Jpn. J. Infect. Dis., 53, 238‑241, 2000

Epidemiological ReportHigh Prevalence of Antibody to Toxoplasma gondii among Humans in･ Surabaya, Indonesia
Eiji Konishi*, Yumi Houki, Kazuyoshi HaranoI**, Retno S･ Mibawani2,
Djoko Marsudi2, Soetrisno Alibasah2 and Woes P･ Dachlan3
Department of Health Sciences, Kobe UniversiO, School ofMedicine,
Tomogaoka 7‑10‑2, Suma‑ku, Kobe 654‑0142, Japan,

lEmergency Medical Care System ofDoctor Soetomo Hospital,
Japan International Cooperation Agency and

2Emergency Unit, Doctor Soetomo Hospital, Surabaya 60286 and3Tropical Disease Center, Airlangga UniversioI, Surabaya 6011 5, Indonesia(Received November 6, 2000. Accepted December 26, 2000)

SUMMARY: Infection with Toxoplasma gondii is of medical importance in relation to a recent increase in casesof acquired immunodeficiency syndrome (AIDS). In the present study, we surveyed antibody to Toxoplasmaamong 1 ,76 1 people in Surabaya, Indonesia. The overall prevalence was 5 8% with significant differences between

males (63%) and females (52%; P < 0･001)･ Although antibody prevalences at 0‑9 years in both genders wereless than l0%, those at ages over 10 years were more than 50% in males or more than 40%infemales, suggestlng
an extremely high transmission rate of the parasite to humans in this area. A bimodal pattem in the frequency
distribution of Toxoplasma antibody levels suggested a persistent feature of Toxoplasma infection in humans･

surveys carried out in this country have revealed a wide rangelNTRODUCTION

from 2% to 63% (6‑8) among a variety of human.popula‑tions. Surabaya is the second largest cityin Indonesia With aToxoplama gondii is an intracellular protozoanparasite that

can infect a varietyofhosts ranging from birds to marrmals.
Humans, once infected with Toxoplasma, persistently harbor

population of approximately 3 million. Two previous suⅣeysof Surabaya populations revealed much different prevalences

anisms carmot elinhate the cyst form of Toxopla!ma. Epidemiol

of9% (9) and 63% (10). We revealed inthe present survey ofover 1 ,700peOple that the overall prevalence was 58% With

logical studies have indicated that this parasite is ubiquitously

a slgnificantly higher prevalence in males than females in

distributed throughout the world (1 )･ Although the mFjority

SOme age grOupS･

this parasite throughout the life, since human defense mech‑of infectionsare found to be asymptomatic, this paraslte Can
cause congenital infections in infants and acute infections in

MATERIALS AND METHODS

imunocompromised individuals. Therefわre, the increase inpatients with acquired immunodeficiency syndrome (AlDS)

Study subjects: A total of I,761 sera were collected fromhas contributed to the increase in Toxoplasma encephalitis

general patients at the Emergency Unit of Doctor Soetomo
Hospltal in Surabaya, Indonesia, from November 1999

(2) and pn.eumonia cases (3)･

through March 2000. The ages of the patients ranged from 0 to

The reglOn Of South and Southeast Asia is reported to havean estimate of 6 million people infected with human immuno‑

1 00 years, and the patients were grouped at 1 0‑yearincrements,

deficiency virus (HIV), the second largest such population in

except for those over 80 years which were grouped in one age

the world. Although the largest population with HIV/AlDS isgroup. Serum samples from babies less than 6 months old,

distributed in sub‑Saharan Africa, the recent rapid growth of
HIV/AIDS populations in Southem and Eastern Asia is awhich may have contained matemally transferred antibodies,were not used in this suⅣey. Age and sex compositions ofserious concem (4). Therefore, the epidemiology of Toxoplasma
infection in this region is important in relation to the possible

acqulSltlOn Of opportunistic TToxoplasma infection. We have

Table. Age and sex compositions of the present survey population

previously surveyed Toxoplasma antibody among people in

Age

the PhilipplneS and revealed an overall prevalence of 1 1% in

Numberof(years)Fn urban area (Metro Manila) and much higher prevalences
ln rural areas, such as Mindoro (61%), andLeyte (30%;

IndividualsMaleFemaletJ 7 2 5 0 2 つJ 2 1 0ノ 史U 5 8 人V ′0 つJ つJ ′0 4

0‑9

To

tat
∠U 2 4 0 4 5 0 0 4 /b

3 4 2 つJ 4 2 5 /b 2 4 0 5 2 1 0 0ノ 0 0ノ 3 7

̲ 0203 0405 0607080‑恥 ̲ 92939495 96979̲ 0 山

Kawashima et al･, in submission)･ These prevalences in γal

12 2 2 7lllIIl ‑areas were relatively high in comparison with our prevlOuS

1 1 1 1‑1 1 911111 8survey data (20%) from arural area in Japan (5).
In this study, we surveyed the prevalence of noxoplasma

antibodies among people in Surabaya, Indonesia. Previous*Corresponding author: Tel/Fax: +81178‑796‑4594, E‑mail:ekon@ams.kobe‑u. acjp**Present ad血ess: St. Mary's Hosp血1, Kurume 830‑8543, Japan

1

238

9 つJ 7 0ノ ′8 5 1 2 nフ lFig. L Geographical map of Indonesia (hatched lines) and neighboring countries. Arrows show the locations of Surabaya
and the capital, Jakarta.

the study subjects are shownin Table. Mean ages (j: standard
deviation 【SD】) were 44.9 (±22. 1) years in males, 45.2 (±19.5)

3 NjlV^jtjd%

y.ears in females and 45･0 (±20･3) years in total with noslgnificant differences between males and females (i ‑ 0.303 ;P > 0.05). The location ofSurabaya in Indonesia is shown in

Fig.1.

Enzyme‑linked immtmosorbent assay (ELISA) system:
Crude soluble IToxoplasma antlgen used for ELISA wasprepared from tachyzoites of the M strain of T. gondii aspreviously described (1 I). Brieny, tachyzoites harvested in

the peritoneal cavityof mice were filtered through a poly‑
carbonate membrane, homogenizedand clarified. The supema‑

tant was stored at ‑30oC untilused for ELISA.
The ELISA for measurlng antibodies to Toxoplasma was
performed as previously described ( 1 2) with some modifica‑

tions( 1 3). ln brief, microplate wells sensitizedwith Toxoplasma0

antlgen Were incubated serially with test sera, alkaline

phosphatase‑conJ ugated anti‑human IgG, and p‑nitrophenyl
phosphate. Absorbance values obtained in duplicate at 4 I 0 nm

20

40

60

80

AGE (YEARS)

were averaged and a4justed with the value fわr the positive

control as I.0 to minimize interplate variations. Sera showlng

Fig. 2. Age‑prevalence curve for Toxoplasma antibody in males (filledadjusted values (EuSA values) of more than 0.357, which is

circle), females (Open circle) andthe total population (filled square).

the cutoffvalue established previously ( I 2, I 3), Were determined

Significant diffTercnces between males and females are shown by*(P<0.001), I (P<0.01)and i (P<0.05).

to be positive for Toxoplasma antibody.

Statistical analysis: Significance of differences in preva‑
lence rates was evaluated by the chi‑square test with the Yates'

correction factor. Significance of differences in mean ELISA

prevalences were also obseⅣed in age groups over 20 years

for both malesand females. Males showed significantly higher

values was evaluated by the Student's i test.

prevalences than females in age groups of20‑29 (X2 ‑ 4.95;

P< 0.05), 30‑39 (X2‑ 14.5;P< 0.001), and 70‑79

RES UIXS(X2 ‑ 8.86; P< 0.01) years.
Distribution of ToxopLasma antibody levels: Figure 3

Prevalencc of ToxopLasma antibody: Figure 2 shows
age‑dependent prevalence curves obtained with 9 14 males,

shows frequency distributions of EuSA values determined

847 fTemales, and a total of 1,761 serum samples. The overall

for male, female and the total populations. The maximum

value was 1.750 in males and I.636 infemales. The distribu‑

prevalence was 63.2% in males, 52.4% in females and 58.0%
in the total population, with a slgnificant difference between
males and females (X2 ‑ 20.7; P < 0.001). The prevalence oftion pattem was bimodal in both 甚enders with the negative

group at a peak ofO.0‑0.I and the positive group at a peak ofantibody at 0‑9 years was less than lO% in both males andfemales, which increased significantly to more than 50% in
males (X2 ‑ 19.4; P < 0.001) and more than 40% in females

0.5‑0.8. The mean ELISA values (±SD) of antibody‑positive
specimens were 0.758 (±0.261) in males and 0.763 (±0.261)

in females without signiflCant differences (t ‑ 0.346; P > 0.05).
Comparison of age groups in aequency distribution ofELISA(X2 ‑ 9.6; P < 0.01) at 10‑19 years. These high antibody

239

study of pregnant women across Europe polnted out that
2 1 0

00

0

the ingestion of raw meat is the major transmission route ofMale

Toxoplasma infection (27)･ Concems about food‑bone parasi.tic

diseases have been raised in some Southeast Asian countrleS(20, 28‑30)･ including Indonesia (3 I )･ However, since lndon?‑siam people do not have a habit of eatlng raw meat, the malnmechanism of TToxoplasma transmission in the Surabaya

SIV⊃凸一≧凸N一山0庄山gM⊃N
2 1 0

00

population is considered to be the accidental ingestion or the

Female‑0oocyst. Positive noxoplasma antibody prevalences among
animal populations in several areas of Indonesia support that

Toxoplasma oocysts are broadly distributed in this country(6, 8, 32).

Males had a higher Toxoplasma antibody prevalence thanfemales in the Surabaya population. 1n the literature, the sex

difference in prevalence has varied from population to popu‑

lation ( 1 ). Some behavioral factors, e.g.,frequent contact withT

4 3 2 0 0 00 0 0soil, are considered relevant to the difference in Toxoplasma
prevalence between males and females. Further studies areneeded to analyze the factors involved in transmission of
Toxoplasma to the Surabaya population･

Based on the persistence of Toxoplasmainfection in humanS,
its prevalence usually increases with age. For instance, ourprevious survey among a Japanese population revealedト

4% in 0‑39 years, 14% in 40‑49 years, 18% in 50‑59 years,
and 30% in 60169 years (13). Therefore, the age prevalence
0.0

1.0

curve of the Surabaya population is very different from thoseof Japanese populations. One particularly distinct polnt is thedifference between prevalences at 0‑9 years and 10‑ 1 9 years･

2.0

ELISA VALUE

Since the survey was a horizontal but not long血dinal one,this is not direct evidence that transmission is currently active.
Fig. 3. Frequency distribution of ELISA values detemined f♭r 914

However, a dramatic increase in prevalence obseⅣed in themales, 847 females and a total of 1,761 serum samples.

Surabaya population suggests that this population has a muchhigher transmission rate than Japanese populations. It is also

values indicated a similar bimodal pattem (data not shown)･

important to note that血e prevalence did not reach near 1 OO%

The mean ELISA values of positive specimens were notsignificantly different among these age groups (P > 0･05)･

in spite Of the possible high transmission rate of Toxoplasma
infection.

A bimodal pattem infrequency distribution of Toxoplasma
antibody levels was found in the Surabaya population. TheDISCUSSION

bimodal pattems were also obseⅣed in our previous (5, 13)

Since the TToxoplasma parasite can evade human immune

and other (33) studies using Japanese populations. Again,

responses and establish a persistent infection, the presence

based on the persistence of Toxoplasma infectioninhumans,of antibodies in an individual indicates that the individual

it is possible that an equilibrium could exist between hostwas infected with the parasite at any time point before theimmunity and parasite activity (34). Equivalent mean anti‑

suⅣey. Therefわre, the antibody prevalence indicates a cumu‑

body levels in seropositive specimens between males andlative rate of individuals with past exposure to Toxoplasma.

females suggest that the equilibrium may be maintained in

The antibody prevalence is considered to reflect the rate ofboth genders at a similar level. Also, Consistent mean antibody

individuals who have a potential to develop toxoplasmosis

levels in seropositive specimens among age groups ranglng

upon acqulSltlOn Of HIV infection. The relatively high preva‑
lence (58%) Obtained in the present survey Fonfirms previous

tained throughout the lifeof infected individuals.

&om 0 to loo years suggest that the equilibrium may be main‑

reports indicating that Toxoplasma is a ser10uS Public healthconcem in Indonesia (6‑8). Varying antibody prevalences &om

ACKNOWLEDGMENTS

2% to 39% have been reported in other countries in Southeast

We thank Drs. Uga and‑ Kataoka for their transportation ofsera. This study was partially supported by the Japan Society

Asia, such as Bangladesh (14,15), Laos (16), Malaysia (17,18), Singapore (19, 20), Thailand (21125), and Vietnam (26).
This suggests that a wide area of Southeast Asia is contami‑

fわr the Promotion of Science.

nated with Toxoplasma by whichpeople arefrequently infected.
Three main mechanisms for Toxoplasma transmission to

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