ABSTRACT
Neurocysticercosis is the infection of the nervous system by the larvae (cysticerci) of the pork tapeworm Taenia solium. Neurocysticercosis is the major cause of acquired epilepsy worldwide and as such, it represents a global health problem. On the other hand, T. solium taeniasis/cysticercosis is one of very few infectious diseases considered to be potentially eradicable. Recently, a large-scale elimination program in Tumbes, Peru, demonstrated the feasibility of interrupting T. solium transmission. On the basis of these advances, the authors propose an initial series of actions to provide the foundations for regional and national programs for the control of taeniasis/cysticercosis, from simple and feasible interventions at the local level.
Keywords:
Cysticercosis; Neurocysticercosis; Taeniasis; Taenia solium; Epidemiology; Communicable disease control
INTRODUCTION
Neurocysticercosis (NCC), an infection of the human nervous system caused by the Taenia solium larvae (cysticerci), is an important cause of epilepsy in Peru and in most developing countries 11. Garcia HH, Nash TE, Del Brutto OH. Clinical symptoms, diagnosis, and treatment of neurocysticercosis. Lancet Neurol. 2014;13(12):1202-15.. It also occurs frequently in developed countries due to migration from endemic regions and is considered a global public health concern 22. Cantey PT, Coyle CM, Sorvillo FJ, Wilkins PP, Starr MC, Nash TE. Neglected parasitic infections in the United States: Cysticercosis. Am J Trop Med Hyg. 2014;90(5):805-9.. Taeniasis/cysticercosis (T/C) by T. solium is one of the few infections considered to be potentially eradicable 33. Schantz PM, Cruz M, Sarti E, Pawlowski Z. Potential eradicability of taeniasis and cysticercosis. Bulletin of the Pan American Health Organization. 1993;27(4):397- 403., which highlights the importance of searching for efficacious and plausible control interventions.
Design and application of control measures for this disease require knowledge of parasite transmission dynamics and of contributing factors. To better understand the epidemiology of taeniasis and cysticercosis by T. solium, it is essential to separate two markedly different scenarios: one occurring in endemic regions 44. Garcia HH, Gonzalez AE, Gilman RH, Moulton LH, Verastegui M, Rodriguez S, et al. Combined human and porcine mass chemotherapy for the control of T. solium. Am J Trop Med Hyg. 2006;74(5):850-5. where transmission is rampant and many people and swine are exposed to this parasite; and what is occurring in non-endemic regions, where the occurrence of cases is less frequent and is related to immigration or tourism 55. Giordani MT, Tamarozzi F, Cattaneo F, Brunetti E. Three cases of imported neurocysticercosis in Northern Italy. J Travel Med. 2014;21(1):17-23..
T. solium is endemic across much of Peru (including the Northern coast, all the Andean region and the Upper jungle) 66. Garcia HH, Gonzalez AE, Rodriguez S, Gonzalvez G, Llanos-Zavalaga F, Tsang VC, et al. Epidemiologia y control de la cisticercosis en el Peru. Rev Peru Med Exp Salud Publica. 2010;27(4):592-7.. In these areas, T. solium exposure is so frequent that in many rural communities, over half of the swine population present antibodies to the parasite. However, viable cysts in the carcass are only detected in some of them (5% to 10% of the total) 44. Garcia HH, Gonzalez AE, Gilman RH, Moulton LH, Verastegui M, Rodriguez S, et al. Combined human and porcine mass chemotherapy for the control of T. solium. Am J Trop Med Hyg. 2006;74(5):850-5.. Another group of animals is likely to have infections with very few cysts, undetectable at necropsy (most of the pigs with viable infections have less than five cysts in the whole carcass) 77. Sciutto E, Martinez JJ, Villalobos NM, Hernandez M, Jose MV, Beltran C, et al. Limitations of current diagnostic procedures for the diagnosis of Taenia solium cysticercosis in rural pigs. Vet Parasitol. 1998;79(4):299-313.. The remaining group of seropositive animals may have had infections that resolved spontaneously.
The situation among human populations in endemic areas is similar, with the presence of many seropositive individuals (5-20%) and a significant proportion of infected individuals. The few epidemiological studies involving computerized axial tomography have shown that 10-20% of the human population develops NCC 88. Montano SM, Villaran MV, Ylquimiche L, Figueroa JJ, Rodriguez S, Bautista CT, et al. Neurocysticercosis: association between seizures, serology, and brain CT in rural Peru. Neurology. 2005;65(2):229- 33.
9. Del Brutto OH, Santibanez R, Idrovo L, Rodriguez S, Diaz-Calderon E, Navas C, et al. Epilepsy and neurocysticercosis in Atahualpa: a door-to-door survey in rural coastal Ecuador. Epilepsia. 2005;46(4):583-7.-1010. Medina MT, Duron RM, Martinez L, Osorio JR, Estrada AL, Zuniga C, et al. Prevalence, incidence, and etiology of epilepsies in rural Honduras: the Salama Study. Epilepsia. 2005;46(1):124-31.. Most of these individuals have residual brain calcifications and apparently do not present with neurological symptoms. At the population level, the proportion of individuals with epilepsy is small (under 2%) and NCC represents 30 to 40% of these cases 1111. Moyano LM, Saito M, Montano SM, Gonzalvez G, Olaya S, Ayvar V, et al. Neurocysticercosis as a cause of epilepsy and seizures in two community-based studies in a cysticercosis-endemic region in Peru. PLoS Negl Trop Dis. 2014;8(2):e2692.. However, when that small fraction of individuals with symptomatic NCC is applied to the population denominator, it results in a substantial number of cases that seek medical care in hospitals and specialized centers. When you look at the clinical information available at these types of centers, the proportion of individuals with brain infections with viable cysts or degenerating cysts increases markedly 1212. Takayanagui OM, Jardim E. [Clinical aspects of neurocysticercosis: analysis of 500 cases].. Arq Neuropsiquiatr. 1983;41(1):50-63
13. Sotelo J, del Brutto OH, Penagos P, Escobedo F, Torres B, Rodriguez-Carbajal J, et al. Comparison of therapeutic regimen of anticysticercal drugs for parenchymal brain cysticercosis. J Neurol. 1990;237(2):69-72.-1414. Garcia HH, Gilman RH, Tovar MA, Flores E, Jo R, Tsang VC, et al. Factors associated with Taenia solium cysticercosis: analysis of nine hundred forty-six Peruvian neurologic patients. Cysticercosis Working Group in Peru (CWG). Am J Trop Med Hyg. 1995;52(2):145-8..
On the other hand, in non-endemic regions, where free-roaming swine breeding is absent, NCC cases occur among migrant and less commonly among individuals with a history of travel to endemic areas 55. Giordani MT, Tamarozzi F, Cattaneo F, Brunetti E. Three cases of imported neurocysticercosis in Northern Italy. J Travel Med. 2014;21(1):17-23.. In this scenario, there is practically no active transmission. Autochthonous cases are rare and are also related to a Taenia carrier, who is commonly an immigrant from an endemic region 1515. Schantz PM, Moore AC, Munoz JL, Hartman BJ, Schaefer JA, Aron AM, et al. Neurocysticercosis in an Orthodox Jewish community in New York City. N Engl J Med 1992;327:692-695..
CONTROL OF Taeniasis/Cysticercosis
There is a long list of transmission and control studies conducted in isolated communities. In the Salama Study in Honduras, a broad health promotion and prevention intervention, emphasizing taeniasis/cysticercosis among other conditions, took place in a population of about 7,000 people 1616. Medina MT, Aguilar-Estrada RL, Alvarez A, Duron RM, Martinez L, Dubon S, et al. Reduction in rate of epilepsy from neurocysticercosis by community interventions: the Salama, Honduras study. Epilepsia. 2011;52(6):1177-85.. This intervention resulted in a gradual decrease of transmission and epilepsy. In Peru, over the last 12 years, the Cysticercosis Working Group of Peru conducted a transmission elimination program in a population of 80,000 people in rural Tumbes. This program demonstrated that interrupting transmission was feasible and that the effect lasted one year or more 1717. Garcia HH, Gonzalez AE, Tsang VC, O'Neal SE, Llanos-Zavalaga F, Gonzalvez G, et al. Elimination of Taenia solium Transmission in Northern Peru. N Engl J Med 2016;375:1196-1197..
Demonstrating that elimination is possible, in light of the results of the above-mentioned program, represents a milestone toward control, elimination, and eradication of Taenia solium. The design of future programs may benefit from important information such as the safety of large-scale niclosamide administration, case identification by means of copro-antigens, mass administration of oxfendazole and TSOL18 vaccine in the swine population, and achieving participation goals. On the other hand, the intervention scheme used was complex and involved several rounds of massive treatment to human and swine population, in addition to a vaccine for swine.
Clearly, the following actions are also required: appropriate coordination with local authorities, identification of population subgroups that may be reluctant to participate and remain as residual infection foci, as well as the design of post-intervention surveillance systems. Our perception of the future agenda is to simplify the program, provide robust and cheap tools, and adjust the intervention approach to different scenarios through pilot studies. It is very important not to jump into unplanned control interventions without appropriate effect measurement, as the result may otherwise be counter-productive. The failure of a control program leads to discouragement among the population and institutions in charge of decision-making.
Based on a concept of organization by regions, we would like to submit for consideration some guidelines that we hope will be useful. A summary is presented in Table 1 with a detailed description in the following pages.
BASELINE MEASURES
This first section presents a basic approach for the registration and management of transmission foci as well as for individual cases of taeniasis and cysticerosis. These systems should be implemented independently regardless of whether an organized program of control/elimination is in place. Depending on the type of action, a local installation needs to be identified, within the Ministries of Health or Agriculture (or a responsible committee), to take charge of the action and its registry. Reports must be centralized at regional and national level at the corresponding agencies and levels.
Confirmation of the presence of T/C / Identification of swine cysticercosis foci. The most important piece of information, not only for a control or elimination program for taeniasis/cysticercosis, but also for the primary management of transmission foci and infection cases, is to define if there is local transmission of T/C in each province or by districts in order to define endemic and non-endemic areas. This would allow for the definition of areas where time and effort need to be invested in implementing diagnosis and case management systems, while at the same time, defining areas that require active control/elimination programs. Exact determination of prevalence levels does not have any practical use and, in general, does not change the need for control activities 1616. Medina MT, Aguilar-Estrada RL, Alvarez A, Duron RM, Martinez L, Dubon S, et al. Reduction in rate of epilepsy from neurocysticercosis by community interventions: the Salama, Honduras study. Epilepsia. 2011;52(6):1177-85.,1818. Garcia HH, Gonzalez AE, Del Brutto OH, Tsang VC, Llanos-Zavalaga F, Gonzalvez G, et al. Strategies for the elimination of taeniasis/cysticercosis. J Neurol Sci. 2007;262(1-2):153-7..
Epidemiological evidence suggests that T/C establishes a usual level of endemicity, within a reasonable range of variation, to maintain its transmission 44. Garcia HH, Gonzalez AE, Gilman RH, Moulton LH, Verastegui M, Rodriguez S, et al. Combined human and porcine mass chemotherapy for the control of T. solium. Am J Trop Med Hyg. 2006;74(5):850-5.,1919. Coral-Almeida M, Gabriel S, Abatih EN, Praet N, Benitez W, Dorny P. Taenia solium Human Cysticercosis: A Systematic Review of Sero-epidemiological Data from Endemic Zones around the World. PLoS Negl Trop Dis. 2015;9(7):e0003919.. In this sense, if the objective of the program is elimination, as it is in our opinion, the degree of endemicity (the exact prevalence level) is of little practical use, since what is being proposed is the elimination of transmission, expanding into geographic areas that are transmission-free. These areas must be defined at places farthest from migration and gradually expand to nearby areas in an concentric manner, independently of its endemicity degree 1717. Garcia HH, Gonzalez AE, Tsang VC, O'Neal SE, Llanos-Zavalaga F, Gonzalvez G, et al. Elimination of Taenia solium Transmission in Northern Peru. N Engl J Med 2016;375:1196-1197..
On the other hand, it may be tempting to estimate the population prevalence of taeniasis, swine cysticercosis, or neurocysticercosis, in order to focalize control actions. This position assumes two concepts: a) that control measures to be proposed are not practical enough or low-cost enough to become implemented in all endemic sites (otherwise it would unnecessarily discriminate low endemicity districts, which still have T/C), and b) control measures do not target elimination (if you are targeting elimination, conducting the activities in non-neighboring areas makes little practical sense and it would encourage failure due to re-introduction from neighboring endemic areas. 1717. Garcia HH, Gonzalez AE, Tsang VC, O'Neal SE, Llanos-Zavalaga F, Gonzalvez G, et al. Elimination of Taenia solium Transmission in Northern Peru. N Engl J Med 2016;375:1196-1197..
Even if one is favoring control over elimination, the relative value of baseline prevalence estimates is very limited.In this sense, we propose that initial actions to confirm the presence of T/C be focused on finding pigs with cysticercosis. In contrast to taeniasis, swine cysticercosis is very well known by the population, who calls it "triquina." Although finding a person with Taenia solium taeniasis confirms a transmission focus, cysticercosis in the swine population is an indicator present at higher prevalence levels, more dynamic because of rapid population renewal 1818. Garcia HH, Gonzalez AE, Del Brutto OH, Tsang VC, Llanos-Zavalaga F, Gonzalvez G, et al. Strategies for the elimination of taeniasis/cysticercosis. J Neurol Sci. 2007;262(1-2):153-7.,2020. Gonzalez AE, Garcia HH, Gilman RH, Tsang VC. Control of Taenia solium. Acta Tropica. 2003;87(1):103-9.. A system based on swine cysticercosis would be more sensitive to changes.
Districts with evidence of active T/C transmission must be identified and a regional and national map of endemic areas must be prepared. In this regard, we propose a definition of active transmission referring to the presence of swine cysticercosis cases in the year before. Swine cysticercosis can be initially defined based on verbal reports, using a previously-defined text to be used when questioning local health agents. In a second stage, cysts could be collected by district or by village for microscopic confirmation. A reporting system for swine cysticercosis must take into consideration health regulations that call for confiscation and incineration of infected carcasses, which, to be practical, annuls the possibility of case reporting on behalf of the farmers for fear of losing their meat. Below is a list of our proposed inclusive definitions:
SUSPECTED CASE OF PORCINE CYSTICERCOSIS
a. A pig in which nodules on the base of the tongue have been detected by palpation or by visual inspection.
b. A pig in which cysts suspicious for cysticercosis (small and whitish) have been detected after slaughter
CONFIRMED CASE OF PORCINE CYSTICERCOSIS
Diagnostic confirmation using microscopic examination of a cyst preserved in alcohol or formaldehyde.
In order to make this record feasible, the first thing to establish is an epidemiological information record (case report) based on the network of local health clinics and/or health promotors. The population must be informed that meat contaminated with cysticercosis should not be eaten, or else, that it should be fried in bite-size pieces. In a following stage, the population may be educated to bring small pieces of tissue with suspected cysts to the health clinic or to the agency responsible for veterinary care. Considering the normal reluctance of the population to report ill animals because of the risk of having their animals confiscated or facing punitive measures, an incentive program may be needed for the initial reports. If this were the case, one of the requirements for incentives must include confirmation of the place of origin of the infected pig.
Actions subsequent to the report of a swine cysticercosis case must be defined. The existing evidence, in addition to common sense, suggests clustering of swine cysticercosis around a human case with taeniasis 2121. Sarti-Gutierrez EJ, Schantz PM, Lara- Aguilera R, Gomez Dandoy H, Flisser A. Taenia solium taeniasis and cysticercosis in a Mexican village. Trop Med Parasitol. 1988;39(3):194-8.
22. Lescano AG, Garcia HH, Gilman RH, Guezala MC, Tsang VC, Gavidia CM, et al. Swine cysticercosis hotspots surrounding Taenia solium tapeworm carriers. Am J Trop Med Hyg. 2007;76(2):376-83.-2323. O'Neal SE, Moyano LM, Ayvar V, Gonzalvez G, Diaz A, Rodriguez S, et al. Geographic correlation between tapeworm carriers and heavily infected cysticercotic pigs. PLoS Negl Trop Dis. 2012;6(12):e1953.. Upon a report of a pig with cysticercosis, a basic intervention scheme would involve oxfendazole administration 2424. Gonzales AE, Garcia HH, Gilman RH, Gavidia CM, Tsang VC, Bernal T, et al. Effective, single-dose treatment or porcine cysticercosis with oxfendazole. Am J Trop Med Hyg. 1996;54(4):391-4.
25. Gonzalez AE, Falcon N, Gavidia C, Garcia HH, Tsang VC, Bernal T, et al. Treatment of porcine cysticercosis with oxfendazole: a dose-response trial.. Veterinary Record. 1997;141(16):420-2.-2626. Gonzalez AE, Falcon N, Gavidia C, Garcia HH, Tsang VC, Bernal T, et al. Time-response curve of oxfendazole in the treatment of swine cysticercosis. Am J Trop Med Hyg. 1998;59(5):832-6. to all the pigs in the house and a screening for taef in all the individuals who dwell in the house and possibly, the neighboring houses. This must include informing the population that animals treated with oxfendazole should not be killed for at least two weeks after treatment. During this two-week period anti-parasitic drug residues may persist in the meat 2727. Moreno L, Lopez-Urbina MT, Farias C, Domingue G, Donadeu M, Dungu B, et al. A high oxfendazole dose to control porcine cysticercosis: pharmacokinetics and tissue residue profiles. Food Chem Toxicol. 2012;50(10):3819-25.. Alternatively, treatment with niclosamide could also be administered to the individuals who dwell in the house. In this case, collecting a fecal sample immediately after treatment to identify infected individuals and to confirm that they have been cured, would be highly recommended. Application of biosafety measures in the treatment of individuals suspected of being T. solium carriers should be emphasized.
Definition of suspected case and confirmed case of taeniasis. T. solium taeniasis is rarely observed by patients, in contrast to T. saginata infections 2828. Flisser A, Vazquez-Mendoza A, Martinez- Ocana J, Gomez-Colin E, Leyva RS, Medina-Santillan R. Short report: evaluation of a self-detection tool for tapeworm carriers for use in public health. Am J Trop Med Hyg. 2005;72(5):510-2.. It is highly probable that a self-reporting system result in the detection of mostly T. saginata cases. The authors hereby propose the addition of suspected case and confirmed case definitions. This may originally be presumed, just like in the above-mentioned item, based on verbal reports, using pre-defined texts to be used in questions to local health personnel. It should match endemicity areas to swine cysticercosis. A second stage may ask for collection of fecal samples and/or parasite material for microscopic confirmation at a second level center. Since sensitivity of microscopic testing of feces for the diagnosis of T. solium taeniasis is rather poor, a negative result does not exclude parasitosis. Ideally, immunological diagnosis through coproantigen test should be available 2929. Allan JC, Avila G, Garcia Noval J, Flisser A, Craig PS. Immunodiagnosis of taeniasis by coproantigen detection. Parasitology. 1990;101 Pt 3:473-7.,3030. Bustos JA, Rodriguez S, Jimenez JA, Moyano LM, Castillo Y, Ayvar V, et al. Detection of Taenia solium taeniasis coproantigen is an early indicator of treatment failure for taeniasis. Clin Vaccine Immunol. 2012;19(4):570-3., at least at the head of each health network. Results from the coproantigen test must be interpreted in relation to the test cut-off point, with the understanding that weak positives often do not correlate with active taeniasis infection.
SUSPECTED CASE OF TAENIASIS
a. Individual reporting having excreted parasites or flat, whitish or yellowish parasite pieces.
b. Dwellers of a house where a pig was identified with live cysts upon slaughter.
CONFIRMED CASE OF TAENIASIS
Positive fecal test by microscopy and coproantigen detection.
According to the above description, actions suggested include collection of fecal samples from suspected cases, pre-processing (fixing in formalin phosphate buffered saline (PBS)) and shipping to a local confirmation center for microscopy and coproantigen test. If positive, adequate treatment must be coordinated as detailed below.
Management of taeniasis by level, criteria for referral and counter-referral, follow up. Treatment of taeniasis is extremely important for the prevention of swine cases and to help control the disease. Biosafety measures for health personnel, for the patient and the environment must be taken into consideration given the fact that manipulation of feces infected with T. solium may result in cysticercosis or neurocysticercosis. This process must be conducted under medical supervision to prevent or manage adverse effects of the purge or medication, and to avoid contamination by contact with infective eggs in feces 3131. Jeri C, Gilman RH, Lescano AG, Mayta H, Ramirez ME, Gonzalez AE, et al. Species identification after treatment for human taeniasis. Lancet. 2004;363(9413):949-50..
The drug of choice is niclosamide. The use of praziquantel in the treatment of taeniasis may generate epileptic seizures in individuals who have asymptomatic NCC, so its use is not recommended unless NCC has been ruled out by neuroimages (computerized axial tomography or magnetic resonance) and serology 11. Garcia HH, Nash TE, Del Brutto OH. Clinical symptoms, diagnosis, and treatment of neurocysticercosis. Lancet Neurol. 2014;13(12):1202-15..
The patient must adhere to a strictly soft diet for at least 2 days. In the morning of treatment day, a light purge will be administered. Once liquid feces are obtained, the appropriate dose of niclosamide must be given (2 gr orally for adults, 1 gr for children older than 6). Two hours after niclosamide intake, a second purge is administered 3030. Bustos JA, Rodriguez S, Jimenez JA, Moyano LM, Castillo Y, Ayvar V, et al. Detection of Taenia solium taeniasis coproantigen is an early indicator of treatment failure for taeniasis. Clin Vaccine Immunol. 2012;19(4):570-3.,3131. Jeri C, Gilman RH, Lescano AG, Mayta H, Ramirez ME, Gonzalez AE, et al. Species identification after treatment for human taeniasis. Lancet. 2004;363(9413):949-50.. The whole process must involve abundant oral hydration to avoid dehydration or electrolyte disorders, and to facilitate purge and elimination of the worm. After taeniasis diagnosis, all fecal samples must be collected in disposable containers and eliminated following biosafety guidelines, which implies defining and establishing a proper elimination system. It is recommended to refer patients to a level 2 health clinic or higher for treatment and observation for a few hours after purge.
Whenever possible, a new fecal sample must be collected 15 days after treatment and sent for coproantigen detection at a reference laboratory in order to confirm patient cure 1717. Garcia HH, Gonzalez AE, Tsang VC, O'Neal SE, Llanos-Zavalaga F, Gonzalvez G, et al. Elimination of Taenia solium Transmission in Northern Peru. N Engl J Med 2016;375:1196-1197.,3030. Bustos JA, Rodriguez S, Jimenez JA, Moyano LM, Castillo Y, Ayvar V, et al. Detection of Taenia solium taeniasis coproantigen is an early indicator of treatment failure for taeniasis. Clin Vaccine Immunol. 2012;19(4):570-3.. Confirmation of cure is very important, because in cases of undetected therapeutic failure, all efforts undertaken would be entirely useless.
Clinical evaluation must be performed. Patients with taeniasis and a history of epileptic seizures and other neurologic symptoms must be referred to a level 3 clinic or higher, to be evaluated for neurocysticercosis.
Definition of suspected and confirmed cases of human neurocysticercosis. There are no operational definitions for cysticercosis cases at endemic population level. The following definition proposals represent the most frequent presentations associated with neurocysticercosis.
SUSPECTED CASE OF NEUROCYSTICERCOSIS
a. Individual with a history of episodes compatible with epileptic crises: loss of consciousness, involuntary movements of hands, arms or legs, light vision, etc., particularly if these episodes start after 15 years of age.
b. Individual with symptoms compatible with increased intracranial pressure: severe headache, dizziness, vomiting.
c. Individual with neurological symptoms and palpable subcutaneous nodules.
CONFIRMED CASE OF NEUROCYSTICERCOSIS
Individual with neurological symptoms and brain imaging (computerized axial tomography or magnetic resonance) showing lesions compatible with NCC, or showing neurological symptoms and a compatible Western blot positive result to cysticercosis antibodies 3232. Tsang VC, Brand JA, Boyer AE. An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis. 1989;159(1):50-9..
Management of NCC by levels, referral and counter-referral criteria, follow up. In cases of suspected cases of NCC (epilepsy or intracranial hypertension in endemic areas), the health personal must follow the clinical practice guidelines for management of cysticercosis, published by the Instituto Nacional de Ciencias Neurologicas 3333. Instituto Nacional de Ciencias Neurologicas. Guia de práctica clínica de neurocisticercosis. Lima, Peru. 2014 [Citado el 21 de Octubre 2017]., both for the management of the condition by levels, and for referral, counter-referral and follow-up.
ACTIONS FOR CONTROL AND ELIMINATION OF TAENIASIS/CYSTICERCOSIS
Initially, community control of T/C must be focused on detection and treatment of taeniasis cases, treatment with oxfendazole for suspected pigs and decreased risk behavior, such as not eating meat with cysticercosis, encouraging hand washing behavior and use of latrines.
In spite of the fact that the feasibility of T. solium elimination has already been demonstrated (17, 30), there is still a long way to go. Areas for improvement include simplifying the program used in Tumbes, defining monitoring and post-intervention surveillance systems, adapting interventions and monitoring to different local realities, etc. There are ongoing evaluation programs for the control interventions used in Tumbes, particularly to simplify the approach and make tools available in endemic areas. These programs include mass treatment of the human population with niclosamide, mass treatment of the swine population with oxfendazole, and vaccination of the swine population. To date, there is not a defined strategy selected or tested for application at a large scale. In this context, and until an optimal program is defined, the above-mentioned control actions provide a first line of action until a regional or national program becomes available.
DEFINITION OF ACHIEVEMENT INDICATORS FOR LEVELS I AND II
It is essential to define appropriate indicators within the operational system of government organizations in order to operationalize actions against taeniasis/cysticercosis. Table 2 shows suggestions for each one of the items described in this manuscript.
The final aim of biomedical research is to improve health and living conditions throughout society. In pursuit of this aim, the role of research groups, such as ours, is to provide evidence and tools so that results of our research become health policies in appropriate instances. At the national level, the Ministry of Health and Ministry of Agriculture are responsible for actions toward control of taeniasis/cysticercosis, in collaboration with regional health directorates and academia. In order to meet the proposed goals, we need an organization at local, regional and national level that encompasses human and veterinary health, as well as education at the social level. This organization must be adequately funded, so that it may meet its operational requirements.
Establishing the above-described organization requires the corresponding decision making at central or at regional level. Neurocysticercosis is a major contributor to neurological diseases in Peru. We hope that the above concepts will serve as a tool for the implementation of activities, with baseline actions at the beginning, but eventually leading to regional or national control programs.
References
- 1Garcia HH, Nash TE, Del Brutto OH. Clinical symptoms, diagnosis, and treatment of neurocysticercosis. Lancet Neurol. 2014;13(12):1202-15.
- 2Cantey PT, Coyle CM, Sorvillo FJ, Wilkins PP, Starr MC, Nash TE. Neglected parasitic infections in the United States: Cysticercosis. Am J Trop Med Hyg. 2014;90(5):805-9.
- 3Schantz PM, Cruz M, Sarti E, Pawlowski Z. Potential eradicability of taeniasis and cysticercosis. Bulletin of the Pan American Health Organization. 1993;27(4):397- 403.
- 4Garcia HH, Gonzalez AE, Gilman RH, Moulton LH, Verastegui M, Rodriguez S, et al. Combined human and porcine mass chemotherapy for the control of T. solium. Am J Trop Med Hyg. 2006;74(5):850-5.
- 5Giordani MT, Tamarozzi F, Cattaneo F, Brunetti E. Three cases of imported neurocysticercosis in Northern Italy. J Travel Med. 2014;21(1):17-23.
- 6Garcia HH, Gonzalez AE, Rodriguez S, Gonzalvez G, Llanos-Zavalaga F, Tsang VC, et al. Epidemiologia y control de la cisticercosis en el Peru. Rev Peru Med Exp Salud Publica. 2010;27(4):592-7.
- 7Sciutto E, Martinez JJ, Villalobos NM, Hernandez M, Jose MV, Beltran C, et al. Limitations of current diagnostic procedures for the diagnosis of Taenia solium cysticercosis in rural pigs. Vet Parasitol. 1998;79(4):299-313.
- 8Montano SM, Villaran MV, Ylquimiche L, Figueroa JJ, Rodriguez S, Bautista CT, et al. Neurocysticercosis: association between seizures, serology, and brain CT in rural Peru. Neurology. 2005;65(2):229- 33.
- 9Del Brutto OH, Santibanez R, Idrovo L, Rodriguez S, Diaz-Calderon E, Navas C, et al. Epilepsy and neurocysticercosis in Atahualpa: a door-to-door survey in rural coastal Ecuador. Epilepsia. 2005;46(4):583-7.
- 10Medina MT, Duron RM, Martinez L, Osorio JR, Estrada AL, Zuniga C, et al. Prevalence, incidence, and etiology of epilepsies in rural Honduras: the Salama Study. Epilepsia. 2005;46(1):124-31.
- 11Moyano LM, Saito M, Montano SM, Gonzalvez G, Olaya S, Ayvar V, et al. Neurocysticercosis as a cause of epilepsy and seizures in two community-based studies in a cysticercosis-endemic region in Peru. PLoS Negl Trop Dis. 2014;8(2):e2692.
- 12Takayanagui OM, Jardim E. [Clinical aspects of neurocysticercosis: analysis of 500 cases].. Arq Neuropsiquiatr. 1983;41(1):50-63
- 13Sotelo J, del Brutto OH, Penagos P, Escobedo F, Torres B, Rodriguez-Carbajal J, et al. Comparison of therapeutic regimen of anticysticercal drugs for parenchymal brain cysticercosis. J Neurol. 1990;237(2):69-72.
- 14Garcia HH, Gilman RH, Tovar MA, Flores E, Jo R, Tsang VC, et al. Factors associated with Taenia solium cysticercosis: analysis of nine hundred forty-six Peruvian neurologic patients. Cysticercosis Working Group in Peru (CWG). Am J Trop Med Hyg. 1995;52(2):145-8.
- 15Schantz PM, Moore AC, Munoz JL, Hartman BJ, Schaefer JA, Aron AM, et al. Neurocysticercosis in an Orthodox Jewish community in New York City. N Engl J Med 1992;327:692-695.
- 16Medina MT, Aguilar-Estrada RL, Alvarez A, Duron RM, Martinez L, Dubon S, et al. Reduction in rate of epilepsy from neurocysticercosis by community interventions: the Salama, Honduras study. Epilepsia. 2011;52(6):1177-85.
- 17Garcia HH, Gonzalez AE, Tsang VC, O'Neal SE, Llanos-Zavalaga F, Gonzalvez G, et al. Elimination of Taenia solium Transmission in Northern Peru. N Engl J Med 2016;375:1196-1197.
- 18Garcia HH, Gonzalez AE, Del Brutto OH, Tsang VC, Llanos-Zavalaga F, Gonzalvez G, et al. Strategies for the elimination of taeniasis/cysticercosis. J Neurol Sci. 2007;262(1-2):153-7.
- 19Coral-Almeida M, Gabriel S, Abatih EN, Praet N, Benitez W, Dorny P. Taenia solium Human Cysticercosis: A Systematic Review of Sero-epidemiological Data from Endemic Zones around the World. PLoS Negl Trop Dis. 2015;9(7):e0003919.
- 20Gonzalez AE, Garcia HH, Gilman RH, Tsang VC. Control of Taenia solium. Acta Tropica. 2003;87(1):103-9.
- 21Sarti-Gutierrez EJ, Schantz PM, Lara- Aguilera R, Gomez Dandoy H, Flisser A. Taenia solium taeniasis and cysticercosis in a Mexican village. Trop Med Parasitol. 1988;39(3):194-8.
- 22Lescano AG, Garcia HH, Gilman RH, Guezala MC, Tsang VC, Gavidia CM, et al. Swine cysticercosis hotspots surrounding Taenia solium tapeworm carriers. Am J Trop Med Hyg. 2007;76(2):376-83.
- 23O'Neal SE, Moyano LM, Ayvar V, Gonzalvez G, Diaz A, Rodriguez S, et al. Geographic correlation between tapeworm carriers and heavily infected cysticercotic pigs. PLoS Negl Trop Dis. 2012;6(12):e1953.
- 24Gonzales AE, Garcia HH, Gilman RH, Gavidia CM, Tsang VC, Bernal T, et al. Effective, single-dose treatment or porcine cysticercosis with oxfendazole. Am J Trop Med Hyg. 1996;54(4):391-4.
- 25Gonzalez AE, Falcon N, Gavidia C, Garcia HH, Tsang VC, Bernal T, et al. Treatment of porcine cysticercosis with oxfendazole: a dose-response trial.. Veterinary Record. 1997;141(16):420-2.
- 26Gonzalez AE, Falcon N, Gavidia C, Garcia HH, Tsang VC, Bernal T, et al. Time-response curve of oxfendazole in the treatment of swine cysticercosis. Am J Trop Med Hyg. 1998;59(5):832-6.
- 27Moreno L, Lopez-Urbina MT, Farias C, Domingue G, Donadeu M, Dungu B, et al. A high oxfendazole dose to control porcine cysticercosis: pharmacokinetics and tissue residue profiles. Food Chem Toxicol. 2012;50(10):3819-25.
- 28Flisser A, Vazquez-Mendoza A, Martinez- Ocana J, Gomez-Colin E, Leyva RS, Medina-Santillan R. Short report: evaluation of a self-detection tool for tapeworm carriers for use in public health. Am J Trop Med Hyg. 2005;72(5):510-2.
- 29Allan JC, Avila G, Garcia Noval J, Flisser A, Craig PS. Immunodiagnosis of taeniasis by coproantigen detection. Parasitology. 1990;101 Pt 3:473-7.
- 30Bustos JA, Rodriguez S, Jimenez JA, Moyano LM, Castillo Y, Ayvar V, et al. Detection of Taenia solium taeniasis coproantigen is an early indicator of treatment failure for taeniasis. Clin Vaccine Immunol. 2012;19(4):570-3.
- 31Jeri C, Gilman RH, Lescano AG, Mayta H, Ramirez ME, Gonzalez AE, et al. Species identification after treatment for human taeniasis. Lancet. 2004;363(9413):949-50.
- 32Tsang VC, Brand JA, Boyer AE. An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis. 1989;159(1):50-9.
- 33Instituto Nacional de Ciencias Neurologicas. Guia de práctica clínica de neurocisticercosis. Lima, Peru. 2014 [Citado el 21 de Octubre 2017].
Publication Dates
- Publication in this collection
Jan-Mar 2018
History
- Received
27 Oct 2017 - Accepted
17 Jan 2018