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  • 2

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    • Export Citation
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    • Export Citation
  • 6

    Margono SS, Subahar R, Hamid A, Wandra T, Sudewi SS, Sutisna P, Ito A, 2001. Cysticercosis in Indonesia: epidemiological aspects. Southeast Asian J Trop Med Public Health 32 (Suppl 2):79–84.

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    Subahar R, Hamid A, Purba W, Wandra T, Karma C, Sako Y, Margono SS, Craig PS, Ito A, 2001. Taenia solium infection in Irian Jaya (west Papua), Indonesia: a pilot serological survey of human and porcine cysticercosis in Jayawijaya district. Trans R Soc Trop Med Hyg 95 :388–390.

    • Search Google Scholar
    • Export Citation
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Seroepidemiologic Survey of Cysticercosis-Taeniasis in Four Central Highland Districts of Papua, Indonesia

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  • 1 Functional Research Unit, National Institute of Health Research and Development in Papua, Jayapura, Papua, Indonesia; Papua Provincial Health Office, Jayapura, Papua, Indonesia; Atlanta Research and Education Foundation, Atlanta, Georgia; Division of Parasitic Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Biology, Georgia State University, Atlanta, Georgia

Cysticercosis and taeniasis are known to be present in Papua, Indonesia. Several small studies have found a high prevalence of cysticercosis (23.5–56.9%) in the central highlands of Papua. A seroepidemiologic survey was carried out in four districts (Jayawijaya, Paniai, Pegunungan Bintang, and Puncak Jaya) of Papua. Anti-cysticercosis and anti-taeniasis antibodies were measured in 2,931 people using recombinant T24 and recombinant ES33 as a measure of cysticercosis and taeniasis exposures, respectively. Prevalence of cysticercosis-taeniasis is high in the Jayawijaya and Paniai districts (20.8% and 29.2% for cysticercosis and 7% and 9.6% for taeniasis, respectively) and lowest in the other two districts (Pegunungan Bintang and Puncak Jaya) (2% and 2% for cysticercosis and 1.7% and 10.7% for taeniasis, respectively). Our data show that the prevalence of cysticercosis and taeniasis are unchanged from that reported nearly 35 years ago at the beginning of cysticercosis-taeniasis epidemics in Papua, Indonesia.

INTRODUCTION

Cysticercosis (a disease in humans and pigs caused by the larval stage of Taenia solium) and taeniasis (a disease only in humans where the adult worm of T. solium is detected in the gastrointestinal tract) have been reported in Papua, Indonesia. On the basis of several small studies in the central highland of Papua, the prevalence of cysticercosis was 23.5–56.9% in humans and the prevalence of taeniasis were 8.6–15.9% in humans.113 Among the porcine population, the prevalence of cysticercosis was 70.4%. 7,10

Because these studies were conducted with small sample sizes and without robust tests for cysticercosis and taeniasis, the data were not a true estimate of the prevalence of these diseases. In an effort to control or even eliminate cysticercosis-taeniasis in Papua, Indonesia, reliable data on the baseline prevalence of cysticercosis and taeniasis are needed. In this study, we report the result of a large seroepidemiologic study using a robust test for cysticercosis and taeniasis that is regarded as the gold standard for immunodiagnosis of cysticercosis in four districts of the central highland of Papua, Indonesia, that was carried out during August–December 2007. 1417

MATERIALS AND METHODS

Ethical approval.

This survey received human subject study approval from the Ethics Commission of Indonesian National Institutes of Health Research and Development.

Sample size.

Survey design used for this study was a three-stage stratified cluster sampling. In the first stage, four central highland districts were chosen on the basis of several studies that reported cysticercosis and taeniasis. These districts were Jayawijaya, Paniai, Pegunungan Bintang, and Puncak Jaya (Figure 1). In the second stage, districts were divided into two strata, flat and hilly regions. For the flat region (Jayawijaya and Paniai), for an estimated prevalence of 50%, a mean household size of 5 persons, an accuracy of three percentage points, an error degree of 5%, and a design effect of 2, we needed 2,134 persons. 18 For the hilly region (Pegunungan Bintang and Puncak Jaya), with an estimated prevalence of 1–2%, the sample size was 406 per district. In the final stage, according to kampong and number of households per kampong data on the basis of probability proportional to size cluster sampling technique, we chose 30 kampongs, 15 households per kampong, and 5 persons per household for the flat region and 30 kampong, 3 households per kampong, and 5 persons per household for the hilly region to fulfill the required sample size. After choosing the kampong based on probability proportional size, for each kampong, households were chosen randomly and all members of households were chosen.

Survey subject.

All household members who were ≥ 6 years of age and provided informed consent were chosen for participation in the survey. In the survey, vital data (name, sex, age), and risk factors for cysticercosis and taeniasis (water source, place of defecation, history of T. solium proglottid expulsion, history of seizure, history of unconsciousness, and cysts in the body) were collected through interviews and physical examination (for cysts in the body).

Blood collection.

Finger prick blood was collected from all participants. Blood was collected by using Nobuto filter paper (catalog no. 800700; Advantec MFS, Inc., Dublin, CA), which collects 100 μL of whole blood in a predefined area. Filter paper was then stored in a 1.5-mL microcentrifuge tube containing 900 μL of StabilZyme Select (catalog no. PN-S203-2000; SurModics, Inc., Eden Prairie, MN). A combination of Nobuto filter paper and StabilZyme storage buffer was to preserve antibodies contained in the blood sample. 19

Detection of antibodies.

Antibodies against cysticercosis and taeniasis were detected by using an enzyme-linked immunoelectrotransfer blot (EITB) strip containing two recombinant antigens specific and sensitive for cysticercosis (rT24H) and taeniasis (rES33) produced at the Centers for Diseases Control and Prevention (Atlanta, GA). 14,16,17 Antibody determination was carried out as follows. An EITB strip was exposed to a blood sample in StabilZyme (serum dilution = 1:20) diluted 1:5 in phosphate-buffered saline (PBS), 0.3% Tween 20, 5% dried-skim milk to give a total volume of 500 μL and incubated at room temperature for 1 hour. The strip was then washed for four times at 5-minute intervals with PBS, 0.3% Tween 20. The strip was then exposed to conjugate (goat antibody against heavy and light chains of human IgG conjugated with horseradish peroxidase) diluted 1:8,000 in PBS, 0.3% Tween 20 for 1 hour and washed twice with PBS, 0.3% Tween 20 and twice with PBS. Color development was established by exposing the strip to diaminobenzidine and 30% H2O2 for 10 minutes. Color development was stopped by washing the strip with distilled water. The result was determined by detecting a reaction line at the place of the two antigens (Figure 2).

Data analysis.

Data were tabulated by district, age, sex, and laboratory results using Microsoft (Redmond, WA) Excel 2003. All statistical analysis was performed using SAS version 9.1 (SAS Institute, Cary, NC).

RESULTS

Distributions of age, sex, water source, and place of defecation.

A total 2,931 persons from 4 districts, 30 subdistricts, and 98 kampongs in Papua were interviewed. Proportions of female and age group in each district were not significantly different. Study population characteristics are shown in Table 1. In general, water sources were rivers, wells, and water catchments (especially in Paniai). None of the households had access to a safe, protected water supply. For place of defecation, most persons used a field or any place they could find. A total of 83% of persons from Paniai reported using pit latrines.

History of illnesses.

The smallest number of persons reporting expulsion of Taenia sp. worms were in Puncak Jaya and the largest number were in Pegunungan Bintang. There was no statistically significant difference between sex and history of worm expulsion, except in Jayawijaya where males reported having more worm expulsion than females.

The largest number of seizures was reported in Jayawijaya and Paniai; males reported more seizures only in Jayawijaya. Unconsciousness was common in Jayawijaya, Paniai, and Pegunungan Bintang. There was no relationship between sex and history of unconsciousness. Cysts were reported most often in Paniai, but there was no relationship between sex and cysts found in the body.

Prevalence of cysticercosis and taeniasis.

Prevalence of cysticercosis and taeniasis is shown in Table 2. The prevalence of cysticercosis and taeniasis was the highest in Paniai and lowest in Puncak Jaya. Cysticercosis prevalence was higher than taeniasis prevalence, but in Pegunungan Bintang, taeniasis prevalence was much higher than in other districts.

Relationship of several risk factors and prevalence of cysticercosis-taeniasis.

The relationship between sex, age group, cysticercosis-taeniasis symptoms with laboratory results is shown in Tables 3–8. Prevalence of cysticercosis and taeniasis among males in Jayawijaya was significantly higher than among females (P < 0.05), but these relationships were not found in other populations. The likelihood of having cysticercosis among persons in Jayawijaya and Paniai increased with age (P < 0.01). This relationship was not found for taeniasis. There was a relationship between having a history of Taenia sp. worm expulsion and cysticercosis among persons from Paniai and Puncak Jaya, (P < 0.05) but not among persons from Jayawijaya and Pegunungan Bintang. There was no similar relationship for taeniasis. History of seizure was statistically related with the likelihood of having a diagnosis of cysticercosis for persons from Jayawijaya and Paniai. For taeniasis, this relationship was observed only for persons from Jayawijaya. A history of unconsciousness was closely related with cysticercosis among persons in Jayawijaya and Pegunungan Bintang. For taeniasis, this relationship was found among persons from Jayawijaya and Kabupaten Pegunungan Bintang, but not in other districts. Finding cysts in the body was significantly related to a diagnosis of cysticercosis among persons in Jayawijaya and Paniai. For taeniasis, a significant relationship was found in only in persons from Jayawijaya.

DISCUSSION

Although the number of persons examined in this survey did not reach the planned number, the number of kampongs and households chosen fulfilled the sample requirement. Thus, the validity of the data in this survey was maintained. The most important reason for a smaller sample size was the erroneous assumption that in Papua, a typical household has five members. In this survey, we found many families with only one or two children and many families without children. Many families clearly mentioned that they were infertile.

Several problems existed during the survey. There was a rumor about poisoned foods and drinks circulating in the community in the Jayawijaya district. People in several chosen kampongs rejected survey takers because of fear that the survey takers brought poisoned materials to the community. In Puncak Jaya, survey takers could not reach some chosen kampongs because of security reasons. In Pegunungan Bintang, lack of money to pay for reaching kampongs only accessible by helicopter meant that several kampongs could not be included in the survey.

Despite these problems, this survey provided enough samples to give a valid and comprehensive picture of cysticercosis-taeniasis situation in the four districts in the central highland in Papua, Indonesia. This study also used EITB strip assay, which is sensitive and specific for cysticercosis and taeniasis. Thus, survey results reflected a true picture of the prevalence of these diseases in the four districts in Papua, Indonesia.

The prevalence of cysticercosis prevalence in the four districts in Papua, Indonesia is high when compared with prevalence in several other countries such as Peru, Cameroon, and the People’s Republic of China. 2022 There has been no real improvement in the prevalence of cysticercosis-taeniasis in Papua for nearly 35 years, albeit the awareness that these conditions are dangerous and detrimental to health, economic conditions for the community, and prevention and treatment efforts. 7,10 This results indicate that all control efforts that have been carried out should be reviewed, and technologies shown to control or eliminate these diseases should be used.

Another discouraging development is that we showed that cysticercosis-taeniasis is present in the Pegunungan Bintang district. A survey conducted by Gajdusek 23 in 1978 indicated that there was cysticercosis in Oksibil, Pegunungan Bintang, but a study conducted by Bangs and others 24 in 1996 did not report taeniasis. One possibility is that Bangs and others used microscopic examination (which has low sensitivity) to find Taenia sp. eggs in the stool. Our survey confirmed the establishment of cysticercosis-taeniasis in Pegunungan Bintang. Detection of cysticercosis-taeniasis in this district that borders Papua New Guinea should raise concern about transmission of cysticercosis-taeniasis into Papua New Guinea, which has not reported any cases of cysticercosis-taeniasis except in refugees from West Papua. 25,26

An interesting finding in the Pegunungan Bintang district is that the prevalence of taeniasis is higher than that of cysticercosis. The high prevalence of taeniasis could be the beginning of early transmission of taeniasis before transmission of cysticercosis. Another possibility is that the highly specific rES33 antigen recognizes unknown cross-reactive antigens found in that community. To resolve this issue, it will be important to test samples from that community with another antigen, such as rES38, which is also a specific and sensitive assay for taeniasis. 17

The prevalence of cysticercosis-taeniasis in the Puncak Jaya district is not as high as the prevalence in two districts that surrounded it. There are several possible explanations. These include 1) the geographic area of Puncak Jaya is more hilly than the other regions; 2) more teachers from Paniai (who brought their infected pigs with them) came to Jayawijaya than to Puncak Jaya; 3) sociocultural differences between Puncak Jaya and Paniai-Jayawijaya tribes; and 4) a health education for burning infected pigs in Puncak Jaya was successful.

Taeniasis prevalence is high in the four study districts on the basis of detecting antibody against T. solium antigen in serum samples. The best method for diagnosis of taeniasis is a coproantigen enzyme-linked immunosorbent assay that detects T. solium antigen in stool samples. However, in the field, it is easier to get blood from a fingerprick than to obtain stool samples. 27 Although antibody against T. solium is not always correlated with the presence of adult worms, screening persons for taeniasis using an EITB strip is an important step in controlling taeniasis rather than giving mass treatment with niclosamide to the entire whole population.

Age, history of seizures, unconsciousness, and finding cysts are risk factors that can determine whether a person has a positive test result for cysticercosis. History of expulsion of Taenia spp. worms shows a correlation with taeniasis. This finding is an important factor because finding persons with taeniasis is a key factor in stopping the spread of cysticercosis-taeniasis.

CONCLUSION

Cysticercosis-taeniasis in the four districts in the central highland of Papua, Indonesia has been detected by a seroepidemiologic survey of a large number of samples, a reliable sampling technique, and highly specific and sensitive serologic tests. The high prevalence of cysticercosis-taeniasis in Jayawijaya and Paniai and the desire to prevent further spread of these diseases in Pegunungan Bintang and Puncak Jaya have created an urgent need to begin a control program for cysticercosis-taeniasis in Papua, Indonesia.

Table 1

Characteristics of the survey population in four districts, Papua, Indonesia, 2007

Table 1
Table 2

Cysticercosis and taeniasis prevalence in four districts of Papua, Indonesia, 2007

Table 2
Table 3

Relationship between sex and cysticercosis-taeniasis prevalence in four districts of Papua, Indonesia, 2007

Table 3
Table 4

Relationship between age groups and cysticercosis-taeniasis prevalence in four districts of Papua, Indonesia, 2007*

Table 4
Table 5

Relationship between history of Taenia sp. worm expulsion and cysticercosis-taeniasis prevalence in four districts of Papua, Indonesia, 2007*

Table 5
Table 6

Relationship between history of seizure and cysticercosis-taeniasis prevalence in four districts of Papua, Indonesia, 2007*

Table 6
Table 7

Relationship between history of unconsciousness and cysticercosis-taeniasis prevalence in four districts of Papua, Indonesia, 2007*

Table 7
Table 8

Relationship between cyst in the body and cysticercosis-taeniasis prevalence in four districts of Papua, Indonesia, 2007*

Table 8
Figure 1.
Figure 1.

Cysticercosis-taeniasis survey area in Papua, Indonesia. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 80, 3; 10.4269/ajtmh.2009.80.384

Figure 2.
Figure 2.

rES33-rT24H enzyme-linked immunoelectrotransfer blot strip. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 80, 3; 10.4269/ajtmh.2009.80.384

*

Address corrrespondence to Sukwan Handali, Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway, Mailstop F-13, Atlanta, GA 30341-3724. E-mail: ahi0@cdc.gov

Authors’ addresses: Lidwina Salim, Functional Research Unit, National Institute of Health Research and Development in Papua, Jayapura, Indonesia, E-mail: upf_papua@litbang.depkes.go.id. Agnes Ang, Papua Provincial Health Office, Kotaraja, Papua, Indonesia. Sukwan Handali, Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway, Mailstop F-13, Atlanta, GA 30341-3724, and Atlanta Research and Education Foundation, Atlanta, GA 30033, E-mail: ahi0@cdc.gov. Cysticercosis Working Group in Papua, Functional Research Unit, National Institute of Health Research and Development in Papua, Jayapura, Indonesia (Anugerah Martha Julian Nenobais, Yunita Jakomina Rachel Mirino, Yose Rizal Ap, Ridwan Oemar, Hanna S. Kawulur, Samuel Sandy, Mirna Widiyanti, Ivonne Ayomi, Evi Iriani Natalia, Ester Lumbanradja, Mardi Raharjo, Eva Fitriana, Yoel G. Kelyanin, and Juniati Bilangla’bi’). Victor C. W. Tsang, Department of Biology, Georgia State University, Atlanta, GA 30302, E-mail: biovct@langate.gsu.edu.

Acknowledgments: We thank the Papua Provincial Health Officers (Drs. Bagus Sukaswara and Tigor Silaban) for support; the cysticercosis group at the Centers for Diseases Control and Prevention, Atlanta, GA (Dr. Patricia Wilkins, Patricia Lee, John Noh, Marita Silva-Ibanez, and Peter Harris) for providing material and equipment for the survey; and Jacquelin M. Roberts for help with statistical analysis.

Financial support: This study was supported by the Papua Provincial Health Budget 2007.

REFERENCES

  • 1

    Coker-Vann MR, Subianto DB, Brown P, Diwan AR, Desowitz R, Garruto RM, Gibbs CJ Jr, Gajdusek DC, 1981. ELISA antibodies to cysticerci of Taenia solium in human populations in New Guinea, Oceania, and Southeast Asia. Southeast Asian J Trop Med Public Health 12 :499–505.

    • Search Google Scholar
    • Export Citation
  • 2

    Diwan AR, Coker-Vann M, Brown P, Subianto DB, Yolken R, Desowitz R, Escobar A, Gibbs CJ Jr, Gajdusek DC, 1982. Enzyme-linked immunosorbent assay (ELISA) for the detection of antibody to cysticerci of Taenia solium. Am J Trop Med Hyg 31 :364–369.

    • Search Google Scholar
    • Export Citation
  • 3

    Handali S, Liying H, Lusikoy C, Senis J, Sihombing D, 1997. A survey report–July 1993: cysticercosis in the Grand Dani Valley, Jayawijaya District, Irian Jaya Province, Indonesia. Southeast Asian J Trop Med Public Health 28 (Suppl 1):22–25.

    • Search Google Scholar
    • Export Citation
  • 4

    Ito A, Putra MI, Subahar R, Sato MO, Okamoto M, Sako Y, Nakao M, Yamasaki H, Nakaya K, Craig PS, Margono SS, 2002. Dogs as alternative intermediate hosts of Taenia solium in Papua (Irian Jaya), Indonesia confirmed by highly specific ELISA and immunoblot using native and recombinant antigens and mitochondrial DNA analysis. J Helminthol 76 :311–314.

    • Search Google Scholar
    • Export Citation
  • 5

    Margono SS, Ito A, Sato MO, Okamoto M, Subahar R, Yamasaki H, Hamid A, Wandra T, Purba WH, Nakaya K, Ito M, Craig PS, Suroso T, 2003. Taenia solium taeniasis/cysticercosis in Papua, Indonesia in 2001: detection of human worm carriers. J Helminthol 77 :39–42.

    • Search Google Scholar
    • Export Citation
  • 6

    Margono SS, Subahar R, Hamid A, Wandra T, Sudewi SS, Sutisna P, Ito A, 2001. Cysticercosis in Indonesia: epidemiological aspects. Southeast Asian J Trop Med Public Health 32 (Suppl 2):79–84.

    • Search Google Scholar
    • Export Citation
  • 7

    Margono SS, Wandra T, Swasono MF, Murni S, Craig PS, Ito A, 2006. Taeniasis/cysticercosis in Papua (Irian Jaya), Indonesia. Parasitol Int 55 (Suppl):S143–S148.

    • Search Google Scholar
    • Export Citation
  • 8

    Subahar R, Hamid A, Purba W, Wandra T, Karma C, Sako Y, Margono SS, Craig PS, Ito A, 2001. Taenia solium infection in Irian Jaya (west Papua), Indonesia: a pilot serological survey of human and porcine cysticercosis in Jayawijaya district. Trans R Soc Trop Med Hyg 95 :388–390.

    • Search Google Scholar
    • Export Citation
  • 9

    Subianto DB, Tumada LR, Margono SS, 1978. Burns and epileptic fits associated with cysticercosis in mountain people of Irian Jaya. Trop Geogr Med 30 :275–278.

    • Search Google Scholar
    • Export Citation
  • 10

    Suroso T, Margono SS, Wandra T, Ito A, 2006. Challenges for control of taeniasis/cysticercosis in Indonesia. Parasitol Int 55 (Suppl):S161–S165.

    • Search Google Scholar
    • Export Citation
  • 11

    Tjahjadi G, Subianto DB, Endardjo S, Margono SS, 1978. Cysticercosis cerebri in Irian Jaya, Indonesia. Southeast Asian J Trop Med Public Health 9 :247–251.

    • Search Google Scholar
    • Export Citation
  • 12

    Wandra T, Ito A, Yamasaki H, Suroso T, Margono SS, 2003. Taenia solium Cysticercosis, Irian Jaya, Indonesia. Emerg Infect Dis 9 :884–885.

    • Search Google Scholar
    • Export Citation
  • 13

    Wandra T, Subahar R, Simanjuntak GM, Margono SS, Suroso T, Okamoto M, Nakao M, Sako Y, Nakaya K, Schantz PM, Ito A, 2000. Resurgence of cases of epileptic seizures and burns associated with cysticercosis in Assologaima, Jayawijaya, Irian Jaya, Indonesia, 1991–95. Trans R Soc Trop Med Hyg 94 :46–50.

    • Search Google Scholar
    • Export Citation
  • 14

    Tsang VC, Brand JA, Boyer AE, 1989. An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis 159 :50–59.

    • Search Google Scholar
    • Export Citation
  • 15

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