P S Craig

University of Salford, Salford, England, United Kingdom

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Publications (237)592.33 Total impact

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    ABSTRACT: Hydatidosis is a zoonotic disease of worldwide distribution caused by Echinococcus granulosus. Our study aimed to determine the prevalence of human and canine echinococcosis as well as the associated risk factors in a rural area of the Limarí province in northern Chile.
    PLoS neglected tropical diseases. 08/2014; 8(8):e3090.
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    ABSTRACT: Ethiopian wolves, Canis simensis, are an endangered carnivore endemic to the Ethiopian highlands. Although previous studies have focused on aspects of Ethiopian wolf biology, including diet, territoriality, reproduction and infectious diseases such as rabies, little is known of their helminth parasites. In the current study, faecal samples were collected from 94 wild Ethiopian wolves in the Bale Mountains of southern Ethiopia, between August 2008 and February 2010, and were screened for the presence of helminth eggs using a semi-quantitative volumetric dilution method with microscopy. We found that 66 of the 94 faecal samples (70.2%) contained eggs from at least one group of helminths, including Capillaria, Toxocara, Trichuris, ancylostomatids, Hymenolepis and taeniids. Eggs of Capillaria sp. were found most commonly, followed by Trichuris sp., ancylostomatid species and Toxocara species. Three samples contained Hymenolepis sp. eggs, which were likely artefacts from ingested prey species. Four samples contained taeniid eggs, one of which was copro-polymerase chain reaction (copro-PCR) and sequence positive for Echinococcus granulosus, suggesting a spillover from a domestic parasite cycle into this wildlife species. Associations between presence/absence of Capillaria, Toxocara and Trichuris eggs were found; and egg burdens of Toxocara and ancylostomatids were found to be associated with geographical location and sampling season.
    Journal of Helminthology 07/2014; · 1.16 Impact Factor
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    ABSTRACT: Toxoplasma gondii is a highly successful parasite with a worldwide prevalence. Small rodents are the main intermediate hosts, and there is growing evidence that T. gondii modifies their behavior. Chronically infected rodents show impaired learning capacity, enhanced activity, and, most importantly, a reduction of the innate fear towards cat odour. This modification of host behavior ensures a successful transmission of T. gondii from rodents to felids, the definitive hosts of the parasite. Given the negative fitness consequences of this behavioral manipulation, as well as an increased mortality during the acute phase of infection, we expect rodents to evolve potent resistance mechanisms that prevent or control infection. Indeed, studies in laboratory mice have identified candidate genes for T. gondii resistance. Of particular importance appear to be the innate immune receptors Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12), which recognize T.gondii profilin and initiate immune responses against the parasite. Here we analyse the genetic diversity of TLR11 and TLR12 in a natural population of wood mice (Apodemus sylvaticus), and test for associations between TLR11 and TLR12 polymorphisms and T. gondii infection, as well as for epistatic interactions between TLR11 and TLR12 on infection status. We found that both TLR11 and TLR12 were polymorphic in wood mice, with four and nine amino acid haplotypes, respectively. However, we found no evidence that TLR11 or TLR12 genotypes or haplotypes were significantly associated with Toxoplasma infection. Despite the importance of TLR11 and TLR12 in T. gondii recognition and immune defence initiation, naturally occurring polymorphisms at TLR11 and TLR12 thus appear to play a minor role in mediating qualitative resistance to T. gondii in natural host populations of A. sylvaticus. This highlights the importance of assessing the role of candidate genes for parasite resistance identified in a laboratory setting in an ecologically meaningful context to quantify their role in mediating host-parasite interactions in the wild.
    Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 06/2014; · 3.22 Impact Factor
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    ABSTRACT: Echinococcosis is a major parasitic zoonosis of public health importance in western China. In 2004, the Chinese Ministry of Health estimated that 380,000 people had the disease in the region. The Qinghai-Tibet Plateau is highly co-endemic with both alveolar echinococcosis (AE) and cystic echinococcosis (CE). In the past years, the Chinese government has been increasing the financial support to control the diseases in this region. Therefore, it is very important to identify the significant risk factors of the diseases by reviewing studies done in the region in the past decade to help policymakers design appropriate control strategies.Review: Selection criteria for which literature to review were firstly defined. Medline, CNKI (China National Knowledge Infrastructure), and Google Scholar were systematically searched for literature published between January 2000 and July 2011. Significant risk factors found by single factor and/or multiple factors analysis were listed, counted, and summarized. Literature was examined to check the comparability of the data; age and sex specific prevalence with same data structures were merged and used for further analysis.A variety of assumed social, economical, behavioral, and ecological risk factors were studied on the Plateau. Those most at risk were Tibetan herdsmen, the old and female in particular. By analyzing merged comparable data, it was found that females had a significant higher prevalence, and a positive linearity relationship existed between echinococcosis prevalence and increasing age. In terms of behavioral risk factors, playing with dogs was mostly correlated with CE and/or AE prevalence. In terms of hygiene, employing ground water as the drinking water source was significantly correlated with CE and AE prevalence. For definitive hosts, dog related factors were most frequently identified with prevalence of CE or/and AE; fox was a potential risk factor for AE prevalence only. Overgrazing and deforestation were significant for AE prevalence only. Tibetan herdsmen communities were at the highest risk of echinococcosis prevalence and should be the focus of echinococcosis control. Deworming both owned and stray dogs should be a major measure for controlling echinococcosis; treatment of wild definitive hosts should also be considered for AE endemic areas. Health education activities should be in concert with the local people's education backgrounds and languages in order to be able to improve behaviors. Further researches are needed to clarify the importance of wild hosts for AE/CE prevalence, the extent and range of the impacts of ecologic changes (overgrazing and deforestation) on the AE prevalence, and risk factors in Tibet.
    Infectious diseases of poverty. 01/2014; 3(1):3.
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    ABSTRACT: Echinococcus granulosus is an important zoonotic infection of dogs. The purpose of the present study assessed the performance of two laboratory diagnostic methods with arecoline purgation and necropsy in infected dogs. In total 65 dogs were successfully experimentally infected with protoscoleces of E. granulosus from ovine infection. At 14–34 days post-infection groups of dogs were purged with arecoline hydrobromide and then necropsied. Faecal samples were tested at weekly intervals by coproantigen ELISA and coproPCR. The necropsy infection rate with E. granulosus was 89.2%. Only 43% of dogs were successfully purged after one arecoline dose; this percentage increased to 76.9% for two doses of arecoline purgation. E. granulosus coproantigen was detected by coproELISA in 82.8% of faeces. The positive and negative predictive values for coproantigen ELISA were 96 and 44.4% respectively. E. granulosus DNA was detected in pre-patent faecal samples by coproPCR in 25.9% of dogs. These results indicate that coproELISA is more sensitive than arecoline purgation for the detection of pre-patent E. granulosus infection in dogs. CoproPCR detected E. granulosus DNA in dog faeces by 21 days post-infection before egg production. # 2006 Elsevier B.V. All rights reserved.
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    ABSTRACT: Toxoplasma gondii is a highly successful parasite with a worldwide prevalence. Small rodents are the main intermediate hosts, and there is growing evidence that T. gondii modifies their behavior. Chronically infected rodents show impaired learning capacity, enhanced activity, and, most importantly, a reduction of the innate fear towards cat odour. This modification of host behavior ensures a successful transmission of T. gondii from rodents to felids, the definitive hosts of the parasite. Given the negative fitness consequences of this behavioral manipulation, as well as an increased mortality during the acute phase of infection, we expect rodents to evolve potent resistance mechanisms that prevent or control infection. Indeed, studies in laboratory mice have identified candidate genes for T. gondii resistance. Of particular importance appear to be the innate immune receptors Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12), which recognize T. gondii profilin and initiate immune responses against the parasite. Here we analyse the genetic diversity of TLR11 and TLR12 in a natural population of wood mice (Apodemus sylvaticus), and test for associations between TLR11 and TLR12 polymorphisms and T. gondii infection, as well as for epistatic interactions between TLR11 and TLR12 on infection status. We found that both TLR11 and TLR12 were polymorphic in wood mice, with four and nine amino acid haplotypes, respectively. However, we found no evidence that TLR11 or TLR12 genotypes or haplotypes were significantly associated with Toxoplasma infection. Despite the importance of TLR11 and TLR12 in T. gondii recognition and immune defence initiation, naturally occurring polymorphisms at TLR11 and TLR12 thus appear to play a minor role in mediating qualitative resistance to T. gondii in natural host populations of A. sylvaticus. This highlights the importance of assessing the role of candidate genes for parasite resistance identified in a laboratory setting in an ecologically meaningful context to quantify their role in mediating host-parasite interactions in the wild.
    Infection, Genetics and Evolution. 01/2014;
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    Parasitology 11/2013; 140(13):1547-1550. · 2.36 Impact Factor
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    ABSTRACT: SUMMARY In the eastern Tibetan plateau both human cystic and alveolar echinococcosis (AE) caused by infection with Echincoccus granulosus or Echinococcus multilocularis, respectively are highly endemic. The domestic dog plays a key role in zoonotic transmission in this region. Our primary objective was to investigate the role of domestic dogs in maintaining transmission of E. multilocularis in Shiqu county, Sichuan. A cohort of 281 dogs was followed up over one year after a single treatment with praziquantel followed by re-infection surveillance at 2, 5 and 12 months post-treatment. Faecal samples were tested by an Echinococcus genus-specific coproantigen ELISA and two species-specific copro-PCR tests. Total Echinococcus coproantigen prevalence in Shiqu at baseline was 21% and 9·6% after 2 months. E. multilocularis copro-PCR was positive in 11·2% of dogs before treatment (vs 3·6% with E. granulosus copro-DNA), 2·9% at 2 months post-treatment, and 0% at 5 month and 12 months. The results suggest that dogs may have the potential to maintain E. multilocularis transmission within local pastoral communities, and thus dog dosing could be an effective strategy to reduce transmission of E. multilocularis as well as E. granulosus in these co-endemic Tibetan communities.
    Parasitology 08/2013; · 2.36 Impact Factor
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    ABSTRACT: SUMMARY Human cysticercosis, caused by accidental ingestion of eggs of Taenia solium, is one of the most pathogenic helminthiases and is listed among the 17 WHO Neglected Tropical Diseases. Controlling the life-cycle of T. solium between humans and pigs is essential for eradication of cysticercosis. One difficulty for the accurate detection and identification of T. solium species is the possible co-existence of two other human Taenia tapeworms (T. saginata and T. asiatica, which do not cause cysticercosis in humans). Several key issues for taeniasis/cysticercosis (T/C) evidence-based epidemiology and control are reviewed: (1) advances in immunological and molecular tools for screening of human and animals hosts and identification of Taenia species, with a focus on real-time detection of taeniasis carriers and infected animals in field community screenings, and (2) spatial ecological approaches that have been used to detect geospatial patterns of case distributions and to monitor pig activity and behaviour. Most recent eco-epidemiological studies undertaken in Sichuan province, China, are introduced and reviewed.
    Parasitology 08/2013; · 2.36 Impact Factor
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    ABSTRACT: SUMMARY Echinococcosis is a re-emerging zoonotic disease in Kyrgyzstan, and the incidence of human infection has increased substantially since the collapse of the Soviet Union in 1991. Domestic dogs are hosts of Echinococcus spp. and play an important role in the transmission of these parasites. The demography, ecology and behaviour of dogs are therefore relevant in studying Echinococcus spp. transmission. Dog demographics, roles of dogs, dog movements and faecal environmental contamination were assessed in four rural communities in the Alay Valley, southern Kyrgyzstan. Arecoline purge data revealed for the first time that E. granulosus, E. canadensis and E. multilocularis were present in domestic dogs in the Alay Valley. Surveys revealed that many households had dogs and that dogs played various roles in the communities, as pets, guard dogs or sheep dogs. Almost all dogs were free to roam, and GPS data revealed that many moved outside their communities, thus being able to scavenge offal and consume rodents. Faecal environmental contamination was high, presenting a significant infection risk to the local communities.
    Parasitology 08/2013; · 2.36 Impact Factor
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    ABSTRACT: Globally, cestode zoonoses cause serious public health problems, particularly in Asia. Among all neglected zoonotic diseases, cestode zoonoses account for over 75% of global disability adjusted life years (DALYs) lost. An international symposium on cestode zoonoses research and control was held in Shanghai, China between 28th and 30th October 2012 in order to establish joint efforts to study and research effective approaches to control these zoonoses. It brought together 96 scientists from the Asian region and beyond to exchange ideas, report on progress, make a gap analysis, and distill prioritizing settings with a focus on the Asian region. Key objectives of this international symposium were to agree on solutions to accelerate progress towards decreasing transmission, and human mortality and morbidity caused by the three major cestode zoonoses (cystic echinococcosis, alveolar echinococcosis, and cysticercosis); to critically assess the potential to control these diseases; to establish a research and validation agenda on existing and new approaches; and to report on novel tools for the study and control of cestode zoonoses.
    Infectious diseases of poverty. 08/2013; 2(1):16.
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    ABSTRACT: SUMMARY Detection of taeniasis carriers of Taenia solium is essential for control of cysticercosis in humans and pigs. In the current study, we assessed the positive detection rate of a self-detection tool, stool microscopy with direct smear and coproPCR for taeniasis carriers in endemic Tibetan areas of northwest Sichuan. The self-detection tool through questioning about a history of proglottid expulsion within the previous one year showed an overall positive detection rate of more than 80% for Taenia saginata, T. solium and T. asiatica. The positive detection rate was similar for T. saginata and T. solium. In 132 taeniid tapeworm carriers, 68 (51·5%) were detected by microscopy and 92 (69·7%) were diagnosed by coproPCR. A combination of microscopy and coproPCR increased the positive detection rate to 77·3%. There remained 10 cases (7·6%) coproPCR negative but microscopy positive. Due to the high cost and complicated process, coproPCR is required for the identification of Taenia species only when necessary, though it had a significant higher positive detection rate than microscopy. Combined use of self-detection and stool microscopy are recommended in community-based mass screening for taeniases in this Tibetan area or in other situation-similar endemic regions.
    Parasitology 07/2013; · 2.36 Impact Factor
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    ABSTRACT: SUMMARY From continental to regional scales, the zoonosis alveolar echinococcosis (AE) (caused by Echinococcus multilocularis) forms discrete patches of endemicity within which transmission hotspots of much larger prevalence may occur. Since the late 80s, a number of hotspots have been identified in continental Asia, mostly in China, wherein the ecology of intermediate host communities has been described. This is the case in south Gansu, at the eastern border of the Tibetan plateau, in south Ningxia, in the western Tian Shan of Xinjiang, and in the Alay valley of south Kyrgyzstan. Here we present a comparative natural history and characteristics of transmission ecosystems or ecoscapes. On this basis, regional types of transmission and their ecological characteristics have been proposed in a general framework. Combining climatic, land cover and intermediate host species distribution data, we identified and mapped 4 spatially distinct types of transmission ecosystems typified by the presence of one of the following small mammal 'flagship' species: Ellobius tancrei, Ochotona curzoniae, Lasiopodomys brandtii or Eospalax fontanierii. Each transmission ecosystem had its own characteristics which can serve as a reference for further in-depth research in the transmission ecology of E. multilocularis. This approach may be used at fine spatial scales to characterize other poorly known transmission systems of the large Eurasian endemic zone, and help in consideration of surveillance systems and interventions.
    Parasitology 06/2013; · 2.36 Impact Factor
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    ABSTRACT: A 43-year-old Tibetan woman living in northwest Sichuan, China, confirmed to be a taeniasis carrier of Taenia solium was treated with pumpkin seeds combined with Areca nut extract in October 2009. All 20 tapeworms except one without scolex were expelled under good conditions. She was free of secondary cysticercosis within one year follow up. Although the first choice for treatment of taeniasis is still praziquantel, it may often cause serious side effect on asymptomatic cysticercosis cases to suddenly become symptomatic within a half day of the treatment. Therefore, the problems in treatment of taeniasis and/or cysticercosis in Asia are briefly overviewed, since other platyhelminthic diseases including schistosomiasis, opisthorchiasis etc. are more common and praziquantel is strongly recommended for mass treatment of these trematodiases with no idea on the co-infection with eggs of T. solium which cause asymptomatic cysticercosis.
    Tropical biomedicine 06/2013; 30(2):164-73. · 0.92 Impact Factor
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    ABSTRACT: The prevalence of the digenean Plagiorchis sp. was investigated in a natural wood mouse population (Apodemus sylvaticus) in a periaquatic environment. Classical identification was complemented with the use of molecular differentiation to determine prevalence and verify species identity. Use of the complete ITS1-5.8S rDNA-ITS2 and partial 28S rDNA gene sequences have confirmed that the species reported at this location was Plagiorchis elegans and not Plagiorchis muris as reported previously. This underlines the difficulties in identification of these morphologically similar parasites. Plagiorchis elegans is typically a gastrointestinal parasite of avian species but has also been reported from small mammal populations. Although the occurrence of this digenean in A. sylvaticus in the UK is rare, in the area immediately surrounding Malham Tarn, Yorkshire, it had a high prevalence (23%) and a mean worm burden of 26.6 ± 61.5. The distribution of P. elegans followed a typically overdispersed pattern and both mouse age-group and sex were determined to be two main factors associated with prevalence. Male mice harboured the majority of worms, carrying 688 of 717 recovered during the study, and had a higher prevalence of 32.4% in comparison to only 8.7% in the small intestine of female mice. A higher prevalence of 43% was also observed in adult mice compared to 14% for young adults. No infection was observed in juvenile mice. These significant differences are likely to be due to differences in the foraging behaviour between the sexes and age cohorts of wood mice.
    Journal of Helminthology 04/2013; · 1.16 Impact Factor
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    ABSTRACT: Echinococcus shiquicus was discovered in foxes and pika wildlife hosts in Sichuan Province, China in 2005. Faecal samples from dogs collected in a previous echinococcosis purgation survey from Shiqu County, Ganzi Tibetan Autonomous Prefecture (Sichuan) were screened by coproPCR to investigate the possible occurrence of E. shiquicus. In addition, coproDNA extracted from 8 necropsied Tibetan foxes (Vulpes ferrilata), the natural host of E. shiquicus, were also included. Thirty (6/20) percent of faecal samples from dogs were positive for E. shiquicus DNA after PCR amplification of a fragment within the ND1 mitochondrial gene. Echinococcus shiquicus was confirmed by sequencing in four dogs and 3 of the 6 dogs were concurrently infected with E. multilocularis. These were also verified by sequencing. Faecal samples from two Tibetan foxes were shown by PCR to harbour both E. multilocularis and E. shiquicus DNA. One of these dual E. multilocularis and E. shiquicus infections in a Tibetan fox was confirmed by sequencing.
    Acta tropica 03/2013; · 2.79 Impact Factor
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    ABSTRACT: BACKGROUND: Human alveolar echinococcocosis (AE) is a highly pathogenic zoonotic disease caused by the larval stage of the cestode E. multilocularis. Its life-cycle includes more than 40 species of small mammal intermediate hosts. Therefore, host biodiversity losses could be expected to alter transmission. Climate may also have possible impacts on E. multilocularis egg survival. We examined the distribution of human AE across two spatial scales, (i) for continental China and (ii) over the eastern edge of the Tibetan plateau. We tested the hypotheses that human disease distribution can be explained by either the biodiversity of small mammal intermediate host species, or by environmental factors such as climate or landscape characteristics. METHODOLOGYFINDINGS: The distributions of 274 small mammal species were mapped to 967 point locations on a grid covering continental China. Land cover, elevation, monthly rainfall and temperature were mapped using remotely sensed imagery and compared to the distribution of human AE disease at continental scale and over the eastern Tibetan plateau. Infection status of 17,589 people screened by abdominal ultrasound in 2002-2008 in 94 villages of Tibetan areas of western Sichuan and Qinghai provinces was analyzed using generalized additive mixed models and related to epidemiological and environmental covariates. We found that human AE was not directly correlated with small mammal reservoir host species richness, but rather was spatially correlated with landscape features and climate which could confirm and predict human disease hotspots over a 200,000 km(2) region. CONCLUSIONSSIGNIFICANCE: E. multilocularis transmission and resultant human disease risk was better predicted from landscape features that could support increases of small mammal host species prone to population outbreaks, rather than host species richness. We anticipate that our study may be a starting point for further research wherein landscape management could be used to predict human disease risk and for controlling this zoonotic helminthic.
    PLoS Neglected Tropical Diseases 03/2013; 7(3):e2045. · 4.57 Impact Factor
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    ABSTRACT: To investigate echinococcosis in co-endemic regions, three polymerase chain reaction (PCR) assays based on the amplification of a fragment within the NADH dehydrogenase subunit 1 (ND1) mitochondrial gene were optimized for the detection of Echinococcus shiquicus, Echinococcus granulosus G1, and Echinococcus multilocularis DNA derived from parasite tissue or canid fecal samples. Specificity using parasite tissue-derived DNA was found to be 100% except for E. shiquicus primers that faintly detected E. equinus DNA. Sensitivity of the three assays for DNA detection was between 2 and 10 pg. Ethanol precipitation of negative PCR fecal samples was used to eliminate false negatives and served to increase sensitivity as exemplified by an increase in detection from 0% to 89% of E. shiquicus coproDNA using necropsy-positive fox samples.
    The American journal of tropical medicine and hygiene 02/2013; · 2.53 Impact Factor
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    ABSTRACT: The prevalence of the digenean Plagiorchis sp. was investigated in a natural wood mouse population (Apodemus sylvaticus) in a periaquatic environment. Classical identification was complemented with the use of molecular differentiation to determine prevalence and verify species identity. Use of the complete ITS1-5.8S rDNA-ITS2 and partial 28S rDNA gene sequences have confirmed that the species reported at this location was Plagiorchis elegans and not Plagiorchis muris as reported previously. This underlines the difficulties in identification of these morphologically similar parasites. P. elegans is typically a gastrointestinal parasite of avian species but has also been reported from small mammal populations. Although, the occurrence of this digenean in A. sylvaticus in the UK is rare, in the area immediately surrounding Malham Tarn, Yorkshire, it had a high prevalence (23%) and a mean worm burden of 26.6±61.5. The distribution of P. elegans followed a typically overdispersed pattern and both mouse age group and sex were determined to be two main factors to be associated with prevalence. Male mice harboured the majority of worms carrying 688 of 717 recovered during the study and had a higher prevalence of 32.4% in comparison to only 8.7% in the small intestine of female mice. A higher prevalence of 43% was also observed in adult mice compared to 14% for young adults. No infection was observed in juvenile mice. These significant differences are likely to be due to differences in the foraging behaviour between the sexes and age cohorts of wood mice.
    Journal of Helminthology 02/2013; · 1.16 Impact Factor
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    ABSTRACT: 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 , age and sex of the dog were also explored. The dependence structure of these diagnostic tests could also be analysed. The most parsimonious result, indicated by deviance-information criteria, suggested that co-infection with spp. was a significant covariate with the infection. The copro-PCRs had estimated sensitivities of 89% and 84% respectively for the diagnoses of and . 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 and 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 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.
    PLoS Neglected Tropical Diseases 02/2013; 7(2):e2068. · 4.57 Impact Factor

Publication Stats

4k Citations
592.33 Total Impact Points

Institutions

  • 1992–2014
    • University of Salford
      • • Ecosystems and Environment Research Centre (EER)
      • • School of Environment and Life Sciences
      Salford, England, United Kingdom
    • Kenya Medical Research Institute
      Nairoba, Nairobi Area, Kenya
  • 2013
    • Institut Universitaire de France
      Lutetia Parisorum, Île-de-France, France
  • 2006–2013
    • Sichuan Center For Disease Control And Prevention
      Hua-yang, Sichuan, China
    • Asahikawa Medical University
      • Department of Parasitology
      Asakhigava, Hokkaidō, Japan
    • Ministry of Health, Indonesia
      Batavia, Jakarta Raya, Indonesia
  • 2002–2013
    • University of Franche-Comté
      Becoinson, Franche-Comté, France
    • Iran University of Medical Science
      Teheran, Tehrān, Iran
  • 2009–2012
    • National University of San Marcos
      Λίμα, Provincia de Lima, Peru
    • Ecole Nationale de Médecine Vétérinaire
      Tunis-Ville, Tūnis, Tunisia
  • 2010
    • The University of Edinburgh
      • Royal (Dick) School of Veterinary Studies
      Edinburgh, SCT, United Kingdom
  • 2009–2010
    • Ningxia Medical University
      Ning-hsia, Ningxia Huizu Zizhiqu, China
  • 2006–2009
    • Queensland Institute of Medical Research
      • Molecular Parasitology Laboratory
      Brisbane, Queensland, Australia
  • 2000–2009
    • Xinjiang Medical University
      Ouroumtchi, Xinjiang Uygur Zizhiqu, China
  • 2007
    • Tottori University
      • Faculty of Agriculture
      Tottori, Tottori-ken, Japan
    • The National School of Veterinary medicine
      L’Ariana, Ariana, Tunisia
  • 2003–2006
    • Pfizer Inc.
      New York City, New York, United States
    • National Institute of Allergy and Infectious Diseases
      Maryland, United States
    • Shenzhen Second People's Hospital
      Shen-ch’üan-shih, Zhejiang Sheng, China
  • 2005
    • University of Liverpool
      • Institute of Infection & Global Health
      Liverpool, ENG, United Kingdom
  • 2004
    • University of Oxford
      • Department of Zoology
      Oxford, ENG, United Kingdom
  • 2001
    • University of Indonesia
      • Faculty of Medicine
      Depok, Daerah Istimewa Yogyakarta, Indonesia
  • 1996–2001
    • University of San Carlos of Guatemala
      • Facultad de Ciencias Médicas
      Guatemala City, Departamento de Guatemala, Guatemala
  • 1999
    • Udayana University
      Badung, Bali, Indonesia
  • 1986–1997
    • Liverpool School of Tropical Medicine
      • Department of Parasitology
      Liverpool, England, United Kingdom
  • 1995
    • The University of Manchester
      Manchester, England, United Kingdom
  • 1993
    • Victoria University Melbourne
      Melbourne, Victoria, Australia