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Evaluación del impacto de un programa de control de la teniasis-cisticercosis (Taenia solium) Translated title: Evaluation of the impact of a control program against taeniasis-cysticercosis (Taenia solium)
research-article
Author(s):
Aline S de Aluja ,
Raúl Suárez-Marín ,
Edda Sciutto-Conde ,
Julio Morales-Soto ,
José Juan Martínez-Maya ,
Nelly Villalobos
Publication date (Print and electronic):
June 2014
Journal:
Salud Pública de México
Publisher:
Instituto Nacional de Salud Pública
Keywords:
pigs,
taenia solium,
cysticercosis,
diagnosis,
education,
vaccination,
Mexico,
cerdos,
taenia solium,
cisticercosis,
diagnóstico,
educación,
vacunación,
México
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Abstract
Objetivo. Evaluar el impacto de un programa de control de la teniasis-cisticercosis por Taenia solium con fines de erradicación, basado en educación de la comunidad y vacunación de cerdos. Material y métodos. Se estimó la prevalencia de cisticercosis porcina por medio de la palpación de lengua, ultrasonido y presencia de anticuerpos en suero, antes de iniciar el programa y tres años después, en tres regiones del estado de Guerrero. Resultados. Se observó una reducción significativa en la prevalencia de cisticercosis porcina de 7 a 0.5% y de 3.6 a 0.3%, estimadas por examen de lengua y ultrasonido, respectivamente (p<0.01), y una disminución no significativa de la seroprevalencia de 17.7 a 13.3%. Conclusiones. La reducción de la prevalencia de teniasis-cisticercosis comprueba la efectividad del programa para prevenir la infección. La presencia sostenida de anticuerpos es compatible con continuos contactos con Taenia solium u otros helmintos relacionados, y señala la necesidad de mantener las intervenciones para lograr su erradicación.
Translated abstract
Objetive. The impact of a control program is evaluated to eventually eradicate taeniasis-cysticercosis (Taenia solium) based on education and vaccination of pigs. Materials and methods. The prevalence of porcine cysticercosis was estimated using tongue inspection, ultrasound and determination of antibodies, before and three years after the application in three regions of the state of Guerrero. Results. A significant reduction in the prevalence of porcine cysticercosis of 7 to 0.5% and 3.6 to 0.3% estimated by tongue examination or ultrasound respectively (p<0.01) and a no significant decrease in seroprevalence from 17.7 to 13.3% were observed. Conclusions. The reduction of the prevalence of taeniasis-cysticercosis establishes the program's effectiveness in preventing infection. The sustained presence of antibodies, compatible with contact of Taenia solium or other related helminths, underlines the importance of maintaining interventions to achieve eradication.
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Most cited references60
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Clinical Manifestations Associated with Neurocysticercosis: A Systematic Review
Introduction Neurocysticercosis (NCC) is primarily found in countries with poor sanitation and hygiene and improper slaughterhouse services. However, due to globalization and immigration, NCC is increasingly being reported in developed countries [1]. Humans become infected by ingesting Taenia solium eggs that later develop into oncospheres. These larvae can migrate to any organ in the body, but most reports have focused on cysts located in the Central Nervous System (CNS), eyes, muscles or subcutaneous tissues. The larvae have been found in several locations in the CNS. This diversity of locations is believed to partly explain the range of NCC's clinical manifestations. In addition, the signs and symptoms associated with NCC depend on the larvae's number, developmental stage (active, transitional or calcified), on the duration of the infection and the host's immune response [2]. Seizures and epilepsy are considered to be the most common manifestations of NCC. However, several other neurological disorders can also occur [3]. Unfortunately, these less common manifestations are rarely recognized as being linked to NCC, especially in low resource countries where imaging technology is scarce [4]. Thus, data on the full range of clinical expression of NCC are lacking, although such data are essential to accurately estimate the burden of NCC on different communities. This systematic review aims to estimate the frequency of the main clinical manifestations associated with NCC. Methods A systematic search of the literature, including documents published from January 1, 1990 to June 1, 2008, was conducted to capture data on clinical manifestations associated with NCC. Search strategy and data source PubMed, Commonwealth Agricultural Bureau (CAB) Abstracts, and 23 international databases were searched for data on NCC manifestations. Articles published in Chinese, English, French, Portuguese, Spanish, Italian, Romanian and German were searched. Two different searches were launched to cover both clinical manifestations and mortality associated with NCC infection. For the clinical manifestations, our search strategy in PubMed included terms: "Cysticercosis/complications" [MeSH] OR "Cysticercosis/history" [MeSH] OR “Cysticercosis/pathology" [MeSH] OR "Cysticercosis/psychology" [MeSH] OR "Cysticercosis/radiography" [MeSH] OR "Cysticercosis/radionuclide imaging" [MeSH] OR "Cysticercosis/ultrasonography" [MeSH]. CAB Abstracts and the international search engines were queried using the following keywords: “Taenia solium”, “taeniasis” or “taeniosis”, “cysticercosis”, and “neurocysticercosis”. One Thesis in Medicine from Burkina Faso was identified through contacts in Sub-Saharan Africa and was included. For mortality associated with NCC, PubMed was searched using the terms: “cysticercosis/mortality” [MeSH] OR "neurocysticercosis/mortality" [MeSH]. In CAB Abstracts and the international search engines the keywords “neurocysticercosis and mortality” were used. Inclusion and exclusion criteria Documents reporting valid (defined as an absence of major biases, see later), original data on clinical manifestations associated with NCC were eligible for inclusion. Books and conference abstracts were excluded because they were unlikely to have sufficient details on the methodology used. All documents retrieved were screened based on the title and the abstract. The exclusion criteria for phase I were: 1) wrong agent; 2) animal data only; 3) no original data on the frequency of NCC's clinical manifestations; 4) case series with less than 20 participants; 5) review article without original data; and 6) editorials or letters to the editors without original data. Documents without abstracts were included in the next phase. After phase I, all eligible full text documents were reviewed qualitatively (phase II) and quantitatively (phase III). The exclusion criteria for phase II were identical to those used in phase I in addition to: 1) high potential for information bias (defined as no neuroimaging (CT-scans or MRI) or autopsies used for the diagnosis of NCC); 2) high potential for selection bias (defined as the study of volunteers or less than 80% of patients with imaging and NCC); or 3) all available data were from before 1990 or after June 1, 2008. The quantitative data from documents included after phase II were extracted in phase III. Articles reporting the proportion of epilepsy cases with lesions of NCC were excluded from the current study and reported in another article [5]. Data extraction Data on studies' characteristics, methodological quality and frequency of clinical manifestations and mortality were collected. Data extraction was conducted independently by at least two investigators. A third investigator checked a random sample of 10% of all of the entries. Discrepancies were resolved through discussion until a consensus was reached. The screening process (phase I) was performed in an Excel® spreadsheet (Microsoft Corp., Redmond, WA). Methodological factors (phase II) and frequency data (phase III) were recorded in standardized electronic forms of a data extraction tool which was developed in Access® (Microsoft Corp., Redmond, WA) specifically for this review (available from the authors on request). Authors of primary studies were contacted when the article being reviewed contained missing or unclear information on the study design or results. Data synthesis and analysis Whenever two or more different studies described the same clinical manifestation, we conducted a meta-analysis and estimated the pooled proportion of the given clinical manifestation among people with NCC. For these analyses, studies reporting “seizures” and those reporting “epilepsy” were combined, as most reports did not discriminate between the two. The definition of epilepsy is the occurrence of at least two unprovoked seizures separated by at least 24 hours [6]. As there was great variability in the characteristics of the included documents, results were expressed as random-effects models using proportion with 95% confidence intervals (95% CI) [7]. The Freeman-Tukey double arcsine transformation was used for pooled estimates of proportion and corresponding 95% CI from the random-effects model [8]–[9]. The Cochran's Q test was used to assess homogeneity across studies and the I2 index was used to summarize the total variability in proportion due to between-study variation [10]. Random-effect models were used due to important heterogeneity between studies. A sensitivity analysis was conducted by estimating the pooled proportion after omitting one study at a time. The analysis was performed with the R META package (Version 0.8–2; Guido Schwarzer in R-META metagen function) from R statistical software (R Development Core Team, www.R-project.org). No study had considerable effect on the pooled estimate and results from the sensitivity analyses are not presented. A mixed-effects regression model was used to determine if the age group (children vs adults) significantly influenced the estimated percentage of seizures and epilepsy among people with NCC. Results Literature search A total of 1569 documents were identified in phase I. Figure 1 shows the number of papers identified in each database and included in each phase and the reasons for exclusions. After phase I, nearly three-quarters of the articles were excluded. An additional 383 articles were excluded during phase II, most of which (n = 200) did not have manifestation data or did not use neuroimaging to diagnose NCC. Fourteen Chinese articles could not be traced and were excluded. Finally, 11 articles were excluded from this review and included in a study on the proportion of epilepsy cases with NCC (see [5]). 10.1371/journal.pntd.0001152.g001 Figure 1 Flowchart describing the number of papers remaining at different phases of the study. Phase III included 21 documents (1.3%) containing quantitative data on various clinical manifestations associated with NCC (Table 1). 10.1371/journal.pntd.0001152.t001 Table 1 Descriptive summary of the studies included for estimating the distribution of manifestations associated with neurocysticercosis. Reference (language) Country, year(s) of study Population Diagnosis of NCC Type of lesions Measurement of manifestations Source Target Study sample size [16] (Portuguese) Brazil, 1987–97 Autopsies of the Serviço de Anatomia Patológica do Hospital de Clínicas da Universidade Federal do Paraná, 1987–97 28 autopsies (>15 years old) 27 (>18–85 years old) Autopsies 100% active Medical chart and necropsy report [15] (Portuguese) Brazil, 1995–6 Catchment population of the Centro de Diagnostico por Imagen do Parana (CEDIP), Hospital das Nacoes, Curitiba, PR, 1995–96 236 neurology patients with NCC (all ages) 236 CT-scan[49] 7.2% active Not specified [11] (English) Brazil, 1993–4 People attending the Section of Neuroinfectious Diseases at the Clinicas da Faculdade de Medicina da Universidade de Sao Paulo, 1993–94 38 neurology patients with NCC (18–60 years old) 38 CT-scan + positive CSF immunological test + MRI (cystic lesions) 76.3% active Interview (depression) and medical charts [25] (Portuguese) Brazil, 1990–01 Catchment population of Ambulatorio de Neurologia do Hospital Universitario Alcides Caeneiro, Paraiba, 1990–01 44 neurology patients with NCC (all ages) 44 CT –scan[50] + CSF (33)+MRI (5) 52.3% active Standardized medical chart reviews [21] (English) Ecuador, 1985–98 Catchment population of the Department of Neurology of the Eugenio Espejo Hospital in Quito, 1985–88 420 neurology patients with a stroke (17–86 years old) 420 CT scan, CSF, immunologic tests, other tests[51] NR Stroke defined according to Kotila, 1984 (neurological examination) [32] (English) Ecuador, 1994–96 Catchment population of the Department of Neurology, Luis Vernaza Hospital, and at the Neuro-Oncology Service, Instituto Oncologico Nacional, Guayaquil, 1994–96 43 neurology patients with cerebral glioma (20–86 years old) 43 CT-scan[52]–[53] 100% inactive Histology of open biopsy (presence of malignant glial cells) [20] (English) Mexico, 1989–96 Catchment pediatric population of the Neurology Department of the Instituto Nacional de Pediatria in Mexico City, 1989–96 122 neurology patients with NCC (14 months to 17 years old) 122 CT-scan, CSF (n = 71), MRI (n = 20), immunological tests 82.0% active Medical charts [12] (English) Mexico, 1993–03 Catchment population of three referral hospitals, Mexico City, 1993–03 206 neurology treatment-free NCC patients (11 months - 62 years old) 206 CT-scan and/or MRI 75.7% active Direct questionnaire (adults, 1 year prospective) or hospital records (children, retrospective) [33] (English) Mexico, 1993–96 People autopsied at the General Hospital of Mexico, 1993–96 113 autopsies with malignant hematological diseases (0–80 years old) 113 Pathological analysis of the brain (autopsy) NR Not provided (autopsy) [34] (Spanish) Mexico, 1986–98 Catchment population of the neurological clinic of the Instituto Nacional y Neurologia Manual Velasco Suarez, 1986–98 63 patients with non-aneurysmal sub-arachnoid hemorraghe (19–82 years old) 50 CT-scan and MRI (no specific definition provided) NA Spontaneous headache or alteration of consciousness w/o trauma and presence of blood in the subarachnoid space [22] (English) USA, 1985–91 Catchment population of the Ben Taug General Hospital of Houston, Houston Texas, 1985–91 112 patients with NCC (1–84 years old) 112 Discharge diagnosis of NCC (definite or probable, no reference) 80.4% active Medical charts [23] (English) USA, 1986–94 Catchment pediatric population of the at Children's Memorial Hospital's emergency room, Chicago, 1986–94 47 children with NCC (1–15 years old) 47 Biopsy or MRI/CT-scan and serological or CSF tests or MRI/CT and epidemiological link 56% active from 45 CT-scans Medical records (medical, laboratory, pathology, outpatient records) [18] (English) India, 1984–87 Pediatric catchment population of the G.B. Pant Hospital, New Delhi, 1984–87 27 children with NCC (3–12 years old) 27 CT-scan and positiveCSF ELISA and MRI and histological exam 81.4% positive for CSF ELISA Not specified [19] (English) India, 1979–90 Pediatric Neurology Clinic patients, New Delhi, 1979–90 50 neurology patients with NCC (1–15 years old) 50 CT-scan supported by MRI (8), history, serum or CSF antibodies, histology of nodules 80% active Medical charts [24] (Chinese) PR China, date? Hospitalised population of the department of neurology, Guangdong Medical University Hospital, Guangdong Province, no dates 36 inpatients with NCC (14–60 years old) 36 CT (31) or MRI (9) of the brain[54] 78% with active lesions Not specified [27] (Chinese) PR China, 1995–01 Catchment population of the department of infectious disease, Huaghan Hospital, Shangai, 1995–01 125 patients with NCC (2–68 years old) 125 MRI or CT scan of the brain showing lesions of NCC (3 were normal) 90 active, 4 inactive, 31 unknown Not specified [26] (Chinese) PR China, 1997–01 Catchment population of the NCC institute of the Jilin University, 1997–01 210 patients with NCC ( 19 years old). N/A represents the period of study missing. 10.1371/journal.pntd.0001152.g003 Figure 3 Forest plots of the proportion of symptomatic neurocysticercosis cases presenting with headaches. The forest plots represent A) all age groups, B) Children (0–19 years old) and C) Adults (>19 years old). N/A represents the period of study missing. 10.1371/journal.pntd.0001152.g004 Figure 4 Forest plots of the proportion of symptomatic neurocysticercosis cases presenting with increased intracranial pressure symptoms. The forest plots represent A) all age groups, B) Children (0–19 years old) and C) Adults (>19 years old). N/A represents the period of study missing. 10.1371/journal.pntd.0001152.g005 Figure 5 Forest plots of the proportion of symptomatic neurocysticercosis cases presenting with focal deficits. N/A represents the period of study missing. 10.1371/journal.pntd.0001152.g006 Figure 6 Forest plots of the proportion of symptomatic neurocysticercosis cases presenting with visual changes. N/A represents the period of study missing. 10.1371/journal.pntd.0001152.g007 Figure 7 Forest plots of the proportion of symptomatic neurocysticercosis cases presenting with altered mental state. 10.1371/journal.pntd.0001152.t003 Table 3 Pooled estimates of the percentage of manifestations among symptomatic NCC patients using random-effect binomial models. Manifestation Age group All Children Adults Seizures/epilepsy 78.8% (65.1%; 89.7%) 78.9% (70.5%; 86.2%) 63.2% (51.9%; 73.8%) Headaches 37.9% (23.3%; 53.7%) 27.7% (20.7%; 35.2%) 25.9% (10.7%; 45.0%) Signs of Intracranial Pressure/Hydrocephalus/Papilledema 11.7% (6.0%; 18.9%) 22.7% (10.2%; 38.5%) 16.3% (5.3%; 31.8%) Meningitis symptoms 7.9% (2.7%; 15.5%) 11.2% (5.2%; 19.0%) 5.6% (1.9%; 12.8%)* Cranial nerve palsy 2.8% (0.1%; 14.5%)* 6.0% (0.6%; 16.2%) NA Gait abnormality/ataxia 6.0% (1.9%; 12.1%) 2.4% (0.2%; 7.2%) 5.6% (1.9%; 12.8%)* Focal deficits 16.0% (9.7%; 23.6%) 12.5% (7.6%; 18.4%) 11.8% (4.1%; 22.9%) Visual changes 5.6% (1.1%; 13.5%) 3.5% (1.3%; 6.7%) NA Altered mental state/psychiatric symptoms 4.5% (1.5%; 9.0%) 4.0% (0.5%; 13.4%)* 28.1% (0.5%; 74.9%) Pyramidal signs NA 11.6% (0.0%; 42.9%) NA *: One study with binomial 95%CI. NA: No data Available. The distribution of manifestations in patients with active and inactive lesions was presented in three studies [12]–[14] (Table 4). There was a considerably higher proportion of patients with inactive NCC who presented with seizures/epilepsy (>88%) as compared with patients with active lesions (60–63%). Conversely, the proportion with signs or symptoms of intracranial hypertension was approximately 25% in patients with active lesions but was not found in patients with inactive NCC lesions. Hydrocephalus and meningitis were reported by only one author and were more frequent with active lesions. 10.1371/journal.pntd.0001152.t004 Table 4 Percentage of manifestations reported in symptomatic NCC patients with active and inactive lesions. Reference Country, year(s) of study Manifestation Type of lesions Percentage 95%CI [14] Portugal, 1983–92 Seizures/Epilepsy Active 60.5% 43.4%–76.0% [12] Mexico, 1993–03 Seizures/Epilepsy Active 62.8% 54.7%–70.4% [13] Portugal, 1983–89 Seizures/Epilepsy Inactive 98.3% 92.6%–99.5% [12] Mexico, 1993–03 Seizures/Epilepsy Inactive 88.0% 75.7%–95.5% [14] Portugal 1983–92 Intracranial Hypertension Active 23.7% 11.1%–40.2% [12] Mexico, 1993–03 Intracranial Hypertension Active 28.8% 21.9%–36.6% [13] Portugal, 1983–89 Intracranial Hypertension Inactive NA NA [12] Mexico, 1993–03 Intracranial Hypertension Inactive 0.0% 0.0%–7.1% [14] Portugal, 1983–92 Hydrocephalus at CT Active 23.7% 11.4%–40.2% [13] Portugal, 1983–89 Hydrocephalus at CT Inactive 3.5% 1.0%–8.7% [14] Portugal, 1983–92 Meningitis Active 5.3% 1.7%–21.4% [13] Portugal, 1983–89 Meningitis Inactive 0.9% 0.0%–4.7% Distribution of manifestations in people with NCC attending an imaging clinic In one study from Brazil [15], 236 patients seen at an imaging clinic had lesions suggestive of NCC of which 219 were inactive lesions. Lesions suggestive of other pathologies were found in 48 (20.3%) of the cases with suspected NCC. The distribution of manifestations was 30% with epilepsy, 51% with headaches, 8% with focal motor/sensory deficits. There were 35% with “other” symptoms found among patients with a CT-scan due to suspected neoplasia or stroke. Among 231 patients with NCC lesions seen in a neuroradiology department, 87 (38%) were asymptomatic, incidental findings in trauma patients and cases of suspected cerebrovascular disease [13]. All of these 87 had inactive lesions. This study is unique because it reports on the possible clinical spectrum of NCC. Distribution of manifestations among autopsied patients In a review of 901 autopsies conducted in a department of pathology and anatomy at the University Hospital of Paraná, Brazil, the authors reported on 28 cases of NCC, with medical charts available for 27 of the cases [16]. Of those, 13 were asymptomatic, nine had seizures as a complicating factor of the clinical picture prior to death, four had increased intracranial pressure, one had meningitis, one had a cerebrovascular form and one had dementia noted at some point during the course of the disease. Only two of the 27 patients had been diagnosed with NCC prior to death, which suggests that NCC is often undiagnosed among patients with neurological symptoms. Proportion of NCC cases seeking care who died The proportion of cases of NCC who sought care and subsequently died were 2.3% (2/88) of adult patients with active lesions in South Africa [17], 18.5% (5/27), 2.0% (1/50) and 1.6% (2/122) of pediatric patients in India [18]–[19] and Mexico [20], respectively, 3.2% (1/31) of adult patients with stroke in Ecuador [21], 5.3% (2/38) of patients with active lesions in Portugal [14], and 0.9% (1/112) of patients in Houston, Texas [22]. Most deaths were associated with complications of shunt surgery for the treatment of hydrocephalus. The duration of patient follow-up and referrals to other facilities were not reported, which limits the interpretation of the data. In a study of 27 autopsied patients in Brazil, the NCC lesions were considered the cause of death in 30% of the autopsied cases [16]. Duration of disease at the time of seeking medical care Several of the studies reported the time from the onset of symptoms to seeking medical care, with an average of 56.8 weeks in adult patients in South Africa [17], a median of 3.5 months (range 0–492 months) in patients in the United States [22], a median of 2 days (range <1 day to 8.75 years) in children presenting to the emergency room in the United States [23], and a range of 5 days to 20 years in inpatients seeking care in China [24]. Percentages of 77.3% [25] and 80% [26] of patients had sought care within one year, 92.8% within three years [27]. The time from onset of symptoms to seeking and receiving medical care will also vary depending on the type of manifestations and the local medical services' capacity. Death rate due to NCC One study in the United States [28] and another in the State of Sao Paolo [29], Brazil, reported age-adjusted annual mortality rates of 0.06 (95% CI: 0.05–0.07) and 1.68 (95% CI: 1.58–1.78) deaths per million population, respectively. The other studies from California [30] and Oregon [31] in the United States reported annual crude mortality rates of 0.33 (95% CI: 0.27 – 0.38) and 0.29 (95%CI: 0.11–0.64) deaths per million population. Proportion of NCC cases among people with specific manifestations In people presenting with glioma [32], malignant hematological disease [33], or non-aneurysmal subarachnoid hemorrhage [34], the proportions with NCC were 18.6%, 6.2% and 4.0%, respectively (Table 5). The proportion of NCC reported in people with stroke was 7.4% [21]. Some correlation between the location of the cyst and the focal neurological deficit was found in all NCC cases. These studies can only be used to encourage physicians to add NCC to their list of differential diagnoses when such a manifestation occurs, especially in endemic countries. 10.1371/journal.pntd.0001152.t005 Table 5 Percentage of NCC among people presenting in specific populations. Reference Country, year Clinical presentation Number of people with NCC Number of people with manifestations % NCC (95% CI) [32] Ecuador, 1994–96 Cerebral Glioma 8 43 18.6% 7.0%–30.2% [33] Mexico, 1993–96 Malignant hematological disease 7 113 6.2% 1.8%–10.6% [19] Ecuador 1985–88 Stroke 31 420 7.4% 5.1%–10.3% [34] Mexico 1986–98 Non-aneurysmal subarachnoid hemorrhage 2 50 4.0% 0.1%–11.6% Association between manifestation and NCC The odds ratio of NCC and cerebral glioma was estimated to be 7.63 (95%CI: 2.03–31.09) when cases of glioma were compared to age-sex-socioeconomic status matched, previously healthy, head trauma controls [32]. The odds ratio of the relation between NCC and malignant hematological diseases was estimated to be 3.54 (95%CI: 1.17–9.79) when autopsied cases were compared to autopsied cases without any type of neoplasm [33]. Discussion This study is the first systematic review of clinical manifestations associated with NCC, which can have a wide spectrum of neurologic and psychiatric manifestations including seizures, epilepsy, headache, cerebrovascular disorders, motor deficits and depression [35]. More than three-quarters of symptomatic NCC patients seen in neurological clinics present with seizures or epilepsy. Although definitions of these conditions were very rarely provided, the estimate was surprisingly consistent across studies as a result of including only studies of a certain quality, making them more comparable to one another and the results more valid. Several recent review papers have reported percentages of NCC cases presenting with seizures and epilepsy varying from 70% to 90% [36]–[42]. The proportion of NCC cases seen in neurological clinics with seizures/epilepsy was higher in children than adults. In a review paper of NCC in childhood from India, the authors reported that from 70% to 90% of children with NCC present with seizures [43], which agrees very well with our finding. However, these results may also reflect the fact that more children with seizures/epilepsy are referred to facilities with CT as compared to adults. In addition, if adults tend to be referred to neurology clinics for a larger spectrum of neurological disorders, this would reduce the proportion of seizure/epilepsy observed. The next most common manifestation was headaches, at a frequency of approximately one-third of symptomatic NCC patients. The between-study estimates were more variable than what was seen for seizures/epilepsy, but were still reasonably consistent. This is surprising, since no study provided a definition for headaches. The proportion of pediatric patients with headaches was similar to that in adults but lower than the estimate for all ages combined. Measuring headaches in toddlers and young children is especially challenging since most of them cannot communicate their symptoms [44]. The effect of NCC on altered mental state and psychiatric symptoms remains poorly described. However, in the studies that were included here, they were the presenting manifestations in about 5% of cases of NCC, except for one study [11], where 52% were found to have depression at presentation. Had the studies also included psychiatry clinics, these estimates may have been higher. The proportion of NCC cases with symptoms of or increased intracranial pressure was similar between children and adults. This could be due to the fact that papilledema, which is more common among children, was included in this category of symptoms. All of the publications found in this review reported on patients with symptomatic NCC seen in neurology clinics where imaging was available. Therefore, the distribution of manifestations over-estimates the true frequency of NCC-associated disease, since patients who are asymptomatic or with only mild symptoms are unlikely to be seen in neurology clinics. Indeed, in two studies which were conducted in neuroimaging departments, about 35% of all NCC cases were asymptomatic [14]–[15]. In an autopsy study, nearly 50% of cases of NCC did not have symptoms noted in their medical charts [16]. There is a lack of knowledge on the proportion of NCC cases who will develop symptoms, when in the course of disease specific symptoms occur, and the frequency with which the manifestations change over time. In a study conducted in Mexico, 9.1% of randomly-selected residents without neurological symptoms were found to have NCC based on CT-scan examinations [45]. In another study conducted in Honduras with sampling based on EITB results, 31 of 148 participants (21%) had lesions of NCC. Of these, 26 (18%) showed no manifestations, two had headaches, two had epilepsy, and one had dizziness [46]. The authors demonstrated that EITB had very poor accuracy in detecting NCC, which would suggest that sampling based on EITB may not introduce any important selection bias. If this is the case, then we could conclude that 16.1% (5/31) of people in that community had prevalent NCC symptoms. Unfortunately, in none of those studies was the history of manifestations reported. Assessing the distribution of manifestations among people with active and inactive lesions can inform us somewhat about the natural history of NCC. Seizures and epilepsy were more frequent among patients with calcified lesions. Those with active lesions were more likely to present with increased intracranial pressure, hydrocephalus or meningitis. If properly defined, the term “epilepsy” would be used to include only persons with unprovoked, recurrent seizures [6]. Thus, any cases of epilepsy that were a result of NCC would, by definition, have to occur in persons with inactive lesions, otherwise they would be acute symptomatic seizures. The higher proportion of seizures/epilepsy in those with inactive lesions may also reflect that NCC and epilepsy may be co-occurring conditions rather than be causally linked. The duration of NCC-associated disease remains unknown. This review of the literature only allowed the estimation of the time between the first recorded or reported symptom and medical care. Some patients will never seek care and the duration of disease will remain unknown since NCC can only be accurately diagnosed with imaging. Once patients are in care, in case of active disease, cysticercosis will be treated and the symptoms will most likely disappear, although in the case of seizures, they may persist beyond the period of active disease. Death was reported in only a few studies. It has been reported that neurologic deterioration in patients with NCC may be a life-threatening event with numerous causes and diverse clinical presentations [40]. In one study, the principal concurrent conditions listed as contributing to death included hydrocephalus, cerebral edema, cerebral compression, and epilepsy/convulsions [28]. The methods to estimate death rates were so heterogeneous that they could not be combined. In order to estimate the global burden of NCC, using a country-specific case fatality rate would be more helpful. Various uncommon clinical manifestations have been reported in numerous case reports, illustrating that clinical manifestations associated with NCC are non-specific and pleomorphic [35], [40]. However, in this review, only case series that had more than 20 participants were included meaning that rarer manifestations are not included. Another important limitation is the lack of definitions of the outcomes of interest. In addition, it is possible that some researchers chose to report on only a certain set of symptoms and not on others. Alertness of medical staff is needed to better recognize and diagnose NCC, including providing symptoms' definitions to improve our knowledge of its clinical spectrum. Other limitations are inherent to NCC itself and result from the difficulty of diagnosing NCC even with neuro-imaging [47]. Brain calcifications or granulomas which represent the most frequently observed feature in NCC are also common in tuberculosis, sarcoidosis and toxoplasmosis [48]. These lesions may lead to false positive NCC diagnoses and biased estimates of symptoms' distribution [46]. This systematic review of the literature shows that NCC imposes a heavy burden in endemic communities causing a wide range of neurological, neuropsychological and psychiatric manifestations and even premature death. Some clinical manifestations have an insidious onset and a slow progression, making their diagnosis difficult and often delayed. Hence, NCC should be kept in mind when confronted with any neurological manifestation in patients with histories of residing in endemic areas. When the clinical presentation suggests NCC infection, it is critical to perform a neuroimaging examination. The development of modern, affordable, valid diagnostic procedures and tests is needed to improve understanding of all the clinical manifestations of NCC and its epidemiology. A highly sensitive, specific and inexpensive diagnostic tool will represent a big step in gaining insight into the morbidity and mortality caused by NCC and will help to accurately estimate its global burden.
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Prevalence and comparison of serologic assays, necropsy, and tongue examination for the diagnosis of porcine cysticercosis in Peru.
Swine cysticercosis, a severe zoonotic disease which is part of the Taenia solium life cycle, causes major economic losses in pig husbandry. Throughout South America, farmers diagnose cysticercosis by examining the tongues of their pigs for cysticercus nodules. Farmers do not bring pigs believed to be infected to the slaughterhouse for fear of confiscation. Therefore, reliable statistics on porcine cysticercosis can only be acquired at the household level. We examined the utility of the tongue test as a diagnostic tool for porcine cysticercosis. The results of the tongue test was compared with 2 serologic methods for the detection of cysticercosis, the enzyme-linked immunosorbent assay (ELISA) and the enzyme-linked immunoelectrotransfer blot assay (EITB), and with necropsy results. We examined 11 animals from an endemic area (Huancayo) and 42 animals from an area free of cysticercosis (Lima). The tongue test has a sensitivity of 70% and a specificity of 100%, the EITB a sensitivity and specificity of 100%, and the ELISA a sensitivity of 79% and a specificity of 75%. Thus, the tongue examination, being a test essentially without cost and having fair sensitivity and high specificity, can be useful in epidemiological surveys. Prevalence for porcine cysticercosis in Huancayo is 23.4% by tongue examination, 31.2% by necropsy, 37.7% by ELISA, and 51.9% by EITB.
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Elimination of Taenia solium transmission to pigs in a field trial of the TSOL18 vaccine in Cameroon
Emmanuel Assana, Craig T. Kyngdon, Charles Gauci … (2010)
Taenia solium is a taeniid cestode parasite which is transmitted between humans and pigs, with pigs acting as the intermediate host. While humans are the obligatory definitive host for the parasite, they can also become infected with the metacestode life cycle stage and in such cases the parasite has a propensity to infect the brain, causing the disease neurocysticercosis. Neurocysticercosis is a debilitating disease prevalent in many parts of the developing world where pigs are allowed to roam free and where latrines are not available or not used (Garcia et al., 2003; Garcia and Del Brutto, 2005). The disease is also a burden in developed countries where immigrants infected with the adult worm can infect other citizens or arrive already suffering neurocysticercosis (Schantz et al., 1992). Neurocysticercosis is a disease associated with poverty. Improvements in public sanitation in developed countries have led to the disappearance of T. solium transmission in many developed countries. Although the disease has been identified as having the potential to be eradicated on a global scale (Schantz et al., 1993), limitations in the usefulness of available tools have inhibited the initiation of widespread T. solium control programs and those that have been undertaken to date have achieved only a temporal decrease in disease transmission (Garcia and Del Brutto, 2005). A problem for T. solium control is that, although the adult tapeworm in humans is readily killed by treatment of infected persons with anthelmintics, in an environment where there are many pigs infected with the parasite new human tapeworm infections can be established and transmission of the disease can continue. Another potential control measure for T. solium is the treatment of infected pigs with anthelmintics to kill the muscle cysts. Taenia solium cysticerci in the muscles of pigs are killed following a single oral treatment with 30 mg/kg of the benzimidazole drug oxfendazole (Gonzales et al., 1996; Gonzalez et al., 1997; Sikasunge et al., 2008). However, there are two limitations to utilisation of this as an effective T. solium control measure. Following anthelmintic treatment, pigs that were not previously infected with T. solium remain susceptible to infection. Any infections acquired after anthelmintic treatment would be mature and capable of transmitting the disease following a period of approximately 6 weeks after the infection occurred. Unless the animals were slaughtered within this time window, anthelmintic treatment of pigs could not be relied upon to eliminate the potential for treated animals to transmit the disease. Coordinating anthelmintic treatment of pigs with their sale and slaughter, taking into consideration a withholding period for the animals after application of the chemical and the nature of most environments in which T. solium occurs, could be problematic. The second limitation to the use of anthelmintic treatment of pigs as a control measure for T. solium relates to the occurrence of substantial lesions in the meat of infected animals arising from the inflammatory reactions that occur in response to the anthelmintic-mediated death of cysticerci in the muscles. These lesions are not of concern for transmission of T. solium because the parasite is dead; however, they are unsightly and if present in significant numbers, make the meat unsuitable for sale. The lesions persist for as long as 6 months after pig treatment (Sikasunge et al., 2008). Vaccination has been identified as a potentially valuable new tool for prevention of T. solium transmission (Lightowlers, 1999). While it may be potentially possible to vaccinate the human population against T. solium, a less expensive option is the vaccination of pigs to prevent the disease transmission thereby indirectly reducing the number of new human cases of neurocysticercosis. Several candidate vaccines have been developed and one has shown some promise in field trials (Huerta et al., 2001; Sciutto et al., 2007; Morales et al., 2008). The TSOL18 vaccine has proven to be the most effective vaccine against T. solium, with independent experimental vaccine trials carried out in Mexico, Peru, Cameroon and Honduras inducing 99.3–100% protection against an experimental challenge infection with T. solium eggs in pigs (Flisser et al., 2004; Gonzalez et al., 2005; Lightowlers, 2006). The far-Northern region of Cameroon is highly endemic for T. solium (Assana et al., 2001, 2010; Zoli et al., 2003). In this region we undertook the first field evaluation of the TSOL18 vaccine in pigs against a natural exposure to the parasite acquired through the consumption of the faeces of humans infected with T. solium taeniasis. The vaccine field trial was conducted from October 2008 to July 2009 in the Mayo-Danay administrative department of the Far North region of Cameroon. This region is characterised by having Sahelian-Sudanese climate (M’Biandoun et al., 2003) with a short rainy season (June–September) and a long dry season (October–May). The total human population is about 600,000 inhabitants. Predominant ethnic groups in the rural areas are animistic or Christian. Forty-one villages (Fig. 1) and 114 pig farms were selected on the basis of epidemiological information collected from a survey of the population and serological results on pigs (Assana et al., 2010). Coordinates of each pig farm were obtained by means of the Global Positioning Systems (GPS) using a handheld Garmin eMap device (Garmin, Olathe, USA). The region and village locations are depicted in Fig. 1 (Arcview GIS 3.2 (Environmental System Research Institute, Redlands, USA)). The general strategy adopted for the trial was to vaccinate piglets at 2–3 months of age and give a booster immunisation 4 weeks later. At the time of the second immunisation, the pigs were given oxfendazole to kill any parasites that may already have established in the animals prior to vaccination. Controls were similarly treated with anthelmintic so that any effects of the procedure could be associated with vaccination per se. Controls were not vaccinated because multiple, independent previous experiments had indicated that vaccination of pigs with all components of the vaccine, other than the TSOL18 protein itself, did not prevent T. solium infection in pigs while the majority of pigs vaccinated with TSOL18 have no parasites following an experimental challenge infection (Flisser et al., 2004; Gonzalez et al., 2005). Vaccinated pigs were given an additional booster immunisation because at the time the trial was initiated there was insufficient information available to predict whether two immunisations would have been sufficient to protect the pigs for the duration of the trial. Vaccinations started at the end of the rainy season after which pigs were allowed to roam free during the dry season. Typical farm practice was for the pigs to roam free around the village all day, return to their owners for feeding in the evening and be penned overnight. Two hundred and eighty, three month-old piglets which appeared to be without T. solium infection (determined using tongue examination) were purchased from amongst the village farms and the animals were distributed in matched pairs (one vaccinated, one control) in 114 selected pig farms. Piglets were doubly labelled using both a numbered earring and a microchip. Sample sizes were calculated using Fisher’s exact test such that differences between control and vaccinated groups would be identified with 80% power where the vaccine showed 90% efficacy, the prevalence of cysticercosis in control animals was 10% and differences between the groups were detected at the P < 0.05 level. One hundred and six pairs were required, however, after allowing for possible losses a total of 240 pigs (120 pairs) were placed in the 114 selected farms, some of which were allocated two or three pairs of animals. TSOL18 was expressed in Escherichia coli, purified and lyophilised prior to transport to Cameroon as described by Flisser et al. (2004) and Gonzalez et al. (2005) except that each dose of vaccine contained 200 μg TSOL18 plus 5 mg Quil A (Brenntag Biosector, Frederikssund, Denmark). Vaccines were supplied in 10 dose vials which were stored refrigerated over a period of up to 5 months prior to their application in the pigs. During field work lyophilized vaccine may have been exposed to ambient temperature (up to 40 °C) for periods up to 12 h. Rehydrated vaccines were used as soon as possible although these may have been exposed to ambient temperature for up to 2 h before injection. Pigs received their first immunisation approximately 2 weeks after they had been placed with their host farm. Pigs were 2–3 months of age at the time of the first immunisation with 1 ml vaccine injected intramuscularly near the base of the ear. A second, identical immunisation was given after an interval of approximately 4 weeks. At the time of the second injection all pigs, both vaccinated and controls, received oxfendazole (Dolthene® Merial) per os at a dose rate of 30 mg/kg which typically was approximately 15 ml per animal. Approximately 3 months after the second immunisation, vaccinated pigs received a third injection of vaccine i.e. when the animals were about 6 months of age. Blood samples were obtained from all animals via the jugular vein at the time of each treatment as well as 2 and 9 weeks after the second immunisation, 2 weeks after the third immunisation and at necropsy. Serum was separated and stored at −20 °C. Any animals that became unavailable during the trial were investigated to determine the circumstances that led to this happening. Farmers were paid 8000 FCFA (12 Euro) every month for hosting the animals during the trial. Pigs were slaughtered between 12–13 months of age. The brain and musculature from half of the carcase, split longitudinally, were dissected from the carcase and the number and viability of cysticerci determined as described by Flisser et al. (2004). Where it was clear that there were many hundreds of cysticerci in a carcase, the total number in muscle was estimated by selecting two, 1 kg muscle samples from different regions of the carcase, counting carefully the number of viable and non-viable cysts in those samples to obtain a mean number per kg and estimating the total number in the remaining half of the carcase from the weight of the associated half carcase musculature. On every occasion the numbers in the entire heart and brain were determined precisely. Serum antibody titres to TSOL18 vaccine in vaccinated pigs were obtained by ELISA using TSOL18 expressed as a maltose binding protein (MBP) fusion as described by Kyngdon et al. (2006). Plates (Nunc®, Polysorb) were incubated with 100 μg per well of TSOL18-MBP (5 μg/ml) in carbonate-bicarbonate buffer, pH 9.6 for 1 h at 37 °C and overnight at 4 °C. Antigen was discarded and wells incubated with 150 μl of PBS plus 2% new-born calf serum, 0.05% Tween20 (PBS-NBCS-T) for 1 h at 37 °C. After washing the plates, test sera were serially diluted from 1/100 to 1/102,400 in PBS-NBCS-T and plates incubated for 1 h at 37 °C. Bound specific antibody was detected after washing the plates and addition of 100 μl of rabbit anti-pig IgG peroxidase conjugate (SIGMA) at optimal dilution followed by adding the chromogen/substrate solution consisting of orthophenylene diamine (DAKO, #S2045) and H2O2 as per the manufacturer’s directions. Plates were incubated at 30 °C for 15 min, the reaction was stopped with 50 μl/well of 4 N H2SO4 and the absorbance measured at 492 nm (Multiscan EX, Termo Labsystems). Titres were calculated as the dilution of serum at which the O.D. equalled 0.5. Geometric mean titres were calculated; a titre of 50 was used in those cases where the O.D. at 1:100 of a vaccinated animal’s serum was greater than the mean + 2 S.D. of the value for control sera at 1:100, but less than O.D. 0.5. McNemar’s test was used to compare the proportion of paired vaccinated pigs that were infected with the proportion of control pigs that were infected. Comparison of the number of cysts in vaccinated and control paired pigs was evaluated by Wilcoxon’s signed rank test. Spearman’s rank correlation coefficient was used to assess the association between the number of cysts in the muscles and the number of cysts in the brain in the 102 control pigs, and in the 20 control pigs which had cysts in the muscles. Stata/SE 11.0 for Windows (StataCorp, College Station, TX, USA) software was used and a two-sided P-value < 0.05 was considered to be statistically significant. Over the duration of the trial, a total of 28 pigs became unavailable for follow-up, 10 from the vaccinated group and 18 control animals. The majority had been killed and consumed by a neighbour. No necropsy information was obtained from these animals. TSOL18 vaccinations were well tolerated by the animals with no adverse reactions noted or reported by the keepers of the pigs. At necropsy no lesions were identified that were likely to have been associated with the injections. Twenty control animals (of 102 available at the end of the trial) were found to harbour cysticerci when autopsies were undertaken when the pigs were 12–13 months of age, representing a prevalence of 19.6%. Numbers of cysticerci ranged from three cysts to more than 37,000 cysts. Thirteen animals had an estimated parasite burden of ⩾1000 cysticerci. All infected animals were found to have viable cysticerci and 98% of the total number of cysts found were viable. The mean number of viable cysts in infected animals was 7142. Three animals were found to have non-viable cysticerci also. Fifteen animals had cysticerci in the brain as well as the muscle. All animals with cysts in the brain had viable cysts with 97% of the brain cysts being viable. Three animals had non-viable as well as viable cysts in the brain. At the completion of the trial, 97 of the control/vaccinated paired pigs had both animals available for necropsy. Eighteen animals which were available for necropsy, comprising five control animals and 13 vaccinated animals, had their partner unavailable for necropsy. Data concerning all animals which were necropsied (97 pairs plus 18 unpaired animals) are detailed in Table 1. No cysticerci were found at necropsy anywhere in any of the vaccinated animals, including both those for which the paired control animals was necropsied as well as the 13 vaccinated animals for which the pair partner was not available for necropsy. Statistical comparison of the pairs of control and vaccinated animals (Table 1) showed a significant reduction in vaccinated animals in total cysts (P < 0.0001), viable cysts in muscles (P < 0.0001), total cysts in the brain (P = 0.0002) and viable cysts in the brain (P = 0.0002). There was a reduction in the prevalence of infection from 19.6% (19/97) in paired control pigs to 0% (0/97) in paired vaccinated pigs (P < 0.0001) (Table 2). Spearman’s correlation coefficient was 0.89 (95% Confidence Interval (CI) 0.84 to 0.92, P < 0.0001, n = 102) when assessing the association between total number of cysts in the muscles and total number of cysts in the brain. The correlation was 0.92 (95% CI 0.81 to 0.97, P < 0.0001) for the 20 pigs with cysts in the muscles. Cysts in the brain only occurred in pigs with at least 479 cysts in the muscles (Table 1). Specific antibody titres against TSOL18 in vaccinated pigs are shown in Fig. 2. All vaccinated animals developed detectable titres of antibody following the initial immunisation. The titre was boosted to a geometric mean titre of 750 detected 2 weeks after the second immunisation. A single animal failed to respond to the second immunisation and a further 11 animals displayed relatively poor responses having titres ⩽300. The response following the third immunisation given 4 months after the first injection was pronounced, with specific antibody titres boosted to a geometric mean titre of 12,000. All those animals which responded poorly to the second immunisation responded well to the third injection. The animal which failed to respond to the second immunisation had an anti-TSOL18 titre of 26,000 after the third immunisation. With the exception of a single animal, all pigs had titres after the third immunisation that were grater than the titre seen after the second immunisation. At the time the animals were necropsied, all vaccinated animals remained seropositive, with titres ranging from 160 to 4000. Vaccination with TSOL18 prevented any detectable infection with T. solium in pigs raised in circumstances where there was a 20% prevalence of infection in unvaccinated animals. This level of protection is consistent with the findings of several previous vaccine trials which were carried out under controlled conditions against an experimental challenge infection (Flisser et al., 2004; Gonzalez et al., 2005; Lightowlers, 2006; Cai et al., 2008). When applied as two immunisations approximately 1 month apart, the vaccine induces complete or almost complete protection against a challenge infection given within a few weeks of the second immunisation. The duration of protection has not been defined in experimental challenge trials, however, data from the field trial detailed here indicates that two immunisations in young pigs, together with a booster immunisation given when the animals are 6–7 months of age, was sufficient to protect the animals through until the age at which they are generally slaughtered for consumption (12–14 months). While it is unclear whether the third immunisation was required in order to maintain immunity to the end of the trial, the antibody response of the pigs to TSOL18 was boosted to a substantially greater level following the third immunisation than seen after the second injection, suggesting that this may have enhanced and prolonged the level of protection. Further field trials involving different groups given one, two or three immunisations would be required in order to determine the minimum as well as the optimal vaccine schedule in order to achieve a useful level of protection from infection. All pigs in the trial were given a single treatment with oxfendazole at the time the vaccinated animals received their second immunisation. The purpose of this treatment in the vaccinated group of pigs was to eliminate any parasites that may already be present in the muscles prior to the animals being rendered immune to subsequent parasite challenge following vaccination. The TSOL18 vaccine utilises an antigen which is present only in the oncosphere and immediate post-oncospheral stages in the parasite’s development (Gauci et al., 2006) and, although the vaccine has not specifically been tested for its effects on post-oncospheral parasites, it is not anticipated to have any effect on established cysticerci. Control animals were also given oxfendazole treatment so as to allow any differences between the vaccinated and control groups to be assigned specifically and uniquely to the TSOL18 vaccine. It is likely that a proportion of the piglets had already been infected with cysticerci prior to their treatment with oxfendazole and that the overall prevalence of T. solium infection of pigs in this region exceeds the 19.6% detected in the control animals which had received oxfendazole at 3–4 months of age. Many unvaccinated animals harboured heavy burdens of infection suggesting that they had directly eaten faeces of a tapeworm carrier. In the Mayo-Danay region of far North Cameroon 90% of pigs are free roaming and more than 40% of houses that keep pigs do not have latrines (Assana et al., 2010). The limited available data suggests that T. solium infection is hyperendemic in northern Cameroon (Assana et al., 2001; Zoli et al., 2003). In Cameroon as well as many other regions of the world, neurocysticercosis is a significant cause of human morbidity and mortality. There is increasing interest in developing new disease control tools for T. solium and in defining control measures that could lead to elimination of the disease (Garcia et al., 2007). The vaccine field trial described here has found that a relatively simple procedure combining the TSOL18 vaccine with a single oxfendazole treatment has the capacity to be implemented as an effective measure to control transmission of T. solium through pigs. Implementation of this approach could potentially lead to a reduction in the number of human taeniasis cases and, thereby, reduction in the number of new human cases of neurocysticercosis. An advantage of using a combination vaccination plus chemotherapy approach to cysticercosis control in pigs, in comparison to using chemotherapy alone, is that use of the vaccine allows a sufficient period of time to elapse after chemotherapy for any lesions in the meat caused by necrotic cysticerci to be resolved prior to the animals being slaughtered for consumption. During this period, all animals (previously infected or otherwise) are protected against T. solium infection by the vaccine. In this field trial the potential for transmission of T. solium was eliminated in the treated animals. TSOL18 vaccination plus chemotherapy in pigs may be a relatively sustainable procedure applicable on a wide scale. It could be anticipated that a combination of both vaccination/oxfendazole treatment of pigs together with anthelmintic treatment of the human population to eliminate the adult tapeworms, particularly when control procedures were first implemented, would have the greatest and most rapid impact on reducing the incidence of neurocysticercosis (Lightowlers, 1999). The data presented here represent a proof-of-principal, demonstrating the potential of pig vaccination to control T. solium transmission; it may not present a protocol that would be readily acceptable for field use. At present, the TSOL18 vaccine is applied as a minimum of two intramuscular immunisations. Future improvements in the vaccine, in relation to minimizing the number of exposures to the recombinant antigen required to induce/maintain protection, and changing the method of delivery from parenteral to an oral route, would enhance the ease with which the vaccine could be applied in undertaking T. solium control.
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Journal
Journal ID (publisher-id): spm
Title:
Salud Pública de México
Abbreviated Title:
Salud pública Méx
Publisher:
Instituto Nacional de Salud Pública
(Cuernavaca, Morelos, Mexico
)
ISSN
(Print):
0036-3634
Publication date
(Print and electronic):
June
2014
Volume: 56
Issue: 3
Pages: 259-265
Affiliations
[03]
México
DF
orgnameUniversidad Nacional Autónoma de México
orgdiv1Instituto de Investigaciones Biomédicas
[04]
México
DF
orgnameUniversidad Nacional Autónoma de México
orgdiv1Facultad de Medicina Veterinaria y Zootecnia
orgdiv2Departamento de Medicina Preventiva
Article
Publisher ID: S0036-36342014000300011 Publisher ID: S0036-3634(14)05600300011SO-VID: 6cbd40d5-eb06-4868-a2a1-6c06afacfb20
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This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
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Keywords: México, vacunación, educación, diagnóstico, cisticercosis, taenia solium, cerdos, Mexico, vaccination, education, diagnosis, cysticercosis, pigs