Review TRENDS in Parasitology
3 March 2006
Toxoplasmosis: beyond animals to
humans
Yaowalark Sukthana
Faculty of Tropical Medicine, Mahidol University, 420/6 Rajvithi Road, Bangkok 10400, Thailand
The parasitic zoonosis toxoplasmosis, which was poorly
understood before the advent of the HIV epidemic, has
become a major clinical problem worldwide. Humans
acquire toxoplasmosis from cats, from consuming raw or
undercooked meat and from vertical transmission to the
foetus through the placenta during pregnancy. Studies of
the unique environmental factors in various commu-
nities indicate the important roles that eating habits and
culture have on the transmission of this infection. The
socioepidemiological aspects of toxoplasmosis are
thought to be important contributing factors for the
spread of this disease. Preventative measures should
consider the cultures and beliefs of people in various
communities more than solving poverty and giving
orthodox health education.
Toxoplasma gondii
Toxoplasma gondii can infect humans, and warm-blooded
domestic and wild animals such as birds and rodents. In
1908, Nicolle and Manceaux (from the Pasteur Institute in
Tunisia) isolated a new parasite from the African rodent
Ctenodactylus gundi, differentiated it from Leishmania
and named it T. gondii a year later [1]. The first congenital
case of toxoplasmosis was described in 1923 and the first
adult case was diagnosed in 1940 [2]. However, its life
cycle was not known until 1969 [1]. The development of
the dye test by Sabin and Feldman in 1948 [2] was an
important milestone and it is now the ‘gold standard’
serological method for diagnosing toxoplasmosis [3].
Cats and other felids are the only definitive hosts of
Toxoplasma in which sexual reproduction occurs to
produce infective oocysts. Warm-blooded animals,
including humans, are intermediate hosts that harbour
tissue cysts in their bodies. Although asymptomatic in
normal hosts, T. gondii can cause severe disease in
immunodeficient subjects. Since the HIV–AIDS pandemic,
concurrent Toxoplasma infection has become an import-
ant health problem, with its frequency increasing
worldwide during the 1980s. Patients with toxoplasmic
encephalitis were first documented in Thailand in 1992,
and the number of cases has been increasing annually,
particularly in the northern part of the country [4].
Early diagnosis is, therefore, crucial. However, diagnosis
of toxoplasmosis is not straightforward because of
pleomorphic clinical manifestations. Laboratory diagnosis
is important in primary infections, in pregnant women and
Corresponding author: Sukthana, Y. (tmymv@mahidol.ac.th).
Available online 30 January 2006
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Vol.22 No.
in congenital toxoplasmosis, whereas clinical manifestations
are more likely to be obvious in late reactivated cases (e.g.
ocular toxoplasmosis) and in immunocompromised individ-
uals. Practical strategies for investigating and interpreting
results should be focused for each of the clinical groups.
Diagnosis and management of congenital infection
The diagnosis of congenital toxoplasmosis relies mainly on
finding specific antibodies in patient serum and on the
isolation of T. gondii DNA from amniotic fluid. Many
serological screening methods can detect IgG and IgM that
are specific for T. gondii. When confirmation of initial serology
is required, ranges of secondary tests are available,
including the Sabin–Feldman dye test and a test for specific
IgM or other immunoglobulin such as IgA, IgE and IgG
avidity [5,6]. The sensitivity and specificity of screening
methods range from 95.6% to 100% and from 94.8% to 99.8%,
respectively [7–10], and they are commercially available and
easy to perform. However, they should be used with caution
for screening pregnant women living in an area with a low
prevalence of Toxoplasma infection, such as in Thailand.
Sukthana et al. [10] found that the commercial latex
agglutination test showed 100% sensitivity and 94.8%
specificity compared with the Sabin–Feldman dye test but
its positive predictive value was only 71.3%. Therefore, the
number of false seropositive cases would be higher than it
ought to be and clinicians would miss a certain number of
seronegative women who should be given preventative
measures to protect them from T. gondii infection during
pregnancy. Therefore, confirmation of seropositivity
is needed.
The immunological response to T. gondii is unique in that
IgM appears first, approximately one or two weeks after
infection, closely followed by IgA and IgE [11]. In most cases,
these acute-phase immunoglobulins peak after approxi-
mately two months. The time at which IgM can no longer
be detected varies depending on the sensitivity of the assay
employed but it is usually between six and nine months after
infection. IgG appears after IgM and reaches maximal levels
after four months, then declines to lower levels over the next
12–24 months, whereas IgG persists at a low-titre level for the
remainder of the subject’s life [11]. Based on all recent data
and antibody dynamics, pregnant women with high positive
titres for Toxoplasma IgG and IgM, or seroconverted mothers
will be offered additional testing using IgA, IgE or IgG avidity
to try to determine the time of primary infection more
accurately [5,6,12,13]. Low avidity is indicative of recent
infection. However, the current consensus is that high IgG
138 Review TRENDS in Parasitology
avidity can be used to rule out recent infection. An IgG avidity
index higher than 0.300 indicates an infection that was
acquired more than four months before testing [14,15].
In 2001, a multicentre evaluation of primary T. gondii
infection in pregnant women from 20 European reference
centres recommended that a combination of two assays,
each 95% specific, would reach a net specificity of 99.75%.
A pair of positive results would be regarded as a positive
diagnosis. Furthermore, the best assay combination was
the measurement of IgM and IgG avidity, which gave a
diagnostic result with specificities of w99% while main-
taining diagnostic sensitivities at 95% or higher [6].
In the past decade, the use of PCR has facilitated major
improvement in the diagnosis of many parasitic infections,
including toxoplasmosis. T. gondii DNA can be detected in
amniotic fluid, foetal tissue, blood, cerebrospinal fluid
(CSF) and other clinical specimens. Primers are selected
from either the P30 or the B1 gene [16–18]. The sensitivity
of amniotic fluid PCR can be increased from 81% to 91%
when combined with mouse inoculation [17].
The routine prenatal screening of all pregnant women
remains controversial and the cost-effectiveness must be
taken into account, especially in areas with a low prevalence
of toxoplasmosis. Although the screening of all pregnant
women would decrease the incidence of congenital
toxoplasmosis compared with targeted screening only when
foetal anomalies are noted, it would cause 18.5 pregnancy
losses from invasive prenatal testing for each child with
congenital toxoplasmosis prevented. Even if all foetuses
identified as being affected were terminated, there would still
be 12.1 pregnancy losses for each case of congenital
toxoplasmosis avoided [19]. Consequently, apart form France
and Austria, postnatal or neonatal screening is preferred in
countries with lower prevalences [20–22].
Recently, the management of congenital toxoplasmosis
has improved because the early diagnosis of Toxoplasma
infection in mother, foetus and newborn can be made by a
combination of serology and PCR methods [23]. Therefore,
the treatment of congenital infection is now initiated before
birth. However, the prevention of infection in pregnant
women should be emphasized by using education about
hygiene and avoidance of the risks of infection. The more time
that elapses after maternal seroconversion and before the
start of treatment, the greater the risk of congenital infection.
In 2001, Gilbert et al. [24] suggested that treatment starting
within four weeks after maternal seroconversion did not
increase the risk of congenital infection, whereas it was 1.29
and 1.44 times higher if treatment commenced between four
and seven weeks, and more than eight weeks, respectively.
When foetal infection is proven, treatment by pyrimethamine
and sulfadiazine is recommended until birth. Folinic acid
should always be administered to prevent bone marrow
suppression. Therapy using pyrimethamine and sulfona-
mides is continued immediately after birth in infants who are
known, from the prenatal diagnosis, to be infected. Alterna-
tive drugs include spiramycin and clindamycin for patients
with early pregnancy. A clinical profile of the infant is
completed by ophthalmological examination and transfonta-
nelle ultrasound scan.
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Vol.22 No.3 March 2006
Diagnosis and management of toxoplasmic reactivation
in HIV–AIDS
For clinically suspected central nervous system (CNS)
toxoplasmosis in AIDS patients, the Centers for Disease
Control and Prevention (http://www.cdc.gov/) criteria should
be applied for presumptive diagnosis. These criteria consist
of: (i) the recent onset of a focal neurological abnormality that
is consistent with intracranial disease or reduced conscious-
ness; (ii) evidence from brain imaging of a lesion with mass
effect or a lesion that appears on a radiograph after injection
of a contrast medium; and (iii) positive serum antibody to T.
gondii or successful response to treatment for toxoplasmosis
[25]. Computerized tomography and magnetic resonance
imaging are preliminary diagnostic tools for clinicians,
although neuroimaging often cannot differentiate cerebral
toxoplasmosis from tumours such as lymphoma. Single-
photon emission computerized tomography could provide a
more precise diagnosis but it is costly and not widely available
at present [26,27].
Serum and intrathecal levels of T. gondii antibody are
always low [28] and parasite isolation from blood and CSF
is successful in !40% of CNS toxoplasmosis cases.
However, in suspected cases, even a low titre of T. gondii
antibody aids the diagnosis. By contrast, when T. gondii
antibody is negative, toxoplasmic encephalitis is unlikely
to have occurred. Brain biopsy is often impracticable,
although direct tissue staining with haematoxylin–eosin
and enhanced by immunocytochemistry could be
applied [29].
DNA-amplification-based techniques greatly contrib-
ute to the diagnostic improvement. Blood PCR as a single
test is not sensitive; CSF PCR has a higher sensitivity
(50–100%) and specificity (97–100%). Repeated testing
and combining both CSF and blood PCR enhance
sensitivity [30–32]. Stage-specific oligonucleotide primers
could provide a more precise laboratory diagnosis of
reactivated toxoplasmic encephalitis, especially in recur-
rent cases [33,34].
The treatment of suspected toxoplasmic encephalitis
using a combination of pyrimethamine and sulfadiazine
with folinic acid is effective. Unfortunately, up to 40–50%
of patients treated develop adverse effects that require a
change of therapy. Clindamycin is an alternative drug in
the case of intolerance to sulfa- compounds [35]. Mainten-
ance therapy using half the dose of therapeutic drugs to
prevent recurrent toxoplasmic encephalitis is necessary
because the available drugs are ineffective against the
tissue cyst that could later be reactivated [35]. The use of
highly active antiretroviral therapy (HAART) suppresses
the HIV viral load and improves the CD4CT-cell count,
followed by a strong reduction of opportunistic infections,
including toxoplasmic encephalitis. The influence of
HAART in reducing toxoplasmic encephalitis has been
confirmed in a randomized, controlled clinical trial and
there is no increase in risk of developing this disorder even
if drug prophylaxis is discontinued* [36].
* J.M. Miro, et al., abstract 796, 10th World AIDS Conference on Retroviruses and
Opportunistic Infection, Boston, February 2003.
 Review TRENDS in Parasitology Vol.22 No.3 March 2006 139

Table 1. Seropositivity rates in Europe, the Americas and infected meat or consuming food contaminated with
Southeast Asia oocysts from cat excreta [37].
Continents and Year Seropositivity (%) Refs A European multicentre study that included selected
countries
cities in Belgium, Denmark, Italy, Norway, Switzerland
Western Europe
Austria 1998 43 [46] and the UK identified the consumption of undercooked
Belgium 1997 50 [47] meat as the strong risk factor for acquiring a T. gondii
France 2001 Up to 75 [39] infection [38]. Consuming raw pork and tasting raw meat
Germany 2004 26–54 [48]
Italy 2001 18–60 [39] during meal preparation were the principal risk factors in
The Netherlands 2004 40.5 [49] Poland [39]. These risk factors have also been associated
Spain 2004 28.6 [50] with seroconversion for T. gondii in case-control studies of
Switzerland 1995 46 [51]
Scandinavia
healthy adults in France [40], Yugoslavia and the USA
Denmark 1999 27.8 [52] [39]. However, whereas the consumption of raw or
Finland 1995 20.3 [53] undercooked meat was consistently identified as a risk
Norway 1998 10.9 [54]
factor, the relative importance of the risk factor and the
Sweden 2001 14.0–29.4 [22]
Central and Eastern type of meat associated with it varied among different
Europe countries (Table 2). These findings might reflect differ-
Croatia 2000 38.1 [55] ences in the eating habits of consumers or different
Poland 2001 46.4–58.5 [56]
Slovenia 2002 34 [57] prevalences of infection in meat-producing animals in
UK 1998 57–93 [58] the affected regions [39].
Yugoslavia 1992 23–33 [59] Domestic cats have a key role in the epidemiology of
The Americas
USA 2004 16–40 [60]
T. gondii infection. Cats and other feline species can
Central America become infected with T. gondii either by ingesting
Costa Rica 1996 76 [61] infectious oocysts from the environment or by ingesting
Cuba 1993 60 [62]
tissue cysts from an intermediate host through feeding on
Mexico 2001 35 [39]
Panama 1988 90 (at 60 years of age) [63] food scraps that contain meat or viscera of livestock or
South America game animals. Depending on the host species, the
Argentina 2001 72 [39] geographic area and the season of the year, up to 73% of
Brazil 2001 59 [39]
West Indies 1991 29.7 [64] small rodents and up to 71% of wild birds might be
Southeast Asia infected with T. gondii [39]. The prepatent period in cats is
Indonesia 2000 58a [65] short and, after a primary infection with T. gondii,
Malaysia 2004 44.8 [66]
Thailand 1992, 1997, 2.3–21.9 [67–70]
domestic cats can shed large numbers of oocysts into the
2000, 2001 household, thereby putting their owners at risk of
a
Male:female ratioZ63:52. infection. Stray or domestic cats that are allowed to
roam about could contaminate the environment with
Epidemiology and transmission oocysts; this might affect livestock that will later be
Geographic distribution slaughtered for human consumption.
T. gondii is found worldwide but its prevalence is uneven Antibody to T. gondii can be detected in up to 74% of the
among people of different countries in the same continent, adult cat population, depending on the type of feeding and
such as those in Western and Central Europe and in whether the cats are kept indoors or outdoors [41].
Southeast Asia (Table 1). Seroprevalences are usually higher in stray or feral cats
than in cats living in an urban or suburban environment.
Between 9% and 46% of pet cats in Europe, South America
Transmission to humans and the USA showed serological evidence of past exposure
Humans become infected with toxoplasmosis mainly by to T. gondii, whereas seroprevalences of T. gondii infection
eating uncooked meat that contains viable tissue cysts or have been estimated to be 6–9% in Asia [39,41].
by ingesting food or water contaminated with oocysts from In Central and South America, where levels of T. gondii
the faeces of infected cats. A high prevalence of infection in infection are high, transmission by consumption of tissue
France has been related to a preference for eating raw or cyst can be excluded because meat is usually well cooked
undercooked meat, whereas it has been related in Central [41]. Access for cats to the outdoor environment, and
America to large numbers of stray cats in a climate that feeding cats with leftovers or with raw viscera and raw
favours the survival of oocysts. A major concern is whether meat were the risk factors for human infection in Mexico
acquired toxoplasmosis is mainly the result of consuming and Brazil [42,43]. A study of residents and workers on

Table 2. Percentage of Toxoplasma infection in humans associated with types of meat consumed
Country Beef (%) Pork (%) Lamb (%) Salami (%) Refs
Belgium 6 2 10 10 [38]
Denmark 27 2 8 4 [38]
France ORZ5.5; (95% CI: 1.1–27.0) – ORZ3.1; (95% CI: 0.85–14.00) – [40]
Italy 12.5 3 0.5 12.5 [38]
Norway 19 3 21 3 [38,71]
Switzerland 8 13 10 5 [38]

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140 Review TRENDS in Parasitology
swine farms in Illinois (USA) showed that canine infection
with T. gondii increases the risk of human infection and
that contact with soil is a probable mechanism of
transmission [44]. The increased risk of seropositivity in
human males is attributed to less attention being paid to
cleanliness in food preparation and consumption than
in females.
In Thailand, cats are kept as pets but they are allowed
to roam freely outdoors. They are rarely trained to
defecate in litter boxes and, thus, do so anywhere, from
the backyard to the roof of the house. Buddhism is the
major religion in Thailand and it has a vital role in Thai
society. Belief in the five precepts of Buddhism, one of
which states that killing is sinful, and practices such as
never killing, or allowing the killing of, unwanted pets
lead to unwanted pet dogs and cats being abandoned in
temples, where monks are obliged to care for them
(Figure 1). It is estimated that w20 000 dogs and
w10 000 cats are left in 500 Buddhist temples in Bangkok
(Thailand).
These animals can roam everywhere in temple grounds
at any time, even when religious functions are being
performed. They are fed with leftover food that, although
plentiful, might not be hygienic. There is no regular
veterinarian visit and no antiparasitic drugs are pre-
scribed. The overcrowded conditions make Buddhist
temples a place of risk for acquiring zoonotic infection.
A seroepidemiological study of T. gondii in cats and
their owners in the metropolitan area of Bangkok was
conducted involving community households and those in
Buddhist temples, covering an area of 106.6 km2
containing 494 931 inhabitants [37]. Serum samples
were collected from 327 household members, monks,
novices and nuns living in the temples and from 315
stray cats in the temple boundary. It was found that
7.3% of the cats studied and 6.4% of the humans
studied were seropositive for Toxoplasma antibody. The
risk of Toxoplasma seropositivity in the exposed human
group was five times that in the non-exposed group [OR
(95% CI) Z5.43 (1.28–23.04): pZ0.01]. Of the studied
cats, up to 80% defecated anywhere, and in most cases
(up to 75%) the excreta of the cats were not buried or
removed. Infected cats with unrestricted defecation
Figure 1. Abandoned cat and dog in a Buddhist temple in Bangkok (Thailand) being
looked after by an obliging monk. Photograph courtesy of Bangklao Nok Temple.
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Vol.22 No.3 March 2006
would contaminate their immediate environment and,
therefore, provided a potential source of human
infection. Thus, it seems that cat ownership is a risk
factor for Toxoplasma infection in Thailand. Risk was
increased in and around temples, particularly if
courtyards were made of earth or grass, suggesting
that ground temperature is an important determinant
of oocyst survival [37].
As mentioned, access for cats to the outdoor environ-
ment, and feeding cats with leftovers or with raw viscera
and raw meat are risk factors for human Toxoplasma
infection in Mexico and Brazil [42,43] but the situation is
different in Thailand. Thai cats eat rice and well-cooked
fish but not raw meat. They also catch rodents in response
to hunting instincts but usually not for eating. This could
explain why the prevalences of Toxoplasma infection in
cats and humans are low in Thailand, even though many
factors seem to promote transmission. Moreover, Dubey
[45] demonstrated that oocysts remain infective for only
one minute at 608C compared with 54 months at 48C.
Thus, oocysts from cat excreta deposited on hot roofs and
stone or concrete courtyards are unlikely to be successful
in disease transmission [37].
Prevention
Although consumption of infected meat and close
association with infected cats are the two main sources
of Toxoplasma infection in humans, details as to how
these are brought about differ in different countries or
even in different ethnic communities that belong to the
same country. Eating habits vary even among inhabi-
tants of the West. For example, the distribution of beef,
pork and lamb consumption in Europe is uneven
(Table 2) and there are religious differences among
Southeast Asian people (e.g. Buddhist or Islamic faith).
Even the manner in which domestic cats are kept and
fed in various communities and countries is not similar.
Cats in Thailand are not kept indoors; they roam about
and are fed on rice and cooked fish but not meat or
livestock viscera as in Mexico. Although the climate and
ground temperature in both countries are similar, the
prevalence of T. gondii in Mexico is higher than in
Thailand. In Southeast Asia, the Toxoplasma seroposi-
tivity rate is much higher in Surabaya (Indonesia), a
predominantly Islamic community in which cats are
better looked after than in Bangkok.
Addressing the problem of disease prevention should,
therefore, take into account ethnic and cultural differ-
ences. Proper hygienic measures when taking food and
when keeping pets will reduce the chance of Toxoplasma
transmission to humans but ignorance and poverty are not
the only important factors that contribute to the high
prevalence of zoonotic diseases. Increasing both the public
awareness of these diseases and the sense of responsibility
for looking after pet animals is important. However, social
science research strategies regarding the importance of
culture, tradition and beliefs in the transmission of
disease are also necessary.
 Review TRENDS in Parasitology
References
1 Dubey, J.P. et al. (1970) The Toxoplasma gondii oocyst from cat feces.
J. Exp. Med. 132, 636–662
2 Frenkel, J.K. and Fishback, J.L. (2000) Toxoplasmosis. In Hunter’s
Tropical Medicine and Emerging Infectious Diseases, pp. 691–701,
Saunders
3 Reiter-Owona, I. et al. (1999) The past and present role of the Sabin–
Feldman dye test in the serodiagnosis of toxoplasmosis. Bull. World
Health Organ. 77, 929–935
4 Sukthana, Y. et al. (2000) Toxoplasma gondii antibody in HIV-infected
persons. J. Med. Assoc. Thai. 83, 681–684
5 Liesenfeld, O. et al. (2001) Effect of testing for IgG avidity in the
diagnosis of Toxoplasma gondii infection in pregnant women:
experience in a US reference laboratory. J. Infect. Dis. 183, 1248–1253
6 Roberts, A. et al. (2001) Multicenter evaluation of strategies for
serodiagnosis of primary infection with Toxoplasma gondii. Eur.
J. Clin. Microbiol. Infect. Dis. 20, 467–474
7 Hofgartner, W.T. et al. (1997) Detection of immunoglobulin G (IgG)
and IgM antibodies to Toxoplasma gondii: evaluation of four
commercial immunoassay systems. J. Clin. Microbiol. 35, 3313–3315
8 Wilson, M. et al. (1997) Evaluation of six commercial kits for detection
of human immunoglobulin M antibodies to Toxoplasma gondii. J. Clin.
Microbiol. 35, 3112–3115
9 Bacigalupo, M. et al. (1996) Evaluation of three immunoassays for
Toxoplasma-specific immunoglobulin G and M. Eur. J. Clin. Chem.
Clin. Biochem. 34, 503–505
10 Sukthana, Y. et al. (2001) Predictive value of latex agglutination test
in screening of toxoplasmosis. Southeast Asian J. Trop. Med. Public
Health 32, 314–318
11 Joynson, D.H. and Guy, E.C. (2001) Laboratory diagnosis of
Toxoplasma infection. In Toxoplasmosis: a Comprehensive Clinical
Guide (Joynson, D.H. and Wreghitt, T.G., eds), pp. 296–318,
Cambridge University Press
12 Montoya, J.G. and Liesenfeld, O. (2004) Toxoplasmosis. Lancet 363,
1965–1976
13 Ashburn, D. et al. (1998) Do IgA, IgE, and IgG avidity tests have any
value in the diagnosis of Toxoplasma infection in pregnancy. J. Clin.
Pathol. 51, 312–315
14 Pelloux, H. et al. (1998) Determination of anti-Toxoplasma gondii
immunoglobulin G avidity: adaptation to the Vidas system (bioMer-
ieux). Diagn. Microbiol. Infect. Dis. 32, 69–73
15 Lappalainen, M. et al. (2004) Serodiagnosis of toxoplasmosis. The
impact of measurment of IgG avidity. Ann. Ist. Super. Sanita 40, 81–83
16 Pelloux, H. et al. (1996) A new set of primers for the detection of
Toxoplasma gondii in amniotic fluid using polymerase chain reaction.
FEMS Microbiol. Lett. 138, 11–15
17 Foulon, W. et al. (1999) Prenatal diagnosis of congenital toxoplasmo-
sis: a multicenter evaluation of different diagnostic parameters. Am.
J. Obstet. Gynecol. 181, 843–847
18 Hohlfeld, P. et al. (1994) Prenatal diagnosis of congenital toxoplasmo-
sis with a polymerase-chain-reaction test on amniotic fluid. N. Engl.
J. Med. 331, 695–699
19 Bader, T.J. et al. (1997) Prenatal screening for toxoplasmosis. Obstet.
Gynecol. 90, 457–464
20 Gilbert, R.E. and Peckham, C.S. (2002) Congenital toxoplasmosis in
the United Kingdom: to screen or not to screen? J. Med. Screen. 9,
135–141
21 Petersson, K. et al. (2000) Seroprevalence of Toxoplasma gondii
among pregnant women in Sweden. Acta Obstet. Gynecol. Scand. 79,
824–829
22 Evengard, B. et al. (2001) Low incidence of Toxoplasma infection
during pregnancy and in newborns in Sweden. Epidemiol. Infect. 127,
121–127
23 Bastien, P. (2002) Molecular diagnosis of toxoplasmosis. Trans. R. Soc.
Trop. Med. Hyg. 96 (Suppl. 1), 205–215
24 Gilbert, R.E. et al. (2001) Effect of prenatal treatment on mother to
child transmission of Toxoplasma gondii: retrospective cohort study of
554 mother–child pairs in Lyon, France. Int. J. Epidemiol. 30,
1303–1308
25 Ammassari, A. et al. (1998) Changing disease patterns in focal brain
lesion-causing disorders in AIDS. J. Acquir. Immune Defic. Syndr.
Hum. Retrovirol. 18, 365–371
www.sciencedirect.com
Vol.22 No.3 March 2006 141
26 Antinori, A. et al. (1997) Diagnosis of AIDS-related focal brain lesions:
a decision-making analysis based on clinical and neuroradiological
characteristics combined with polymerase chain reaction assay in
cerebrospinal fluid. Neurology 48, 687–694
27 Skiest, D.J. (2000) SPECT thallium-201 with Toxoplasma serology for
the presumptive diagnosis of focal central nervous system mass
lesions in patients with AIDS. J. Infect. 40, 274–281
28 Borges, A.S. and Figueiredo, J.F. (2004) Evaluation of intrathecal
synthesis of specific IgG antibodies against Toxoplasma gondii in the
diagnosis assessment of presumptive Toxoplasma encephalitis in
AIDS patients. Rev. Soc. Bras. Med. Trop. 37, 480–484
29 Ferguson, D.J.P. et al. (2004) Use of molecular and ultrastructural
markers to evaluate stage conversion of Toxoplasma gondii in both the
intermediate and definitive host. Int. J. Parasitol. 34, 347–360
30 Joseph, P. et al. (2002) Optimization and evaluation of a PCR assay for
detecting toxoplasmic encephalitis in patients with AIDS. J. Clin.
Microbiol. 40, 4499–4503
31 Cingolani, A. et al. (1996) PCR detection of Toxoplasma gondii DNA in
CSF for the differential diagnosis of AIDS-related focal brain lesions.
J. Med. Microbiol. 45, 472–476
32 Bretagne, S. (2003) Molecular diagnostics in clinical parasitology and
mycology: limits of the current polymerase chain reaction (PCR)
assays and interest of the real-time PCR assays. Clin. Microbiol.
Infect. 9, 505–511
33 Contini, C. et al. (2002) The role of stage-specific oligonucleotide
primers in proving effective laboratory support for the molecular
diagnosis of reactivated Toxoplasma gondii encephalitis in patients
with AIDS. J. Med. Microbiol. 51, 879–890
34 Cultrera, R. et al. (2002) Efficacy of a novel reverse transcriptase–
polymerase chain reaction (RT–PCR) for detecting Toxoplasma gondii
bradyzoite gene expression in human clinical specimens. Mol. Cell.
Probes 16, 31–39
35 Katlama, C. (1996) Pyrimethamine–clindamycin vs. pyrimethamine–
sulfadiazine as acute and long-term therapy for toxoplasmic encepha-
litis in patients with AIDS. Clin. Infect. Dis. 22, 268–275
36 Pozio, E. (2004) Highly active antiretroviral therapy and opportunistic
protozoan infections. Parassitologia 46, 89–93
37 Sukthana, Y. et al. (2003) Toxoplasma gondii antibody in Thai cats and
their owners. Southeast Asian J. Trop. Med. Public Health 34,
733–737
38 Cook, A.J.C. et al. (2000) Sources of Toxoplasma infection in pregnant
women: European multicentre case-control study. BMJ 321, 142–147
39 Tenter, A.M. et al. (2000) Toxoplasma gondii: from animals to humans.
Int. J. Parasitol. 30, 1217–1258
40 Baril, L. et al. (1999) Risk factors for Toxoplasma infection in
pregnancy: a case-control study in France. Scand. J. Infect. Dis. 31,
305–309
41 Meireles, L.R. et al. (2004) Toxoplasma gondii spreading in an urban
area evaluated by seroprevalence in free-living cats and dogs. Trop.
Med. Int. Health 9, 876–881
42 Galvan Ramirez, M.L. et al. (1999) Presence of anti-Toxoplasma
antibodies in humans and their cats in the urban zone of Guadalajara.
Rev. Soc. Bras. Med. Trop. 32, 483–488
43 Lucas, S.R. et al. (1999) Toxoplasma gondii infection in Brazilian
domestic outpatient cats. Rev. Inst. Med. Trop. Sao Paulo 41, 221–224
44 Weigel, R.M. et al. (1999) Risk factors for infection with Toxoplasma
gondii for residents and workers on swine farms in Illinois. Am.
J. Trop. Med. Hyg. 60, 793–798
45 Dubey, J.P. (1998) Toxoplasma gondii oocyst survival under defined
temperatures. J. Parasitol. 84, 862–865
46 Moese, J.R. and Vander-Moese, A. (1998) Mother–child pass in Austria
and primary toxoplasmosis infections in pregnant women. Cent. Eur.
J. Public Health 6, 261–264
47 Luyasu, V. et al. (1997) A seroepidemiological study on toxoplasmosis.
Acta Clin. Belg. 52, 3–8
48 Gross, U. (2004) Prevalence and public-health aspects of toxoplasmo-
sis. Bundesgesundheitsblatt Gesundheitsforschung Gesund-
heitsschutz 47, 692–697
49 Kortbeek, L.M. et al. (2004) Population-based Toxoplasma seropreva-
lence study in The Netherlands. Epidemiol. Infect. 132, 839–845
50 Munoz Batet, C. et al. (2004) Toxoplasmosis and pregnancy. Multi-
center study of 16,362 pregnant women in Barcelona. Med. Clin.
(Barc.) 123, 12–16
142 Review TRENDS in Parasitology Vol.22 No.3 March 2006

51 Jacquier, P. et al. (1995) Epidemiology of toxoplasmosis in Switzer-
land: national study of seroprevalence monitored in pregnant women
1990–1991. Schweiz. Med. Wochenschr. Suppl. 65, 29S–38S
52 Lebech, M. et al. (1999) Feasibility of neonatal screening for
toxoplasma infection in the absence of prenatal treatment. Danish
Congenital Toxoplasmosis Study Group. Lancet 353, 1834–1837
53 Lappalainen, M. et al. (1995) Cost–benefit analysis of screening for
toxoplasmosis during pregnancy. Scand. J. Infect. Dis. 28, 211–212
54 Jenum, P.A. et al. (1998) Diagnosis of congenital Toxoplasma gondii
infection by polymerase chain reaction (PCR) on amniotic fluid
samples. The Norwegian experience. APMIS 106, 680–686
55 Punda-Polic, V. et al. (2000) Prevalence of antibodies to Toxoplasma
gondii in the female population of the County of Split Dalmatia.
Croatia. Eur. J. Epidemiol. 16, 875–877
56 Sroka, J. et al. (2001) Seroepidemiology of toxoplasmosis in the Lubin
region. Ann. Agric. Environ. Med. 8, 25–31
57 Logar, J. et al. (2002) Prevalence of congenital toxoplasmosis in
Slovania by serological screening of pregnant women. Scand. J. Infect.
Dis. 34, 201–204
58 Joynson, D.H. (1992) Epidemiology of toxoplasmosis in the UK.
Scand. J. Infect. Dis. Suppl. 84, 65–69
59 Bobic, B. et al. (1998) Risk factors for Toxoplasma infection in a
reproductive age female population in the area of Belgrade,
Yugoslavia. Eur. J. Epidemiol. 14, 605–610
60 Dubey, J.P. (2004) Toxoplasmosis – a waterborne zoonosis. Vet.
Parasitol. 126, 57–72
61 Arias, M.L. et al. (1996) Seroepidemiology of toxoplasmosis in
humans: possible transmission routes in Costa Rica. Rev. Biol. Trop.
44, 377–381
62 Machin Sanchez, R. et al. (1993) The National Toxoplasma Survey. I.
Prevalence by sex and age. Cuba, 1987. Rev. Cubana Med. Trop. 45,
146–151
63 Sousa, O.E. et al. (1988) Toxoplasmosis in Panama: a 10-year study.
Am. J. Trop. Med. Hyg. 38, 315–322
64 Prabhakar, P. et al. (1991) Seroprevalence of Toxoplasma gondii,
rubella virus, cytomegalovirus herpes simplex virus (TORCH) and
syphilis in Jamaican pregnant women. West Indian Med. J. 40,
166–169
65 Konishi Houki, Y. et al. (2000) High prevalence of antibody to
Toxoplasma gondii among humans in Surabaya. Jpn. J. Infect. Dis.
53, 238–241
66 Nissapatorn, V. et al. (2004) Review on human toxoplasmosis in
Malaysia: the past, present and prospective future. Southeast Asian
J. Trop. Med. Public Health 35, 24–30
67 Daenseekaew, W. et al. (1992) Seroprevalence of Toxoplasma gondii in
pregnant women in Ubon Rachthani province. J. Med. Assoc. Thai. 75,
609–610
68 Taechowisan, T. et al. (1997) Immune status in congenital infection by
TORCH agents in pregnant Thais. Asian Pac. J. Allergy Immunol. 15,
93–97
69 Sukthana, Y. et al. (2000) Prevalence of toxoplasmosis in selected
populations in Thailand. Trop. Med. Parasitol. 23, 53–58
70 Wanachiwanawin, D. et al. (2001) Toxoplasma gondii antibodies in
HIV and non-HIV infected Thai pregnant women. Asian Pac.
J. Allergy Immunol. 19, 291–293
71 Kapperud, G. et al. (1996) Risk factors for Toxoplasma gondii infection
in pregnancy: results of a prospective case-control study in Norway.
Am. J. Epidemiol. 144, 405–412

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