Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 601–612 Contents lists available at ScienceDirect Transactions of the Royal Society of Tropical Medicine and Hygiene journal homepage: http://www.elsevier.com/locate/trstmh Detecting spatial clusters of Taenia solium infections in a rural block in South India M. Venkata Raghava a,∗, V. Prabhakaran b, T. Jayaraman b, J. Muliyil a, A. Oommen b, P. Dorny c,d, J. Vercruysse c,d, V. Rajshekhar b a Department of Community Health, Christian Medical College, Vellore 632 002, Tamil Nadu, India b Department of Neurological Sciences, Christian Medical College, Vellore, India c Department of Virology, Parasitology and Immunology, Ghent University, Belgium d Institute of Tropical Medicine, Antwerp, Belgium article info abstract Article history: Neurocysticercosis (NCC) is a major cause of seizures/epilepsy in countries endemic for the Received 18 November 2009 disease. The objectives of this study were to spatially map the burden of active epilepsy Received in revised form 11 June 2010 (AE), NCC, taeniasis, seroprevalence for cysticercal antibodies and positivity to circulating Accepted 11 June 2010 cysticercal antigens in Kaniyambadi block (approximately 100 villages comprising 100 000 Available online 17 July 2010 population) of Vellore district and to detect spatial clusters of AE, NCC, taeniasis and sero- prevalence. Using geographic information system (GIS) techniques, all 21 study villages Keywords: with over 8000 houses (population of 38 105) were mapped. Clustering of different indices Cysticercosis clusters of Taenia solium infection was determined using a spatial scan statistic (SaTScan). There epilepsy was a primary spatial cluster of AE with a log likelihood ratio (LLR) of 10.8 and relative geographic information systems risk (RR) of 22.4; however, no significant clustering for NCC was detected. Five significant taeniasis spatial clusters of seropositivity for cysticercal antibodies, two clusters of seropositivity for cysticercal antigens and one for taeniasis were detected (LLR of 8.35 and RR of 36.67). Our study has demonstrated the use of GIS methods in mapping and identifying ‘hot spots’ of various indices of T. solium infection in humans. This spatial analysis has identified pockets with high transmission rates so that preventive measures could be focused on an intensive scale. © 2010 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. 1. Introduction biased since most available data are from hospital based populations.1 Taeniasis is an intestinal disease acquired by ingestion Human cysticercosis frequently affects the central ner- of viable Taenia solium metacestode larvae from pork, while vous system and is a major cause of acquired epilepsy.2–4 cysticercosis is acquired by the ingestion of T. solium eggs. In Asia and Africa, the subcutaneous form of cysticerco- Taenia solium infection is widely endemic in the rural areas sis which is concomitant with intracerebral infection is of developing countries in Asia, Africa, South and the Cen- the most common variety and accounts for more than tral Americas. In Asia, the exact geographic origin and the 30% of cases.5 Neurocysticercosis (NCC) is a major cause epidemiological factors associated with transmission are of seizures/epilepsy in countries endemic for the disease. In African countries, studies have shown that in about 30 to 50% of cases, epilepsy had been documented to T. ∗ 1 Corresponding author. Tel.: +91 416 228 4207; fax: +91 416 226 2268. solium infection. Earlier community based studies carried E-mail address: [email protected] (M.V. Raghava). out in Kaniyambadi block (a block is a sub district level 0035-9203/$ – see front matter © 2010 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2010.06.002 602 M.V. Raghava et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 601–612 Figure 1. Map of the study area in the state of Tamilnadu, south India. organization of rural areas under the Community Devel- studies have reported the application of GIS to study the opment Programme of the Government of India and clustering of cysticercosis or taeniasis. Lescano et al.24 comprises of approximately 100 villages and 100 000 pop- used GIS to study swine cysticercosis risk gradient sur- ulation), a rural development block in Vellore district of rounding human tapeworm carriers in Peru. They also the state of Tamil Nadu in India have demonstrated active studied human cysticercosis seroprevalence gradient and and continuous transmission of cysticercosis. This is evi- cysticercosis related seizures surrounding tapeworm car- dent from the high prevalence of NCC as a cause of over riers using GIS techniques.25 The objectives of this study a third of all cases of active epilepsy (AE).6 The preva- were: to spatially map the burden of AE, NCC, taeniasis lence of taeniasis in the community, as diagnosed by and seroprevalence of cysticercal antibodies and positivity using a coproantigen assay, was 30.2 per 1000 population to circulating cysticercal antigens in Kaniyambadi block; (Raghava et al., unpublished data). A high seroprevalence and to detect and map spatial clusters of AE, NCC, taenia- of cysticercal antibodies at 17.7% in the seizure-free gen- sis, seroprevalence of cysticercal antibodies and positivity eral population in the same community also indicates high rates for circulating antigens. exposure to cysticercal antigens.7 This provided an impetus for us to study the spatial distribution of the disease in this community. 2. Methods In the last decade, geographical information systems (GIS) have provided a powerful tool to display epidemi- Kaniyambadi block is located in Vellore district of Tamil ological data in a spatial format in the form of maps. Not Nadu State in India, spanning a geographic area of 184 km2 only is a spatial display of the distribution of a disease pos- with a population of 106 000 (current updated census, sible, but also it is possible to perform statistical analyses 2006, of the Community Health Department of Christian to determine whether there is a disproportionate con- Medical College (CMC), Vellore). There are 82 settlements centration of disease in some pockets of the geographical distributed across 33 revenue villages (three or four settle- areas surveyed. These clusters or ‘hot spots’ may provide ments grouped for administrative and revenue purposes) a target for surveillance and control strategies. Studies in the block. The study area is bordered by Vellore town on using GIS have been done mainly to study clustering of the northeastern side, Anaicut block on the western side patients with various types of cancers.8–13 A few stud- and Arani block on the southern part of the study area and ies involving infectious diseases such as cholera, malaria, situated between 12◦40Nto12◦55N latitudes and 79◦0E leprosy, tuberculosis and giardiasis have been reported in to 79◦15E longitudes (Figure 1). The adult literacy in this recent years.14–22 Efforts are under way to develop GIS and block is 79% and the primary occupation is agriculture. The remote sensing based models for various parasitic diseases population under study was selected from 21 randomly including schistosomiasis, which are now being expanded selected settlements from the block and is representative to include widespread infectious diseases.23 Only a few of the state of Tamil Nadu. M.V. Raghava et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 601–612 603 Figure 2. GIS map of Kaniyambadi block in Vellore district showing the villages and study clusters. We used data from the following sources for our study: Detection of cysticercal antibodies in serum was by an EITB using lentil lectin specific T. solium glycoproteins as Master Health Census collected with geo-locations antigens, standardized in our laboratory.28 A sample was sourced from Community Health Department of CMC, Vel- considered positive for cysticercal antibodies by the crite- lore. ria of Tsang et al.,26 i.e. reaction to one or more T. solium GIS data pertaining to the block, its villages, and people glycoproteins of molecular weights 50, 38–42, 24, 21, 18, from the existing Geodatabase of the Department of Com- 14 and 13 kDa. munity Health, CMC, Vellore. Circulating T. solium metacestode antigens were assayed in all sera by an ELISA using monoclonal antibodies 2.1. Study population to excretory/secretory products of T. saginata metaces- todes established by Brandt et al.29 and modified by Dorny The study population covered 38 105 people between et al.30 The ELISA is 94% sensitive for cysticercosis with the ages of 2 and 60 yrs who had been screened for AE no cross reactivity with sera of other parasitic infec- from 16 randomly selected rural clusters. Rural clusters tions. A sample was considered positive for cyst antigens in the study are village panchayats (settlements of peo- above the Mean+3 SD absorbance of 6 negative control ple with local self-governance). Figure 2 shows the spatial sera assayed with the study samples on each microtitre location of all the village settlements and the study clusters plate. in Kaniyambadi block. Each case in the block was linked with the master Cen- sus database using a unique identification number and 2.2. Epidemiological survey the geographic coordinates (latitude, longitude) extracted from this database. Twenty households were randomly The survey methods and screening tools used for deter- selected from each study cluster and 729 early morning mining the AE rates have been published previously.6 stool samples were collected from the study population Briefly, patients with AE were identified using a validated aged between 2 and 60 years and tested for the presence questionnaire administered, in a door-to-door survey, by of coproantigens.31,32 The same households provided 960 health workers.