Toxoplasma gondii

Toxoplasma gondii (Nicolle and Manceaux, 1908)   Nicolle and Manceaux, 1909

 

ETYMOLOGY: Toxoplasma (Toxo=arc shaped; plasma = cell) gondii for the type intermediate

host, Ctenodactylus gundi

SYNONYMS: Leishmania gondii Nicolle and Manceaux, 1908; Several authors have described

species of Toxoplsama from additional hosts but they are not valid (see Levine, 1977a).

TYPE INTERMEDIATE HOST: The gondi (Ctenodactylus gundi) a North African rodent.

OTHER INTERMEDIATE HOSTS: Most mammals and birds are susceptible to T. gondii

infection. Some animal species, such as Australian marsupials, arborial monkeys, and lemurs are

highly susceptible to toxoplasmosis.

TYPE DEFINITIVE HOST: Domestic cat, Felis catus.

OTHER DEFINITIVE HOSTS: mountain lion (Felis concolor), ocelot (F. pardalis), margay

(F. weidii), jaguarundi (F. yagouaroundi), bobcat (F. rufus), bengal tiger (F. bengalensis), and

Iriomote cats (F. iriomotensis).

GEOGRAPHIC DISTRIBUTION: Worldwide

HISTORY: The complete life cycle of T. gondii was not fully described until 1970 about 62

years after its discovery in 1908. The first case of human toxoplasmosis was reported in 1923

in a 11-month-old congenitally infected infant that had hydrocephalus and microphthalmia

with coloboma (Remington et al., 1995). In the late 1930's and early 1940's it became well

established that toxoplasmosis is an important disease of humans and that infections in infants

were acquired prenatally. The rate of congenital toxoplasmosis in humans was too low to explain

the high seroprevalence of T. gondii in the populations examined. Carnivorism was suggested

by several researchers and conclusively proven in 1965. Ingestion of infected meat, however,

did not explain T. gondii infection in vegetarians or herbivores and other modes of transmission

had to be present. Hutchison first found resistant T. gondii in cat feces in 1965 and thought it

was enclosed in the eggs of Toxocara cati (Dubey and Beattie, 1988). Several studies disproved

the association of T. gondii with Toxocara cati and in 1969-1970 several groups of researchers

reported the presence of a coccidial oocyst in cat feces that was T. gondii (Figs 1-3 and 1-4).

Toxoplasma gondii oocyst excretion has been observed in several species of felids in addition to

the domestic cat (Miller et al., 1972; Jewell et al., 1972). The first case of fatal toxoplasmosis in

a cat was reported in 1942 (Dubey and Beattie, 1988). Fatal toxoplasmosis has been reported in

wild felids in Zoos and from pelt farms (Dubey et al., 1987).

Life Cycle Toxoplasma gondii in Cats: The life cycle of T. gondii is complex. Cats serve as

both definitive and intermediate hosts for the parasite. There are 2 distinct types of asexual

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stages that are present in extraintestinal tissues of cats and other intermediate hosts (Dubey

and Frenkel, 1972, 1976) These stages are intracellular except for brief periods of time when

they have ruptured host cells and are actively seeking new host cells. Tachyzoites are rapidly

dividing stages that cause tissue damage and disseminate the infection in host tissues. After a

period of multiplication (about 3 days) some tachyzoites will begin to produce the latent tissue

cyst stages that contain bradyzoites. Bradyzoites are slowly dividing stages that are found in

tissue cysts. Both tachyzoites and bradyzoites divide into 2 by endodyogeny. Bradyzoites can

transform into tachyzoites (Fig. 1-5). Bradyzoites are the only life cycle stage that can give rise

to the enteroepithelial developmental cycle (oocyst producing cycle) in the cats intestine. Tissue

cysts are present for up to 1.3 years (probably until host death) after inoculation in cats and most

tissue cysts are located in the heart (Dubey, 1977).

The life cycle of T. gondii in the cat varies based on the developmental stage that the cat

ingests (Dubey and Frenkel, 1972; 1976, Dubey, 1979; Freyre et al., 1989). When cats ingest

tissue cysts the bradyzoites are released after passage through the stomach. Some bradyzoites

will penetrate enterocytes and begin the enteroepithelial cycle that will terminate in oocyst

production (Dubey, 1979) (Fig. 1-6). However, some bradyzoites will penetrate into the

intestinal lamina propria and begin development as tachyzoites. Infectious stages of T. gondii are

present in the liver and mesenteric lymph nodes as early as 8 hours after tissue cysts are ingested

and chronic infections are produced by these stages. Five structurally distinct types of schizonts

are produced in the enterocytes of the small and large intestine prior to the formation of sexual

stages at 3-4 days (Dubey and Frenkel, 1972; Dubey, 1979). The prepatent period is 3 to 10 days

for tissue cyst induced infections. Oocysts are excreted in the feces for 7 to >20 days with most

being excreted between days 5 and 8.

Ingestion of sporulated T. gondii oocysts or tachyzoites results in oocyst excreting

infections in only 16 to 20% of cats as compared with 97% of cats that are fed tissue cysts

(Dubey and Frenkel, 1976; Freyre et al., 1989; Dubey, 1996). The prepatent period in oocyst

excreting cats is greater 18 days or more in these cats as compared to 3 to 10 days in cats that are

fed tissue cysts (Dubey , 1996). The reason for the extended prepatent period is that the

sporozoites or tachyzoites must first produce tissue cysts that contain bradyzoites. These

bradyzoites will then find their way back to the intestine to produce the enteroepithelial cycle

that results in oocyst production.

Oocyst Biology: Unsporulated T. gondii oocysts are spherical to subspherical, and

contain a single mass (sporont) (Fig. 1-3). Sporulation occurs in the environment and is

dependent on temperature and moisture (Dubey et al. 1970a). Sporulation is asynchronous and

some oocysts will be sporulated before others. Completely infectious oocysts are present by 24

hr at 25 C (room temperature); by 5 days at 15 C, and by 21 days at 11 C (Dubey et 1970b).

Unsporulated oocysts do not survive freezing but can remain viable at 4 C for several months

and become infectious if placed under the appropriate conditions. Unsporulated oocysts die if

kept at 37 C for 24 hours and are killed by 10 minute exposure to 50 C.

A small population of unsporulated oocysts can survive anaerobic conditions for 30 days

and remain capable of developing. Oocysts do not sporulate in 0.3% formalin, 1% ammonium

hydroxide solution or in 1% iodine in 20% ethanol but can sporulate in 5% sulfuric acid, 20%

ethanol, 10% ethanol plus 10% ether, 1% hydrochloric acid, 1% phenol and in tap water (Dubey

et al. , 1970a, 1970b). Drying kills T. gondii oocysts. Cockroaches, flies, earthworms and other

phoretic hosts can serve to distribute T. gondii oocysts from the site of defecation in the soil

(Dubey and Beattie, 1988).

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Sporulated T. gondii oocysts are subspherical to ellipsoidal and each contains 2

ellipsoidal sporocysts which enclose 4 sporozoites (Fig. 1-4). Sporulated oocysts are more

resistant to environmental and chemical stresses than are unsporulated oocysts. Viable oocysts of

T. gondii have been isolated from soil samples (Ruiz et al., 1973; Coutinho et al., 1982; Frenkel

et al., 1995) and experimentally they can survive for over 18 months in the soil (Frenkel et al.,

1975) . Sporulated oocysts can not survive freezing or temperatures of 55 C or greater (Ito el al.,

1975, Dubey, 1998). Sporulated oocysts survive for several years at 4 C in liquid medium

(Dubey, 1998).

TOXOPLASMA GONDII OOCYST EXCRETION: All ages, sexes, and breeds of domestic

cats are susceptible to T. gondii infection (Dubey et al., 1977). Transplacentally or lactogenically

infected kittens will excrete oocysts but the prepatent period is usually 3 weeks or more because

the kittens are infected with tachyzoites (Dubey et al., 1995). Domestic cats under 1 year of age

produce the most numbers of T. gondii oocysts. Cats that are born and raised outdoors usually

become infected with T. gondii shortly after they are weaned and begin to hunt. Toxoplasma

gondii naive adult domestic cats will excrete oocysts if fed tissue cysts but they usually will

excrete fewer numbers of oocysts and excrete oocysts for a shorter period of time than recently

weaned kittens.

IMMUNITY TO OOCYST-EXCREETION: Intestinal immunity to T. gondii is strong in

cats that have excreted oocysts (Frenkel and Smith, 1982a, 1982b, Dubey 1995). Duration of

Immun. Primary T. gondii infection in cats does not cause immunosuppression (Lappin et al.,

1992a; Davis and Dubey, 1995). Serum antibody does not play a significant role in resistance

to intestinal infection and intestinal immunity is most likely cell mediated. Oocysts begin to be

excreted in the feces before IgM, IgG or IgA antibodies are present in the serum (Lappin et al.,

1989a; Lin and Bowman, 1991; Burney et al., 1995). Partial development of the enteroepithelial

stages occur in the intestines of immune cats but oocyst production is prevented (Davis and

Dubey, 1995). Most cats that have excreted oocysts once do not re-excrete oocysts if challenged

within 6 months to 1 year. Intestinal immunity will last up to 6 years in about 55% of cats

(Dubey, 1995).

Immunosuppression with high doses of corticosteroid (10 to 80 mg/kg

methylprednisolone acetate IM weekly or 10 to 80 prednisone orally daily) will cause some

chronically infected cats to re-excrete T. gondii oocysts (Dubey and Frenkel, 1974). However,

clinically relevant doses of 5 to 20 mg/kg corticosteroid given weekly for 4 weeks do not cause

recently or chronically infected cats to re-excrete T. gondii oocysts (Lappin et al., 1991). Doses

of 5 mg/kg cortisone acetate for 7 days will not cause oocyst excretion in chronically infected

cats (Hagiwara et al., 1981).

Cats that are chronically infected with T. gondii and then undergo a primary feline

immunodefincy virus infection demonstrate an increase in T. gondii antibody titers suggesting

some reactivation of encysted stages. However, experimental studies indicate that there is no

reactivation of T. gondii oocyst excretion or development of clinical toxoplasmosis (Lappin et

al., 1992b; 1993; 1996b; Lin and Bowman, 1992; Lin et al., 1992a). Rarely has clinical disease

been associated with re-activated toxoplasmosis in FIV positive cats. Experimental feline

leukemia virus infection prior to T. gondii challenge does not appear to predispose cats to acute

toxoplasmosis and has no effect on oocyst excretion (Patton et al., 1991).

There is an interesting relationship that exists between the intestinal coccidium Isospora

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felis and T. gondii in cats (Chessum, 1972; Dubey, 1976). Cats that have previously recovered

from a T. gondii infection will re-excrete T. gondii oocysts if they obtain a primary I. felis

infection afterwards. Cats that have a primary I. felis infection followed by a primary T. gondii

infection develop strong immunity to T. gondii and will not re-excrete T. gondii oocysts if

challenged with I. felis (Dubey, 1978). The mechanism for this unusual relationship is not known.

TOXOPLASMOSIS IN CATS: Dubey and Carpenter (1993a) examined 100 cases of

histologically confirmed toxoplasmosis in domestic cats and provide the definitive report on

clinical toxoplasmosis in cats. Eleven of 100 cats were purebred, cats ranged in age from 2

weeks to 16 years, and 65 were male 34 were female and the sex of 1 was not determined. Of

the 100 cats 36 had generalized, 26 had pneumonia, 16 had abdominal, 7 had neurologic, 9 had

neonatal, 2 had hepatic, 2 had cutaneous, 1 had pancreatic, and 1 had cardiac toxoplasmosis (figs

1-7 through 1-11).

Fever (40.0 to 41.7 C) is present in many cats with toxoplasmosis. Clinical signs of

dyspnea, polypnea, icterus, and signs of abdominal discomfort are frequent findings. Gross and

microscopic lesions are found in many organs but are most common in the lungs. Gross lesions

in the lungs consiste of diffuse edema and congestion, failure to collapse, and multifocal areas of

firm, white to yellow, discoloration. Pericardial and abdominal effusions may be present. The

liver is the most frequently affected abdominal organ and diffuse necrotizing hepatitis may be

visible grossly. Gross lesions associated with necrosis can also be observed in the mesenteric

lymph nodes and pancreas.

Occular lesions are also common in cats but the actual prevalence is not known. Most

lesions are in the anterior segment (Lappin et al. 1989c). Cats with occular lesions have a higher

seroprevalence than cats with normal eyes. Occular findings are varried, they include aqueous

flares, hyphema, velvety iris, mydriasis, anisocoria, retinal hemorrhages, retinal atrophy,

retinochoriditis and slow pupilary reflex.

Central nervous system toxoplasmosis is not common in cats. Neurological signs

including hypothermia, partial or total blindness, stupor, incoordination, circling, torticollis,

anisocoria, head bobbing, ear twich, atypical crying, and increased affectionate behavior have

been reported (Dubey and Carpenter, 1993a).

Congenital toxoplasmosis occurs in cats but the frequency is not known (Dubey and

Carpenter, 1993b) (Figs 1-12 through 1-14).

Clinical Signs of Feline Toxoplasmosis: The severe central nervous system involvement

observed in congenitally infected infants and AIDS patients and the tendency of tissue cysts

to develop in the brains of humans and mice have led to the erroneous assumption by many

that toxoplasmosis in all animals is a central nervous system disease. Central nervous system

infections do occur in cats but neurologic signs are not the most common clinical sign of

infection in cats (Dubey and Carpenter, 1993a).

Fever (40.0 to 41.7 C) is present in many cats with toxoplasmosis. Clinical signs of

dyspnea, polypnea, icterus, and signs of abdominal discomfort were the most frequent findings

in 100 cats with histologically confirmed toxoplasmosis (Dubey and Carpenter, 1993a). Uveitis

and retinochoroiditis are also common clinical signs in cats with toxoplasmosis. Gross and

microscopic lesions are found in many organs but are most common in the lungs. Gross lesions

in the lungs consist of edema and congestion, failure to collapse, and multifocal areas of firm,

white to yellow, discoloration. Pericardial and abdominal effusions may be present. The liver is

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the most frequently affected abdominal organ and diffuse necrotizing hepatitis may be visible

grossly. Gross lesions associated with necrosis can also be observed in the mesenteric lymph

nodes and pancreas.

Ocular lesions of toxoplasmosis are common in cats. The actual prevalence is not known

but antibodies to T. gondii were observed in the sera of 80% of cats with uveitis in one study

(Chavkin et al., 1992). indicating a high prevalence in infected cats. Most lesions are in the

anterior segment (Lappin et al., 1992c).

hyphema, iritis, mydriasis, anisocoria, retinal hemorrhages, retinal atrophy, retinochoroiditis and

slow pupillary reflex.

Central nervous system toxoplasmosis is not common in cat. In one study, only 7 of 100

cases of histologically confirmed cases of toxoplasmosis had neurological signs (Dubey and

Carpenter, 1993a). Neurological signs including hypothermia, partial or total blindness, stupor,

incoordination, circling, torticollis, anisocoria, head bobbing, ear twitch, atypical crying, and

increased affectionate behavior have been reported.

Congenital toxoplasmosis occurs in cats but the frequency is not known. Disease in

congenitally infected kittens can be severe and fatal (Dubey and Carpenter, 1993b). The most

common clinical signs are anorexia, lethargy, hypothermia and sudden death (Dubey et al.,

1995b).

Diagnosis of feline toxoplasmosis:The diagnosis of clinical toxoplasmosis requires that

3 criteria be fulfilled (Lappin, 1990). The cat must have clinical signs consistent with

toxoplasmosis, serological evidence of recent or active infection, and the patient must respond to

anti-T. gondii treatment or have T. gondii demonstrated in its tissues or body fluids.

Toxoplasmosis should be suspected in cats with anterior uveitis, retinochoroiditis, fever,

dyspnea, polypnea, abdominal discomfort, icterus, anorexia, seizures, ataxia and weight loss.

Fecal examination only rarely detects oocysts in cats and most cats with clinical toxoplasmosis

will not be excreting oocysts at the time of presentation. Thoracic radiographs maybe helpful.

Diffusely disseminated and poorly demarcated foci of increased radiodensity caused by

interstitial and alveolar pneumonia are suggestive of but not definitive for T. gondii in febrile

cats.

Serological tests for active toxoplasmosis: Several serological tests are available for the

diagnosis of active toxoplasmosis in cats (Table 1). Titers obtained in one type of test may not

correlate with titers obtained in other tests (Patton et al., 1991, Dubey and Thulliez, 1989, Lappin

and Powell, 1991). Most tests rely on the detection of IgG antibodies which do not develop until

about 2 weeks postinfection and may remain at high levels for several years to the life of the cat

(Dubey et al., 1995a). Therefore, diagnosis of active toxoplasmosis in cats using an IgG based

test requires that a rising titer be demonstrated (Lindsay et al., 1997a).

Table 1. Serological tests for the demonstration of Toxoplasma gondii antibodies* in cats.

_____________________________________________________________

Test Detected Comments (cutoff titer)

IgG-ELISA 2 weeks Test detects IgG, 4 fold increase

Ocular findings are varied, they include aqueous flare,

Antibody first

in titer over 2 to 3 weeks

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indicates active infection (1:64)

IgM-ELISA 1-2 weeks Test detects IgM, titer of >1:256

indicative of active infection,

positive IgM with negative IgG

indicates active infection. (1:64)

modified direct agglutination

formalin fixed (FF) antigen 2 weeks Test detects IgG, 4 fold increase

in titer over 2 to 3 weeks

indicates active infection, titers

remains high. (1:25)

acetone fixed (AC) antigen 1-2 weeks Test detects IgG, titers high

during acute infection. High AC

and low FF titer indicates active

infection. (1:100)

IHT, LAT, IgG-IFA 2 weeks Tests detect IgG, IHT is

insensitive, 4 fold increase in

titer over 2 to 3 weeks indicates

active infection. (1:64)

IgM-IFA 1-2 weeks Detects IgM, positive IgM with

negative or low IgG indicates

active infection. (1:64)

Sabin-Feldman dye test 1-2 weeks Detects IgG and IgM, 4 fold

increase in titer over 2 to 3

weeks indicates active infection.

(1:16)

_____________________________________________________________

* Titers on paired serum samples should be examined on the same day to avoid test variability.

(Adapted from Lindsay et al., 1997a).

Diagnostic tests based on detection of IgM antibodies (Lappin et al., 1989a; 1989c, Lin

and Bowman, 1991), circulating parasite antigens (AG) (Lappin et al., 1989b) or acetone-fixed

(AF) tachyzoite antigens (Dubey et al., 1995a). can detect early infections at 1 to 2 weeks post

exposure. The T. gondii specific IgM levels in cats peak at 3 to 6 weeks and drop to negative by

12 weeks post exposure in the IgM-ELISA teat. However, some cats will have sporadic low IgM-
ELISA levels for up to 1 year post exposure. Peak detection of circulating T. gondii antigens

occurs about 21 days post exposure but some cats will have circulating T. gondii antigens for at

least 1 year in the AG- ELISA; overall, the test is not very useful in diagnosis (Lappin et al.,

1989b). Reactivity to AF-tachyzoites in the modified direct agglutination test (MAT, normally

formalin-fixed [FF] tachyzoites are used) remains present for up to 70 months (Dubey et al.,

1995a). The IgA-ELISA produces variable results in detecting serum antibodies in cats and is

not used to detect early infections (Burney et al., 1995). The use of an early detection test

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coupled with an IgG detection test can provide valuable information on the kinetics of the T.

gondii infection. For example, a high IgM-ELISA titer and a negative or low IgG-ELISA titer

would indicate active infection. The reverse would be true for a chronic infection. Serology can

often be difficult to interpret and should never be the sole bases for diagnosis.

Serological tests for ocular and CNS toxoplasmosis : Detection of T. gondii antibodies

in aqueous humor has been used as an aid in the diagnosis of ocular toxoplasmosis in cats

(Patton et al., 1991, Lappin et al., 1992c, 1995, Lin et al., 1992b). Calculating the Goldman-
Witmer coefficient (C-value) helps correct for antibodies that may have leaked across a damage

vasculature and not been produced directly in the eye (Lappin et al., 1992c) Experimentally

infected cats begin to have detectable IgA and IgG levels in aqueous humor at 4 weeks post

exposure while IgM is either not present or at levels to low to detect (Lappin et al., 1995)

however all 3 antibody isotypes have been found in the aqueous humor of naturally infected

cats. Cats with C-values < 1 are considered to have antibodies that have leaked across a damaged

vasculature while C-values of 1 to 8 are highly suggestive of clinical ocular toxoplasmosis

(Lappin et al., 1992c, 1995). Cats with C-values >8 are considered to have conclusive evidence

of ocular antibody production due to T. gondii infection (Chavkin et al., 1994) Most cats with C-
values >1 will respond to specific antitoxoplasmal treatment (Lappin et al., 1992c) Although not

conclusive, a trend toward association of T. gondii-specific IgA in the serum of cats with ocular

disease has been reported (Burney et al., 1995).

Toxoplasma gondii antibodies have been demonstrated in the cerebrospinal fluid (CSF)

of cats with experimental infections but no clinical signs of encephalitis using the FF-MAT

(Patton et al., 1991) a modified ELISA (Lin et al., 1992b) and IgG- ELISA (Munana et al.,

1995). No IgM was detected in the CSF of experimentally infected cats using the IgM-ELISA.

Little else is available on the diagnosis toxoplasmic encephalitis in cats using CSF. Because T.

gondii-specific IgG has been observed in the CSF of clinically normal cats, it has been suggested

that the diagnosis of central nervous system toxoplasmosis in cats not be based solely on

detection of intrathecally synthesized T. gondii- specific IgG (Munana et al., 1995).

Serological tests for neonatal toxoplasmosis: Neonatal toxoplasmosis is difficult to

diagnosis antemortem because the clinical signs are vague and kittens will have nursed prior to

examination. Serological indications can be inferred in some cases by comparing titers in queens

with their kittens (Dubey et al., 1995b) Transplacental transfer of T. gondii antibodies does not

occur in cats (Dubey et al., 1995b). If the queen is seronegative then it is unlikely that the kittens

have toxoplasmosis because transplacental transmission is unlikely if the queen has acquired

the infection with less than 2 weeks left in pregnancy which is the time it takes or a detectable

antibody response. If the queen has a positive IgM titer or the queen and kittens have rising

IgG titers then transplacental or lactogenic transmission is possible. Western blot analysis of

serum from the queen and kitten can be helpful in diagnosing neonatal toxoplasmosis in kittens

(Cannizzo et al., 1996). Antigen recognition patterns are different for congenitally infected

kittens when compared to queens or kittens that have maternally acquired antibody. Serum for

congenitally infected kittens usually will usually recognize an antigen with a molecular mass

between 27 to 29 kD (Cannizzo et al., 1996).

Other methods of detection of T. gondii infections: Direct demonstration of T. gondii stages

can be used to make a method of antemortem diagnosis. Examination of brocheolavage material

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or material collected by abdominocentesis can be used to detect suspected cases of disseminated

toxoplasmosis in cats or neonatal toxoplasmosis in kittens. Examination of CSF may also

demonstrate organisms in cases of encephalitis.

The polymerase chain reaction (PCR) has been widely used in human medicine to detect

T. gondii in secretions and fluids and methods are currently under development for use in cats

(Stiles et al., 1996; Lappin et al., 1996b; Burney et al., 1998) The primers have been developed

that amplify portions of the parasites B1 gene and used to detect tachyzoites in serum, blood,

aqueous humor, and CSF. The PCR test can detect DNA from as few as 10 tachyzoites in serum,

CSF, and aqueous humor (Stiles et al., 1996, Lappin et al., 1996b) and DNA from as few as 100

tachyzoites in blood (Stiles et al., 1996).The use of PCR combined with traditional antibody

testing maybe useful in the antemortem diagnosis of toxoplasmosis in cats. Results of PCR

testing alone should never be used as the sole method of diagnosis of toxoplasmosis.

Postmortem diagnosis can be made by demonstration of the parasite in tissue sections

using routine methods or by supplementing histopathologic examinations with

immunohistochemical staining for specific for T. gondii. Other methods, such as, bioassays in

cats or mice can be used but are not practical.

Vaccination Against Oocyst Excretion: A vaccine that prevents oocyst excretion in cats

would be beneficial for both veterinary and public health reasons (Fishback and Frenkel, 1990;

Frenkel et al., 1991; Freyre et al., 1993). Vaccination of cats would decrease environmental

contamination with oocysts. This would aid in preventing exposure of animals and humans to

oocysts and lead to a decreased prevalence of the encysted parasite in food animals.

Killed or recombinant tachyzoite based vaccines do not stimulate intestinal immunity and

are of no value in preventing oocyst excretion.. Technically it is not presently possible to

produce sufficient numbers of bradyzoites or enteroepithelial stages to develop killed or

recombinant vaccines based on these stages.

Intestinal immunity can be induced by infecting cats with an oocyst-producing strain of

T. gondii and by prophylactically treating the cats for 8 to 19 days with anti-T. gondii

chemotherapy (Frenkel and Smith, 1982a, 1982b). Oocyst excretion can be prevented during the

immunizing phase and 80 to 85% of the cats become immune. Although, effective this method

of vaccination is impractical for many technical and safety reasons.

The life cycle of T. gondii can be manipulated by extensive passage of the parasite in

mice (Frenkel et al., 1976) or in cell cultures (Lindsay et al., 1991).so that the bradyzoites lose

the ability to produce oocyst-excretion in cats. Unfortunately, none of these oocyst-less strains of

T. gondii stimulate sufficient intestinal immunity and the cats will excrete oocysts when

challenged with an oocyst producing strain.

Vaccination of cats against intestinal T. gondii infection has been success fully achieved

using a chemically-induced mutant strain (T-263) of the parasite (Frenkel et al., 1991; Freyre et

al., 1993). Oral administration of strain T-263 bradyzoites results in intestinal infection but does

not result in oocyst production in cats. These vaccinated cats do not excrete oocysts when

challenged with oocyst producing strains of T. gondii. The T-263 strain is safe to use in healthy

cats. It will not be recommended for use in pregnant cats or FeLV positive cats or

immunocompromised cats (Choromanski et al., 1994, 1995). It has only limited ability to persist

in the tissues of cats and can not survive more than 3 back-passages in cats. No reversion to

oocyst excretion or increase in virulence has been observed in over 200 inoculated cats. The T-

263 strain is rapidly cleared from the mouth of inoculated cats.

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Treatment of feline toxoplasmosis: No chemotherapeutic agents are approved for the treatment

of toxoplasmosis in cats. Table 2 lists agents that are used to treat toxoplasmosis in cats.

Table 2. Treatment of feline toxoplasmosis

Product Treatment regimen

clindamycin hydrochloride Oral, 10-12 mg/kg BID for 4 weeks clindamycin

phosphate IM, 12.5-25 mg/kg BID for 4 weeks

pyrimethamine plus Oral, 0.25-0.5 mg/kg combined with

sulfonamide 30 mg/kg sulfonamide b.i.d. for 2 to 4 weeks

trimethoprim + sulfadiazine Oral 15 mg/kg BID for 4 weeks

_____________________________________________________________

Clindamycin is the drug of choice for the treatment of disseminated toxoplasmosis in cats

(Lappin et al., 1989c). Clinically, the drug has been widely used with good response

Cats can also be treated with pyrimethamine or trimethoprim combined with a

sulfonamide. Pyrimethamine is active at lower concentrations than is trimethoprim. Sulfadiazine

or sulfamethoxazole are the sulfonomides most often used. Bone marrow suppression can occur

with the use of pyrimethamine or trimethoprim-sulfonamide combinatioins and can be corrected

with the addition of folinic acid (5 mg per day) or the addition of yeast (100 mg/kg BWT) to the

cats diet.

Prevention of Toxoplasma gondii infection in cats and humans: Measures can be taken to

prevent or lower the risk of exposure of cats and humans to T. gondii. They are based on a

detailed knowledge of the parasites life cycle and are presented in Table 3. They are based on

preventing exposure to sporulated oocysts or tissue cysts.

Table 3. Prevention of Toxoplasma gondii infection in cats and humans.

Recommendation/Reason

_____________________________________________________________

Cats

1. Do not feed raw or rare meat to cats/Prevent exposure to tissue cysts.

2. Keep cats indoors and do not allow cats to hunt/Prevent exposure to tissue cysts in prey

animals.

3. Vaccination?/Prevent oocyst excretion.

Humans

1. Do not eat raw or rare meat/Prevent ingestion of viable tissue cysts.

2. Wash hands and food preparation surfaces with warm soapy water after handling and

preparing raw meat/Inactivate tissue cysts.

3. Wear gloves while gardening or wash hands after gardening/Prevent exposure to oocysts in

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the soil.

4. Wash all fruits and vegetables before eating/Remove any oocysts that may be present.

5. Change litter box daily. Pregnant women and immunosuppressed individuals should not

change litter box/Remove oocysts before they become infective and prevent exposure of high risk

individuals.

_____________________________________________________________

 

Pork is the most likely source of tissue cysts for people in the United States. This is

because cattle are naturally resistant and other T. gondii infected meats such as sheep and goat

are not consumed in significant amounts (Dubey,1994). Chickens are susceptible to T. gondii

infection but because chicken is often frozen and seldom eaten rare it is not considered a

primary source of infection. Tissue cysts in meat are killed by cooking to temperatures of 58 C

for 10 minutes or 61 C for 4 minutes (Dubey et al., 1990a). Tissue cysts are believed to be killed

instantaneously by exposure to -13 C, however, they will survive for up to 3 weeks at -3 C and

11 days at -6 C (Kotula, et al., 1991). Gamma irradiation at an absorbed dose of 0.4 kGy is

lethal for tissue cysts in meat (Dubey and Thayer, 1994).

Cutting boards, knives, and other surfaces that raw meat has contacted should be washed

in warm soapy water to kill the tissue cysts and any bradyzoites that may have been liberated

during handling. Hands should also be washed in warm soapy water after contact with raw meat.

Cat Ownership and the Risk of Toxoplasmosis: It is logical to assume that veterinarians, who

have more exposure to cats (both sick and healthy) than the general public, would be at a greater

risk for developing toxoplasmosis. However, serological studies do not confirm this assumption

(Behymer et al., 1973; Sengbusch and Sengbusch, 1976, DiGiacomo et al., 1990). In one study

in AIDS patients it was conclusively shown that owning cats did not increase the risk of

developing toxoplasmosis (Wallace et al., 1993). However, the role of cat ownership and

exposure to T. gondii is not completely clear at present. Many studies have been conducted to

determine the association between cat ownership or cat exposure and the prevalence of T. gondii

infection in humans. Many studies do not find a positive relationship (Partono and Cross, 1975;

Ulmanen and Leinikki, 1975; Durfee et al., 1976; Zigas, 1976; Tizard et al., 1977; Gandahusada,

1978; Sedaghat et al., 1978; Ganley and Comstock, 1980; Stray-Pedersen and Lorentzen-Styr,

1980; Konishi and Takahashi, 1987; Arias et al., 1996; Bobic et al., 1998; Flegr et al., 1998)

while many find a positive relationship (Clarke et al., 1975; Frenkel and Ruiz, 1980, 1981;

Barbier et al., 1983; Martinez-Sanchez et al., 1991; Ahmed, 1992; MacKnight and Robinson,

1992; Etheredge and Frenkel, 1995; del Castillo and Herruzo, 1998; Rey and Ramalho, 1999). It

must be remembered that preventing exposure to cats is not the same as preventing exposure to

T. gondii oocysts. One study indicated that exposure to dogs was more of a risk factor than

exposure to cats (Frenkel et al., 1995). If dogs are fed sporulated T. gondii oocysts many will

pass out in the dogs feces and remain infectious (Lindsay et al., 1997b) and it has been suggested

that dogs consume cat feces or roll in cat feces and thereby increase human contact with T.

gondii oocysts when they return home (Frenkel and Parker, 1996). Pregnant women or

immunocompromised individuals should not change the cat’s litter box. If feces are removed

daily this will also help prevent exposure by removing oocysts before they can sporulate. Oocyst

can survive in the soil for years and can be disseminated from the original site of deposition by

erosion, other mechanical means, and by phoretic vectors. Inhalation of oocysts stirred up in the

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dust by horses has been associated with an outbreak of human toxoplasmosis at a riding stable

(Teutsch et al., 1979). Oocysts are not likely to remain in the air for extended periods of time.

Washing fruits and vegetables and wearing gloves while gardening are means of preventing

exposure to oocysts. Oocysts are killed by exposure to 0.25 kGy gamma irradiation will kill

oocysts and is a potential means of kill oocysts on contaminated fruit and vegetables (Dubey et

al., 1996).

Toxoplasma gondii oocysts were not isolated from the fur of oocyst-excreting cats

(Dubey, 1995).

Tachyzoites are not likely to be present in the oral cavity of cats with active T. gondii infection

and none would be in a chronic infection; therefore, it is unlikely that a cat bite would transmit

T. gondii infection. Cat scratches are also unlikely to transmit T. gondii infection.

Important aspects of human maternal toxoplasmosis: Pregnant women and

immunocompromised patients should follow the prevention guidelines in Table 3.

Immunocompetent women with T. gondii antibody titers prior to becoming pregnant are

considered immune and will not transmit the parasite to the fetus if exposed during pregnancy.

It is important for a pregnant woman to know her titer because it can serve as a baseline if

exposure is suspected during pregnancy. About 60% of women infected with T. gondii during

pregnancy will transmit the infection to the fetus. The age at which the fetus becomes infected

determines the severity of subsequent disease. Few cases of fetal infection occur when the

mother is infected during weeks 1 to 10, however severe disease occurs in the infants that do

become infected (Remington et al., 1995). Pregnant women are at greatest risk of delivering a

severely infected infant if infected during weeks 10 to 24 of gestation (Remington et al., 1995).

If T. gondii infection of the mother occurs at weeks 26 to 40 there is a low risk of delivery of a

severely infected infant but most infants will be infected and have mild symptoms (Remington et

al., 1995).

References:

Ahmed MM. 1992. Seroepidemiology of Toxoplasma infection in Riyadh, Saudi Arabia. J Egypt

Soc Parasitol 22:407-143.

Arias ML, Chinchilla M, Reyes L, Linder E. 1996. Seroepidemiology of toxoplasmosis in

humans: possible transmission routes in Costa Rica. Rev Biol Trop 44:377-381.

Barbier D, Ancelle T, Martin-Bouyer G. 1983. Seroepidemiological survey of toxoplasmosis in

La Guadeloupe, French West Indies. Am J Trop Med Hyg 32:935-942

Behymer RD, Harlow DR, Behymer DE, Franti CE. 1973. Serologic diagnosis of toxoplasmosis

and prevalence of Toxoplasma gondii antibodies in selected feline, canine, and human

populations. J. Am Vet Med Assoc 162:959-963.

Bobic B, Jevremovic I, Marinkovic J, Sibalic D, Djurkovic-Djakovic O. 1998. Risk factors for

Toxoplasma infection in a reproductive age female population in the area of Belgrade,

Yugoslavia. Eur J Epidemiol 14:605-610

Burney DP, Lappin MR, Cooper C, Spilker MM. 1995. Detection of Toxoplasma gondii-specific

IgA in the serum of cats. Am J Vet Res 56:769-773.

Burney DP, Chavkin MJ, Dow SW, Potter TA, Lappin MR. 1998. Polymerase chain reaction for

the detection of Toxoplasma gondii within aqueous humor of experimentally-inoculated

cats. Vet Parasitol 79:181-186.

Therefore, it is unlikely that infection can be obtained by petting a cat.

C:\Aa Old D\Dwight\CATBOOK\complete\chap1\chap1-with figs.doc

Page 28 of 112

112

Feline Clinical Parasitology – Chapter 1

Cannizzo KL, Lappin MR, Cooper CM, Dubey JP. 1996. Toxoplasma gondii antigen recognition

by serum immunoglobulins M, G, and A of queens and their neonatally infected kittens.

Am J Vet Res 57:1327-1330

Chavkin MJ, Lappin MR, Powell CC, Cooper CM, Munana KR, Howard LH. 1994. Toxoplasma

gondii-specific antibodies in the aqueous humor of cats with toxoplasmosis. Am J Vet

Res 55:1244-1249

Chavkin MJ, Lappin MR, Powell CC, et al.: Seroepidemiology and clinical observations of 93 cases of uveitis in cats. Prog Vet Comp Ophthalmol 2:29- 36, 1992.

Chessum BS. 1972. Reactivation of Toxoplasma oocyst production in the cat by infection with

Isospora felis. Brit Vet J 128:33-36, 1972.

Choromanski L, Freyre A, Brown K, Popiel I, Shibley G. 1994. Safety aspects of a vaccine for

cats containing a Toxoplasma gondii mutant strain. J Eukaryot Microbiol 41:8S

Choromanski L, Freyre A, Popiel R, Brown K, Grieve R, Shibley G. 1995.Safety and efficacy of

modified live feline Toxoplasma gondii vaccine. Dev Biol Stand 84:269-281.

Clarke MD, Cross JH, Carney WP, Hadidjaja P, Joesoef A, Putrali J, Sri Oemijati1975.

Serological study of amebiasis and toxoplasmosis in the Lindu Valley,Central Sulawesi,

Indonesia. Trop Geogr Med 27::274-278

Coutinho SG, Lobo R, Dutra G. 1982. Isolation of Toxoplasma from the soil during an outbreak

of toxoplasmosis in a rural area in Brazil. J Parasitol 68:866-868

Davis SW, Dubey JP. 1995. Mediation of immunity to Toxoplasma gondii oocyst shedding in

cats. J Parasitol 81:882-886.

del Castillo F, Herruzo R. 1998. Risk factors for toxoplasmosis in children. Enferm Infecc

Microbiol Clin 16:224-229

DiGiacomo RF, Harris NV, Huber NL, Cooney MK. 1990. Animal exposures and antibodies to

Toxoplasma gondii in a university population. Am J Epidemiol 131:729-733

Dubey JP. 1976. Reshedding of Toxoplasma oocysts by chronically infected cats. Nature

262:213-214.

Dubey JP. 1977. Persistence of Toxoplasma gondii in the tissues of chronically infected cats. J.

Parasitol. 63:156-157.

Dubey JP. 1978. Effect of immunization of cats with Isospora felis and BCG on immunity to

reexcretion of Toxoplasma gondii oocysts. J. Protozool. 25:380-382.

Dubey JP. 1978. A comparison of cross protection between BCG, Hammondia hammondi,

Besnoitia jellisoni and Toxoplasma gondii in hamsters. J. Protozool. 25:382-384.

Dubey JP. 1979. Direct development of enteroepithelial stages of Toxoplasma in the intestines of

cats fed cysts. Am. J. Vet. Res. 40:1634-1637.

Dubey JP. 1994. Toxoplasmosis. JAVMA 205:1593-1598.

Dubey JP. 1995. Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. J

Parasitol 81:410-415.

Dubey JP. 1996 Infectivity and pathogenicity of Toxoplasma gondii oocysts for cats. J Parasitol

82: 957-961

Dubey JP. 1998. Toxoplasma gondii oocyst survival under defined temperatures. J Parasitol

84:862-865

Dubey JP, Beattie CP. 1988. Toxoplasmosis of Animals and Man. Boca Raton, CRC Press, pp. 1-

40.

Dubey JP, Carpenter JL. 1993a. Neonatal toxoplasmosis in littermate cats. J Am Vet Med Assoc

203:1546-1549.

C:\Aa Old D\Dwight\CATBOOK\complete\chap1\chap1-with figs.doc

Page 29 of 112

112

Feline Clinical Parasitology – Chapter 1

Dubey JP, Carpenter JL. 1993b.Histologically confirmed clinical toxoplasmosis in cats: 100

cases (1952-1990). J Am Vet Med Assoc 203:1556-1566.

Dubey JP, Frenkel JK. 1972. Cyst-induced toxoplasmosis in cats. J. Protozool. 19:155-177.

Dubey JP, Frenkel JK. 1974. Immunity to feline toxoplasmosis: Modification by administration

of corticosteroids. Vet. Path. 11:350-379.

Dubey JP, Frenkel JK. 1976. Feline toxoplasmosis from acutely infected mice and the

development of Toxoplasma cysts. J. Protozool. 23:537-546.

Dubey and Thayer 1994.Killing of different strains of Toxoplasma gondii tissue cysts by

irradiation under defined conditions. J Parasitol 80:764-767.

Dubey JP, Thulliez P. 1989. Serologic diagnosis of toxoplasmosis in cats fed Toxoplasma gondii

tissue cysts. JAVMA 194:1297-1299.

Dubey JP, Miller NL, Frenkel JK. 1970a. Characterization of the new fecal form of Toxoplasma

gondii. J Parasitol

Dubey JP, Miller NL, Frenkel JK. 1970b. The Toxoplasma gondii oocyst from cat feces. J Exp

Med 132:636-662.

Dubey JP, Hoover EA, Walls KW. 1977. Effect of age and sex on the acquisition of immunity to

toxoplasmosis in cats. J. Protozool. 24:184-186.

Dubey JP, Quinn WJ, Weinandy D. 1987 Fatal neonatal toxoplasmosis in a bobcat (Lynx rufus).

J Wildl Dis 23:324-327.

Dubey JP, Kotula AW, Sharar AK, Sharar A, Andrews CD, Lindsay DS. 1990. Effect of high temperature on infectivity of Toxoplasma gondii tissue cysts in pork. J Parasitol 76:201-204.

Dubey JP, Lappin MR, Thulliez P.1995a. Long-term antibody responses of cats fed Toxoplasma

gondii tissue cysts. J Parasitol 81:887-893.

Dubey JP, Lappin MR, Thulliez P. 1995b. Diagnosis of induced toxoplasmosis in neonatal cats.

JAVMA 207:179-185.

Dubey JP, Jenkins MC, Thayer DW, Kwok OC, Shen SK.1996. Killing of Toxoplasma gondii

oocysts by irradiation and protective immunity induced by vaccination with irradiated

oocysts. J Parasistol 82:724-727.

Durfee PT, Cross JH, Rustam, Susanto. 1976. Toxoplasmosis in man and animals in South

Kalimantan (Borneo), Indonesia. Am J Trop Med Hyg 25:42-47.

Etheredge GD, Frenkel JK. 1995. Human Toxoplasma infection in Kuna and Embera children in

the Bayano and San Blas, eastern Panama. Am J Trop Med Hyg 53:448-457.

Fishback JL,Frenkel JK. 1990. Prospective vaccines to prevent feline shedding of Toxoplasma

oocysts. Comp. Cont. Ed. Pract. Vet.12:643-651.

Flegr J, Hrda S, Tachezy J. 1998. The role of psychological factors in questionnaire-based

studies on routes of human toxoplasmosis transmission. Cent Eur J Public Health 6:45-

50.

Frenkel JK, Parker BB. 1996. An apparent role for dogs in the transmission of Toxoplasma

gondii: the probable role of xenosmophilia. Ann. NY Acad. Sci. 791:402-407.

Frenkel JK, Ruiz A. 1980. Human toxoplasmosis and cat contact in Costa Rica. Am J Trop Med

Hyg 29:1167-1180.

Frenkel JK, Ruiz A. 1981. Endemicity of toxoplasmosis in Costa Rica. Am J Epidemiol 113:254-

269

Frenkel JK, Smith DD. 1982a. Immunization of cats against shedding of Toxoplasma oocysts. J.

Parasitol. 68:744-748.

Frenkel JK, Smith DD. 1982b. Inhibitory effects of monensin on shedding of Toxoplasma

oocysts by cats. J. Parasitol. 68:851-855.

C:\Aa Old D\Dwight\CATBOOK\complete\chap1\chap1-with figs.doc

Page 30 of 112

112

Feline Clinical Parasitology – Chapter 1

Frenkel JK, Dubey JP, Miller NL. 1970. Toxoplasma gondii in cats: Fecal stages identified as

coccidian oocysts. Science 167:893-896.

Frenkel JK, Ruiz A, Chinchilla M. 1975. Soil survival of Toxoplasma oocysts in Kansas and

Costa Rica. Am J Trop Med Hyg 24:439-443

Frenkel JK, Dubey JP, Hoff RL1976. Loss of stages after continuous passage of Toxoplasma

gondii and Besnoitia jellisoni. J Protozool 23:421-424.

Frenkel JK, Pfefferkorn ER, Smith DD, Fishback JL. 1991. Prospective vaccine prepared from a

new mutant of Toxoplasma gondii for use in cats. Am J Vet Res 52:759-63.

Frenkel JK, Hassanein KM, Hassanein RS, Brown E, Thulliez P, Quintero-Nunez R. 1995.

Transmission of Toxoplasma gondii in Panama City, Panama: a five-year prospective

cohort study of children, cats, rodents, birds, and soil. Am J Trop Med Hyg 53:458-468

Freyre A, Dubey JP, Smith DD, Frenkel JK. 1989. Oocyst- induced Toxoplasma gondii

infections in cats. J. Parasitol. 75:750-755.

Freyre A, Choromanski L, Fishback JL, Popiel I. 1993. Immunization of cats with tissue cysts, bradyzoites, and tachyzoites of the T-263 strain of Toxoplasma gondii. J Parasitol 79:716-719.

Gandahusada S. 1978. Serological study for antibodies to Toxoplasma gondii in Jakarta,

Indonesia. Southeast Asian J Trop Med Public Health 9:308-311

Ganley JP, Comstock GW. 1980. Association of cats and toxoplasmosis. Am J Epidemiol

111:238-246

Hagiwara T, Katsube Y, Muto T, Imaizumi K. 1981. Experimental feline toxoplasmosis. Japn J Vet Sci 43:329-336.

Ito S, Tsunoda K, Taki T, Nishikawa H, Matsui T. 1975. Destructive effect of heating against

Toxoplasma oocysts. Natl Inst Anim Health Q (Tokyo) 15:128-310

Jewell ML, Frenkel JK, Johnson KM, Reed V, and Ruiz A. 1972. Development of Toxoplasma

oocysts in neotropical felidae. Am. J. Trop. Med. Hyg. 21:512-517.

Konishi E, Takahashi J. 1987. Some epidemiological aspects of Toxoplasma infections in a

population of farmers in Japan. Int J Epidemiol 16:277-281

Kotula AW, Dubey JP, Sharar AK, Andrews CD, Shen SK, Lindsay DS. 1991. Effect offreezing

on infectivity of Toxoplasma gondii tissue cysts in pork. J Food Prot 54:687-690, 1.

Lappin MR. 1990. Challenging cases in internal medicine: What’s your diagnosis? Vet Med

84:448-455, 1990.

Lappin MR, Greene CE, Prestwood AK, Dawe DL, Tarleton RL. 1989a. Diagnosis of recent

Toxoplasma gondii infection in cats by use of an enzyme-linked immunosorbent assay for

immunoglobulin M. Am. J. Vet. Res. 50:1580-1585.

Lappin MR, Greene CE, Prestwood AK, Dawe DL, Tarleton RL. 1989b. Enzyme-linked

immunosorbent assay for the detection of circulating antigens of Toxoplasma gondii in

the serum of cats. Am. J. Vet. Res. 50:1586-1590.

Lappin MR, Greene CE, Winston S, Toll SL, Epstein ME. 1989c. Clinical feline

toxoplasmosis: Serological diagnosis and theraputec management of 15 cases. J. Vet. Int. Med.

3:139-143.

Lappin MR, Powell CC. 1991. Comparison of latex agglutination, indirect hemagglutination,

and ELISA techniques for the detection of Toxoplasma gondii-specific antibodies in

the serum of cats. J Vet Intern Med 5:299-301.

Lappin MR, Dawe DL, Lindl PA, Greene CE, Prestwood AK. 1991. The effect of glucocorticoid

administration on oocyst shedding, serology, and cell-mediated immune responses of cats

with recent or chronic toxoplasmosis. J. Am. Anim. Hosp. Assoc. 27:625-632.Lappin

MR, Dawe DL, Lindl P, Greene CE, Prestwood AK. 1992a. Mitogen and antigen-specific

induction of lymphoblast transformation in cats with subclinical toxoplasmosis. Vet

C:\Aa Old D\Dwight\CATBOOK\complete\chap1\chap1-with figs.doc

Page 31 of 112

112

Feline Clinical Parasitology – Chapter 1

Immunol Immunopathol 30:207-220.

Lappin MR, Gasper PW, Rose BJ, Powell CC. 1992b. Effect of primary phase feline

immunodeficiency virus infection on cats with chronic toxoplasmosis. Vet. Immunol.

Immunopathol. 35:121-131.

Lappin MR, Roberts SM, Davidson MG, Powell CC, Reif JS. 1992c. Enzyme-linked

immunosorbent assays for the detection of Toxoplasma gondii-specific antibodies and

antigens in the aqueous humor of cats. JAVMA 201:1010- 1016.

Lappin MR, Burney DP, Hill SA, Chavkin A. 1995. Detection of Toxoplasma gondii-specific IgA in the aqueous humor of cats. Am J Vet Res 56:774-778.

Lappin MR, Marks A, Greene CE, Rose BJ, Gasper PW, Powell CC, Reif JS. 1993.Effect of

feline immunodeficiency virus infection on Toxoplasma gondii-specific humoral and

cell-mediated immune responses of cats with serologic evidence of toxoplasmosis. J Vet

Intern Med 7:95-100

Lappin MR, Burney DP, Dow SW, Potter TA. 1996a. Polymerase chain reaction for the

detection of Toxoplasma gondii in aqueous humor of cats. Am J Vet Res 57:1589-1593.

Lappin MR, George JW, Pedersen NC, Barlough JE, Murphy CJ, Morse LS. 1996b. Primary

and secondary Toxoplasma gondii infections in normal and feline immunodeficiency

virus infected cats. J Parasitol 82: 733-742.

Levine ND. 1977. Taxonomy of Toxoplasma. J. Protozool. 24:36-41.

Lin DS, and Bowman DD. 1991. Cellular responses of cats with primary toxoplasmosis. J.

Parasitol. 77:272-279.

Lin DS, and Bowman DD. 1992. Macrophage functions in cats experimentally infected with

feline immunodeficiency virus and Toxoplasma gondii. Vet. Immunol. Immunopathol.

33:69-78.

Lin DS, Bowman DD, and Jacobson RH. 1992a. Immunological changes in cats with concurrent

Toxoplasma gondii and feline immunodeficiency virus infections. J. Clin. Microbiol.

30:17-24.

Lin DS, Bowman DD, Jacobson RH. 1992b. Antibody responses to Toxoplasma gondii antigens

in aqueous and cerebrospinal fluids in cats infected with T. gondii and FIV. Comp

Immuno Microbiol Infect Dis 15:293-299.

Lindsay DS, Dubey JP, Blagburun BL. 1997a. Feline toxoplasmosis and the importance of the

Toxoplasma gondii oocyst. Comp. Contin. Ed. Pract. Vet. 19:448-461.

Lindsay DS, Dubey JP, Butler JM, Blagburn BL. 1997b. Mechanical transmission of Toxoplasma gondii oocysts by dogs. Vet. Parasitol. 73:27-33.

Lindsay DS, Dubey JP, Blagburn BL, Tovio-Kinnucan MA. 1991. Examination of tissue cyst

formation by Toxoplasma gondii in cell cultures using bradyzoites, tachyzoites, and

sporozoites. J Parasitol 77:126-132.

MacKnight KT, Robinson HW. 1992. Epidemiologic studies on human and feline

toxoplasmosis. J Hyg Epidemiol Microbiol Immunol 36:37-47.

Martinez Sanchez R, Machin Sanchez R, Fachado Carvajales A, Pividal Grana J, Cruz de la

Paz R, Suarez Hernandez M. 1991. Several results of a Toxoplasma survey. Invest Clin

32:13-26.

Miller NL, Frenkel JK, Dubey JP. 1972. Oral infections with Toxoplasma cysts and oocysts in

felines, other mammals, and in birds. J Parasitol 58:928-937.

Muñana KR, Lappin MR, Powell CC, et al.1995. Sequential measurement of Toxoplasma

gondii- specific antibodies in the cerebrospinal fluid of cats with experimentally induced

toxoplasmosis. Prog Vet Neuorl 6:27-31.

Partono F, Cross JH. 1975. Toxoplasma antibodies in Indonesian and Chinese medical students

C:\Aa Old D\Dwight\CATBOOK\complete\chap1\chap1-with figs.doc

Page 32 of 112

112

Feline Clinical Parasitology – Chapter 1

in Jakarta. Southeast Asian J Trop Med Public Health 6:472-476

Patton S, Legendre AM, McGavin MD, Pelletier D. 1991. Concurrent infection with Toxoplasma

gondii and feline leukemia virus. J Vet Intern Med 5:199-201, 1991.

Remington JS, McLeod R, Desmonts G: Toxoplasmosis, in Remington JS, Klein JO (eds):

Infectious Diseases of the Fetus and Newborn Infant, 4th Edition, Philadelphia WB

Saunders, 1995, pp 140-267.

Rey LC, Ramalho IL. 1999. Seroprevalence of toxoplasmosis in Fortaleza, Ceara, Brazil. Rev

Inst Med Trop Sao Paulo 41:171-174

Ruiz A, Frenkel JK, Cerdas L.1973. Isolation of Toxoplasma from soil. J Parasitol 59:204-206.

Sedaghat A, Ardehali SM, Sadigh M, Buxton M. 1978. The prevalence of Toxoplasma infection

in southern Iran. J Trop Med Hyg 81:204-207

Sengbusch HG, Sengbusch LA. 1976. Toxoplasma antibody prevalence in veterinary personnel

and a selected population not exposed to cats. Am J Epidemiol 103:595-597

Stiles J, Prade R, Greene C. 1996. Detection of Toxoplasma gondii in feline and canine

biological samples by use of the polymerase chain reaction. Am J Vet Res 57:264- 267, 1996.

Stray-Pedersen B, Lorentzen-Styr AM. 1980. Epidemiological aspects of Toxoplasma infections

among women in Norway. Acta Obstet Gynecol Scand 59:323-326

Teutsch SM, Juranek DD, Sulzer A, Dubey JP, Sikes RK.1979. Epidemic toxoplasmosis

associated with infected cats. N Engl J Med 300:695-699.

Tizard IR, Chauhan SS, Lai CH. 1977. The prevalence and epidemiology of toxoplasmosis in

Ontario. J Hyg (Lond) 78:275-282.

Ulmanen I, Leinikki P. 1975. The role of pet cats in the seroepidemiology of toxoplasmosis.

Scand J Infect Dis 7:67-71.

Wallace MR, Rossetti RJ, Olson PE. 1993. Cats and toxoplasmosis risk in HIV- infected adults. J Am Med Assoc 269:76-77.

Zigas V. 1976. Prevalence of Toxoplasma antibodies in New Britain, Papua New Guinea. P N G

Med J 19:225-230

Figure 1-3 Toxoplasma gondii. Oocyst passed in the feces of a cat.

Figure 1-4. Toxoplasma gondii. Sporulated oocyst.

Figure 1-5. Toxoplasma gondii. Cyst of strain T264 in the brain of experimentally infected

mouse.

Figure 1-6. Toxoplasma gondii. Gametogocytes and schisonts in the epithelial cells of an

experimentally infected cat (From: Dubey JP, Frenkel JK. 1972. Cyst-induced toxoplasmosis

in cats. J Protozool 29:155-177).

Figure 1-7. Toxoplasma gondii. Focus of necrosis in a cat (H&E stained histological section,

1000X). Note numerous tachyzoites (arrows) at the periphery of the lesion.

Figure 1-8. Toxoplasma gondii. Necrotizing abscess in the brain of a naturally infected cat that

contained numerous dividing tachyzoites.

Figure 1-9. Toxoplasma gondii. Higher power view of abscess in the brain showing the

organisms.

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Figure 1-10. Toxoplasma gondii. Macrophage from the abdominal cavity of a naturally infected

cat containing numerous tachyzoites.

Figure 1-11. Toxoplasma gondii. Electron micrograph of a tachyzoite of the RH strain showing

the structures typical of this apicomplexan parasite, e.g., apical complex, rhoptries, and dense

granules. (Image kindly supplied by the late Dr. John Cummings.).

Figure 1-12. Toxoplasma gondii. Glial nodule in the cerebrum of a congenitally infected kitted

(H&E stained histological section, X300). A tissue cyst (arrow) and tachyxoites (arrowhead) are

present at the periphery of the nodule.

Figure 1-13. Toxoplasma gondii. Liver of a congenitally infected kitten.

Figure 1-14. Toxoplasma gondii. Alveolar macrophage of a cat with tachyzoites after 40 hours

of in-vitro co-culture.

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