away from the original location regardless
of cat presence. Moreover, insects and other
invertebrates can serve as transport hosts for oocysts
of T. gondii.
Comparison of chances of infection by T. gondii
between those contacting or not contacting cats in
the neighborhood and comparison of cat ownership
proportions between the groups infected and un-
infected by T. gondii did not show any significant
differences (P . 0.05) in each case. This finding may
be due to the few relevant papers available and the
small number of samples included in those that were
relevant.
Infection by T. gondii in pregnant women and
immunocompromised patients may result in serious
illness (Montoya and Liesenfeld, 2004; Li et al.,
2014), and contacting cats will increase the risk of
infection (Liu et al., 2009; Walle et al., 2013).
Pregnant women and HIV/acquired immune deficien-
cy syndrome (AIDS) patients should practice general
hygiene measures that lessen the chances of acquiring
T. gondii. This meta-analysis confirmed that contact-
ing cats was a significant risk factor for infection by
T. gondii. The risk of infection was significantly
higher in those people who had cat contact than in

Table 7. Summary of meta-analysis results.

Classification Number of articles OR 95% CI* P-value

Immune competent 18 1.413 1.1631.717 P 5 0.001

Immune suppressed/pregnant 17 1.558 1.1732.069 P 5 0.002
Special occupation 5 1.493 1.0882.049 P 5 0.013
Cat ownership 21 1.421 1.1741.721 P 5 0.000
Cats in the neighborhood 3 1.544 0.9142.606 P 5 0.104
Proportion of cat ownership in T. gondii
infected individuals and uninfected individuals 4 1.375 0.6662.840 P 5 0.389

* CI, confidence interval.

18 COMPARATIVE PARASITOLOGY, 83(1), JANUARY 2016
Figure 5. Funnel plot showing publication bias. a. The analysis of the association between chances of infection by T.
gondii and contacting cats by cat owners. b. The funnel plot of the publication bias analysis performed using the
nonparametric trim-and-fill method in Stata.
those reporting no cat contact in the general population
as well as in people with weakened immune systems,
people with special occupations, or cat owners. While
contact with cats may not be the most substantial risk
factor for infection by T. gondii in humans, infection
by T. gondii in pregnant women and immunocompro-
mised patients can cause serious results, and cat
contact increases this risk.
ACKNOWLEDGMENTS
This study was supported by funding from the
National Natural Science Foundation of China (Nos.
81572012, 81271866), Guangdong Province Univer-
sities, and the Colleges Pearl River Scholar Funded
Scheme (2014). The study was conceived and designed
by H.J.P. and D.S.L. H.X.W., C.H., and P.L.Y.
performed the experiments, while H.X.W., C.H., and
P.L.Y. analyzed the data. H.X.W., C.H., P.L.Y., and
D.S.L. contributed reagents/materials/analysis tools,
and H.J.P., H.X.W., and C.H. wrote the paper.
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