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1.  A Systematic Review of the Literature on Cystic Echinococcosis Frequency Worldwide and Its Associated Clinical Manifestations 
A systematic literature review of cystic echinoccocosis (CE) frequency and symptoms was conducted. Studies without denominators, original data, or using one serological test were excluded. Random-effect log-binomial models were run for CE frequency and proportion of reported symptoms where appropriate. A total of 45 and 25 articles on CE frequency and symptoms met all inclusion criteria. Prevalence of CE ranged from 1% to 7% in community-based studies and incidence rates ranged from 0 to 32 cases per 100,000 in hospital-based studies. The CE prevalence was higher in females (Prevalence Proportion Ratio: 1.35 [95% Bayesian Credible Interval: 1.16–1.53]) and increased with age. The most common manifestations of hepatic and pulmonary CE were abdominal pain (57.3% [95% confidence interval [CI]: 37.3–76.1%]) and cough (51.3% [95% CI: 35.7–66.7%]), respectively. The results are limited by the small number of unbiased studies. Nonetheless, the age/gender prevalence differences could be used to inform future models of CE burden.
PMCID: PMC3752796  PMID: 23546806
3.  Quality of Life in Patients with Neurocysticercosis in Mexico 
The objective of this study was to compare quality of life measures in patients with neurocysticercosis (NCC) to those of a matched control group. The NCC outpatients and their controls were recruited from two neurology referral hospitals in Mexico City, Mexico during 2007–2008. The quality of life of 224 NCC patients was compared with 224 age-sex-hospital-day matched controls using the short form 12 v2 (SF-12 v2) quality of life survey. Medical chart reviews were also conducted for the NCC outpatients to evaluate presenting clinical manifestations. Compared with the controls, NCC patients had a significantly lower score for each of the eight domains of health evaluated and significantly lower Physical and Mental Component Summary scores. Chart reviews indicated that hydrocephalus (48%), severe headaches (47%), and epilepsy (31%) were the most common clinical manifestations in these NCC outpatients.
PMCID: PMC3083747  PMID: 21540389
4.  Latent-Class Methods to Evaluate Diagnostics Tests for Echinococcus Infections in Dogs 
The diagnosis of canine echinococcosis can be a challenge in surveillance studies because there is no perfect gold standard that can be used routinely. However, unknown test specificities and sensitivities can be overcome using latent-class analysis with appropriate data.
We utilised a set of faecal and purge samples used previously to explore the epidemiology of canine echinococcosis on the Tibetan plateau. Previously only the purge results were reported and analysed in a largely deterministic way. In the present study, additional diagnostic tests of copro-PCR and copro-antigen ELISA were undertaken on the faecal samples. This enabled a Bayesian analysis in a latent-class model to examine the diagnostic performance of a genus specific copro-antigen ELISA, species-specific copro-PCR and arecoline purgation. Potential covariates including co-infection with Taenia, age and sex of the dog were also explored. The dependence structure of these diagnostic tests could also be analysed.
Principle findings
The most parsimonious result, indicated by deviance-information criteria, suggested that co-infection with Taenia spp. was a significant covariate with the Echinococcus infection. The copro-PCRs had estimated sensitivities of 89% and 84% respectively for the diagnoses of Echinococcus multilocularis and E. granulosus. The specificities for the copro-PCR were estimated at 93 and 83% respectively. Copro-antigen ELISA had sensitivities of 55 and 57% for the diagnosis of E. multilocularis and E. granulosus and specificities of 71 and 69% respectively. Arecoline purgation with an assumed specificity of 100% had estimated sensitivities of 76% and 85% respectively.
This study also shows that incorporating diagnostic uncertainty, in other words assuming no perfect gold standard, and including potential covariates like sex or Taenia co-infection into the epidemiological analysis may give different results than if the diagnosis of infection status is assumed to be deterministic and this approach should therefore be used whenever possible.
Author Summary
Dogs are a key definitive host of Echinococcus spp; hence, accurate diagnosis in dogs is important for the surveillance and control of echinococcosis. A perfect diagnostic test would detect every infected dog (100% sensitivity) whilst never giving a false positive reaction in non-infected dogs (100% specificity). Since no such test exists, it is important to understand the performance of available diagnostic techniques. We used the results of a study that used three diagnostic tests on dogs from the Tibetan plateau, where there is co-endemicity of E. granulosus and E. multilocularis. In this study opro-antigen ELISA and copro-PCR diagnostic tests were undertaken on faecal samples from all animals. The dogs were also purged with arecoline hydrobromide to recover adult parasites as a highly specific but relatively insensitive third diagnostic test. We used a statistical approach (Bayesian latent-class models) to estimate simultaneously the sensitivities of all three tests and the specificities of the copro-antigen and copro-PCR tests. We also analysed how some determinants of infection can affect parasite prevalence. This approach provides a robust framework to increase the accuracy of surveillance and epidemiological studies of echinococcosis by overcoming the problems of poor diagnostic test performance.
PMCID: PMC3573084  PMID: 23459420
5.  The Monetary Burden of Cystic Echinococcosis in Iran 
Cystic echinococcosis (CE) is a globally distributed parasitic infection of humans and livestock. The disease is of significant medical and economic importance in many developing countries, including Iran. However, the socioeconomic impact of the disease, in most endemic countries, is not fully understood. The purpose of the present study was to determine the monetary burden of CE in Iran. Epidemiological data, including prevalence and incidence of CE in humans and animals, were obtained from regional hospitals, the scientific literature, and official government reports. Economic data relating to human and animal disease, including cost of treatment, productivity losses, and livestock production losses were obtained from official national and international datasets. Monte Carlo simulation methods were used to represent uncertainty in input parameters. Mean number of surgical CE cases per year for 2000–2009 was estimated at 1,295. The number of asymptomatic individuals living in the country was estimated at 635,232 (95% Credible Interval, CI 149,466–1,120,998). The overall annual cost of CE in Iran was estimated at US$232.3 million (95% CI US$103.1–397.8 million), including both direct and indirect costs. The cost associated with human CE was estimated at US$93.39 million (95% CI US$6.1–222.7 million) and the annual cost associated with CE in livestock was estimated at US$132 million (95% CI US$61.8–246.5 million). The cost per surgical human case was estimated at US$1,539. CE has a considerable economic impact on Iran, with the cost of the disease approximated at 0.03% of the country's gross domestic product. Establishment of a CE surveillance system and implementation of a control program are necessary to reduce the economic burden of CE on the country. Cost-benefit analysis of different control programs is recommended, incorporating present knowledge of the economic losses due to CE in Iran.
Author Summary
Cystic echinococcosis (CE), caused by the tapeworm Echinococcus granulosus, is a zoonotic infection that occurs worldwide. The adult parasite resides in the small intestines of dogs and the cyst form can develop in the liver and lungs of both humans and livestock. CE causes medical, veterinary, and economic losses in endemic areas. However, data on the economic consequences of CE are lacking. The present study estimated the monetary burden of CE in Iran. We used epidemiological and economic information to estimate direct and indirect costs of human and livestock CE in the country. Costs associated with human CE included the costs of surgery and hospital services in addition to lost wages due to work absenteeism during hospitalization and recovery. Costs associated with CE in livestock included losses due to condemnation of livers and lungs during carcass inspections, decreased carcass weight, reproductive losses, and reductions in milk and other animal products. We estimated the overall annual cost of CE in Iran at US$232.25 million, with the cost of the disease estimated to be approximately 0.03% of the country's gross domestic product. Implementation of a control program is necessary to reduce the economic burden of CE on Iran.
PMCID: PMC3510083  PMID: 23209857
6.  Estimating the Non-Monetary Burden of Neurocysticercosis in Mexico 
Neurocysticercosis (NCC) is a major public health problem in many developing countries where health education, sanitation, and meat inspection infrastructure are insufficient. The condition occurs when humans ingest eggs of the pork tapeworm Taenia solium, which then develop into larvae in the central nervous system. Although NCC is endemic in many areas of the world and is associated with considerable socio-economic losses, the burden of NCC remains largely unknown. This study provides the first estimate of disability adjusted life years (DALYs) associated with NCC in Mexico.
DALYs lost for symptomatic cases of NCC in Mexico were estimated by incorporating morbidity and mortality due to NCC-associated epilepsy, and morbidity due to NCC-associated severe chronic headaches. Latin hypercube sampling methods were employed to sample the distributions of uncertain parameters and to estimate 95% credible regions (95% CRs).
In Mexico, 144,433 and 98,520 individuals are estimated to suffer from NCC-associated epilepsy and NCC-associated severe chronic headaches, respectively. A total of 25,341 (95% CR: 12,569–46,640) DALYs were estimated to be lost due to these clinical manifestations, with 0.25 (95% CR: 0.12–0.46) DALY lost per 1,000 person-years of which 90% was due to NCC-associated epilepsy.
This is the first estimate of DALYs associated with NCC in Mexico. However, this value is likely to be underestimated since only the clinical manifestations of epilepsy and severe chronic headaches were included. In addition, due to limited country specific data, some parameters used in the analysis were based on systematic reviews of the literature or primary research from other geographic locations. Even with these limitations, our estimates suggest that healthy years of life are being lost due to NCC in Mexico.
Author Summary
Neurocysticercosis (NCC) is a major public health problem caused by the larvae of the parasite Taenia solium. The condition occurs when humans ingest eggs of the pork tapeworm Taenia solium, which then develop into larvae in the central nervous system. The disease is predominantly found and considered important in Latin American, Asian, and African countries and is associated with a large social and economic burden. Very few studies have been conducted to evaluate the burden of NCC and there are no estimates from Mexico. We estimated the disability adjusted life years (DALYs) lost due to NCC in Mexico incorporating morbidity and mortality due to NCC-associated epilepsy, and morbidity due to NCC-associated severe chronic headaches. NCC-associated epilepsy and severe chronic headaches were estimated to cause a loss of approximately 0.25 healthy year of life per 1,000 persons annually in Mexico. This is the first estimate of DALYs associated with NCC in Mexico. However, this value is likely to be underestimated since only the clinical manifestations of epilepsy and severe chronic headaches were included.
PMCID: PMC3283554  PMID: 22363827
7.  Clinical Manifestations Associated with Neurocysticercosis: A Systematic Review 
The clinical manifestations of neurocysticercosis (NCC) are poorly understood. This systematic review aims to estimate the frequencies of different manifestations, complications and disabilities associated with NCC.
A systematic search of the literature published from January 1, 1990, to June 1, 2008, in 24 different electronic databases and 8 languages was conducted. Meta-analyses were conducted when appropriate.
A total of 1569 documents were identified, and 21 included in the analysis. Among patients seen in neurology clinics, seizures/epilepsy were the most common manifestations (78.8%, 95%CI: 65.1%–89.7%) followed by headaches (37.9%, 95%CI: 23.3%–53.7%), focal deficits (16.0%, 95%CI: 9.7%–23.6%) and signs of increased intracranial pressure (11.7%, 95%CI: 6.0%–18.9%). All other manifestations occurred in less than 10% of symptomatic NCC patients. Only four studies reported on the mortality rate of NCC.
NCC is a pleomorphic disease linked to a range of manifestations. Although definitions of manifestations were very rarely provided, and varied from study to study, the proportion of NCC cases with seizures/epilepsy and the proportion of headaches were consistent across studies. These estimates are only applicable to patients who are ill enough to seek care in neurology clinics and likely over estimate the frequency of manifestations among all NCC cases.
Author Summary
Neurocysticercosis is an infection of the brain with the flatworm Taenia solium which is normally transmitted between humans and pigs. Sometimes, humans can infect other humans and the larva of the parasite can go the brain, causing the disease neurocysticercosis. There has never been a systematic review of what clinical signs are found among people with neurocysticercosis. We conducted a thorough review of the literature to answer this question. We reviewed 1569 and 21 were of a sufficient quality to be included in the final analysis. Among neurocysticercosis patients who are seeking care in neurology clinics, about 79% have seizures/epilepsy, 38% severe headaches, 16% focal deficits and 12% signs of increased intracranial pressure. Several other symptoms were also reported in less than 10% of patients. People with neurocysticercosis who seek care in neurology clinics show a whole range of manifestations. Clinicians should be encouraged to consider neurocysticercosis in their differential diagnosis when a patient presented with one of the symptoms described in this review. This would ultimately improve the estimates of the frequency of symptoms associated with neurocysticercosis.
PMCID: PMC3101170  PMID: 21629722
8.  Economic Impact of Cystic Echinococcosis in Peru 
Cystic echinococcosis (CE) constitutes an important public health problem in Peru. However, no studies have attempted to estimate the monetary and non-monetary impact of CE in Peruvian society.
We used official and published sources of epidemiological and economic information to estimate direct and indirect costs associated with livestock production losses and human disease in addition to surgical CE-associated disability adjusted life years (DALYs) lost.
The total estimated cost of human CE in Peru was U.S.$2,420,348 (95% CI:1,118,384–4,812,722) per year. Total estimated livestock-associated costs due to CE ranged from U.S.$196,681 (95% CI:141,641–251,629) if only direct losses (i.e., cattle and sheep liver destruction) were taken into consideration to U.S.$3,846,754 (95% CI:2,676,181–4,911,383) if additional production losses (liver condemnation, decreased carcass weight, wool losses, decreased milk production) were accounted for. An estimated 1,139 (95% CI: 861–1,489) DALYs were also lost due to surgical cases of CE.
This preliminary and conservative assessment of the socio-economic impact of CE on Peru, which is based largely on official sources of information, very likely underestimates the true extent of the problem. Nevertheless, these estimates illustrate the negative economic impact of CE in Peru.
Author Summary
Cystic echinococcosis (CE), caused by infection with the larval stage of the cestode Echinococcus granulosus, constitutes an important public health problem in Peru. Despite its high prevalence in endemic communities no studies have attempted to estimate the economic impact of CE in Peruvian society. We used official and published sources of epidemiological and economic information to estimate direct and indirect costs associated with livestock production losses and human disease. We also used disability adjusted life years (DALYs) which is an overall measure of disease burden, expressed as number of years lost due to ill-health, disability or early death due to CE. We found that the total estimated cost of human CE in Peru was U.S.$2,420,348 per year. Total estimated livestock-associated costs due to CE ranged from U.S.$196,681 to U.S.$3,846,754. An estimated 1,139 DALYs were also lost due to surgical cases of CE which is comparable to DALY losses from Amebiasis or Malaria in Peru. This conservative assessment found significant economic losses caused by this CE in Peruvian society. The findings of this study are important as these data can serve to prioritize those areas that may need to be targeted in a control program.
PMCID: PMC3101191  PMID: 21629731
9.  A Systematic Review of the Frequency of Neurocyticercosis with a Focus on People with Epilepsy 
The objective of this study is to conduct a systematic review of studies reporting the frequency of neurocysticercosis (NCC) worldwide.
Methods/Principal Findings
PubMed, Commonwealth Agricultural Bureau (CAB) abstracts and 23 international databases were systematically searched for articles published from January 1, 1990 to June 1, 2008. Articles were evaluated for inclusion by at least two researchers focusing on study design and methods. Data were extracted independently using standardized forms. A random-effects binomial model was used to estimate the proportion of NCC among people with epilepsy (PWE). Overall, 565 articles were retrieved and 290 (51%) selected for further analysis. After a second analytic phase, only 4.5% of articles, all of which used neuroimaging for the diagnosis of NCC, were reviewed. Only two studies, both from the US, estimated an incidence rate of NCC using hospital discharge data. The prevalence of NCC in a random sample of village residents was reported from one study where 9.1% of the population harboured brain lesions of NCC. The proportion of NCC among different study populations varied widely. However, the proportion of NCC in PWE was a lot more consistent. The pooled estimate for this population was 29.0% (95%CI: 22.9%–35.5%). These results were not sensitive to the inclusion or exclusion of any particular study.
Only one study has estimated the prevalence of NCC in a random sample of all residents. Hence, the prevalence of NCC worldwide remains unknown. However, the pooled estimate for the proportion of NCC among PWE was very robust and could be used, in conjunction with estimates of the prevalence and incidence of epilepsy, to estimate this component of the burden of NCC in endemic areas. The previously recommended guidelines for the diagnostic process and for declaring NCC an international reportable disease would improve the knowledge on the global frequency of NCC.
Author Summary
Neurocysticercosis (NCC) is a parasitic infection of the brain caused by the tapeworm Taenia solium, which infects humans and pigs. There have been increasing case reports and epidemiological studies on this disease, but its global frequency has never been determined, partly due to the fact that blood tests are not very good for the diagnosis of NCC. We present here a systematic review of the literature on the frequency of NCC diagnosed with neuroimaging worldwide. Overall, 565 articles were retrieved and 290 (51%) selected for further review. Of those, only 26 had information valid enough to estimate the frequency of NCC in various populations. Only one study estimated the prevalence of NCC in the general population. The most striking finding was that the proportion of NCC among persons with epilepsy was very consistent and estimated at 29.6% (95%CI: 23.5%–36.1%) from 12 studies conducted in Latin America, Sub-Saharan Africa and Southeast Asia. A reinforcement of the suggested universal guidelines for the diagnostic process, declaring NCC an international reportable disease and standardizing procedures for data collection could improve our understanding of the frequency of NCC worldwide and hence its global burden.
PMCID: PMC2970544  PMID: 21072231
10.  Multiyear Surveillance for Avian Influenza Virus in Waterfowl from Wintering Grounds, Texas Coast, USA 
Emerging Infectious Diseases  2010;16(8):1224-1230.
This surveillance can help in assessments of the prevalence of wild animal-to-human transmission.
We studied the prevalence of influenza A virus in wintering waterfowl from the Central Flyway on the Gulf Coast of Texas. Of 5,363 hunter-harvested migratory and resident waterfowl and wetland-associated game birds sampled during 3 consecutive hunting seasons (September–January 2006–07, 2007–08, and 2008–09), real-time reverse transcription–PCR detected influenza A matrix sequences in 8.5% of samples, H5 in 0.7%, and H7 in 0.6%. Virus isolation yielded 134 influenza A viruses, including N1–N9, H1–H7, H10, and H11 subtypes. Low-pathogenicity H7 subtype was isolated during January, September, and November 2007 and January 2008; low-pathogenicity H5 subtype was isolated during November and December 2007.
PMCID: PMC3298295  PMID: 20678315
Avian influenza; wild ducks; migratory waterfowl; surveillance; Texas; waterfowl; wintering grounds; zoonoses; research
12.  Pasture Types and Echinococcus multilocularis, Tibetan Communities 
Emerging Infectious Diseases  2006;12(6):1008-1010.
Our study showed that open pastures had more small mammal burrows than fenced pastures in Tibetan pastoralist communities in 2003. This characteristic was linked to a higher prevalence of Echinococcus multilocularis in dogs and indicates that pasture type may affect E. multilocularis transmission.
PMCID: PMC3373058  PMID: 16707064
Echinococcus multilocularis; pasture type; pastoralist communities; mammals; alveolar echinococcosis; dispatch
13.  Global Socioeconomic Impact of Cystic Echinococcosis 
Emerging Infectious Diseases  2006;12(2):296-303.
Because the human and economic losses of cystic echinococcosis are substantial, global prevention and control measures should be increased.
Cystic echinococcosis (CE) is an emerging zoonotic parasitic disease throughout the world. Human incidence and livestock prevalence data of CE were gathered from published literature and the Office International des Epizooties databases. Disability-adjusted life years (DALYs) and monetary losses, resulting from human and livestock CE, were calculated from recorded human and livestock cases. Alternative values, assuming substantial underreporting, are also reported. When no underreporting is assumed, the estimated human burden of disease is 285,407 (95% confidence interval [CI], 218,515–366,133) DALYs or an annual loss of US $193,529,740 (95% CI, $171,567,331–$217,773,513). When underreporting is accounted for, this amount rises to 1,009,662 (95% CI, 862,119–1,175,654) DALYs or US $763,980,979 (95% CI, $676,048,731–$857,982,275). An annual livestock production loss of at least US $141,605,195 (95% CI, $101,011,553–$183,422,465) and possibly up to US $2,190,132,464 (95% CI, $1,572,373,055–$2,951,409,989) is also estimated. This initial valuation demonstrates the necessity for increased monitoring and global control of CE.
PMCID: PMC3373106  PMID: 16494758
echinococcosis; cestodes; cost of illness; burden of illness; economics; zoonoses

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