Hector H Garcia

Universidad Peruana Cayetano Heredia, Λίμα, Lima, Peru

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Publications (261)1587.59 Total impact

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    ABSTRACT: Neurocysticercosis is caused by Taenia solium infecting the central nervous system and is the leading cause of acquired epilepsy and convulsive conditions worldwide. Research into the pathophysiology of the disease and appropriate treatment is hindered by lack of cost-effective and physiologically similar animal models. We generated a novel rat neurocysticercosis model using intracranial infection with activated T. solium oncospheres. Holtzman rats were infected in two separate groups: the first group was inoculated extraparenchymally and the second intraparenchymally, with different doses of activated oncospheres. The groups were evaluated at three different ages. Histologic examination of the tissue surrounding T. solium cysticerci was performed. Results indicate that generally infected rats developed cysticerci in the brain tissue after 4 months, and the cysticerci were observed in the parenchymal, ventricle, or submeningeal brain tissue. The route of infection did not have a statistically significant effect on the proportion of rats that developed cysticerci, and there was no dependence on infection dose. However, rat age was crucial to the success of the infection. Epilepsy was observed in 9% of rats with neurocysticercosis. In histologic examination, a layer of collagen tissue, inflammatory infiltrate cells, perivascular infiltrate, angiogenesis, spongy change, and mass effect were observed in the tissue surrounding the cysts. This study presents a suitable animal model for the study of human neurocysticercosis. Copyright © 2015 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.
    American Journal Of Pathology 08/2015; 185(8):2259-68. DOI:10.1016/j.ajpath.2015.04.015 · 4.60 Impact Factor
  • Epilepsia 06/2015; 56(6):975-6. DOI:10.1111/epi.12986 · 4.58 Impact Factor
  • The Lancet Infectious Diseases 03/2015; 15(3). DOI:10.1016/S1473-3099(15)70047-2 · 19.45 Impact Factor
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    ABSTRACT: Cysticidal treatment of neurocysticercosis, an infection of humans and pig brains with Taenia solium, results in an early inflammatory response directed to cysts causing seizures and focal neurological manifestations. Treatment-induced pericystic inflammation and its association with blood brain barrier (BBB) dysfunction, as determined by Evans blue (EB) extravasation, was studied in infected untreated and anthelmintic-treated pigs. We compared the magnitude and extent of the pericystic inflammation, presence of EB-stained capsules, the level of damage to the parasite, expression of genes for proinflammatory and regulatory cytokines, chemokines, and tissue remodeling by quantitative PCR assays between treated and untreated infected pigs and between EB-stained (blue) and non stained (clear) cysts. Inflammatory scores were higher in pericystic tissues from EB-stained cysts compared to clear cysts from untreated pigs and also from anthelmintic-treated pigs 48 hr and 120 hr after treatment. The degree of inflammation correlated with the severity of cyst wall damage and both increased significantly at 120 hours. Expression levels of the proinflammatory genes for IL-6, IFN-γ, TNF-α were higher in EB-stained cysts compared to clear cysts and unaffected brain tissues, and were generally highest at 120 hr. Additionally, expression of some markers of immunoregulatory activity (IL-10, IL-2Rα) were decreased in EB-stained capsules. An increase in other markers for regulatory T cells (CTLA4, FoxP3) was found, as well as significant increases in expression of two metalloproteases, MMP1 and MMP2 at 48 hr and 120 hr post-treatment. We conclude that the increase in severity of the inflammation caused by treatment is accompanied by both a proinflammatory and a complex regulatory response, largely limited to pericystic tissues with compromised vascular integrity. Because treatment induced inflammation occurs in porcine NCC similar to that in human cases, this model can be used to investigate mechanisms involved in host damaging inflammatory responses and agents or modalities that may control damaging post treatment inflammation.
    PLoS Neglected Tropical Diseases 03/2015; 9(3):e0003577. DOI:10.1371/journal.pntd.0003577 · 4.49 Impact Factor
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    ABSTRACT: The CRONICAS Centre of Excellence in Chronic Diseases, based at Universidad Peruana Cayetano Heredia, was created in 2009 with support from the U.S. National Heart, Lung, and Blood Institute (NHLBI). The vision of CRONICAS is to build a globally recognized center of excellence conducting quality and innovative research and generating high-impact evidence for health. The center's identity is embedded in its core values: generosity, innovation, integrity, and quality. This review has been structured to describe the development of the CRONICAS Centre, with a focus on highlighting the ongoing translational research projects and capacity-building strategies. The CRONICAS Centre of Excellence is not a risk-averse organization: it benefits from past experiences, including past mistakes, and improves upon them and thus challenges traditional research approaches. This ethos and environment are key to fostering innovation in research. Copyright © 2015 World Heart Federation (Geneva). All rights reserved.
    03/2015; 10(1):13-19. DOI:10.1016/j.gheart.2014.12.012
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    ABSTRACT: AbstracObjectives To examine the prevalence of seizures, epilepsy, and seropositivity to cysticercosis in rural villagers (cysticercosis-endemic setting), rural-to-urban migrants into a non-endemic urban shantytown, and urban inhabitants of the same non-endemic shanty town.Methods Three Peruvian populations (n=985) originally recruited into a study about chronic diseases and migration, were studied. These groups included rural inhabitants from an endemic region (n=200), long-term rural-to-urban migrants (n=589), and individuals living in the same urban setting (n=196). Seizure disorders were detected by a survey and a neurologist examined positive respondents. Serum samples from 981/985 individuals were processed for cysticercosis antibodies on immunoblot.ResultsEpilepsy prevalence (per 1,000 people) was 15.3 in the urban group, 35.6 in migrants, and 25 in rural inhabitants. A gradient in cysticercosis antibody seroprevalence was observed: urban 2%, migrant 13.5%, and rural group 18% (p<0.05). A similarly increasing pattern of higher seroprevalence was observed among migrants by age at migration. In rural villagers, there was strong evidence of an association between positive serology and having seizures (p=0.011) but such an association was not observed in long-term migrants or in urban residents. In the entire study population, compared to seronegative participants, those with strong antibody reactions (≥4 antibody bands) were more likely to have epilepsy (p<0.001).Conclusions It is not only international migration that affects cysticercosis endemicity; internal migration can also affect patterns of endemicity within an endemic country. The neurologic consequences of cysticercosis infection likely outlast the antibody response for years after rural-to-urban migration.This article is protected by copyright. All rights reserved.
    Tropical Medicine & International Health 01/2015; 20(4). DOI:10.1111/tmi.12456 · 2.30 Impact Factor
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    ABSTRACT: To develop a better understanding of mechanisms of seizures and long-term epileptogenesis using neurocysticercosis. A workshop was held bringing together experts in epilepsy and epileptogenesis and neurocysticercosis. Human neurocysticercosis and parallel animal models offer a unique opportunity to understand basic mechanisms of seizures. Inflammatory responses to degenerating forms and later-stage calcified parasite granulomas are associated with seizures and epilepsy. Other mechanisms may also be involved in epileptogenesis. Naturally occurring brain infections with neurocysticercosis offer a unique opportunity to develop treatments for one of the world's most common causes of epilepsy and for the development of more general antiepileptogenic treatments. Key advantages stem from the time course in which an acute seizure heralds a start of the epileptogenic process, and radiographic changes of calcification and perilesional edema provide biomarkers of a chronic epileptic state. Wiley Periodicals, Inc. © 2014 International League Against Epilepsy.
    Epilepsia 12/2014; 56(2). DOI:10.1111/epi.12849 · 4.58 Impact Factor
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    ABSTRACT: Neurocysticercosis is a leading cause of seizures and epilepsy in most of the world, and it occurs when Taenia solium larval cysts infect the central nervous system. T. solium tapeworm infection is endemic in much of Peru, but there are scarce data on the prevalence in many rural highland communities where it is likely to be hyper-endemic. Peace Corps Volunteers live and work in these communities; however, to our knowledge, they have not been used to facilitate public health research. We utilized Peace Corps Volunteers to estimate the prevalence of T. solium tapeworm infection in seven rural communities in northern Peru. A convenience non-random sampling frame was used. Peace Corps Volunteers facilitated the collection of stool samples (N = 2,328), which were analyzed by sedimentation and microscopy. Niclosamide treatment and purgation preceded species identification, which was done by PCR-REA. Taenia sp. egg-positive stool samples were found in three of the seven communities we surveyed. The overall prevalence of Taenia sp. egg positivity was 2.1% (49/2,328) (95% CI = 1.6-2.8%) with prevalence up to 4.3% (42/977) (95% CI = 3.1-5.8%) by community. All 34 of the specimens tested by PCR-REA were T. solium. The overall prevalence of T. solium tapeworm infection was 1.5% (34/2,328) (95% CI = 1.0-2.0%). Prevalence up to 2.9% (28/977) (95% CI = 1.9-4.1%) by community was observed. This study recorded high T. solium tapeworm prevalence, and identified hyper-endemic rural communities. It demonstrates that synergy between researchers and Peace Corps Volunteers can be an effective means to conducting large-scale, community-based studies in remote areas of Peru.
    PLoS ONE 12/2014; 9(12):e113239. DOI:10.1371/journal.pone.0113239 · 3.53 Impact Factor
  • Epilepsia 12/2014; 55(12). DOI:10.1111/epi.12899 · 4.58 Impact Factor
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    ABSTRACT: The infection of the nervous system by the cystic larvae of Taenia solium (neurocysticercosis) is a frequent cause of seizure disorders. Neurocysticercosis is endemic or presumed to be endemic in many low-income countries. The lifecycle of the worm and the clinical manifestations of neurocysticercosis are well established, and CT and MRI have substantially improved knowledge of the disease course. Improvements in immunodiagnosis have further advanced comprehension of the pathophysiology of this disease. This knowledge has led to individualised treatment approaches that account for the involvement of parenchymal or extraparenchymal spaces, the number and form of parasites, and the extent of degeneration and associated inflammation. Clinical investigations are focused on development of effective treatments and reduction of side-effects induced by treatment, such as seizures, hydrocephalus, infarcts, and neuroinjury. Copyright © 2014 Elsevier Ltd. All rights reserved.
    The Lancet Neurology 12/2014; 13(12):1202-1215. DOI:10.1016/S1474-4422(14)70094-8 · 21.82 Impact Factor
  • The Lancet Neurology 12/2014; 13(12):1173. DOI:10.1016/S1474-4422(14)70275-3 · 21.82 Impact Factor
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    ABSTRACT: Calcified neurocysticercosis has been associated with hippocampal atrophy in patients with refractory epilepsy, but the relevance of this association in the population at large is unknown. We assessed calcified cysticerci and its association with hippocampal atrophy in elderly persons living in Atahualpa, an Ecuadorian village endemic for neurocysticercosis. All Atahualpa residents ≥ 60 years of age were invited to undergo computed tomography/magnetic resonance imaging for neurocysticercosis detection. Twenty-eight (11%) out of 248 enrolled persons had calcified cysticerci (case-patients) and were matched 1:1 by age, sex, and years of education to individuals without neurocysticercosis on computed tomography/magnetic resonance imaging (controls). Four case-patients and none of the controls had epilepsy (P = 0.134). Cognitive performance was similar across both groups. The Scheltens' medial temporal atrophy scale was used for hippocampal rating in case-patients and matched controls without neurocysticercosis. Mean score in the Scheltens' scale was higher in case-patients than in controls (p < 0.001). Atrophic hippocampi were noticed in 19 case-patients and five controls (P = 0.003). Atrophy was bilateral in 11 case-patients and unilateral in eight. All case-patients with unilateral hippocampal atrophy had at least one ipsilateral calcification. This study shows an association between calcified cysticerci and hippocampal atrophy and raises the possibility of an inflammation-mediated hippocampal damage as the responsible mechanism for these findings.
    The American journal of tropical medicine and hygiene 10/2014; 92(1). DOI:10.4269/ajtmh.14-0453 · 2.74 Impact Factor
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    ABSTRACT: Taenia solium infection causes severe neurological disease in humans. Even though infection and exposure to swine cysticercosis is scattered throughout endemic villages, location of the tapeworm only explains some of the nearby infections and is not related to location of seropositive pigs. Other players might be involved in cysticercosis transmission. In this study we hypothesize that pigs that carry nematodes specific to dung beetles are associated with cysticercosis infection and/or exposure. We carried out a cross-sectional study of six villages in an endemic region in northern Peru. We euthanized all pigs (326) in the villages and performed necropsies to diagnose cysticercosis. For each pig, we counted cysticerci; measured anti-cysticercus antibodies; identified intestinal nematodes; tabulated distance to nearest human tapeworm infection; and recorded age, sex, productive stage, and geographic reference. For the purpose of this paper, we defined cysticercosis infection as the presence of at least one cysticercus in pig muscles, and cysticercosis exposure as seropositivity to anti-cysticercus antibodies with the presence of 0-5 cysticerci. Compared to pigs without nematode infections, those pigs infected with the nematode Ascarops strongylina were significantly associated with the presence of cysticerci (OR: 4.30, 95%CI: 1.83-10.09). Similarly, pigs infected with the nematode Physocephalus sexalatus were more likely to have cysticercosis exposure (OR: 2.21, 95%CI: 1.50-3.28). In conclusion, our results suggest that there appears to be a strong positive association between the presence of nematodes and both cysticercosis infection and exposure in pigs. The role of dung beetles in cysticercosis dynamics should be further investigated.
    PLoS Neglected Tropical Diseases 10/2014; 8(10):e3247. DOI:10.1371/journal.pntd.0003247 · 4.49 Impact Factor
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    ABSTRACT: Background Taenia solium is a major cause of preventable epilepsy in developing nations. Screening and treatment of human intestinal stage infection (taeniasis) within high-risk foci may reduce transmission and prevent epilepsy by limiting human exposure to infective eggs. We piloted a ring-strategy that involves screening and treatment for taeniasis among households located nearby pigs heavily-infected with the larval stage (cysticercosis). These pigs mark areas of increased transmission and can be identified by tongue examination. Methodology We selected two villages in northern Peru for a controlled prospective interventional cohort pilot study. In the intervention village (1,058 residents) we examined the tongues of all pigs every 4 months for nodules characteristic of cysticercosis. We then screened all residents living within 100-meters of any tongue-positive pig using enzyme-linked immunosorbent assay to detect Taenia antigens in stool. Residents with taeniasis were treated with niclosamide. In both the intervention and control (753 residents) we measured incidence of exposure by sampling the pig population every 4 months for serum antibodies against cysticercosis using enzyme-linked immunoelectrotransfer blot. Principal Findings Baseline seroincidence among pigs born during the study was 22.6 cases per 100 pigs per-month (95% confidence interval [CI] 17.0–30.0) in the intervention and 18.1 (95% CI 12.7–25.9) in the control. After one year we observed a 41% reduction in seroincidence in the intervention village compared to baseline (incidence rate ratio 0.59, 95% CI 0.41–0.87) while the seroincidence in the control village remained unchanged. At study end, the prevalence of taeniasis was nearly 4 times lower in the intervention than in the control (prevalence ratio 0.28, 95% CI 0.08–0.91). Conclusions/Significance Ring-screening reduced transmission of T. solium in this pilot study and may provide an effective and practical approach for regions where resources are limited. However, this strategy requires validation in larger populations over a greater period of time.
    PLoS Neglected Tropical Diseases 09/2014; 8(9):e3125. DOI:10.1371/journal.pntd.0003125 · 4.49 Impact Factor
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    ABSTRACT: Background Neurocysticercosis causes a substantial burden of seizure disorders worldwide. Treatment with either praziquantel or albendazole has suboptimum efficacy. We aimed to establish whether combination of these drugs would increase cysticidal efficacy and whether complete cyst resolution results in fewer seizures. We added an increased dose albendazole group to establish a potential effect of increased albendazole concentrations. Methods In this double-blind, placebo-controlled, phase 3 trial, patients with viable intraparenchymal neurocysticercosis were randomly assigned to receive 10 days of combined albendazole (15 mg/kg per day) plus praziquantel (50 mg/kg per day), standard albendazole (15 mg/kg per day), or increased dose albendazole (22·5 mg/kg per day). Randomisation was done with a computer generated schedule balanced within four strata based on number of cysts and concomitant antiepileptic drug. Patients and investigators were masked to group assignment. The primary outcome was complete cyst resolution on 6-month MRI. Enrolment was stopped after interim analysis because of parasiticidal superiority of one treatment group. Analysis excluded patients lost to follow-up before the 6-month MRI. This trial is registered with ClinicalTrials.gov, number NCT00441285. Findings Between March 3, 2010 and Nov 14, 2011, 124 patients were randomly assigned to study groups (41 to receive combined albendazole plus praziquantel [39 analysed], 43 standard albendazole [41 analysed], and 40 increased albendazole [38 analysed]). 25 (64%) of 39 patients in the combined treatment group had complete resolution of brain cysts compared with 15 (37%) of 41 patients in the standard albendazole group (rate ratio [RR] 1·75, 95% CI 1·10–2·79, p=0·014). 20 (53%) of 38 patients in the increased albendazole group had complete cyst resolution at 6-month MRI compared with 15 (37%) of 41 patients in the standard albendazole group (RR 1·44, 95% CI 0·87–2·38, p=0·151). No significant differences in adverse events were reported between treatment groups (18 in combined treatment group, 11 in standard albendazole group, and 19 in increased albendazole group). Interpretation Combination of albendazole plus praziquantel increases the parasiticidal effect in patients with multiple brain cysticercosis cysts without increased side-effects. A more efficacious parasiticidal regime without increased treatment-associated side-effects should improve the treatment and long term prognosis of patients with neurocysticercosis. Funding National Institute of Neurological Disorders and Stroke (NINDS), National Institutes of Health.
    The Lancet Infectious Diseases 08/2014; 14(8). DOI:10.1016/S1473-3099(14)70779-0 · 19.45 Impact Factor
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    ABSTRACT: Objective Neurocysticercosis (NCC) is a major cause of seizures and epilepsy in endemic countries. Antiparasitic treatment of brain cysts leads to seizures due to the host's inflammatory reaction, requiring concomitant steroids. We hypothesized that increased steroid dosing will reduce treatment-associated seizures.Methods Open-label randomized trial comparing 6 mg/day dexamethasone for 10 days (conventional) with 8 mg/day for 28 days followed by a 2-week taper (enhanced) in patients with NCC receiving albendazole. Follow-up included active seizure surveillance and brain imaging. Study outcomes were seizure days and patients with seizures, both measured in days 11–42. Additional analyses compared days 1–10, 11–21, 22–32, 33–42, 43–60, and 61–180.ResultsThirty-two individuals were randomized into each study arm; two did not complete follow-up. From days 11 to 42, 59 partial and 6 generalized seizure days occurred in 20 individuals, nonsignificantly fewer in the enhanced arm (12 vs. 49, p = 0.114). The numbers of patients with seizures in this period showed similar nonsignificant differences. In the enhanced steroid arm there were significantly fewer days and individuals with seizures during antiparasitic treatment (days 1–10: 4 vs. 17, p = 0.004, and 1 vs. 10, p = 0.003, number needed to treat [NNT] 4.6, relative risk [RR] 0.1013, 95% confidence interval [CI] 0.01–0.74) and early after dexamethasone cessation (days 11–21: 6 vs. 27, p = 0.014, and 4 vs. 12, p = 0.021, NNT 4.0, RR 0.33, 95% CI 0.12–0.92) but not after day 21. There were no significant differences in antiparasitic efficacy or relevant adverse events.SignificanceIncreased dexamethasone dosing results in fewer seizures for the first 21 days during and early after antiparasitic treatment for viable parenchymal NCC but not during the first 11–42 days, which was the primary predetermined time of analysis.
    Epilepsia 07/2014; 55(9). DOI:10.1111/epi.12739 · 4.58 Impact Factor
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    ABSTRACT: Cysticidal drug treatment of viable Taenia solium brain parenchymal cysts leads to an acute pericystic host inflammatory response and blood brain barrier breakdown (BBB), commonly resulting in seizures. Naturally infected pigs, untreated or treated one time with praziquantel were sacrificed at 48 hr and 120 hr following the injection of Evans blue (EB) to assess the effect of treatment on larval parasites and surrounding tissue. Examination of harvested non encapsulated muscle cysts unexpectedly revealed one or more small, focal round region(s) of Evans blue dye infiltration (REBI) on the surface of otherwise non dye-stained muscle cysts. Histopathological analysis of REBI revealed focal areas of eosinophil-rich inflammatory infiltrates that migrated from the capsule into the tegument and internal structures of the parasite. In addition some encapsulated brain cysts, in which the presence of REBI could not be directly assessed, showed histopathology identical to that of the REBI. Muscle cysts with REBI were more frequent in pigs that had received praziquantel (6.6% of 3736 cysts; n = 6 pigs) than in those that were untreated (0.2% of 3172 cysts; n = 2 pigs). Similar results were found in the brain, where 20.7% of 29 cysts showed histopathology identical to muscle REBI cysts in praziquantel-treated pigs compared to the 4.3% of 47 cysts in untreated pigs. Closer examination of REBI infiltrates showed that EB was taken up only by eosinophils, a major component of the cellular infiltrates, which likely explains persistence of EB in the REBI. REBI likely represent early damaging host responses to T. solium cysts and highlight the focal nature of this initial host response and the importance of eosinophils at sites of host-parasite interaction. These findings suggest new avenues for immunomodulation to reduce inflammatory side effects of anthelmintic therapy
    PLoS ONE 06/2014; 9(6). DOI:10.1371/journal.pone.0097321 · 3.53 Impact Factor
  • Hector H. Garcia, Silvia Rodriguez, Jon S. Friedland
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    ABSTRACT: The life cycle of Taenia solium, the pork tapeworm, is continuously closed in many rural settings in developing countries when free roaming pigs ingest human stools containing T. solium eggs and develop cysticercosis, and humans ingest pork infected with cystic larvae and develop intestinal taeniasis, or may also accidentally acquire cysticercosis by fecal-oral contamination. Cysticercosis of the human nervous system, neurocysticercosis, is a major cause of seizures and other neurological morbidity in most of the world. The dynamics of exposure, infection and disease as well as the location of parasites result in a complex interaction which involves immune evasion mechanisms and involutive or progressive disease along time. Moreover, existing data is limited by the relative lack of animal models. This manuscript manuscript revises the available information on the immunology of human taeniasis and cysticercosis.This article is protected by copyright. All rights reserved.
    Parasite Immunology 06/2014; 36(8). DOI:10.1111/pim.12126 · 1.85 Impact Factor
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    ABSTRACT: Background Human cysticercosis is a zoonotic disease causing severe health disorders and even death. While prevalence data become available worldwide, incidence rate and cumulative incidence figures are lacking, which limits the understanding of the Taenia solium epidemiology. Methodology/Principal findings A seroepidemiological cohort study was conducted in a south-Ecuadorian community to estimate the incidence rate of infection with and the incidence rate of exposure to T. solium based on antigen and antibody detections, respectively. The incidence rate of infection was 333.6 per 100,000 person-years (95% CI: [8.4–1,858] per 100,000 person-years) contrasting with a higher incidence rate of exposure 13,370 per 100,000 person-years (95% CI: [8,730–19,591] per 100,000 person-years). The proportion of infected individuals remained low and stable during the whole study year while more than 25% of the population showed at least one antibody seroconversion/seroreversion during the same time period. Conclusions/Significance Understanding the transmission of T. solium is essential to develop ad hoc cost-effective prevention and control programs. The estimates generated here may now be incorporated in epidemiological models to simulate the temporal transmission of the parasite and the effects of control interventions on its life cycle. These estimates are also of high importance to assess the disease burden since incidence data are needed to make regional and global projections of morbidity and mortality related to cysticercosis.
    PLoS Neglected Tropical Diseases 05/2014; 8(5):e2887. DOI:10.1371/journal.pntd.0002887 · 4.49 Impact Factor
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Publication Stats

6k Citations
1,587.59 Total Impact Points

Institutions

  • 1991–2015
    • Universidad Peruana Cayetano Heredia
      • Facultad de Ciencia y Filosofía
      Λίμα, Lima, Peru
  • 2000–2014
    • Johns Hopkins University
      • Department of International Health
      Baltimore, Maryland, United States
    • Icahn School of Medicine at Mount Sinai
      Borough of Manhattan, New York, United States
    • Baylor College of Medicine
      • Section of Infectious Diseases
      Houston, TX, United States
  • 2012
    • Pfizer Inc.
      New York, New York, United States
    • Oregon Health and Science University
      • Department of Public Health & Preventive Medicine
      Portland, Oregon, United States
  • 2008–2012
    • Instituto Latinoamericano de Ciencias
      Λίμα, Lima, Peru
  • 1995–2011
    • National University of San Marcos
      • Facultad de Medicina Veterinaria
      Λίμα, Lima, Peru
  • 1991–2011
    • Centers for Disease Control and Prevention
      • • Center for Global Health
      • • Division of Parasitic Diseases and Malaria
      Atlanta, MI, United States
  • 2010
    • Georgia State University
      • Department of Biology
      Atlanta, Georgia, United States
  • 2004–2010
    • Johns Hopkins Bloomberg School of Public Health
      • Department of International Health
      Baltimore, Maryland, United States
    • National Institute of Allergy and Infectious Diseases
      • Laboratory of Parasitic Diseases (LPD)
      Maryland, United States
  • 2006
    • University of Melbourne
      Melbourne, Victoria, Australia
  • 2005
    • National Institute of Health of Peru
      Λίμα, Provincia de Lima, Peru
    • University of Georgia
      • Department of Cellular Biology
      Athens, GA, United States
  • 2002–2005
    • Environmental Working Group
      Washington, Washington, D.C., United States
  • 2001
    • National Institutes of Health
      • Laboratory of Parasitic Diseases
      베서스다, Maryland, United States