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Taenia solium is an etiologic agent of taeniasis and cysticercosis, an important zoonotic infection involving humans and swine. Cysticercosis is caused by the ingestion of eggs of T. solium by susceptible intermediate hosts. Pigs are the common intermediate hosts. However, humans and even dogs can also contract cysticercosis by ingesting eggs of T. solium.1 Human cysticercosis warrants special attention when cysticerci are located in the nervous system because it is a major cause of seizures and epilepsy.2 The disease is highly endemic in Latin America, Asia, and Africa.2,3 Cysticercosis in pigs is also a cause of carcass condemnations particularly in heavy infections, constituting an economical problem. Thus, the interruption of the cycle in definitive and intermediate hosts is key strategy for the control of this morbid condition.4–6
Brazil is a country known to be endemic for cysticercosis.2 Cases of human cysticercosis have mainly been reported in southern states of Brazil with sporadic notifications in the northeast region, including Piauí state.7 According to the Brazilian Department of Animal Origin Products Inspection (DIPOA) of the Ministry of Agriculture, Livestock and Food Supply (MAPA), reports of swine cysticercosis are mainly from southern and southeastern states. However, it had not been notified by slaughter houses in the Piauí state in the period between 2002 and 2004,8 when this survey was carried out.
Brazil is politically divided into 5 regions: north, south, northeast, west central, and southeast. Northeast region, which includes Piauí state, can be divided into 4 different ecosystems: Coastal Region, Semi-arid Region, Forest Zone, and the Middle-North also known as Palm Zone.
The Middle-North is characterized as the transitional area between the semi-arid region of the Northeast and the Amazon region. It is characterized by increasing humid climate and exuberant vegetation towards the West. Middle-North also concerns the northern areas of the Tocantins state and parts of the states of Maranhão and Pará. All these areas have similar climatic and geographical characteristics, and consequently similar human and animal occupation, including socio-behavioral aspects.
This study was conducted in Cocal dos Alves city, Piracuruca region, Piauí state, Middle-North of Brazil (Figure 1
, Figure 2A), in November of 2003. Cocal dos Alves city is a principal city for pork production for neighboring cities and located in the main route from Teresina (the state capital) to Ceará state and to the Parnaíba river delta and "Sete Cidades" National Park, the most important and popular tourist areas of Piauí state. Although the region is designated in endemic area for cysticercosis,2 there is no documented report of cysticercosis in this region. Therefore, this study was carried out to confirm the presence of human and porcine cysticercosis in Cocal dos Alves.
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). One hundred and ninety-seven people were questioned in a socio-behavioral–epidemiologic survey focused on the taeniasis-cysticercosis complex, including questions regarding lifestyle, food consumption behavior, sanitary management of water and wastewater, medicine consumption, past and present diseases, and symptoms. The data generated was analyzed using Epi InfoTM (Centers for Disease Control and Prevention, Atlanta, GA) software version 3.3.2.
Seven asymptomatic individuals residing in the risk area volunteered to provide blood samples. For detection of specific antibodies for cysticercosis in humans, ELISA was performed using both highly specific glycoproteins (GPs) in cyst fluid purified by isoelectric focusing and recombinant chimeric antigens (RecTs) prepared as previously described.10,11
Specimens were collected from a pig necropsied after tested positive for the tongue inspection (Figure 2B). Identification of taeniid cysticerci collected from the infected pig was carried out based on nucleotide sequence of cytochrome c oxidase subunit 1 gene (cox1) amplified by multiplex PCR.12 Samples for DNA sequencing were prepared with an ABI PRISM BigDye Terminator Cycle Sequencing Ready Reaction kit, and the amplicon was sequenced on an ABI Prism 310 Genetic Analyzer.
According to the data of hospital morbidity from 2002 (Brazilian Single Health System) for Cocal dos Alves city,9 1.8% of hospital admissions were due to mental disorder or idiopathic behavioral disorder in the population with age between 15 and 49 years; although specific neurologic diagnoses were not reported. From this study, it became evident that most residents were pig farmers. Socioeconomic standings are low and sanitary facilities are poor. Many socio-behavioral characteristics of the population suggested the existence of the taeniasis-cysticercosis complex. The surveyed population widely practiced pork consumption; 65.3% raise pigs mostly by extensive farming (91.4%). There is no public sewage treatment. The use of septic tanks by 45.7% of the population indicates a concern about the sewage disposal; however 54.3% do not use any kind of sewage management. According to the data obtained in this epidemiologic survey, 61.4% of the surveyed population was familiar with anti-parasitic medication. However, the drugs mentioned for the management of parasitic diseases were mebendazole (36.4%) and metronidazole (5.3%), which are not indicated for the treatment of Taenia spp. infections. For this reason, the specific treatment of taeniasis was considered nonexistent in the studied area.
Other aggravating factors for infectious and parasitic diseases are associated with the water supply; 55.3% of the population use water from cisterns without treatment, 13.8% uses other sources without treatment, and only 30.9% of the population use treated water. Another problem is the population misinformation leading to improper diagnosis of taeniasis.13 Although there was no report of pathognomonic signs and symptoms of taeniasis and cysticercosis in the studied population, the analysis of the results of the epidemiologic survey pointed out several factors suggesting the occurrence and maintenance of the taeniasis/cysticercosis cycle in the region.
Due to the high specificity of available immunodiagnostic tests, serology is one of the best presumptive diagnostic methodologies.6,10,11 Multiplex PCR was used for the confirmation of parasitological material; the technique is highly specific and allows identification of parasitological material even when the morphologic identification is not possible.12
Of the 7 asymptomatic volunteers tested serologically, one was positive by ELISA with the use of GPs (OD 0.031) and RecTs (0.042) with a cutoff of 0.029 and 0.038 for GPs and RecTs, respectively. This case was considered to be a highly suspicious cysticercosis case, since the test used is highly specific for cysticercosis and no cross-reaction was observed from other diseases so far we examined.6,10,11 It is also important to consider that 43.3–91% of autopsies in endemic areas reveal asymptomatic NCC.14
In the field, diagnosis of cysticercosis is made through tongue inspection. This examination can be performed antemortem in swine and aim to find superficial cysts. However, this technique has low sensitivity and specificity.6 Usually, the tongue inspection method only detects pigs with heavy infections.
The necropsy of a "tongue inspection positive" pig revealed numerous cysts in the muscles (Figures 2C, 2D). The cysticerci were collected and mitochondrial DNA analysis was performed to identify taeniid species. As a result, a 720-bp cox1 gene fragment was successfully amplified by multiplex PCR (Figure 3A). The product amplified was sequenced (AB243755) and aligned with similar sequences previously described.15 It confirmed Afro-American genotype of T. solium with 100% of similarity. The homology of differential nucleotides at positions 619, 690, 723, 861, 867, and 1065 confirmed to be the American origin genotype (Figure 3B).
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Nowadays Cocal dos Alves city, a major supplier of pork for the region of Piracuruca, is expected to be a natural reservoir for taeniasis and cysticercosis, since there has been no action for the control of the disease. Therefore, the present situation has lead to the existence of tapeworm carriers around the region, neighbor states, and even other countries. It should be kept in mind that the city is in the route of tourists circulating from Teresina (the state capital) to the Parnaíba River delta, "Sete Cidades" National Park, and also in the route from Teresina to Fortaleza, the capital of its neighbor state Ceará (see Fig. 1). The population consuming food in the region is expected to be susceptible to the infection by the adult and the metacestode forms of T. solium.
Currently it is now evident that both taeniasis and cysticercosis are endemic in the Middle-North of Brazil. Consequently, a very important initial task is to establish the natural history of the taeniasis-cysticercosis complex inside the region. It is necessary to perform more studies comprising a wider area as well as a larger number of specimens. The epidemiologic mapping of taeniasis and cysticercosis in the Middle-North of Brazil will then provide essential information for the subsequent establishment of programs for the control and eradication of this important zoonosis.
Received March 21, 2006. Accepted for publication July 7, 2006.
Acknowledgments: The authors gratefully acknowledge the contribution of Prof. Nicodemus Alves de Macedo and Dr. Ivete Lopes de Mendonça of the Centro de Ciências Agrárias of the Universidade Federal do Paiuí and Dr. Silvaneide Escórcio de Resende, Chief of Piracuruca City Slaughterhouse for their help and cooperation on providing facilities and local information for this project.
Financial support: This work was supported in part by a grant-in-aid for the Scientific Research sponsored by the Japan Society for Promotion of Science (14256001, 17256002) to AI.
* Address correspondence to Akira Ito, Department of Parasitology, Asahikawa Medical College, Midorigaoka Higashi 2-1-1-1, Asahikawa, Hokkaido, Japan, 078-8510. E-mail: akiraito{at}asahikawa-med.ac.jp 
These authors contributed equally.
Authors’ addresses: Marcello Otake Sato, Yasuhito Sako, Minoru Nakao, Hiroshi Yamasaki, and Akira Ito, Department of Parasitology, Asahikawa Medical College, Midorigaoka Higashi 2-1-1-1, Asahikawa, 078-8510, Hokkaido, Japan, Telephone: 81-166-682420, Fax: 81-166-682429, E-mail: marcello{at}asahikawa-med.ac.jp, yasusako{at}asahikawa-med.ac.jp, nakao{at}asahikawa-med.ac.jp, hyamasak{at}asahikawa-med.ac.jp, akiraito{at}asahikawa-med.ac.jp. Marcello Otake Sato, Tânia Vasconcelos Cavalcante, Escola de Medicina Veterinária e Zootecnia, Universidade Federal do Tocantins, BR153 Km112 CP132, Araguaína 77804-970, Brazil, Telephone: 55-63-34141802, Fax: 55-63-34151648, E-mail: otake{at}uft.edu.br, taniavet2001{at}yahoo.com.br; Ana Patrícia Yatsuda, Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto 14040-903, Brazil, Telephone: 55-16-36024724, Fax: 55-16-36024725, E-mail: ayatsuda{at}fcfrp.usp.br; Kazuhiro Nakaya, Animal Laboratory for Medical Research, Asahikawa Medical College, Midorigaoka Higashi 2-1-1-1, Asahikawa, 078-8510, Hokkaido, Japan, Telephone: 81-166-682683, Fax: 81-166-682429, E-mail: nky48{at}asahikawa-med.ac.jp.
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