socioeconomic conditions as determining factors in the prevalence of systemic and ocular...

Correspondence and reprint requests to:Prof. Carlos Alexandre de AmorimGarciaDept. OphthalmologyFed. Univ. Rio Grande do NorteRua Ceará Mirim, 316Tirol, Natal/RNBrazilTel.: +55-84-211-5888E-mail: [email protected]

Abstractobjective To determine the prevalence of systemic and ocular toxo-plasmosis among 1024 students in the city of Natal, NortheasternBrazil, and correlate it with demographic, socioeconomic and epi-demiological risk factors.

methods The study population was randomly selected, asked to fillout a questionnaire, provide a blood sample for IgG and IgM (MEIA)serology and a hemogram, and undergo an eye examination.

results The seroprevalence for IgG was 46% (95% CI = 42.9–49.2%)and that for IgM was 1.4% (95% CI = 0.8–2.4%). The prevalence ofocular lesions was 1.15% (95% CI = 0.6–2.0%). In the univariate analy-ses, confirmed by multivariate analysis, the socioeconomic conditionswere determinants in the prevalence of systemic and ocular toxoplas-mosis (mother’s schooling = literacy/OR = 2.9 and p < 0.001).

conclusions The prevalence of systemic toxoplasmosis, althoughhigh, was lower than that found in studies performed in the South andSoutheast of Brazil, and the incidence of ocular lesions was totally different, being lower by a factor varying from 5 to 17. Although im-portant epidemiological variables, such as owning a cat, drinking unfil-tered water or having had contact with lakes or rivers, were found to

Systemic & ocular toxoplasmosis in Northeastern Brazil 301

Ophthalmic Epidemiology0928-6586/04/US$ 22.00

Ophthalmic Epidemiology– 2004, Vol. 11, No. 4,pp. 301–317DOI: 10.1080/09286580490515170© 2004 Taylor & Francis Ltd.

Accepted 5 May 2004

Socioeconomic conditions as determiningfactors in the prevalence of systemic

and ocular toxoplasmosis in Northeastern Brazil

Carlos Alexandre de Amorim Garcia1

Fernando Oréfice5

Clélia de Oliveira Lyra2

Alexandre Bezerra Gomes1

Mardone França3

Carlos Alexandre de Amorim Garcia Filho4

Departments of 1Ophthalmology, 2Nutrition & Epidemiology,3Statistics and 4Undergraduate Medicine, Federal University of

Rio Grande do Norte, and 5Department of Ophthalmology,Federal University of Minas Gerais, Brazil

Original article

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

be correlated with toxoplasmosis in the preliminary analysis, they losttheir influence when included in the logistic model. However, furtherstudies must be undertaken to identify the reasons for these findings,including the determination of the strains of Toxoplasma gondiiencountered in different regions of the country and the sources of thewater utilized by these populations.

Key words Toxoplasmosis prevalence; socioeconomic factors; riskfactors; ocular toxoplasmosis; water pollution; Brazil

Introduction Toxoplasmosis is a cosmopolitan zoonosis caused bythe protozoon parasite Toxoplasma gondii (T. gondii). In humans, itmost often causes subclinical infections (or symptoms of the commoncold). However, it can lead to serious conditions, especially in immuno-suppressed hosts. It can cause miscarriage and congenital infection ifcontamination occurs during pregnancy. Toxoplasmic retinochoroiditiscan have grave effects, including total loss of vision.1,2

The reported prevalence in the general population elsewhere in theworld varies from 0% in Eskimos to 94% in Costa Ricans andGuatemalans.3,4 In Brazil, the prevalence of positive serology variesfrom 41.9% to 74.8%.5–11

The presence of anti-T. gondii antibodies in different populations ofthe world differs according to socioeconomic factors, age and geo-graphical area. The prevalence is high in tropical regions and relativelylow in hot and arid regions, as well as in cold countries such asNorway.12

Most T. gondii infections in humans are caused by eating raw orundercooked meat containing T. gondii cysts or eating food that hasbeen cross-contaminated with raw/undercooked meat, by ingestingoocysts from the soil, or by acquiring congenital infection through theplacenta.2

Epidemiological studies have identified a number of risk factors forT. gondii. Societies that consume large amounts of raw or undercookedmeat or meat by-products and regions lacking basic sanitation or witha high number of inhabitants per household present higher infectionrates.6,11–14 Other risk factors include: living with cats, cleaning out thecat litter box,6,14–16 having contact with soil,17,18 eating raw or unwashedvegetables or fruit, eating raw vegetables, and having poor handhygiene.6,19 Besides these, having contact with lake or river water anddrinking unfiltered water are risk factors that are currently being inves-tigated as the principal sources of toxoplasmosis transmission.5,20–23

Ocular toxoplasmosis can be congenital or acquired. The congenitalocular form may be present at birth or appear months or even yearsafterwards. The acquired form may be concomitant, occurring simulta-neously with systemic disease, or later, when there is a variable timelag between systemic and ocular disease.24–26

It is universally accepted that ocular toxoplasmosis is the principalcause of posterior uveitis; in Brazil, it is responsible for approximately70% of the cases. Fernandes and Oréfice observed that of a total of7680 cases of uveitis, 43.1% were diagnosed as ocular toxoplasmosisand of a total of 1955 cases of posterior uveitis, 72.9% were diagnosed

302 C.A. de Amorim Garcia et al.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

as toxoplasmic in origin.27 Garcia et al.28 in Natal/RN found ocularlesions due to toxoplasmosis in 54.9% of posterior uveitis patients.

In studies performed in Brazil, the prevalence of ocular toxoplasmo-sis in random population samples varied from 4.7% to 17.7%, muchlower than the prevalence of positive serology.1 In Maryland (USA), aprevalence of only 0.6% was observed.29

In view of the high prevalence of T. gondii infection and ocular tox-oplasmosis in the South and Southeast regions of Brazil reported in theliterature, the objective of this study was to estimate the prevalence ofT. gondii infection and ocular toxoplasmosis in a student population,from 5 to 21 years of age, in the northeastern city of Natal, verifyingthe possible associations with demographic, socioeconomic and epi-demiological risk factors.

Materials and methods

study area Natal, the capital of Rio Grande do Norte State, has apopulation of 700,000 and lies on the northeast coast of Brazil. ThePotengi river divides the city into two zones: the North, where approx-imately 250,000 people live, and the South, with 450,000 inhabitants. Itsclimate is tropical, with temperatures varying between 25 and 30°C, andit is situated at sea level. Only 92% of the residents receive treatedwater and of these, 15% are connected to the sewer system. Approxi-mately 80% of the residences have septic tanks and 5% have opensewers.

The city is divided into four sanitation districts: North, South, Eastand West.The West and North districts are considered to have the worstsanitary and socioeconomic conditions, but the other districts also havepockets of poverty.

study population The study population was composed of studentsbetween 5 and 21 years of age enrolled in public and private schoolsin Natal in 2001 at the primary or secondary level. Four sample popu-lations, corresponding to the four sanitation districts that divide the cityof Natal, were considered for purposes of the methodological model.

The number of students enrolled in public and private schools was119,116, distributed over the four districts of the city. The size of thesample was calculated from this population. The procedure for sampleselection comprised two separate stages: determining the generalsample size and the random selection of the schools and pupils.

The sample size was determined from parameters obtained by thesimple random sampling method for proportion, with 3% error, anexpected prevalence of 50% (as there was no a priori informationregarding this, maximum variance was used), and a confidence interval(CI) of 95%.

The calculated sample size was 1100 pupils, distributed proportion-ally throughout the 341 schools in all four districts, in such a way as toestablish the number of pupils that should be examined in each of thedistricts. Subsequently, the number of schools to be selected from eachdistrict was determined. Of 341 schools, 79 were chosen by the pro-portional probability of size method (PPS), using Delphi language soft-


Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

ware, to make up the sample, according to the nature of the institution(public and private), its level (elementary and secondary), and thestudy period (morning, afternoon and evening). Once the school wasselected and the classes per study period randomly drawn, studentswere then drawn from the class attendance sheet, obeying the propor-tionality observed in the population, and sent to the OphthalmologyDepartment, Onofre Lopes University Hospital (HUOL), Federal Uni-versity of Rio Grande do Norte (UFRN).The protocol of the study wassubmitted to and approved by the UFRN Ethics Commission, number18/01. All pupils were examined after submission of a consent formsigned by their parents or guardians.

questionnaire The pupils’ examinations were conducted betweenMarch and May of 2001. To evaluate the risk factors, a modified ques-tionnaire from a prevalence study, with 68 questions, was utilized toreveal known sources of T. gondii infection.20 The questionnaire wasfilled out by previously trained medical students and ophthalmologyresidents from UFRN. It was standardized in this manner so that bothliterate and illiterate parents would have no need to read, thus avoid-ing possible information bias.

The variables studied were categorized and divided into three groups:a) Demographic: age, sex, race, address, place of birth, district of resi-dence, type of school, study period; b) Socioeconomic: number of res-idents, rooms and bathrooms, whether the residence had a computer,refrigerator, automobile, television and videocassette player; parents’schooling and occupation; c) Epidemiological: if there were dogs or catsin the domicile, contact with dogs or cats in the neighborhood, contactwith other animals, lifestyle, such as: handling soil, going barefoot, goingto the beach or farm, contact with rivers or lakes, drinking untreatedor unfiltered water, eating raw or undercooked meat, where meat, milk,eggs, fruit and vegetables were purchased, if the residence had indoorplumbing, type of sewage disposal and pre-existing diseases.

ocular examination After filling out the questionnaire, the stu-dents underwent an ophthalmologic examination at the HUOL oph-thalmology services facility. The examination consisted of: clinicalhistory, average visual acuity using a Snellen table, ocular motility andadnexae examination, anterior segment biomicroscopy, and aplanationtonometry with a Goldman tonometer. A drop of 1% tropicamide and1% cyclopentholate was instilled and 40 minutes later, refraction andindirect binocular ophthalmoscopy were performed by two retina spe-cialists. In students who presented with chorioretinitis, the lesions werephotographed with a Canon retinograph, using the OIS digital imagingsystem, and afterwards biomicroscopy was done with a 78-diopter lensor three-mirror Goldman lens in order to classify the lesions. Thefundus photographs were analyzed by Oréfice et al.

As described by Oréfice,1 utilizing the modified classification ofGlasner et al., the cicatricial ocular lesions were classified as:*Type I: lesions with well-marked borders, generally encircled by a pig-

mentary halo and characterized by substantial retinal and choroidaldestruction; lesions with an atrophic central area with little or no pig-


Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

Fig. 1. Ocular toxoplasmosis lesiontype I (see the text for adescription).

mentation; and lesions with typical macular “cartwheel” scars, withor without a satellite lesion (see Figure 1).

*Type II: lesions characterized by a central area, typically hyperpig-mented and surrounded by a hypopigmented halo. These lesionspresent a lower degree of tissue destruction than type I, with orwithout a satellite lesion (see Figure 2).

*Type III: lesions defined as areas of pigmentary epithelium hyperpla-sia (EPR) or with less tissue destruction than type I and II lesions.Both type I and type II lesions fulfil all the morphological criteriafor probably being caused by T. gondii infection. On the other hand,the clinical presentation of type III lesions places them among agroup with uncertain etiology (see Figure 3).

serologic tests and hemogram After the ophthalmologic exam-ination, 10ml of blood was collected from a peripheral vein utilizing atube containing anticoagulant (ethylenediamine tetra-acetate) for thehemogram and another tube without anticoagulant for the serologictests. The hemogram was obtained with an automatic hematologic ana-lyzer, Cell-Dyn SL (Abbot), following the manufacturer’s instructions.


Fig. 2. Ocular toxoplasmosis lesiontype II (see the text for adescription).

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

Fig. 3. Ocular toxoplasmosis lesiontype III (see the text for adescription).

Serum samples were examined in the HUOL laboratory using theAxsym method from Abbott for toxo-G and toxo-M (microparticleimmunoassay -MEIA- to determine IgG and IgM antibodies to T.gondii in serum or human plasma). The sensitivity of this test for IgGis 99.7% (95% CI 98.8–100%) and the specificity is 99.1% (95% CI98.2–99.6%), while for IgM the sensitivity is 96.3% (95% CI92.1–98.6%) and the specificity 99.8% (95% CI 99.3–100%). Duringthe tests, a cut-off of 3 IU for a positive serology for IgG and 0.6 IU forIgM was utilized, in strict adherence to the manufacturer’s instructions.

test of reproductibilty All serum samples were refrozen afterserologic testing and a reproductibilty test was performed in 77 ran-domly selected cases 15 days after conclusion of the study for IgGserology, and in 10 cases for IgM serology.

statistical analysis The data bank was organized with the EPI-INFO program, version 6.04, in which pre-codification of the study vari-ables and information editing were performed. Data were enteredtwice to minimize the possibility of error.

For this study, frequency distribution, chi-square, odds ratios andlogistic model adjustment were utilized to detect covariables (riskfactors) with a major influence in relation to toxoplasmosis prevalencein the study population. Odds ratio association measurement was optedfor instead of the prevalence ratio to enable comparison with theregression model. Chi-square for linear tendency was performed inrelation to the variable level of schooling of the parents.

The significant variables for the occurrence of positive IgG serologywere selected for the final multivariate model in which logistic regres-sion was done, adjusting for all included variables and calculating theodds ratio as risk estimates, with a 95% confidence interval, using theSPSS statistics package for Windows, version 10.0. The model wasadjusted for the 802 cases in which there was information relative tothe variables included in it. Pearson correlation was performed for thereproductibility analysis.


Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

table 1. Prevalence oftoxoplasmosis in students associatedwith age group, skin color, district ofresidence, type of school and studyperiod – 2001.

Results Of the 1100 students in the sample, 1024 appeared for thestudy. Of these, 990 underwent toxoplasmosis serology and 31 wereexcluded for being outside the age range of interest. Of 959 toxoplas-mosis IgG serology cases, 441 (46%; 95% CI 42.9–49.2%) were posi-tive and 518 (54%; 95% CI 50.8–57.2%) negative. For IgM, 13 (1.4%;95% CI 0.8–2.4%) were positive and 946 (98.6%; 95% CI 97.6–99.2%)negative. The reproductibility test showed R = 0.91 (p < 0.001) for IgGand R = 0.89 (p < 0.001) for IgM.

Table 1 shows the toxoplasmosis prevalence in relation to age group,district of residence, type of school and study period. The toxoplasmo-sis prevalence was found to increase from 36.5% in the 5–10 year agegroup to 48.4% in the up to 21 years age group (p = 0.009). In relationto race, it was observed that the highest toxoplasmosis prevalence(58.0%) was seen among blacks and the lowest among whites (p =0.009). As to the district of residence, the prevalence was found to varyfrom 32.0% in the South District to 58.7% in the West (OR = 3.02).Analysis by school type showed a higher prevalence of toxoplasmosisamong students in the public system (49.1%) than in the private system(27.9%), the difference being significant (p < 0.001). With regard to thestudy period, the prevalence was similar between those who studied inthe morning and in the afternoon (43.0% and 45.9%, respectively);however, this percentage was much higher (66.7%) for those whostudied in the evening. There was no stastistically significant difference


Variable/ N Positive Odds Ratio 95% CI p ValueCategory Serology

n %

Age group5–10 years 203 74 36.5 1.00 p = 0.00911–15 years 444 216 48.6 1.65 1.16–2.3616–21 years 312 151 48.4 1.63 1.12–2.39

Skin colorWhite 352 143 40.6 1.00 p = 0.009Brown 519 247 47.6 1.33 1.00–1.76Black 81 47 58.0 2.02 1.20–3.40

District of residenceSouth 197 63 32.0 1.00 p < 0.001*North 344 147 42.7 1.59 1.08–2.33East 132 64 48.5 2.00 1.24–3.24West 264 155 58.7 3.02 2.02–4.54

Type of schoolPrivate 140 39 27.9 1.00Public 808 397 49.1 2.50 1.68–3.71 p < 0.001*

Study periodMorning 409 176 43.0 1.00 p = 0.005*Afternoon 492 226 45.9 1.12 0.86–1.48Evening 54 36 66.7 2.65 1.40–5.03

(*) Significant association at the 5% level.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

table 2. Distribuition of thestudents according to socioeconomiccharacteristics.

between sexes. However, women 15 years of age or older had a 51.0%chance of acquiring a T. gondii infection (data not shown in the table).

The prevalence of toxoplasmosis according to the socioeconomicvariables is shown in Table 2. The prevalence was higher among students whose residences had more than four inhabitants than amongthose who had 1–4 inhabitants (OR = 1.37; 95% CI 1.05–1.78).The rela-tion between the number of rooms and the results of serology demon-


Variable/Category N Positive Odds Ratio 95% CI p ValueSerology

N %

No of residents1–4 491 207 42.2 1.00 p = 0.016*5–17 467 233 49.9 1.37 1.05–1.78No of rooms5–17 720 314 43.6 1.00 p = 0.012*1–4 236 125 53.0 1.46 1.08–1.95No of bathrooms2 or more 280 103 36.8 1.00 p < 0.001*0 or 1 676 336 49.7 1.69 1.27–2.26ComputerYes 125 36 28.8 1.00 p < 0.001*No 823 399 48.5 2.33 1.52–3.58RefrigeratorTwo or more 132 47 35.6 1.00 p = 0.01*One 771 362 47.0 1.60 1.07–2.39None 54 30 55.6 2.26 1.13–4.53CarYes 308 113 36.7 1.00 p < 0.001*No 648 325 50.2 1.74 1.30–2.32No of television setsTwo or more 406 150 36.9 1.00 p < 0.001*One 528 274 51.9 1.84 1.40–2.42None 23 15 65.2 3.20 1.24–8.46VideocassetteYes 363 133 36.6 1.00 p < 0.001*No 586 301 51.4 1.83 1.38–2.41Mother’s level of schoolingUniversity Graduate 65 14 21.5 1.00 p < 0.001*Secondary Complete 153 48 31.4 1.67 0.80–3.50Elementary Complete/Secondary Incomplete 147 65 44.2 2.89 1.40–6.01Illiterate/Elementary Incomplete 509 271 53.2 4.15 2.16–8.07Father’s level of schoolingUniversity Graduate 60 15 25.0 1.00 p < 0.001*Secondary Complete 164 51 31.1 1.35 0.66–2.80Elementary Complete/Secondary Incomplete 122 48 39.3 1.95 0.93–4.11Illiterate/Elementary Incomplete 459 239 52.1 3.26 1.71–6.30


Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

strated that the toxoplasmosis prevalence was higher among studentswho had 1–4 rooms in their homes than among those who had 5 ormore rooms (OR = 1.46; 95% CI 1.08–1.95). As to the number of bath-rooms, there was a higher percentage of positive serology among thosewhose residences contained 0–1 bathroom (49.7%) than among thosewho had two or more bathrooms (36.8%), and there was also a signif-icant association between the two variables (OR = 1.69; 95% CI =1.27–2.26). With regard to the absence of a computer in the home(48.5%), an automobile (50.2%) or a videocassette player (51.4%), thetoxoplasmosis prevalence was higher among those who did not ownthese items than among those who did (p < 0.001). Among the eco-nomic variables, not owning a refrigerator or television set were sig-nificant risk factors for having a positive serology (OR = 2.26; 95% CI= 1.13–4.53; OR = 3.20; 95% CI = 1.24–8.46; respectively).A lower levelof parental schooling increased the toxoplasmosis prevalence (mother:c2 for linear tendency = 39.5, p < 0.001; father: c2 for linear tendency =32.5, p < 0.001).

Among the variables selected as epidemiological characteristics(Table 3), contact with rivers or lakes (OR = 1.31; 95% CI = 1.01–1.70),owning a cat (OR = 1.47; 95% CI = 1.13–1.92), going barefoot (OR =1.33; 95% CI = 1.03–1.72), drinking untreated water (OR = 1.46; 95%CI = 1.01–2.11), purchasing meat (OR = 1.50; 95% CI = 1.14–1.98) andvegetables (OR = 1.35; 95% CI = 1.03–1.76) in open-air markets andresiding in houses with open sewers (OR = 2.91; 95% CI = 1.46–5.86)were found to be risk factors for a positive serology. As to thehemogram, a number of eosinophils greater than 5% was the only vari-able that demonstrated a significant statistical relation with the serol-ogy (OR = 1.74; 95% CI = 1.33–2.27).

In Table 4, the variables included in the logistic model from thebivariate analysis and the variables selected at a 15.0% significancelevel for the final model are presented with estimates, the significanceof each category and odds ratios. These were: age group, mother’s levelof schooling, type of sewer system, district of residence, percentage ofeosinophils and the presence of cats in the domicile. Except for the cat-in-domicile variable, the others were significant at the 5% level. Theestimates and p- and OR values show that the probability of a positiveserology for toxoplasmosis increases with age, an eosinophil countgreater than or equal to 5%, a decreasing level of maternal schooling,and living in a residence with an open sewer; it is highest among resi-dents of the West District, followed by residents in the East and lowestamong residents in the South. There was no significant differencebetween the absolute and adjusted ORs for all variables, except for thedistrict of residence, for which the risk was diminished (West, ORabsolute = 3.02; p < 0.001, and OR adjusted = 2.0; p = 0.003). The result-ing model was significant according to the Verisimilitude Ratio for statistical results, whose value was p < 0.001 for the occurrence of toxoplasmosis.

Of 13 students who presented a positive serology for IgM, 11 (84.6%)were females, 9 (69.2%) resided in the North and West Districts, 8(61.5%) of their mothers had a low level of schooling (elementaryschool incomplete), 12 (92.3%) did not own a computer and 12 (92.3%)


Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.


table 3. Distribution of thestudents according toepidemiological characteristics.

Variable/Category N Positive Odds Ratio 95% CI p ValueSerology

N %

Contact with rivers or lakesNo 453 192 42.4 1.00 p = 0.02*Yes 500 246 49.2 1.31 1.01–1.70Where meat purchasedSupermarket 596 253 42.4 1.00 p = 0.003*Butcher’s, open-air 346 182 52.6 1.50 1.14–1.98

marketNo of dogsTwo or more 170 69 40.6 1.00 p = 0.168One 327 146 44.6 1.18 0.80–1.75None 458 223 48.7 1.39 0.96–2.02Cats in the houseNo 598 253 42.3 1.00 p = 0.004*Yes 349 181 51.9 1.47 1.13–1.92Type of sewer systemSeptic tank 715 309 43.2 1.00 p = 0.001*Indoor plumbing 168 88 52.4 1.45 1.02–2.05Open sewers 45 31 68.9 2.91 1.46–5.86Walks barefootNo 411 172 41.8 1.00 p = 0.017*Yes 543 266 49.0 1.33 1.03–1.72Consumes untreated waterNo 809 360 44.5 1.00 p = 0.024*Yes 135 73 54.1 1.46 1.01–2.11Where vegetables purchasedSupermarket 518 220 42.5 1.00 p = 0.022*Open-air market 435 217 49.9 1.35 1.03–1.76EosinophilsUp to 4.99 469 183 39.0 1.00 p < 0.001*5.00 or more 486 256 52.7 1.74 1.33–2.27


did not consume raw meat.All the students with a positive serology forIgM were also positive for IgG and studied in public schools (Table 5).

The prevalence of ocular lesions due to toxoplasmosis was 1.15% (n= 11; 95% CI = 0.6–2.0%); six students presented only type II lesions,one had type III and four had type II and III. Only one student had atype II lesion in both eyes and a visual acuity of 20/20. Only two stu-dents presented with a visual acuity of 20/200 or worse in the affectedeye. The average age was 14.4 years. The majority had no contact withcats (7 students of 11) and studied in public schools (9 of 11). All of theparents had a low level of schooling and treated water in their resi-dences. With regard to serology, all were negative for IgM and 9 had apositive serology for IgG.

Discussion The prevalence of a positive serology for toxo-plasmosis was found to be similar to that reported in the majority of

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.


table 4. Results of logistic regression for toxoplasmosis prevalence.

Variables included in the Selected variables Parameter estimates P-value Odds Ratioinitial model for the final model

1- Age group (in years) 1 – Age group (in years) P = 0.002*5–10 5–1011–15 11–15 0.708 P < 0.001* 2.03016–21 16–21 0.792 P < 0.001* 2.2052- Mother’s schooling 2 Mother’s schooling P < 0.001*Illiterate/Elementary incomplete Illiterate/Elementary incomplete 1.061 P = 0.002* 2.889Elementary complete/Secondary Elementary complete/Secondary 0.822 P = 0.028* 2.274

incomplete incompleteSecondary complete Secondary complete 0.307 P = 0.413* 1.359University graduate University graduate3- Number of residents 4 Sewer system P = 0.045*1–4 Indoor plumbing5–23 Septic tank -0.270 P = 0.172 0.764

Open-air sewer 0.555 P = 0.171* 1.7424 Sewer systemIndoor plumbing 5 District of Residence P = 0.009*Septic tank WestOpen-air sewer East 0.692 P = 0.003* 1.998

North 0.567 P = 0.038* 1.7645- District of Residence South 0.220 P = 0.324 1.246WestEast 11 – EosinophilsNorth Up to 4.99 0.429 P = 0.005* 1.536South 5.00 or more6- Type of school 12 – Cat in the housePublic Yes 0.246 P = 0.118 1.279Private No7- Study periodMorningAfternoonEvening8- ComputerYesNoContact with rivers or lakesYesNo10- Consumes untreated waterYesNo11- EosinophilsUp to 4.995.00 or more12- Cat in the houseYesNo

(*) Parameter significant to the 5% level.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

table 5. Seropositive cases for IgMand selected variables in studentsfrom Natal, Brazil – 2001.

other countries. Notably, however, a lower prevalence was observedwhen these data were compared with those of national studies (Table 6).2,5–10,14–16,18,30–36 This could be due to the fact that these studieswere concentrated in the South/Southeast regions of the country, wherethe population habitually eats undercooked meat (one of the riskfactors for toxoplasmosis), and also because of the age group selectedfor the study.15,30,37

In a study conducted in Natal by Araújo et al.,10 the seroprevalencein blood donors was 80% in the 17–59 year age group and 60% in theup to 21 years age group. This probably occurred because the popula-tion consisted of adults, and because the sanitary and living conditionswere more precarious at that time. The positive serology findings differfrom those found in the south of the country, Rio de Janeiro andParana, when the same age groups are compared.7,9 In contrast to Joneset al.,2 there was significantly more positive serology among the blackstudents, possibly due to the socioeconomic conditions of this group inBrazil.

Consistent with other studies,14,38,39 the socioeconomic findings werestrongly associated with a positive serology for toxoplasmosis. Resi-dence in the West district (the poorest of the city), studying in publicschools, where the family income is usually very low, studying in theevening (due to the fact that evening students are from the lowestsocioeconomic classes, requiring them to work during the day), as wellas residences with the poorest living conditions and the fewest domes-tic appliances were socioeconomic factors that increased the risk oftoxoplasmosis infection. The parents’ level of schooling showed astrong association with positive seroprevalence: the lesser the parents’schooling, the higher the probability of acquiring toxoplamosis, in con-trast to the study of Jones et al.2

In 1999, Aramine et al. found that domestic cats contaminated waterreservoirs with T. gondii oocytes.23 The results of bivariate analysis indi-


Age Sex IgM IgG District M. S. Computer Bathroom Raw meat Schoolconsumption

7 F 0.688 15,000.0 NI NI No 1 No Public10 F 1.150 130.1 West EI No 1 No Public11 F 0.612 40.5 West EI No 1 No Public12 M 0.683 248.3 East EI Yes 1 No Public12 M 0.976 764.1 West EI No 0 No Public13 F 0.756 1,591.7 North NI No 2 or + No Public13 F 1.170 331.9 North EI No 1 No Public15 F 1.626 3,000.0 South S No 1 No Public16 F 1.041 66.7 West S No 1 No Public16 F 2.700 149.4 West EI No 1 No Private17 F 0.682 333.7 East EI No 2 or + No Public18 F 1.170 178.1 North S No 2 or + Yes Public21 F 0.609 250.1 North EI No 1 No Public

M = Male, F = Female, EI = Elementary school incomplete, S = Secondary school, NI = No Information, M.S. = Mother’sschooling.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

cated higher ORs in students who had contact with lakes or rivers anddrank untreated water. In studies carried out in Taiwan in 200221 andin the Dominican Republic in 1987,22 a relation was also observedbetween consuming untreated water and toxoplasmosis seropreva-lence. In Brazil, Bahia-Oliveira et al.20 confirmed this association, ver-ifying that individuals who drank untreated water had almost threetimes as high a probability of acquiring toxoplasmosis.

In contrast to other studies,15,30,37 the habit of consuming raw meatwas not associated with positive seroprevalence. Another finding wasthe positive association between toxoplamosis and those who boughtmeat and vegetables in open-air markets, since these establishments donot provide adequate hygienic conditions for their products.

Several studies have reported an association between toxoplasmosisand the presence of cats in the domicile.6,14,30,35 Despite this associationnot having been found positive in multiple logistic regression, there wasa 47% greater probability in bivariate analysis compared to those whodid not own a cat, confirming the important role that these animals playin the epidemiology of the disease.

Anderson et al.40 suggested that eosinophilia may serve as an earlydiagnostic marker for toxoplasmosis. It should be pointed out thateosinophilia was the only hemogram parameter that showed any asso-ciation (in this case positive) with toxoplasmosis: the greater the per-centage of eosinophils, the greater the prevalence, in contrast to theresults obtained by Hakim et al.41 and Rocha et al.42 This fact deservesfurther study, since feces parasitology was not done to confirm a highprevalence of verminosis, which is a common cause of eosinophilia.


Study Prevalence Sample Age Group Location

IgG% IgM

Garcia, CA, 2001 46.0 1.3% 959 5–21, years Natal, RN/BrazilJones, JL et al., 20012 22.5 – 27.145 12–70 USACoura, JR et al., 19935 65.8 – 406 – Middle Solimöes Area, BrazilRey, LC et al., 19996 58.4 – 584 7–18 Ceará, BrazilSouza, WJS et al., 19877 68.4 NR* 608 6–14 RJ, BrazilCantos, GA et al., 19998 41.9 0.87% 2994 – SC, BrazilGarcia, JL et al., 19999 82.9 – 82 7–82 Jaguapita, PR, BrazilAraújo, IF et al., 197510 82.5 – 183 17–58 Natal-RN, BrazilDíaz-Suárez et al., 200114 36.6 – 254 1–76 Maracaibo, VenezuelaIihoshi, N et al., 199715 57.6 – 394 – Santa Cruz de la Sierra, BoliviaChacin-Bonilla, L et al., 200116 49.7 – 447 1–69 VenezuelaSanchez, RM et al., 198918 55.9 – 284 1–30 Ciego de Ávila Province, CubaArias, ML et al., 199630 76.0 – 1234 1–30 Costa RicaMeisheri, YV et al., 199731 30.9 NR* 165 18–50 Bombay, IndiaDuong, TH et al., 199232 63.0 19.0 1178 6 months–30 years Libreville, GabonLopez, R et al., 199333 15.35 3.28 274 1–15 Havana, CubaCatar, G et al., 199234 15.3 – 640 3–70 Vientiane Province, LaosPereira, LH et al., 199235 3.3 – 998 1–17 Nova Scotia, CanadaBarbier, D et al., 198336 60.0 – 3238 0–78 Guadalupe, French Guyana

NR, Negative response

table 6. Comparative studiesrelated to seropositive prevalence fortoxoplasmosis.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.


A positive serology for IgM in relation to toxoplasmosis confirmsrecent infection and, in pregnant women, becomes the principal riskfactor for developing congenital toxoplasmosis (cerebral and ocular)or undergoing a miscarriage during the first three months of preg-nancy.43 In this study, IgM seroprevalence was 1.3% higher than thatencountered by Cantos et al.,8 in a study in Santa Catarina (Brazil),which was 0.87% and thus lower than that observed in Libreville,Gabon (19%)32 and in Cuba (3.28%).33 All 608 students tested for IgMserology for toxoplasmosis by Souza et al.7 in Rio de Janeiro, Brazilwere negative, in contrast to the findings presented in this study.

The age group for this study was selected on the basis of Glasner’sresults,44 which showed a greater prevalence of ocular toxoplasmosis(25.5%) in the up-to-21 age group and 17.5% in the population as awhole. This was the first study on the prevalence of ocular toxoplas-mosis conducted in the Northeast region of Brazil. The prevalence ofocular toxoplasmosis encountered was similar to that of the study inMaryland (USA);29 however, this is not a valid comparison since all agegroups were investigated and the results are totally discordant with theprevalence observed in studies performed in the South and Southeastof Brazil by Glasner et al.,44 who found 17.7%, Abreu et al.45 (11.2%)and Oréfice1 (10%). However, it should be noted that although theprevalence of a positive serology for IgG was high (46%), the incidenceof toxoplasmosis in this specific population of students up to 21 yearsof age was low (1.15%). Ocular lesions type II and III were found inonly 11 cases, in contrast to the study of Glasner et al.44 who encoun-tered 128 cases of type I lesions, considered to be the classic toxoplas-mosis ocular lesion, out of a total of 184. It should be pointed out thatthe Glasner et al. Type 1 classification corresponds to the Oréfice Type1 classification. It was expected that with a prevalence of positive serol-ogy of 46%, ocular toxoplasmosis (OT) would be more common thanwas actually encountered, as was observed by Silveira; in this study, IgG= 46% and OT = 1.15%, while in that of Silveira,11 IgG = 75% and OT= 17.7%. Of 11 cases with ocular lesions suggestive of toxoplasmosis,two presented negative serology, which corroborates other studies.11,46

In contrast to Glasner et al.,44 we found a significant associationbetween socioeconomic conditions and the prevalence of ocular toxo-plasmosis (p < 0.001).

The limitations of a prevalence study of this nature are related to thepossible exclusion of cases among students who do not attend schooldue to various problems (health, socioeconomic, etc.), as well as to thefact that it is not possible to translate the results to another populationthat has not yet been studied.

On the basis of these findings, it can be stated that the prevalance ofT. gondii infection, although considered to be high, was lower than thatencountered in studies in the South and Southeast of Brazil.The preva-lences of positive serology for IgG, IgM and ocular toxoplasmic lesionswere strongly associated with the socioeconomic conditions. Althoughimportant epidemiological variables such as owning a cat, drinkinguntreated water and having contact with rivers or lakes showed a rela-tion in preliminary analysis, they lost their influence when included inthe logistic model. It is surprising that the prevalence of ocular toxo-

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.


References1 Oréfice F. Uveíte: Clínica &

Cirúrgica: Atlas e Texto. Rio deJaneiro: Cultura Médica, 2000.

2 Jones JL, Kruszon-Moran D, WilsonM, et al. Toxoplasma gondiiinfection in the United States:seroprevalence and risk factors.Am J Epidemiol. 2001;154(4):357–365.

3 Gibson GL, Coleman N. Theprevalence of toxoplasma antibodiesin Guatemala and Costa Rica. Am JTrop Med Hyg. 1958;7:334–338.

4 Feldman HA. Epidemiology ofToxoplasma infection. EpidemiolRev. 1982;4:204–213.

5 Coura AJR, Willcox HPF,Albuquerque BC, et al. Aspectosepidemiológicos, sociais e sanitáriosem áreas do Médio Solimões. I –Estudo das localidades de SãoFrancisco do Laranjal, Aranaí e SãoLázaro do Surubim, município deCoari, Amazonas. Acad Nac Med.1993;153(3):122–126.

6 Rey LC, Ramalho IL.Seroprevalence of toxoplasmosis inFortaleza-Ceará, Brazil. Rev InstMed Trop São Paulo. 1999;41(3):171–174.

7 Souza WJ, Coutinho SG, LopesCWG, et al. Epidemiological aspectsof toxoplasmosis in school childrenresiding in localities with urban orrural characteristics within the cityof Rio de Janeiro, Brazil. Mem InstOswaldo Cruz. 1987;82(4):475–482.

8 Cantos GA, Prando MD, SiqueiraMV, Teixeira RM. Toxoplasmose:ocorrência de anticorpos anti-Toxoplasma gondii e diagnóstico.Rev Inst Ciênci Saúde. 1999;17(1):7–14.

9 Garcia JL, Navarro IT, Ogawa L,et al. Seroepidemiology oftoxoplasmosis and ocular evaluationby Amsler grid in patients from the

rural area treated at the Jaguapitacounty health center, Parana State,Brazil. Rev Soc Bras Med Trop.1999;32(6):671–676.

10 Araújo IF, Sant’anna B, HyakutakeS. Prevalência de anticorpos anti-Toxoplasma gondii em doadores desangue de Natal (RN). Rev FarmBioqim Univ S. Paulo. 1975;13(2):417–425.

11 Silveira CAM. Toxoplasmose:Dúvidas e Controvérsias.Erechim/RS: Editora FAPES,2000.

12 Jenum PA, Kapperud G, Stray-Pedersen B, et al. Prevalence ofToxoplasma gondii specificimmunoglobulin G antibodiesamong pregnant women in Norway. Epidemiol Infect. 1998;120:87–92.

13 Amato Neto V, Medeiros EAS, LeviGC, Duarte MIS. Toxoplasmose. SãoPaulo: Sarvier, 1995.

14 Díaz-Suárez O, Parra AM, Araujo-Fernández M. Seroepidemiology of toxoplasmosis in a marginalcommunity of the Municipality of Maracaibo, Zulia State,Venezuela. Invest Clin. 2001;42(2):107–121.

15 Ihoshi N, Gianella A. Toxoplasmosisen un grupo de estudiantes de SantaCruz de la Sierra. Bol Cientif deCENETROP. 1997;XVI:46–48.

16 Chacin-Bonilla L, Sanchez-ChavezY, Monsalve F, Estevez J.Seroepidemiology of toxoplasmosisin Amerindians from WesternVenezuela. Am J Trop Med Hyg.2001;65(2):131–135.

17 Cook AJ, Gilbert RE, Buffolano W.Sources of toxoplasma infection inpregnant women: Europeanmulticentre case-control study.European Research Network onCongenital Toxoplasmosis. Br MedJ. 2000;321:142–147.

plasmosis was so different from that found in studies in the South andSoutheast of Brazil. It is suggested that other studies be conducted toidentify the reason for this discrepancy, for example by identifying thestrains of T. gondii encountered in different regions of Brazil and thesources of water utilized by these populations.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

18 Sanchez RM, Sanchez RM,Hernandez MS, Carvajales AF.Aspectos seroepidemiologicos de latoxoplasmosis en 2 municipios de laProvincia de Ciego de Avila.Septiembre 1985. Rev Cubana MedTrop. 1989;41(2):214–225.

19 Baril L, Ancelle T, Goulet V. Riskfactors for toxoplasma infection inpregnancy: a case-control study inFrance. Scand J Infect Dis.1999;31:305–309.

20 Bahia-Oliveira LMG, Jones JL,Azevedo-Silva J, et al. Highlyendemic, waterborne toxoplasmosisin North Rio de Janeiro State,Brazil. Emerg Infect Dis. 2003;9(1):55–62.

21 Fan CK, Su KE, Wu GH, Chiou HY.Seroepidemiology of Toxoplasmagondii infection among twomountain aboriginal populationsand southeast Asian laborers inTaiwan. J Parasitol. 2002;88(2):411–414.

22 Guzmán A, Bautista I, Grassais A,et al. Prevalencia de anticuerpospara Toxoplasma gondii enadolescentes femeninas de estratossocio-económicos diferentes. ArchDominicana Pediatr. 1987;23(3):S/135–S/137.

23 Aramine JJ, Stephen C, Dubey UP,et al. Potential contamination ofdrinking water with Toxoplasmagondii oocysts. Epidemiol Infect.1999;122:305–315.

24 Beniz J. Toxoplasmose ocularadquirida (relato de 3 casos). ArqBras Oftalmol. 1993;56:134–136.

25 Montoya JG, Remington JS.Toxoplasmic chorioretinitis in the setting of acute acquiredtoxoplasmosis. Clin Infect Dis. 1996;23:277–282.

26 Burnett AJ, Shortt SG, Isaac-RentonJ, et al. Multiple cases of acquiredtoxoplasmosis retinitis presenting inan outbreak. Ophthalmology. 1998;105(6):1032–1037.

27 Fernandes LC, Oréfice F. Aspectosclínicos e epidemiológicos dasuveítes em serviço de referência emBelo Horizonte 1970–1993, Parte I.Rev Bras Oftalmol. 1996;55:569–578.

28 Garcia CAA, Gomes AHB, BarbosaMFA, et al. Aspectos clínicos eepidemiológicos das uveítes emNatal – RN. Rev Bras Oftalmol.2002;61(2):121–129.

29 Smith RE, Ganley JP. Ophthalmicsurvey of a community. 1.Abnormalities of the ocular fundi.Am J Ophthalmol. 1972;74:1126.

30 Arias ML, Chinchilla M, Reyes LL,Linder E. Seroepidemiology oftoxoplasmosis in humans: possibletransmission routes in Costa Rica.Rev Biol Trop. 1996;44(2A):377–381.

31 Meisheri YV, Mehta S, Patel U. Aprospective study of seroprevalenceof Toxoplasmosis in generalpopulation, and in HIV/AIDSpatients in Bombay, India. JPostgrad Med. 1997;43:93–97.

32 Duong TH, Dufillot D, Martz M, etal. Etude sero-epidemiologique de latoxoplasmose a Libreville, Gabon.Ann Soc Belg Med Trop. 1992;72(4):289–293.

33 López R, Pérez X, Collazo JE,Acosta C. Anticuerpo anti-toxoplasma gondii en niños cubanos.Biomedica. 1993;13(4):183–186.

34 Catár G, Giboda M, Gutvirth J,Hongvanthong B.Seroepidemiological study oftoxoplasmosis in Laos. SoutheastAsian J Trop Med Publ Health.1992;23(3):491–492.

35 Pereira LH, Staudt M, Tanner CE,Embil JA. Exposure to Toxoplasmagondii and cat ownership in NovaScotia. Pediatrics. 1992;89(6 Pt2):1169–1172.

36 Barbier D, Ancelle T, Martin-BouyerG. Seroepidemiological survey oftoxoplasmosis in La Guadeloupe,French West Indies. Am J Trop MedHyg. 1983;32(5):935–942.

37 Couver J, Desmont G. Les modes depropagation de la toxoplasmosehumaine. Arch Franc Pediatr.1965;18:1026–1032.

38 Sadaruddin A, Agha F, Ghafoor A.Seroepidemiology of Toxoplasmagondii infection in young schoolchildren in Islamabad. J Pak MedAssoc. 1991;41(6):131–134.


Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.


39 Velasco-Castrejon O, Salvatierra-Izaba B, Valdespino JL, et al.Seroepidemiology of toxoplasmosisin Mexico. Salud Publ Mex. 1992;34(2):222–229.

40 Anderson KP, Atlas E, Ahern MJ,Weisbrot IM. Central nervoussystem toxoplasmosis in homosexualmen. Am J Med. 1983;75:877–881.

41 Hakim SL, Radzan T, Nazman M.Distribution of anti-Toxoplasmagondii antibodies among Orang Asli(aborigines) in Peninsular Malaysia.Southeast Asian J Trop Med PublHealth. 1994;25(3):485–489.

42 Rocha OM, Carvalho MG, SilvaMBS, Lignani C. RemanescentesXakriabá em Minas Gerais:Prevalência da doença de Chagas etoxoplasmose e avaliação do quadrohematológico dos infectados. RevFarm Bioquím. 1987;8:19–27.

43 Koppe JG, Loewer-Sieger DH,Roever BH. Results of 20-yearfollow-up of congenitaltoxoplasmosis. Lancet. 1986;1(8475):254–256.

44 Glasner PD, Silveira C, Kruszon-Moran D, et al. An unusually highprevalence of ocular toxoplasmosisin southern Brazil. Am JOphthalmol. 1992;114(2):136–144.

45 Abreu MT, Boni D, Belfort Jr R, etal. Toxoplasmose ocular em VendaNova do Imigrante, ES, Brasil.Arq Bras Oftalmol. 1998;61:540–545.

46 Adams WH, Kindermann WR, WallsKW, Heotis PM. Toxoplasmaantibodies and retinochoroiditis inthe Marshall Islands and theirassociation with exposure toradioactive fallout. Am J Trop MedHyg. 1987;36(2):315–320.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

Oph

thal

mic

Epi

dem

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Mel

bour

ne o

n 11

/16/

14Fo

r pe

rson

al u

se o

nly.

socioeconomic conditions as determining factors in the prevalence of systemic and ocular...

Documents