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Selcuk MA, Aslan Celik B, Celik F, Celik OY, Ercan K, Uslug M, Tekin AS, Simsek S. A pilot study on the epidemiology, diagnosis and characterization of Echinococcus granulosus sensu lato in sheep, goats and dogs in Siirt province of Türkiye revealed remarkable adaptation of Echinococcus canadensis (G6/G7) in goats. Vet Parasitol 2024; 332:110320. [PMID: 39383687 DOI: 10.1016/j.vetpar.2024.110320] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/20/2024] [Revised: 09/29/2024] [Accepted: 09/30/2024] [Indexed: 10/11/2024]
Abstract
Cystic echinococcosis (CE), caused by Echinococcus granulosus sensu lato (s.l.), represents one of the most significant zoonotic diseases globally, affecting both humans and animals. The objective of this study was to ascertain the prevalence of E. granulosus sensu lato in sheep and goats in a pilot region with a one-year slaughterhouse follow-up period and to determine the genetic differences and haplotypes among sheep, goat, and dog isolates. To this end, the prevalence of CE cysts was determined by monitoring the slaughter of sheep and goats at least three days a week at a slaughterhouse in the Siirt province of Türkiye during 2023. Additionally, faecal samples were collected from stray dogs and analysed using both flotation and molecular techniques. The presence of CE cysts was identified in 569 (11.12 %) of the 5119 sheep and 66 (2.31 %) of the 2860 goats after slaughtering. The highest positivity was observed in November (20.39 %), while the lowest was recorded in July (5.62 %). Of the sheep that detected positive, 25 (4.39 %) were less than one year old, while 544 (95.61 %) were older than one year. Of the infected sheep, 26 (4.57 %) were male and 543 (95.43 %) were female. 204 (35.85 %) sheep exhibited fluid-filled CE cysts, 338 (59.40 %) displayed calcification, and 27 (4.75 %) demonstrated the presence of newly developed cysts. The highest positivity was observed in December (5.83 %), while the lowest was recorded in May (0.62 %) in goats. Of the positive goats, two (3 %) were less than one year old, while the remaining 64 (97 %) were older than one year. Of the goats infected with CE cysts, 10 (15.15 %) were male and 56 (84.85 %) were female. Of the cysts, 56.1 % were fluid-filled, 42.4 % were calcified and 1.5 % were newly developed. Following DNA sequence analysis of CE cyst isolates obtained from the slaughterhouse, all 61 sheep sequences were identified as E. granulosus s.s. (G1/G3). Of the 13 goat isolates, seven were identified as E. granulosus s.s. (G1/G3), while the remaining six were classified as E. canadensis (G6/G7). The centrifugal flotation method was employed to detect the presence of Isospora spp. oocysts in eight dogs, Toxocara canis and hookworm eggs in three dogs each, and Dipyllidium caninum eggs in one dog. A total of 54 dog faeces were examined. No Taeniid eggs were observed in any of the dogs. Following PCR analysis of the mt-CO1 gene region in the dog faecal samples, four samples were positive for a 875 bp band. Only one of these bands was suitable for sequence analysis, which confirmed it as E. granulosus s.s. (G1/G3).
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Affiliation(s)
- Muhammed Ahmed Selcuk
- Siirt University, Faculty of Veterinary Medicine, Department of Parasitology, Siirt, Türkiye; Firat University, Faculty of Veterinary Medicine, Department of Parasitology, Elazig, Türkiye
| | - Burcak Aslan Celik
- Siirt University, Faculty of Veterinary Medicine, Department of Parasitology, Siirt, Türkiye
| | - Figen Celik
- Firat University, Faculty of Veterinary Medicine, Department of Parasitology, Elazig, Türkiye
| | - Ozgur Yasar Celik
- Siirt University, Faculty of Veterinary Medicine, Department of Internal Medicine, Siirt, Türkiye
| | - Kerem Ercan
- Siirt University, Faculty of Veterinary Medicine, Department of Internal Medicine, Siirt, Türkiye
| | - Muhammet Uslug
- Firat University, Faculty of Veterinary Medicine, Department of Parasitology, Elazig, Türkiye
| | - Afra Sena Tekin
- Firat University, Faculty of Veterinary Medicine, Department of Parasitology, Elazig, Türkiye; Cukurova University, Faculty of Veterinary Medicine, Department of Parasitology, Adana, Türkiye
| | - Sami Simsek
- Firat University, Faculty of Veterinary Medicine, Department of Parasitology, Elazig, Türkiye.
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Bonelli P, Serra E, Dei Giudici S, Peruzzu A, Crotti S, Danesi P, Carvelli A, Piseddu T, Masala G. Molecular phylogenetic analysis of Echinococcus granulosus sensu lato infecting sheep in Italy. Acta Trop 2024; 252:107151. [PMID: 38367944 DOI: 10.1016/j.actatropica.2024.107151] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2023] [Revised: 01/27/2024] [Accepted: 02/15/2024] [Indexed: 02/19/2024]
Abstract
Cystic Echinococcosis (CE), caused by the larval form of Echinococcus granulosus sensu lato, is a neglected zoonosis still threatening public health worldwide. In Italy different epidemiological scenarios were reported depending on the geographical area and associated socio-economic activities. Although in northern Italy the occurrence of E. granulosus is considered sporadic, in the southern regions and, particularly in Sardinia, CE prevalence reaches high levels. We analysed CE cysts collected from infected sheep from various areas of mainland Italy and the Sardinia island, with the main objective to investigate intergenotypic and intragenotypic variations at national level. CE cysts were collected from slaughtered sheep following post mortem inspection at local abattoirs. Total genomic DNA was extracted and amplification and sequencing of the partial mitochondrial genes nad5 and cox1 were performed. A Bayesian phylogenetic tree was estimated on a nad5 dataset (n = 260) composed of E. granulosus samples from this study (n = 126) and all the nad5 haplotypes available in GenBank (n = 134). In addition, haplotype network, diversity and neutrality analysis were performed on nad5 and cox1 sequences of Italian origin obtained in this study. E. granulosus sensu stricto (s.s.) was found to be the only Echinococcus species infecting sheep in Italy, mainly represented by G1 genotype (76 %) and, to a lower extent, by G3 genotype (24 %). Phylogenetic analyses revealed 40 nad5 and 33 cox 1 haplotypes, and the presence of two founder haplotypes, belonging to G1 and G3 genotype, showing 100 % similarity with DNA sequences from different geographic regions. The lack of geographical segregation, high haplotype and low nucleotide diversity coupled with significant negative values of Tajima's D and Fu's Fs observed in this study indicated high genetic variation and demographic expansion of E. granulosus s.s. in Italy.
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Affiliation(s)
- Piero Bonelli
- Istituto Zooprofilattico Sperimentale della Sardegna, WOAH Reference Laboratory for Echinococcosis, National Reference Laboratory of Echinococcosis (CeNRE), Via Vienna 2, Sassari, 07100, Italy.
| | - Elisa Serra
- Istituto Zooprofilattico Sperimentale della Sardegna, WOAH Reference Laboratory for Echinococcosis, National Reference Laboratory of Echinococcosis (CeNRE), Via Vienna 2, Sassari, 07100, Italy
| | - Silvia Dei Giudici
- Istituto Zooprofilattico Sperimentale della Sardegna, Diagnostica virologica, Sassari, 07100, Italy
| | - Angela Peruzzu
- Istituto Zooprofilattico Sperimentale della Sardegna, WOAH Reference Laboratory for Echinococcosis, National Reference Laboratory of Echinococcosis (CeNRE), Via Vienna 2, Sassari, 07100, Italy
| | - Silvia Crotti
- Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche, Perugia, 06126, Italy
| | - Patrizia Danesi
- Istituto Zooprofilattico Sperimentale della Venezie, Legnaro, 35020, Italy
| | - Andrea Carvelli
- Istituto Zooprofilattico Sperimentale del Lazio della Toscana, Roma, 00178, Italy
| | - Toni Piseddu
- Istituto Zooprofilattico Sperimentale della Sardegna, WOAH Reference Laboratory for Echinococcosis, National Reference Laboratory of Echinococcosis (CeNRE), Via Vienna 2, Sassari, 07100, Italy
| | - Giovanna Masala
- Istituto Zooprofilattico Sperimentale della Sardegna, WOAH Reference Laboratory for Echinococcosis, National Reference Laboratory of Echinococcosis (CeNRE), Via Vienna 2, Sassari, 07100, Italy
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Kaethner M, Preza M, Kaempfer T, Zumstein P, Tamponi C, Varcasia A, Hemphill A, Brehm K, Lundström-Stadelmann B. Establishment and application of unbiased in vitro drug screening assays for the identification of compounds against Echinococcus granulosus sensu stricto. PLoS Negl Trop Dis 2023; 17:e0011343. [PMID: 37540716 PMCID: PMC10431624 DOI: 10.1371/journal.pntd.0011343] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2023] [Revised: 08/16/2023] [Accepted: 07/13/2023] [Indexed: 08/06/2023] Open
Abstract
Echinococcus multilocularis and E. granulosus s.l. are the causative agents of alveolar and cystic echinococcosis, respectively. Drug treatment options for these severe and neglected diseases are limited to benzimidazoles, which are not always efficacious, and adverse side effects are reported. Thus, novel and improved treatments are needed. In this study, the previously established platform for E. multilocularis in vitro drug assessment was adapted to E. granulosus s.s. In a first step, in vitro culture protocols for E. granulosus s.s. were established. This resulted in the generation of large amounts of E. granulosus s.s. metacestode vesicles as well as germinal layer (GL) cells. In vitro culture of these cells formed metacestode vesicles displaying structural characteristics of metacestode cysts generated in vivo. Next, drug susceptibilities of E. multilocularis and E. granulosus s.s. protoscoleces, metacestode vesicles and GL cells were comparatively assessed employing established assays including (i) metacestode vesicle damage marker release assay, (ii) metacestode vesicle viability assay, (iii) GL cell viability assay, and (iv) protoscolex motility assay. The standard drugs albendazole, buparvaquone, mefloquine, MMV665807, monepantel, niclosamide and nitazoxanide were included. MMV665807, niclosamide and nitazoxanide were active against the parasite in all four assays against both species. MMV665807 and monepantel were significantly more active against E. multilocularis metacestode vesicles, while albendazole and nitazoxanide were significantly more active against E. multilocularis GL cells. Albendazole displayed activity against E. multilocularis GL cells, but no effects were seen in albendazole-treated E. granulosus s.s. GL cells within five days. Treatment of protoscoleces with albendazole and monepantel had no impact on motility. Similar results were observed for both species with praziquantel and its enantiomers against protoscoleces. In conclusion, in vitro culture techniques and drug screening methods previously established for E. multilocularis were successfully implemented for E. granulosus s.s., allowing comparisons of drug efficacy between the two species. This study provides in vitro culture techniques for the reliable generation of E. granulosus s.s. metacestode vesicles and GL cell cultures and describes the validation of standardized in vitro drug screening methods for E. granulosus s.s.
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Affiliation(s)
- Marc Kaethner
- Institute of Parasitology, Vetsuisse Faculty, University of Bern, Switzerland
- Graduate School for Cellular and Biomedical Sciences, University of Bern, Switzerland
| | - Matías Preza
- Institute of Parasitology, Vetsuisse Faculty, University of Bern, Switzerland
| | - Tobias Kaempfer
- Institute of Parasitology, Vetsuisse Faculty, University of Bern, Switzerland
- Graduate School for Cellular and Biomedical Sciences, University of Bern, Switzerland
| | - Pascal Zumstein
- Institute of Parasitology, Vetsuisse Faculty, University of Bern, Switzerland
| | - Claudia Tamponi
- Department of Veterinary Medicine, University of Sassari, Italy
| | | | - Andrew Hemphill
- Institute of Parasitology, Vetsuisse Faculty, University of Bern, Switzerland
| | - Klaus Brehm
- Institute of Hygiene and Microbiology, University of Würzburg, Germany
| | - Britta Lundström-Stadelmann
- Institute of Parasitology, Vetsuisse Faculty, University of Bern, Switzerland
- Multidisciplinary Center for Infectious Diseases, University of Bern, Bern, Switzerland
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Alvi MA, Alshammari A, Ali RMA, Ul Haq S, Bashir R, Li L, Saqib M, Sajid MS, Ghafoor M, Imran M, Ijaz MU, Fu BQ, Saeed M, Ahmad I, Liu YY, Yan HB, Jia WZ. Revealing novel cytb and nad5 genes-based population diversity and benzimidazole resistance in Echinococcus granulosus of bovine origin. Front Vet Sci 2023; 10:1191271. [PMID: 37396990 PMCID: PMC10312306 DOI: 10.3389/fvets.2023.1191271] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/21/2023] [Accepted: 05/17/2023] [Indexed: 07/04/2023] Open
Abstract
Cystic echinococcosis (CE) is a neglected zoonotic disease caused by Echinococcus granulosus (sensu stricto). The parasite affects a wide range of livestock and wild animals. In this study, the population diversity of the Echinococcus species was investigated based on mitochondrial cytochrome b (cytb) and NADH dehydrogenase subunit 5 (nad5) genes. In addition to this, β-tubulin gene isoforms of Echinococcus granulosus were amplified to determine the resistance against benzimidazoles. For this purpose, 40 cyst samples from cattle (n = 20) and buffaloes (n = 20) were collected from the main abattoir of Sialkot. DNA extraction was performed using Qiagen Blood and Tissue Kits. Amplification was performed through PCR. Each amplicon was confirmed by GelRed™ stained agarose gel (2%). Samples were sequenced in a DNA analyzer and viewed for any misread nucleotide by using MEGA (v.11). Corrections in nucleotide sequence and multiple sequence alignment were made through the same software. NCBI-BLAST was used for sample specific sequences to identify them as belonging to a particular species. Diversity indices were estimated using DnaSP (v.6) while phylogenetic analysis was inferred using the Bayesian method using MrBayes (v.1.1). β-tubulin gene isoforms sequence analysis was performed to find out the candidate gene causing benzimidazole resistance. All 40 isolates were found positive for E. granulosus. BLAST-based searches of sequences of each isolate for each gene (nad5 and cytb) confirmed their maximum similarity with the G1 genotype. Overall, high haplotype diversity (Hd nad5 = 1.00; Hd cytb = 0.833) and low nucleotide diversity (π nad5 = 0.00560; π = cytb = 0.00763) was identified based on diversity indices. For both the genes, non-significant values of Tajima's D (nad5 = -0.81734; cytb = -0.80861) and Fu's Fs (nad5 = -1.012; cytb = 0.731) indicate recent population expansion. Bayesian phylogeny-based results of nad5 and cytb sequences confirmed their genotypic status as distinct from other Echinococcus species. This study shed light on the status of benzimidazole resistance in Echinococcus granulosus for the very first time from Pakistan. The findings of this study will significantly add in the information available on genetic diversity of Echinoccous granulosus based on cytb and nad5 genes sequences.
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Affiliation(s)
- Mughees Aizaz Alvi
- State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, National Para-Reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | - Ayed Alshammari
- Department of Biology, College of Science, University of Hafr Al Batin, Hafr Al Batin, Saudi Arabia
| | - Rana Muhammad Athar Ali
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | - Shahbaz Ul Haq
- Key Laboratory of Veterinary Pharmaceutical Development, Ministry of Agriculture and Rural Affairs, Lanzhou Institute of Husbandry and Pharmaceutical Sciences, Chinese Academy of Agricultural Sciences, Lanzhou, China
| | - Rizwan Bashir
- Veterinary Disease Diagnostic Laboratory Sialkot, Livestock and Dairy Development Department, Government of Punjab, Lahore, Pakistan
| | - Li Li
- State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, National Para-Reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
| | - Muhammad Saqib
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | | | - Muzafar Ghafoor
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | - Muhammad Imran
- Department of Pathology, University of Agriculture, Faisalabad, Pakistan
| | - Muhammad Umar Ijaz
- Department of Zoology, Wildlife and Fisheries, University of Agriculture, Faisalabad, Pakistan
| | - Bao-Quan Fu
- State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, National Para-Reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
| | - Mohd Saeed
- Department of Biology, College of Science, University of Hail, Hail, Saudi Arabia
| | - Irfan Ahmad
- Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Khalid University, Abha, Saudi Arabia
| | - You-Yu Liu
- State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, National Para-Reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
| | - Hong-Bin Yan
- State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, National Para-Reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
| | - Wan-Zhong Jia
- State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, National Para-Reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
- Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease, Yangzhou, China
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Molecular Epidemiology of Cystic Echinococcosis in Rural Baluchistan, Pakistan: A Cross-Sectional Study. Pathogens 2022; 12:pathogens12010040. [PMID: 36678388 PMCID: PMC9863174 DOI: 10.3390/pathogens12010040] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/31/2022] [Revised: 12/09/2022] [Accepted: 12/19/2022] [Indexed: 12/28/2022] Open
Abstract
Cystic echinococcosis (CE), or hydatid cyst disease (HCD), is a zoonosis of significant importance caused by the cestode of Echinococcus granulosus sensu lato (s. l.) that affects mainly nomadic populations and has substantial economic consequences. Due to the 76% rural and nomadic population, Baluchistan is a highly endemic region in Pakistan for CE; however, it has not yet been investigated for CE. For this purpose, this study was carried out to investigate the molecular epidemiology of CE in this region. In total, 23 human hydatid cyst samples were collected from tertiary health care units in Baluchistan and processed for DNA extraction, which was then followed by sequencing of the cox1 mitochondrial gene of all 23 collected samples, genotyping, and phylogenetic and haplotype analysis. Most subjects were livestock owners (39.13%) in rural settings (73.91%). Most patients (73.19%) were pet owners (dogs) and used water from open sources for drinking. The liver was the most affected organ (52.17%), followed by the lungs (17.39%). Sequence analysis based on the cox1 gene revealed that EG genotype 1 (G1) was the most prevalent (56.52%), followed by G3 (34.78%), while some samples (8.7%) were identified as the Echinococcus canadensis (G6/7) genotype. A total of five haplotypes were detected with high haplotype diversity (0.80) and low nucleotide diversity (0.033). Phylogenetic analysis revealed two diverse sub-clades, each of G1 and G3 isolates from Baluchistan, that were evolutionarily related to previously reported G1 and G3 isolates from Pakistan and China. On the other hand, the G6/7 isolates of this study were evolutionarily identical to the already reported G6/7 isolates from Pakistan, Turkey, and Kazakhstan. This study concludes that diverse G1 and G3 EG isolates are present in this part of Pakistan, while the G6/G7 genotype was reported for the first time from Baluchistan.
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Porcu F, Cantacessi C, Dessì G, Sini MF, Ahmed F, Cavallo L, Nonnis F, Gibson K, Varcasia C, Joanny G, Scala A, Tamponi C, Varcasia A. 'Fight the parasite': raising awareness of cystic echinococcosis in primary school children in endemic countries. Parasit Vectors 2022; 15:449. [PMID: 36461072 PMCID: PMC9717558 DOI: 10.1186/s13071-022-05575-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/06/2022] [Accepted: 11/03/2022] [Indexed: 12/04/2022] Open
Abstract
BACKGROUND Cystic echinococcosis (CE) is a widespread zoonosis and a significant economic concern and cause of morbidity in humans. A scarcity of education on the sources of CE infection and containment measures is considered to be a key factor responsible for persistent transmission within communities. Recently, edutainment approaches have captured the attention of health education (HE) professionals due to the benefits of integrating cognitive and emotional learning processes. METHODS A study was carried out in Sardinia, Italy, between 2020 and 2022, amid the SARS-Covid-19 pandemic. The project, designed to involve primary school children (via remote or face-to-face learning depending on the evolving Covid-19 containment measures) consisted of four distinct phases: (i) creation of material for school children and teachers focused on cystic echinococcosis; (ii) pre-intervention evaluation of CE knowledge (i.e. True False Don't Know [TFD] pre-intervention questionnaire based on CE-related knowledge and practices); (iii) edutainment activity (e.g. interactive lessons enhanced by the comic booklet and the "Fight the parasite" cartoon video, hands-on educational activities and drawing activities on CE); and (iv) post-intervention evaluation of CE knowledge (via TFD post-intervention questionnaire [same questionnaire as used for the pre-intervention assessment] on CE-related knowledge and practices) and on-site edutainment tour in primary schools taking part to the project. RESULTS The percentage of correct answers increased from 65% for the questionnaire administered pre-intervention to 87.9% for the same questionnaire administered post-intervention (χ2 = 648.12, df = 1, P < 0.0001), while the percentage of uncertain answers (i.e. 'I don't know') decreased from 23% pre-intervention to 5% post-intervention (χ2 = 603.44, df = 1, P < 0.0001). These differences indicate a significantly enhanced understanding of CE among participating school children after the intervention. CONCLUSIONS The results of the present survey indicate that the use of digital educational tools, the use of video animations as a model for science communication, as well as other participatory teaching methods, enabled children to retain key knowledge of the routes of CE transmission and ways to prevent it.
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Affiliation(s)
- Francesca Porcu
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Cinzia Cantacessi
- grid.5335.00000000121885934Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
| | - Giorgia Dessì
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Maria Francesca Sini
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Fahad Ahmed
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Lia Cavallo
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Francesca Nonnis
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Katherine Gibson
- grid.5335.00000000121885934Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
| | - Cecilia Varcasia
- grid.34988.3e0000 0001 1482 2038Free University of Bozen, Bolzano, Italy
| | - Gaelle Joanny
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Antonio Scala
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Claudia Tamponi
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Antonio Varcasia
- grid.11450.310000 0001 2097 9138Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
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Kırış MT, Ergün S, Akıncı O, Ergin S, Velidedeoğlu M, Kocazeybek BS, Göksoy E. Evaluation of <em>Echinococcus</em> DNA by polymerase chain reaction (PCR) in cystic <em>Echinococcosis</em> of the liver. Turk J Surg 2022; 38:196-201. [PMID: 36483165 PMCID: PMC9714648 DOI: 10.47717/turkjsurg.2022.5427] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/24/2021] [Accepted: 06/08/2022] [Indexed: 12/24/2022]
Abstract
OBJECTIVES The aim of this study was to determine the DNA and genotypes of Echinococcus granulosus in liver cyst hydatids isolated in humans. MATERIAL AND METHODS This study was conducted prospectively at the Department of General Surgery of the Cerrahpaşa School of Medicine, University of İstanbul-Cerrahpaşa, between January 2015 and June 2016 in 30 patients who were operated on for cystic Echinococcosis. E. granulosus DNA was analyzed using the Polymerase Chain Reaction (PCR) method in the cyst samples (protoscolex and/or germinative membrane) obtained during the operation, and genotype was determined in the PCR positive samples by sequence analysis. At the same time, indirect hemagglutination (IHA) was used to test for the presence of antibodies in the patients' blood. RESULTS E. granulosus DNA was found in 29 out of 30 cystic Echinococcosis of the liver samples. All of the 29 cystic Echinococcosis samples were found to be G1 (sheep) species. Also, IHA was positive in 22 patients and negative in eight patients. CONCLUSION In the present study, G1 species was the most commonly seen liver cystic Echinococcosis species. We suggest that a vaccine, which could be developed against prevalent regional genotypes, would be efficacious in the prevention of the disease with a cause of mortality and morbidity.
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Affiliation(s)
- Mehmet Tolga Kırış
- Department of General Surgery, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
| | - Sefa Ergün
- Department of General Surgery, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
| | - Ozan Akıncı
- Department of General Surgery, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
| | - Sevgi Ergin
- Department of Medical Microbiology, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
| | - Mehmet Velidedeoğlu
- Department of General Surgery, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
| | - Bekir Sami Kocazeybek
- Department of Medical Microbiology, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
| | - Ertuğrul Göksoy
- Department of General Surgery, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Türkiye
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Avcioglu H, Bia MM, Balkaya I, Kirman R, Akyuz M, Guven E. Cystic echinococcosis in slaughtered sheep in Erzurum province, Turkey. Acta Trop 2022; 233:106559. [PMID: 35688264 DOI: 10.1016/j.actatropica.2022.106559] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2021] [Revised: 03/03/2022] [Accepted: 06/06/2022] [Indexed: 11/01/2022]
Abstract
Cystic echinococcosis (CE) is an important zoonotic infection caused by the larval stages of the genus Echinococcus. Turkey is a highly endemic region for CE and the disease is one of the major public health problems. The study was aimed to assess the situation of the CE in sheep in Turkey and also to provide data on circulating genotypes in the country. A total of 3319 sheep at slaughter were screened during the study. The prevalence of CE in the study area was 31.7% (1052/3319). The lungs were the most frequently CE infected organ (52.6%, 526/1052). Microscopic examination revealed that overall cyst fertility was 68.1%. Molecular analysis of partial fragments of 12S and COI gene regions were included for 351 selected cyst samples and all of them were identified as E. granulosus sensu stricto. Sequence analysis showed that the predominant genotype in the study areas was G1 (77.1%), and the rest were G3 (22.9%). The prevalence rate of CE in sheep in the study area is lower compared to previous years except for one province. Considering the high cyst fertility rate and the predominance of E. granulosus G1 which is particularly pathogenic to humans, calls for serious control measures like public awareness about the disease, sufficient dog deworming programs, continuity of monitoring the disease should be taken.
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Affiliation(s)
- Hamza Avcioglu
- Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey.
| | - Mohammed Mebarek Bia
- Department of Parasitology, Parasitology Research Center and Parasite Resource Bank, Chungbuk National University, School of Medicine, Cheongju 28644, Korea
| | - Ibrahim Balkaya
- Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
| | - Ridvan Kirman
- Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
| | - Muzaffer Akyuz
- Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
| | - Esin Guven
- Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
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Molecular Study of Echinococcus granulosus Cestodes in Ukraine and the First Genetic Identification of Echinococcus granulosus Sensu Stricto (G1 Genotype) in the Country. Acta Parasitol 2022; 67:244-254. [PMID: 34279774 DOI: 10.1007/s11686-021-00450-z] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/09/2021] [Accepted: 06/28/2021] [Indexed: 12/16/2022]
Abstract
INTRODUCTION Cystic echinococcosis is a globally distributed zoonotic disease of great medical and veterinary importance, which is caused by the cestode Echinococcus granulosus sensu lato. In Ukraine, two areas of the prominent circulation of the parasite are established, the southern steppe zone with sheep as the main transmitter, and the northern forest-steppe zone and Polissia, where pigs are mainly responsible for maintaining the E. granulosus transmission. METHODS Given that only a few studies have so far addressed the genetic diversity of the parasite in Ukraine, we have sequenced partial mitochondrial genes of cytochrome c oxidase 1 (789 bp), NADH dehydrogenase 1 (602 bp) and 12S rRNA (333-334 bp) in pig metacestodes from the Sumy region (farms close to Sumy, northeastern Ukraine) and the Kyiv region (a farm in Bila Tserkva, central Ukraine). RESULTS Four isolates from four pigs in the Sumy region were identified as E. canadensis (G7 genotype), the major E. granulosus s.l. species circulating in Eastern Europe, including the three microvariants (G7A, G7B, G7C). Three isolates from the two pigs in the Kyiv region were classified as E. granulosus s.s. (G1 genotype), including one microvariant (G1A). CONCLUSION To our knowledge, this is the first genetic record of E. granulosus s.s. with the presumed highest infectivity and virulence among the E. granulosus s.l. species in Ukraine. The finding has implications for public health as local control programmes should take into consideration different development rate of this parasite in dogs and the greater risk of the species for human infection.
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Kesik HK, Celik F, Simsek S, Kilinc SG, Ahmed H, Gul A. Molecular Characterization and Haplotype Analyses of Lung Hydatid Cyst Isolates of Cattle and First Report of Echinococcus canadensis (G6/G7) in Cattle Isolates in Turkey. Acta Parasitol 2021; 66:1538-1547. [PMID: 34121135 DOI: 10.1007/s11686-021-00432-1] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/10/2021] [Accepted: 06/01/2021] [Indexed: 01/22/2023]
Abstract
PURPOSE Cystic echinococcosis (CE) is a zoonotic disease, caused by parasite known as Echinococcus granulosus sensu lato complex, leading to substantial economic losses in rural areas with public health problems. This study was carried out to understand the haplotypic profiles of the partial mitochondrial cytochrome c oxidase (mt-CO1) gene of cattle lung hydatid cyst samples which were obtained from two provinces in Turkey. METHODS In this study, forty (n = 40) hydatid cyst samples from the lungs of slaughtered cattle were obtained. The germinal layers were taken separately for each individual cyst then stored in 70% ethanol. From each individual cyst sample, total genomic DNA was extracted. Amplification of the partial mt-CO1 gene (875 bp) was performed using a specific primer set by PCR, and then, the amplicons were sequenced. All sequences were analyzed individually, followed by alignment, and haplotype and phylogenetic analyses were then performed. RESULTS By the sequence alignment process, 39 out of the 40 sequences were characterized as E. granulosus sensu stricto. However, one of them was matched with E. canadensis (G6/G7). The haplotype analyses of the E. granulosus s.s. isolates were arranged in a star-like orientation with a main haplotype, which was separated from other haplotypes by 1-10 mutation steps, and 26 haplotypes were identified. In the mt-CO1 sequences, 29 polymorphic sites were determined, and 34.5% (10/29) of them were parsimony informative. CONCLUSIONS The findings of this study provide the first report of E. canadensis (G6/G7 genotype) among cattle in Turkey.
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Affiliation(s)
- Harun Kaya Kesik
- Department of Parasitology, Faculty of Veterinary Medicine, Bingol University, Bingol, Turkey
| | - Figen Celik
- Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Turkey
| | - Sami Simsek
- Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Turkey.
| | - Seyma Gunyakti Kilinc
- Department of Parasitology, Faculty of Veterinary Medicine, Bingol University, Bingol, Turkey
| | - Haroon Ahmed
- Department of Biosciences, COMSATS University Islamabad (CUI), Islamabad, Pakistan
| | - Abdurrahman Gul
- Department of Parasitology, Faculty of Veterinary Medicine, Bingol University, Bingol, Turkey
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11
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Olivastri A, Paoletti B, Lauteri C, Pennisi L, Paludi D, Festino AR, Vergara A. Parasitic cysts in wild boars hunted in Central Italy: The sanitary controls in the wild game meats chain. Ital J Food Saf 2021; 10:9383. [PMID: 34497779 PMCID: PMC8404528 DOI: 10.4081/ijfs.2021.9383] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/05/2020] [Accepted: 03/22/2021] [Indexed: 11/23/2022] Open
Abstract
Seven hundred sixty-five (765) adult wild boars were examined during the 2016/2017 hunting season for the research of parasites. Post mortem inspection was carried out at the slaughterhouse by the Official Veterinarian on the plucks (heart, tongue, lungs, diaphragm, and liver) of the killed animals presented by hunters. Of these, 0.8% (6/765) were positive for Echinococcus granulosus sensu lato (s.l.), and 2.6% (20/765) were positive for the metacestode stage of Taenia hydatigena (Cysticercus tenuicollis), while 0.5% (4/765) animals showed a mixed infection (Echinococcus granulosus s.l. and Taenia hydatigena). Sixty-three (63) cystic lesions were found. Of these 25,4% (16/63) were caused by Echinococcus granulosus s.l. and 74,6% (47/63) were caused by Cysticercus tenuicollis. The more involved organs were liver and lungs, in a less extension omentum and diaphragm. Parasitological analyses showed an overall prevalence of 3.9% for metacestodes in the hunted animals examined (Paoletti et al., 2018). Hydatids were molecularly characterized as E. granulosus sensu stricto. Trichinella spp. examination results showed no evidences of parasitic cysts. The products of hunting used for own consumption and direct sale to the final consumer or retailer, according to Regulation (EC) No 853/2004, lack of overall control by the Competent Authority. This is a critical point in the food chain of the game meat. The data obtained show the importance of the post mortem inspection and the central role of the Competent Authority to ensure not only the food safety of game meat but also to collect data for extensive epidemiological investigations on live-stocks wildlife settings having a direct impact on public health.
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Affiliation(s)
| | | | | | - Luca Pennisi
- Faculty of Veterinary Medicine, University of Teramo, Italy
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12
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Mehmood N, Dessì G, Ahmed F, Joanny G, Tamponi C, Cappai MG, Varcasia A, Scala A. Genetic diversity and transmission patterns of Echinococcus granulosus sensu stricto among domestic ungulates of Sardinia, Italy. Parasitol Res 2021; 120:2533-2542. [PMID: 34146127 PMCID: PMC8263412 DOI: 10.1007/s00436-021-07186-9] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/15/2020] [Accepted: 05/05/2021] [Indexed: 12/22/2022]
Abstract
Cystic echinococcosis (CE), a parasitic zoonosis of public health and economic concern, is highly endemic in Sardinia, Italy. The study involved examining the intraspecific variability and demographic structure of Echinococcus granulosussensu stricto (s.s.) in common hosts of this parasite. Molecular surveillance included the fragment amplification of a partial mitochondrial gene, cox1 (750 bp), for a total of 69 isolates derived from sheep (n = 52), cattle (n = 11), pigs (n = 4), and goats (n = 2). It was ascertained that E. granulosus s.s. was the primary agent of infection among these ungulates and G1 genotype was highly prevalent (79.71%). Considerable intraspecific variation was found, revealing the existence of 22 haplotypes with relatively high haplotype (0.8555 ± 0.033) and low nucleotide diversities (0.00281 ± 0.00030). Population demographics indicated an expanding parasitic population signifying negative deviation from neutrality indices. Little genetic differentiation was found between the subpopulations of E. granulosus s.s. in the island. Moreover, the geographic dispersal of genotypes G1 and G3 also indicated similarity between Sardinian and mainland Echinococcus granulosus s.s. populations reaffirming the sympatric occurrence and efficient transmission of G1 and G3 genotypes. Molecular survey of CE has the potential to yield baseline information on the infective genotypes among the intermediate hosts and helps in devising suitable control strategies for curtailing the disease.
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Affiliation(s)
- Naunain Mehmood
- Department of Zoology, University of Sargodha, Sargodha, Pakistan
| | - Giorgia Dessì
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
| | - Fahad Ahmed
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
| | - Gaelle Joanny
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
| | - Claudia Tamponi
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
| | - Maria Grazia Cappai
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
| | - Antonio Varcasia
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
| | - Antonio Scala
- Dipartimento Di Medicina Veterinaria, Università Degli Studi Di Sassari, Via Vienna, 2, 07100 Sassari, Italy
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Joanny G, Mehmood N, Dessì G, Tamponi C, Nonnis F, Hosri C, Saarma U, Varcasia A, Scala A. Cystic echinococcosis in sheep and goats of Lebanon. Parasitology 2021; 148:871-878. [PMID: 33757607 PMCID: PMC11010058 DOI: 10.1017/s0031182021000494] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/01/2021] [Revised: 02/21/2021] [Accepted: 03/11/2021] [Indexed: 02/06/2023]
Abstract
Cystic echinococcosis (CE), a zoonotic disease caused by the species complex of Echinococcus granulosus sensu lato (s.l.), is endemic in Middle East and the Mediterranean basin, where pastoral activity is widespread. Despite the chronic endemicity of the disease in Lebanon and neighbouring countries, recent data are scant. The objectives of this survey were to evaluate the current epidemiology of CE in Lebanon, investigate the prevalence and determine the infecting genotypes in locally raised sheep and goats. A multidimensional approach combining post-mortem inspection of slaughtered animals and molecular diagnosis of the parasite was conducted to this end. From 2018 to 2020, 62.9% of the sheep and 20.9% of the goats were found positive for CE. The presence of hydatids varied between organs, showing higher prevalence in the liver of sheep vs the lungs of goats, however, a higher fertility rate of hydatid cyst was observed in lungs for both animals. Molecular diagnosis based on partial mitochondrial cox1 gene (795 bp) showed that the majority of isolates were identified as E. granulosus sensu stricto (98.7%) and only one isolate from goat was identified as Echinococcus canadensis (genotype G7; 1.3%). Echinococcus granulosus s.s. population among the sheep and goats was represented by 22 haplotypes having very little genetic differentiation and relatively moderate haplotype diversity. Population demographics explored through neutrality indices suggested expanding population within the intermediate hosts. These results document the high prevalence of CE in the livestock of Lebanon and reveal for the first time the presence of three different genotypes G1, G3 and G7.
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Affiliation(s)
- Gaelle Joanny
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Naunain Mehmood
- Department of Zoology, University of Sargodha, Sargodha, Pakistan
| | - Giorgia Dessì
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Claudia Tamponi
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Francesca Nonnis
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Chadi Hosri
- Faculty of Agronomy and Veterinary Medicine, Lebanese University, Dekwaneh, Lebanon
| | - Urmas Saarma
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Antonio Varcasia
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Antonio Scala
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
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14
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Genchi M, Vismarra A, Favilli A, Bonilauri P, Prati P, Ciuca L, Passeri B, Armando F, Kramer L. First report of Echinococcus granulosus sensu lato genotype G6/G7 in domestic pigs from mainland Italy. VETERINARY PARASITOLOGY- REGIONAL STUDIES AND REPORTS 2021; 23:100536. [PMID: 33678389 DOI: 10.1016/j.vprsr.2021.100536] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/23/2020] [Revised: 01/04/2021] [Accepted: 01/19/2021] [Indexed: 02/04/2023]
Abstract
Cystic echinococcosis (CE; Echinococcus spp.) is widespread in many domestic animal species in Italy, with the G1-G3 genotype predominating. The G7 genotype ("pig strain"), which is much less common, has only been reported in pigs and wild boar from the island of Sardinia and in wild boars from southern mainland Italy. Ten pig livers with hydatid cysts were identified in a slaughterhouse in northwestern Italy. Multiplex PCR for Echinococcus granulosus gave positive results for two of these and subsequent sequencing confirmed the species as Echinococcus granulosusu s.l. G6/G7. Affected pigs came from an intensive farm in northeastern Italy. This is, to the authors' knowledge, the first report of CE by Echinococcus granulosusu s.l. G6/G7 in the domestic pig in mainland Italy. E. granulosus s.l. G6/G7 is zoonotic and its circulation in Italy should be of concern for public health.
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Affiliation(s)
- Marco Genchi
- Università di Parma, Dip. Scienze Medico-Veterinarie, Parassitologia e Malattie Parassitarie, Parma, Italy
| | - Alice Vismarra
- Università di Parma, Dip. Scienze Medico-Veterinarie, Parassitologia e Malattie Parassitarie, Parma, Italy.
| | - Alessandra Favilli
- Agenzia di Tutela della Salute (ATS) di Pavia, Dipartimento Veterinario e Sicurezza degli Alimenti di Origine Animale, Pavia, Italy
| | - Paolo Bonilauri
- Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna "Bruno Ubertini", Reggio Emilia, Italy
| | - Paola Prati
- Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna "Bruno Ubertini", Pavia, Italy
| | - Lavinia Ciuca
- Università di Napoli Federico II, Dip. Scienze Medico-Veterinarie, Parassitologia e Malattie Parassitarie, Napoli, Italy
| | - Benedetta Passeri
- Università di Parma, Dip. Scienze Medico-Veterinarie, Anatomia Patologica, Parma, Italy
| | - Federico Armando
- Università di Parma, Dip. Scienze Medico-Veterinarie, Anatomia Patologica, Parma, Italy
| | - Laura Kramer
- Università di Parma, Dip. Scienze Medico-Veterinarie, Parassitologia e Malattie Parassitarie, Parma, Italy
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Tamarozzi F, Legnardi M, Fittipaldo A, Drigo M, Cassini R. Epidemiological distribution of Echinococcus granulosus s.l. infection in human and domestic animal hosts in European Mediterranean and Balkan countries: A systematic review. PLoS Negl Trop Dis 2020; 14:e0008519. [PMID: 32776936 PMCID: PMC7440662 DOI: 10.1371/journal.pntd.0008519] [Citation(s) in RCA: 38] [Impact Index Per Article: 7.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/11/2020] [Revised: 08/20/2020] [Accepted: 06/25/2020] [Indexed: 12/22/2022] Open
Abstract
Cystic echinococcosis (CE) is a neglected zoonosis caused by infection with the cestode Echinococcus granulosus sensu lato. We carried out a systematic literature review on E. granulosus s.l. human and animal (cattle, sheep, dog) infection in European Mediterranean and Balkan countries in 2000–2019, to provide a picture of its recent epidemiology in this endemic area. MEDLINE, EMBASE, Scopus, Google Scholar and Open Grey databases were searched. Included cases were: i) for humans, data from hospital records and imaging studies; ii) for dogs, data from necropsy and coprological studies; iii) for ruminants, cases based on slaughter inspection. The NUTS (Nomenclature of Territorial Units for Statistics) classification was used to categorize extracted data in epidemiological units, defined as data referred to one NUTS2 (basic region) in one year time. Data were then aggregated to NUTS1 level (major regions), calculating the average incidence value of included epidemiological units. For prevalence studies covering different epidemiological units, the pooled prevalence was estimated. Data were extracted from 79 publications, 25 on human infection (covering 437 epidemiological units), and 54 on animal infection (52 epidemiological units for cattle, 35 for sheep and 25 for dogs). At NUTS1 level, average annual incidence rates of human CE ranged from 0.10–7.74/100,000; pooled prevalence values ranged from 0.003–64.09% in cattle, 0.004–68.73% in sheep, and 0–31.86% in dogs. Southern and insular Italy, central Spain, Romania and Bulgaria reported the highest values. Bovine data showed a more similar pattern to human data compared to sheep and dogs. Limitation of evidence included the paucity of human prevalence studies, data heterogeneity, and the patchy geographical coverage, with lack of data especially for the Balkans. Our results confirm Italy, Spain, and Eastern Europe being the most affected areas, but data are extremely heterogeneous, geographical coverage very patchy, and human prevalence studies extremely scant. Results also highlight the notorious problem of underreporting of E. granulosus s.l. infection in both humans and animals. Cystic echinococcosis (CE) is a neglected zoonosis caused by infection with the parasite Echinococcus granulosus sensu lato, naturally transmitted between canids and livestock; CE in humans can be a serious condition. In endemic areas, CE is responsible for significant health and economic losses, but its real burden is difficult to estimate. E. granulosus s.l. is especially present in areas where livestock breeding is practiced, including European Mediterranean and Balkan countries. We carried out a systematic literature review on the epidemiology of E. granulosus s.l. human and animal infection in this area in 2000–2019. Data were extracted from 79 publications, and referred to Nomenclature of Territorial Units for Statistics (NUTS) levels per year. Average annual incidence rates of human CE ranged from 0.10–7.74/100,000; pooled prevalences ranged from 0.003–64.09% in cattle, 0.004–68.73% in sheep, and 0–31.86% in dogs. Bovine data showed a more similar pattern to human data compared to sheep and dogs. Our results confirm that Italy, Spain, and Eastern Europe are the most affected areas, but data are extremely heterogeneous, geographical coverage very patchy, and human prevalence studies extremely scant. Results also highlight the well-known problem of underreporting of E. granulosus s.l. infection in both humans and animals.
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Affiliation(s)
- Francesca Tamarozzi
- Department of Infectious-Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, Negrar (Verona), Italy
| | - Matteo Legnardi
- Department of Animal Medicine, Production and Health, University of Padova, Legnaro (Padova), Italy
| | - Andrea Fittipaldo
- Department of Infectious-Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, Negrar (Verona), Italy
| | - Michele Drigo
- Department of Animal Medicine, Production and Health, University of Padova, Legnaro (Padova), Italy
| | - Rudi Cassini
- Department of Animal Medicine, Production and Health, University of Padova, Legnaro (Padova), Italy
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Varcasia A, Dessì G, Lattanzio S, Marongiu D, Cuccuru C, Carta S, Meloni MP, Tamponi C, Scala A. Cystic echinococcosis in the endemic island of Sardinia (Italy): has something changed? Parasitol Res 2020; 119:2207-2215. [PMID: 32447517 DOI: 10.1007/s00436-020-06717-0] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/10/2019] [Accepted: 05/13/2020] [Indexed: 10/24/2022]
Abstract
Cystic echinococcosis (CE) is a disease of livestock and humans caused by the larval stage of the Echinococcus granulosus sensu lato (s.l.) species complex and occurs especially in areas where sheep breeding is widespread. This survey evaluates, after more than a decade since the last epidemiological survey, the current situation and trend of CE in sheep of the highly endemic island of Sardinia (Italy). From 2012 to 2018, out of a total of 1416 sheep, 65.3% were found positive for CE. Cyst fertility has increased slightly from 10.3% in 2006 (Scala et al. 2006) to 11.7% in the present survey (χ2 = 1.07; P = 0.30018) with a peak of 14.0% in the province of Sassari. Overall, 6815 hydatids were found and classified as sterile (26.2%), fertile (14.4%), caseous (5.3%), or calcified (54.1%) based on their morphology. All isolates were identified as E. granulosus sensu stricto (former G1/G3, strains). Results shown as the implementation of new European Council Regulations and in particular of 21/2004 that established a system for the individual identification and tracking of sheep could be a step forward towards a better control of animal movement, preventing illegal slaughtering on the island as well as in other countries experiencing similar problems. Even if at first sight the general situation of Sardinia regarding CE seems a little better compared with the past, our findings indicate that in some Provinces the epidemiological situation is not improved since 2006.
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Affiliation(s)
- Antonio Varcasia
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy.
| | - Giorgia Dessì
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Silvia Lattanzio
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | | | - Cesare Cuccuru
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Silvia Carta
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Maria Pina Meloni
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Claudia Tamponi
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Antonio Scala
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
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Bonelli P, Dei Giudici S, Peruzzu A, Piseddu T, Santucciu C, Masu G, Mastrandrea S, Delogu ML, Masala G. Genetic diversity of Echinococcus granulosus sensu stricto in Sardinia (Italy). Parasitol Int 2020; 77:102120. [PMID: 32259586 DOI: 10.1016/j.parint.2020.102120] [Citation(s) in RCA: 20] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/16/2019] [Revised: 03/29/2020] [Accepted: 03/31/2020] [Indexed: 11/28/2022]
Abstract
Cystic echinococcosis (CE) is a severe parasitic zoonosis caused by the metacestode of the tapeworm Echinococcus granulosus sensu lato (s.l.). The disease has a global distribution representing a significant public health concern. Based on mitochondrial DNA analysis E. granulosus s.l. has been subdivided into five species: E. granulosus sensu stricto (s.s.) (G1, G3 genotype), E. equinus (G4 genotype), E. ortleppi (G5 genotype), E. canadensis (G6-G8, G10 genotype) and E. felidis. E. granulosus s.s., and in particular G1, is the most widespread genotype and the major responsible of human CE cases worldwide. In Italy G1 genotype is higly represented with larger percentages in some hyperendemic areas such as Sardinia. Molecular studies represent a valuable tool to improve our understanding of the E. granulosus epidemiology and CE control strategies. In the present study we investigated genetic variability of E. granulosus s.s. in Sardinia. To this purpose 83 hydatid cysts were collected from different animal species including humans and the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene was partially sequenced (720 bp). Nucleotide sequences from Mediterranean basin were also analyzed for comparison. The phylogenetic network revealed 30 haplotypes grouped around a predominant isolate that had been already reported from other world regions. Haplotype diversity (0.8495 ± 0.0336) and nucleotide diversity (0.003305 ± 0.002014) were similar in Sardinia respect to other Mediterranean countries. Neutrality indices obtained by Tajima's D and Fu's Fs test were significantly negative (p ≤ .01) suggesting expansion of Sardinian population. Low Fixation indices (Fst), ranging from negative values (Algeria, Greece, Spain, other part of Italy) to 0.089 (Albania, France), indicated absence of genetic differentiation, and gene flow between Sardinia and other Mediterranean countries.
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Affiliation(s)
- Piero Bonelli
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy.
| | - Silvia Dei Giudici
- Laboratory of Diagnostic Virology, Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
| | - Angela Peruzzu
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
| | - Toni Piseddu
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
| | - Cinzia Santucciu
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
| | - Gabriella Masu
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
| | - Scilla Mastrandrea
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
| | | | - Giovanna Masala
- OIE Reference Laboratory for Echinococcosis, National Reference Laboratory for Cystic Echinococcosis (CeNRE), Istituto Zooprofilattico della Sardegna (IZS), Via Vienna 2, 07100 Sassari, Italy
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National survey and molecular diagnosis of Echinococcus granulosus sensu lato in livestock in France, 2012. Parasitology 2020; 147:667-672. [PMID: 32046794 DOI: 10.1017/s0031182020000190] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/16/2022]
Abstract
The parasitic species of the Echinococcus granulosus sensu lato (sl) complex are the causative agents of cystic echinococcosis in humans. The lifecycle of E. granulosus sl is essentially domestic, and is based on the consumption by dogs of hydatid cysts in viscera of livestock species. The aim of this study was to survey E. granulosus sensu lato in livestock in France. A 1-year national survey of E. granulosus sl in livestock at the slaughterhouse was organized in 2012 in France, with systematic molecular confirmation. The prevalence of E. granulosus ss nationally was 0.002% in sheep, mainly focused in the Alpine area, and 0.001% in cattle, with the distribution of cases throughout the country. Echinococcus canadensis G6/7 was observed only in Corsica in pigs, with a prevalence of nearly 1% in the island. A national prevalence of 0.0002% was estimated for E. ortleppi in cattle, due to seven cases distributed in two foci. The results of this survey are of particular interest because of the zoonotic risk associated with the presence of these parasite species, for which systematic control at the slaughterhouse should enable their elimination.
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Determination of Echinococcus Granulosus Genotypes in Livestock Slaughtered in Shush County, Southwest Iran Using PCR-RFLP. Helminthologia 2019; 56:196-201. [PMID: 31662691 PMCID: PMC6799581 DOI: 10.2478/helm-2019-0023] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/10/2019] [Accepted: 06/14/2019] [Indexed: 01/03/2023] Open
Abstract
Echinococosis is a zoonotic disease caused by the larval stages of Echinococcus spp. that occurs in most parts of the world. Herein, we aimed to evaluate the genotypes of isolated hydatid cysts from slaughtered animals in Shush county, southwestern Iran. Totally, 96 hydatid cysts were collected, including 11 buffaloes, 13 cattle, 12 goat and 60 sheep. The PCR was done by a primer pair (BDI and 4s) to amplify ITS1 fragment. Four restriction endonucleases including AluI, HpaII, RsaI, and TaqI were used for RFLP products and enzymatic reactions were electrophoresed. Finally, twenty PCR products were sent for sequencing and phylogenetic tree was drawn with MEGA6. Molecular identification of 96 hydatid cysts demonstrated a distinctive 1000 bp fragment in all samples from four animal hosts. RFLP analysis showed similar digestion patterns in all samples. AluI digestion yielded 800 bp and 200 bp fragments, HpaII digestion made 700 bp and 300 bp fragments and RsaI digestion entailed 655 and 345segments. Moreover, TaqI rendered no digestion pattern on rDNA-ITS1 region. Additionally, E. granulosus sensu stricto (G1-3 complex) was the prevailing genotype in all livestock samples, according to PCR-RFLP and sequencing analyses.
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Sgroi G, Varcasia A, Dessi G, D'Alessio N, Tamponi C, Saarma U, Laurimäe T, Kinkar L, Santoro M, Caputo V, Sarnelli P, Fusco G, Varuzza P, Fioretti A, Scala A, Veneziano V. Cystic echinococcosis in wild boars ( Sus scrofa) from southern Italy: Epidemiological survey and molecular characterization. Int J Parasitol Parasites Wildl 2019; 9:305-311. [PMID: 31338291 PMCID: PMC6626981 DOI: 10.1016/j.ijppaw.2019.04.013] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/08/2019] [Revised: 04/29/2019] [Accepted: 04/30/2019] [Indexed: 11/20/2022]
Abstract
Cystic Echinococcosis (CE) caused by Echinococcus granulosus sensu lato (s.l.) is one of the most important parasitic zoonotic diseases in the world and it represents an important public health and socio-economic concern. In the Mediterranean basin, CE is widespread and it is endemic in Italy, with major prevalence in southern areas. Several studies have investigated CE in domestic pigs, however, such data in wild boars are scant. In the last decades the wild boar population in Italy has increased and this ungulate could play an important role in the spreading of CE in the wild. Here we report on the prevalence and fertility rate of hydatid cysts in wild boars that were shot during two hunting seasons (2016-2017) in the Campania region of southern Italy. For each animal, a detailed inspection of the carcass and organs (lungs, liver and spleen) was performed and when cysts were found, their number, morphology and fertility were determined by visual and microscopic examination. Cysts were classified morphologically as fertile, sterile, caseous and calcified. Protoscoleces and germinal layers were collected from individual cysts and DNA was extracted to identify different strains/genotypes of E. granulosus s.l. Out of a total of 2108 wild boars 93 (4.4%) were found positive for CE. Infected animals were 45 males and 48 females, aged between 1 and 8 years. The average number of cysts per wild boar was 1.3 (min 1 - max 13). The total number of cysts collected was 123, of which 118 (95.9%) in the liver, 4 (3.3%) in the lungs and 1 (0.8%) in the spleen. Of all analyzed cysts, 70 (56.9%) were fertile and 53 (43.1%) sterile/acephalous. The presence of fertile cysts in 19.4% of CE-positive animals is noteworthy. Overall, molecular diagnosis showed 19 wild boars infected with the pig strain (G7).
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Affiliation(s)
- Giovanni Sgroi
- Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
| | - Antonio Varcasia
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
- Inter-University Centre for Research in Parasitology, Naples, Italy
| | - Giorgia Dessi
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Nicola D'Alessio
- Istituto Zooprofilattico Sperimentale del Mezzogiorno, Portici, Italy
| | - Claudia Tamponi
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Urmas Saarma
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Teivi Laurimäe
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Liina Kinkar
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Mario Santoro
- Istituto Zooprofilattico Sperimentale del Mezzogiorno, Portici, Italy
| | - Vincenzo Caputo
- Regional Reference Center of Urban Veterinary Hygiene (CRIUV),Naples, Italy
| | - Paolo Sarnelli
- UOD Prevenzione e Sanità Pubblica Veterinaria Regione Campania, Naples, Italy
| | - Giovanna Fusco
- Istituto Zooprofilattico Sperimentale del Mezzogiorno, Portici, Italy
| | - Paolo Varuzza
- Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
| | - Alessandro Fioretti
- Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
| | - Antonio Scala
- Department of Veterinary Medicine, University of Sassari, Sassari, Italy
- Inter-University Centre for Research in Parasitology, Naples, Italy
| | - Vincenzo Veneziano
- Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
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Laurimäe T, Kinkar L, Varcasia A, Dessì G, Sgroi G, D'Alessio N, Veneziano V, Saarma U. First detection of zoonotic tapeworm Echinococcus granulosus sensu lato genotype G7 in continental Italy. Parasitol Res 2019; 118:2193-2201. [PMID: 31134335 DOI: 10.1007/s00436-019-06346-2] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/14/2019] [Accepted: 04/30/2019] [Indexed: 10/26/2022]
Abstract
The larval stage of the species complex Echinococcus granulosus sensu lato (s.l.) is the cause of a widespread zoonotic disease known as cystic echinococcosis (CE). The disease is highly prevalent in southern Italy and represents a serious public health issue. The main aim of this study was to characterize E. granulosus s.l. genotypes from wild boar on a continental area of Italy (Campania region), using recently developed mtDNA markers of nad2 and nad5 for reliable identification of different genotypes. Here, nad5 (680 bp) allowed for a clear identification of G1 and G3, whereas a combination of nad2 (714 bp) and nad5 (1394 bp in total) did the same for genotype G7 and its haplogroups G7a and G7b. The results of this study revealed for the first time the presence of genotype G7 in continental Italy. While haplogroup G7b was previously shown to be restricted to the islands of Corsica and Sardinia, here we demonstrate that haplogroup G7b is also present on the mainland of Italy. This work has implications in designing future strategies to reduce CE in Italy.
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Affiliation(s)
- Teivi Laurimäe
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003, Tartu, Estonia
| | - Liina Kinkar
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003, Tartu, Estonia
| | - Antonio Varcasia
- Laboratorio di Parassitologia e Malattie Parassitarie, Ospedale Didattico Veterinario Dipartimento di Medicina Veterinaria, Università degli Studi di Sassari, Via Vienna 2, 07100, Sassari, Italy
| | - Giorgia Dessì
- Laboratorio di Parassitologia e Malattie Parassitarie, Ospedale Didattico Veterinario Dipartimento di Medicina Veterinaria, Università degli Studi di Sassari, Via Vienna 2, 07100, Sassari, Italy
| | - Giovanni Sgroi
- Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
| | - Nicola D'Alessio
- Istituto Zooprofilattico Sperimentale del Mezzogiorno, Portici, Italy
| | - Vincenzo Veneziano
- Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
| | - Urmas Saarma
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003, Tartu, Estonia.
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Varcasia A, Sanna D, Casu M, Lahmar S, Dessì G, Pipia AP, Tamponi C, Gaglio G, Hrčková G, Otranto D, Scala A. Species delimitation based on mtDNA genes suggests the occurrence of new species of Mesocestoides in the Mediterranean region. Parasit Vectors 2018; 11:619. [PMID: 30514366 PMCID: PMC6278086 DOI: 10.1186/s13071-018-3185-x] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/14/2018] [Accepted: 11/06/2018] [Indexed: 01/18/2023] Open
Abstract
BACKGROUND This study is the first contribution to the molecular taxonomy of Mesocestoides spp. from domestic and wild carnivores in the Mediterranean area. A total of 13 adult worms and 13 larval stages of Mesocestoides spp. were collected from domestic and wild carnivore hosts in Italy and Tunisia. Samples collected in the Slovak Republic were used as comparative samples from outside the Mediterranean. The genes cytochrome c oxidase subunit 1 (cox1) and NADH dehydrogenase subunit 1 (nad1) of the mitochondrial genome were used as molecular markers to investigate the presence of cryptic Mesocestoides species in the area analysed. RESULTS Results were consistent in showing three well-supported clusters of Mesocestoides spp. in southern Italy and Tunisia, which were strongly divergent from Mesocestoides litteratus, M. corti and M. lineatus. High levels of genetic variation and no evidence of geographical structuring was found between the clusters. CONCLUSIONS Considering the low dispersal capability of the intermediate hosts of Mesocestoides spp., the lack of geographical structuring among the Mediterranean regions could be due to a high potential for dispersion of the definitive hosts. This study provides a foundation for future formal descriptions of new species of the genus Mesocestoides in the Mediterranean area.
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Affiliation(s)
- Antonio Varcasia
- Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy.
| | - Daria Sanna
- Dipartimento di Scienze Biomediche, Università di Sassari, Sassari, Italy
| | - Marco Casu
- Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
| | - Samia Lahmar
- National School of Veterinary Medicine, Laboratory of Parasitology, Sidi Thabet, Tunisia
| | - Giorgia Dessì
- Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
| | - Anna Paola Pipia
- Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
| | - Claudia Tamponi
- Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
| | - Gabriella Gaglio
- Dipartimento di Scienze Veterinarie, Università di Messina, Messina, Italy
| | - Gabriela Hrčková
- Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovak Republic
| | - Domenico Otranto
- Dipartimento di Medicina Veterinaria, Università di Bari, Bari, Italy
| | - Antonio Scala
- Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
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Paoletti B, Della Salda L, Di Cesare A, Iorio R, Vergara A, Fava C, Olivastri A, Dessì G, Scala A, Varcasia A. Epidemiological survey on cystic echinococcosis in wild boar from Central Italy. Parasitol Res 2018; 118:43-46. [PMID: 30315356 DOI: 10.1007/s00436-018-6112-3] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/21/2018] [Accepted: 10/07/2018] [Indexed: 12/27/2022]
Abstract
Despite the wide distribution of wild boar populations in Italy and the increase of its diffusion in urbanized areas, only one case report has described the occurrence of Echinococcus granulosus s.l. in a wild boar from Marche (Central Italy). The present study investigated the presence of E. granulosus sensu lato with an epidemiological survey on wild boars from central Italy that had been killed during hunting season. Seven hundred sixty-five (765) adult wild boars were examined during the 2016-2017 hunting season. Of these animals, 1.0% (8/765) were positive to E. granulosus s.l. with a fertility of 0.3% (2/765), and 2.9% animals (22/765) were positive for the metacestode stage of Taenia hydatigena (Cysticercus tenuicollis), while 0.5% (4/765) showed mixed infection (E. granulosus s.l. + T. hydatigena). Sixteen hydatids were found, of which 12.5% were fertile, 37.5% were sterile, 31.3% were caseous, and 18.8% were calcified. Eight hydatids (two fertile and six sterile cysts) were molecularly characterized by analysis of the mitochondrial gene, cytochrome c oxidase subunit 1 (cox1), and the NADH dehydrogenase subunit 1 (ND1). Hydatids found in wild boars were characterized as E. granulosus sensu stricto (G1 genotype). The present survey represents the first epidemiological study on cystic echinococcosis in wild boar in Italy which highlights the need for more extensive epidemiological investigations to determine the causal factors, economic impact, and public health importance of the disease in this livestock-wildlife setting.
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Affiliation(s)
- Barbara Paoletti
- Faculty of Veterinary Medicine, University of Teramo, Teramo, Italy.
- Faculty of Veterinary Medicine, Teaching Veterinary Hospital, Località Piano D'Accio snc, 64100, Teramo, Italy.
| | | | - Angela Di Cesare
- Faculty of Veterinary Medicine, University of Teramo, Teramo, Italy
| | - Raffaella Iorio
- Faculty of Veterinary Medicine, University of Teramo, Teramo, Italy
| | - Alberto Vergara
- Faculty of Veterinary Medicine, University of Teramo, Teramo, Italy
| | - Camilla Fava
- Faculty of Veterinary Medicine, University of Teramo, Teramo, Italy
| | | | - Giorgia Dessì
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Antonio Scala
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
| | - Antonio Varcasia
- Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Sassari, Italy
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Laurimäe T, Kinkar L, Romig T, Omer RA, Casulli A, Umhang G, Gasser RB, Jabbar A, Sharbatkhori M, Mirhendi H, Ponce-Gordo F, Lazzarini LE, Soriano SV, Varcasia A, Rostami Nejad M, Andresiuk V, Maravilla P, González LM, Dybicz M, Gawor J, Šarkūnas M, Šnábel V, Kuzmina T, Saarma U. The benefits of analysing complete mitochondrial genomes: Deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. INFECTION GENETICS AND EVOLUTION 2018; 64:85-94. [PMID: 29906638 DOI: 10.1016/j.meegid.2018.06.016] [Citation(s) in RCA: 52] [Impact Index Per Article: 7.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/12/2018] [Revised: 06/04/2018] [Accepted: 06/11/2018] [Indexed: 12/18/2022]
Abstract
Cystic echinococcosis (CE) is a zoonotic disease caused by the larval stage of the species complex Echinococcus granulosus sensu lato. Within this complex, genotypes G6 and G7 have been frequently associated with human CE worldwide. Previous studies exploring the genetic variability and phylogeography of genotypes G6 and G7 have been based on relatively short mtDNA sequences, and the resolution of these studies has often been low. Moreover, using short sequences, the distinction between G6 and G7 has in some cases remained challenging. The aim here was to sequence complete mitochondrial genomes (mitogenomes) to obtain deeper insight into the genetic diversity, phylogeny and population structure of genotypes G6 and G7. We sequenced complete mitogenomes of 94 samples collected from 15 different countries worldwide. The results demonstrated that (i) genotypes G6 and G7 can be clearly distinguished when mitogenome sequences are used; (ii) G7 is represented by two major haplogroups, G7a and G7b, the latter being specific to islands of Corsica and Sardinia; (iii) intensive animal trade, but also geographical isolation, have likely had the largest impact on shaping the genetic structure and distribution of genotypes G6 and G7. In addition, we found phylogenetically highly divergent haplotype from Mongolia (Gmon), which had a higher affinity to G6.
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Affiliation(s)
- Teivi Laurimäe
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003 Tartu, Estonia
| | - Liina Kinkar
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003 Tartu, Estonia
| | - Thomas Romig
- Institute of Zoology, Parasitology Unit, University of Hohenheim, 70599 Stuttgart, Germany
| | - Rihab A Omer
- National University Research Institute, National University Sudan, Khartoum, Sudan
| | - Adriano Casulli
- World Health Organization Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis (in humans and animals), Istituto Superiore di Sanità, Viale Regina Elena 299, 00161 Rome, Italy; European Union Reference Laboratory for Parasites (EURLP), Istituto Superiore di Sanità, Viale Regina Elena 299, 00161 Rome, Italy
| | - Gérald Umhang
- Anses, Wildlife Surveillance and Eco-epidemiology Unit, National Reference Laboratory for Echinococcus spp., Nancy Laboratory for Rabies and Wildlife, 54220 Malzéville, France
| | - Robin B Gasser
- Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria 3010, Australia
| | - Abdul Jabbar
- Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria 3010, Australia
| | - Mitra Sharbatkhori
- Laboratory Science Research Center, Golestan University of Medical Sciences, Gorgan, Iran
| | - Hossein Mirhendi
- Department of Parasitology and Mycology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran
| | - Francisco Ponce-Gordo
- Department of Parasitology, Faculty of Pharmacy, Complutense University, Plaza Ramón y Cajal s/n, 28040 Madrid, Spain
| | - Lorena E Lazzarini
- Department of Microbiology and Parasitology, Faculty of Medical Sciences, Comahue National University, Buenos Aires, 1400, 8300 Neuquén, Argentina
| | - Silvia V Soriano
- Department of Microbiology and Parasitology, Faculty of Medical Sciences, Comahue National University, Buenos Aires, 1400, 8300 Neuquén, Argentina
| | - Antonio Varcasia
- Laboratorio di Parassitologia e Malattie Parassitarie, Ospedale Didattico Veterinario Dipartimento di Medicina Veterinaria, Università degli Studi di Sassari, Via Vienna 2, 07100 Sassari, Italy
| | - Mohammad Rostami Nejad
- Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Vanessa Andresiuk
- Laboratorio de Zoonosis Parasitarias, FCEyN, UNMdP, Funes 3350, CP: 7600, Mar del Plata, Buenos Aires, Argentina
| | - Pablo Maravilla
- Hospital General "Dr. Manuel Gea Gonzalez", Departamento de Ecologia de Agentes Patogenos, DF 14080, Mexico
| | - Luis Miguel González
- Parasitology Department, Centro Nacional de Microbiologia, Instituto de Salud Carlos III, Majadahonda, Madrid 28220, Spain
| | - Monika Dybicz
- Department of General Biology and Parasitology, 5 Chałubińskiego Str., 02-004 Warsaw, Medical University of Warsaw, Poland
| | - Jakub Gawor
- W. Stefański Institute of Parasitology, Polish Academy of Science, Twarda51/55, Warsaw 00-818, Poland
| | - Mindaugas Šarkūnas
- Department of Veterinary Pathobiology, Veterinary Academy, Lithuanian University of Health Sciences, Tilžes Street 18, 47181 Kaunas, Lithuania
| | - Viliam Šnábel
- Institute of Parasitology, Slovak Academy of Sciences, Košice, Hlinkova 3, 040 01 Košice, Slovakia
| | - Tetiana Kuzmina
- I.I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, 01030 Kyiv, Ukraine
| | - Urmas Saarma
- Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003 Tartu, Estonia.
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Maurelli MP, Bosco A, Pepe P, Ianniello D, Amadesi A, Cringoli G, Rinaldi L. Innovative tools for the diagnosis of Echinococcus granulosus in definitive hosts. Parasitol Res 2018; 117:2607-2612. [PMID: 29858944 DOI: 10.1007/s00436-018-5952-1] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/25/2018] [Accepted: 05/25/2018] [Indexed: 01/21/2023]
Abstract
The aim of this study was to develop and validate an innovative protocol for the diagnosis of Echinococcus granulosus and other Taeniidae in dogs. For this purpose, three experiments were performed, using faecal samples from naturally infected dogs. Firstly, the FLOTAC technique was calibrated with five flotation solutions: saturated sodium chloride (specific gravity, s.g. = 1.20), zinc sulphate (s.g. = 1.35), zinc chloride (s.g. = 1.45), Breza (s.g. = 1.30) and modified Breza (s.g. = 1.40). Then, FLOTAC was compared with four techniques of flotation in centrifuge using: zinc sulphate (s.g. = 1.20), Breza (s.g. = 1.30), modified Breza (s.g. = 1.40), and zinc chloride (s.g. = 1.45). Finally, four different protocols of DNA extraction were compared for Taeniidae identification: QIAamp Tissue Kit and QIAamp Stool from eggs; QIAamp Stool and Wizard Magnetic Purification System for Food from faeces. FLOTAC with zinc sulphate was the most efficient method to detect Taeniidae eggs, showing highest mean of eggs per gram (EPG) of faeces. The QIAamp Stool, using eggs concentrated by FLOTAC, was the best method for DNA extraction. The combination of these protocols provided the highest number of positive samples with PCR, i.e., 47/50 (94.0%). The three negative samples showed a low faecal egg count (2 EPG) below the detection limit (4 EPG) of the protocol. From sequencing of the 47 positive samples: 6 samples were identified as E. granulosus sensu stricto (s.s.), 28 as Taenia hydatigena and 6 as T. pisiformis. A co-infection between different genera of Taeniidae was found in 7 samples.
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Affiliation(s)
- Maria Paola Maurelli
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy.
| | - Antonio Bosco
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy
| | - Paola Pepe
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy
| | - Davide Ianniello
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy
| | - Alessandra Amadesi
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy
| | - Giuseppe Cringoli
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy
| | - Laura Rinaldi
- Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR Campania Region, Naples, Italy
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Conchedda M, Caddori A, Caredda A, Capra S, Bortoletti G. Degree of calcification and cyst activity in hepatic cystic echinococcosis in humans. Acta Trop 2018; 182:135-143. [PMID: 29486175 DOI: 10.1016/j.actatropica.2018.02.027] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/17/2017] [Revised: 02/15/2018] [Accepted: 02/23/2018] [Indexed: 12/28/2022]
Abstract
To evaluate the relationship between cyst activity and calcification degree in cystic echinococcosis (CE) in humans, 99 hepatic cysts at successive stages of involution, surgically excised from 72 Sardinian patients, have been analyzed. Cysts were classified into 4 groups according to calcification extent: CALC 0 (no calcification); CALC 1 (scattered punctate calcifications); CALC 2 (large coarse segmental/partial calcifications); CALC 3 (complete or nearly complete circumferential ring of calcification up to thick wall of osseous consistency/calcified content of cyst). In addition the possible correlation with antibody response has been explored analyzing IgG1, IgG4 and IgE produced against somatic PSCAg. Results showed that calcification is not restricted to the inactive WHO cyst types CE4 and CE5, but occurs to a varying extent in all morphotypes of metacestode, from active classic unilocular or multivesicular cysts to the more complicated and highly degenerate stages, where cyst wall appears massively calcified. Prevalence of calcification increases with progression of cyst degenerative process, but is not synonymous with parasite inactivity and can be misleading as signs of calcification may coexist with still metabolically active cysts. On the contrary, detection of entirely firmly solidified content seems a reliable indication of cyst inactivity. IgG4 is the dominant isotype associated particularly with the evolutive phase. Positive rates and OD levels, higher in active vs inactive stages, are stable or increase slightly in weakly and moderately calcified cysts (CALC 1/CALC 2), compared to non-calcified ones (CALC 0), strongly decreasing in highly calcified forms (CALC 3). In conclusion, evaluation of calcification extent may be pertinent for staging CE, and immunological tests, particularly for IgG4, and IgE may help to better define cyst activity.
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Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as two distinct species. Parasitology 2018; 145:1929-1937. [PMID: 29781421 DOI: 10.1017/s0031182018000719] [Citation(s) in RCA: 64] [Impact Index Per Article: 9.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/18/2023]
Abstract
Tapeworms of the species complex of Echinococcus granulosus sensu lato (s. l.) are the cause of a severe zoonotic disease - cystic echinococcosis, which is listed among the most severe parasitic diseases in humans and is prioritized by the World Health Organization. A stable taxonomy of E. granulosus s. l. is essential to the medical and veterinary communities for accurate and effective communication of the role of different species in this complex on human and animal health. E. granulosus s. l. displays high genetic diversity and has been divided into different species and genotypes. Despite several decades of research, the taxonomy of E. granulosus s. l. has remained controversial, especially the species status of genotypes G6-G10. Here the Bayesian phylogeny based on six nuclear loci (7387 bp in total) demonstrated, with very high support, the clustering of G6/G7 and G8/G10 into two separate clades. According to the evolutionary species concept, G6/G7 and G8/G10 can be regarded as two distinct species. Species differentiation can be attributed to the association with distinct host species, largely separate geographical distribution and low level of cross-fertilization. These factors have limited the gene flow between genotypic groups G6/G7 and G8/G10, resulting in the formation of distinct species. We discuss ecological and epidemiological differences that support the validity of these species.
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Prevalence and genotyping of Echinococcus granulosus in sheep in Narok County, Kenya. Parasitol Res 2018; 117:2065-2073. [PMID: 29736732 DOI: 10.1007/s00436-018-5889-4] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2017] [Accepted: 04/19/2018] [Indexed: 12/26/2022]
Abstract
Cystic echinococcosis (CE) is a zoonotic disease caused by the larval stage of Echinococcus granulosus species (sensu lato, s.l.). In East Africa, several species/strains occur in livestock, wildlife, and humans, but there is limited information on frequencies of infection by different genotypes in the various mammalian hosts. We have obtained data on E. granulosus infection prevalence in sheep sampled from abattoirs in Narok County, southern Kenya. We inspected carcasses for the presence of hydatid cysts in 180 sheep randomly selected in five sub-locations. The overall prevalence was 16.0% (144/900 animals), with the majority of cysts (50.7%) found in the liver, followed by the lungs (36.8%), while infections involving the liver and lungs were detected in 12.5% of the sheep. PCR-RFLP genotyping of the mitochondrial nad-1 gene in all the 343 cysts identified E. granulosus G1-G3 (sensu stricto, s.s.) as the only genotype. The majority of the cysts (62.1%) were fertile, and 35.2% were sterile, while 2.7% were calcified. Considering cyst fertility, 73.02% of lung cysts were fertile compared to 53.4% in liver cysts. Our data extends previous CE studies in livestock and indicates a high level of CE infection of sheep in Narok, with a predominance of E. granulosus s.s., which is highly pathogenic and commonly infects humans. Given the high fertility rates observed in the cysts, there is an urgent need to determine whether there is a significant incidence of human infection in Narok, and initiate "One Health" control measures.
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Abstract
AbstractAs a significant zoonosis, cystic echinococcosis (CE) is endemic in some parts of the world, such as the Middle East. There are studies on the prevalence of this infection in animal and human reservoirs in Iran; hence, we conducted this meta-analysis to elucidate the prevalence of CE in Iran. English (PubMed, Scopus, Web of Science, Science Direct and Google Scholar) and Persian (Magiran, Iran Medex, Iran Doc and SID) databases were explored. In the case of definitive, animal and human intermediate hosts, 37, 90 and 33 studies, respectively, have been included in the current review from January 1990 to December 2015. According to outcomes of the heterogeneity test, either Der Simonian and Laird's random-effects method or Mantel–Haenszel's fixed-effects method were employed to pool the estimations. The pooled prevalence ofEchinococcus granulosusinfection in definitive hosts was calculated as 23.6% (95% confidence interval (CI) = 17.6–30.1%). The weighted prevalence of animal and human hydatidosis was calculated as 15.6% (95% CI = 14.2–17.1%) and 4.2% (95% CI = 3.0–5.5%), respectively. Meanwhile, most cases of human hydatidosis were in southern Iran, with a prevalence of 5.8% (3.2–9.2%). In terms of human hydatidosis, more infections were found in rural regions, and mostly in female individuals. Egger's regression test revealed publication bias, with a remarkable impact on total prevalence of the infection in animal intermediate hosts (P< 0.001), while it was not significant in human hosts (P= 0.4) and definitive hosts (P= 0.3). According to the weighted estimated prevalence of cystic echinococcosis and its financial burden, implementing appropriate control programmes should be compulsory to decrease the burden of the disease in Iran.
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Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J, Thompson RCA, Jenkins EJ. Global Distribution of Alveolar and Cystic Echinococcosis. ADVANCES IN PARASITOLOGY 2017; 95:315-493. [PMID: 28131365 DOI: 10.1016/bs.apar.2016.11.001] [Citation(s) in RCA: 621] [Impact Index Per Article: 77.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 02/08/2023]
Abstract
Alveolar echinococcosis (AE) and cystic echinococcosis (CE) are severe helminthic zoonoses. Echinococcus multilocularis (causative agent of AE) is widely distributed in the northern hemisphere where it is typically maintained in a wild animal cycle including canids as definitive hosts and rodents as intermediate hosts. The species Echinococcus granulosus, Echinococcus ortleppi, Echinococcus canadensis and Echinococcus intermedius are the causative agents of CE with a worldwide distribution and a highly variable human disease burden in the different endemic areas depending upon human behavioural risk factors, the diversity and ecology of animal host assemblages and the genetic diversity within Echinococcus species which differ in their zoonotic potential and pathogenicity. Both AE and CE are regarded as neglected zoonoses, with a higher overall burden of disease for CE due to its global distribution and high regional prevalence, but a higher pathogenicity and case fatality rate for AE, especially in Asia. Over the past two decades, numerous studies have addressed the epidemiology and distribution of these Echinococcus species worldwide, resulting in better-defined boundaries of the endemic areas. This chapter presents the global distribution of Echinococcus species and human AE and CE in maps and summarizes the global data on host assemblages, transmission, prevalence in animal definitive hosts, incidence in people and molecular epidemiology.
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Affiliation(s)
- P Deplazes
- University of Zürich, Zurich, Switzerland
| | - L Rinaldi
- University of Naples Federico II, Napoli, Italy
| | | | | | - M F Harandi
- Research centre of Hydatid Disease in Iran, Kerman University of Medical Sciences, Kerman, Iran
| | - T Romig
- University of Hohenheim, Stuttgart, Germany
| | - D Antolova
- Institute of Parasitology SAS, Kosice, Slovak Republic
| | - J M Schurer
- University of Saskatchewan, Saskatoon, SK, Canada; University of Washington, Seattle, WA, United States
| | - S Lahmar
- National School of Veterinary Medicine, Sidi Thabet, Tunisia
| | - G Cringoli
- University of Naples Federico II, Napoli, Italy
| | - J Magambo
- Meru University of Science and Technology, Meru, Kenya
| | | | - E J Jenkins
- University of Saskatchewan, Saskatoon, SK, Canada
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Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, Wassermann M, Takahashi K, de la Rue M. Ecology and Life Cycle Patterns of Echinococcus Species. ADVANCES IN PARASITOLOGY 2017; 95:213-314. [PMID: 28131364 DOI: 10.1016/bs.apar.2016.11.002] [Citation(s) in RCA: 292] [Impact Index Per Article: 36.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Subscribe] [Scholar Register] [Indexed: 01/31/2023]
Abstract
The genus Echinococcus is composed of eight generally recognized species and one genotypic cluster (Echinococcus canadensis cluster) that may in future be resolved into one to three species. For each species, we review existing information on transmission routes and life cycles in different geographical contexts and - where available - include basic biological information of parasites and hosts (e.g., susceptibility of host species). While some Echinococcus spp. are transmitted in life cycles that involve predominantly domestic animals (e.g., dog - livestock cycles), others are wildlife parasites that do or do not interact with domestic transmission. In many cases, life cycle patterns of the same parasite species differ according to geography. Simple life cycles contrast with transmission patterns that are highly complex, involving multihost systems that may include both domestic and wild mammals. Wildlife transmission may be primary or secondary, i.e., resulting from spillovers from domestic animals. For most of the species and regions, existing information does not yet permit a conclusive description of transmission systems. Such data, however, would be highly relevant, e.g., for anticipation of geographical changes of the presence and frequency of these parasites in a warming world, or for initiating evidence-based control strategies.
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Affiliation(s)
- T Romig
- University of Hohenheim, Stuttgart, Germany
| | - P Deplazes
- University of Zürich, Zurich, Switzerland
| | - D Jenkins
- Charles Sturt University, Wagga Wagga, NSW, Australia
| | - P Giraudoux
- University of Franche-Comté and Institut Universitaire de France, Besancon, France
| | - A Massolo
- University of Calgary, Calgary, Alberta, Canada
| | - P S Craig
- University of Salford, Greater Manchester, United Kingdom
| | | | | | - M de la Rue
- University of Santa Maria, Santa Maria RS, Brazil
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High-resolution phylogeography of zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain. Parasitology 2016; 143:1790-1801. [PMID: 27572265 DOI: 10.1017/s0031182016001530] [Citation(s) in RCA: 47] [Impact Index Per Article: 5.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/07/2022]
Abstract
Echinococcus granulosus is the causative agent of cystic echinococcosis. The disease is a significant global public health concern and human infections are most commonly associated with E. granulosus sensu stricto (s. s.) genotype G1. The objectives of this study were to: (i) analyse the genetic variation and phylogeography of E. granulosus s. s. G1 in part of its main distribution range in Europe using 8274 bp of mtDNA; (ii) compare the results with those derived from previously used shorter mtDNA sequences and highlight the major differences. We sequenced a total of 91 E. granulosus s. s. G1 isolates from six different intermediate host species, including humans. The isolates originated from seven countries representing primarily Turkey, Italy and Spain. Few samples were also from Albania, Greece, Romania and from a patient originating from Algeria, but diagnosed in Finland. The analysed 91 sequences were divided into 83 haplotypes, revealing complex phylogeography and high genetic variation of E. granulosus s. s. G1 in Europe, particularly in the high-diversity domestication centre of western Asia. Comparisons with shorter mtDNA datasets revealed that 8274 bp sequences provided significantly higher phylogenetic resolution and thus more power to reveal the genetic relations between different haplotypes.
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A study of morphological aspects of cystic echinococcosis in sheep in Sardinia. Acta Trop 2016; 159:200-10. [PMID: 27060775 DOI: 10.1016/j.actatropica.2016.04.003] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/02/2015] [Revised: 03/15/2016] [Accepted: 04/05/2016] [Indexed: 12/28/2022]
Abstract
We have investigated the morphological and structural aspects of hydatid cysts recovered from sheep raised in southern Sardinia during two surveys conducted over the 20 years since the last control attempt at the end of the 1980s. In the first study carried out during 1995-1997, a few years after the last control attempt, a total of 10,334 cysts were examined, recovered from 1029 infected sheep out of a total of 1375 inspected (prevalence 74.84%). In the second survey, conducted ten years later during the period 2005-2010 in the absence of specific control measures, a total of 6249 cysts were recovered from 916 parasitized sheep out of the 1414 examined (prevalence 64.78%). Cysts were grouped into 5 different types: "Unilocular", "Multisepted", "Calcified", "Caseous", "Hyperlaminated". Unilocular: fertile, consist of a single fluid-filled cavity; multisepted: generally sterile, fluid filled, with cavity divided into spheroidal chambers (3-dozen); calcified: sterile, small, with internal chambers almost virtual due to the thickening of internal septa; caseous: sterile, the cavity filled with a thick yellowish matrix; hyperlaminated: sterile, with a virtual cavity filled with extensively folded and overlapping sheets of hyperproduced laminated tissue. A thorough knowledge and the precise characterization of each type of lesion, making it possible to establish detailed parameters for cyst classification, appears very useful for the harmonization of data collection. From a surveillance and control perspective it is proposed that, in addition to other relevant epidemiological information, data from meat inspection be further improved, including morpho-functional indications about cyst type.
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Cases of Echinococcus granulosus Sensu Stricto Isolated from Polish Patients: Imported or Indigenous? BIOMED RESEARCH INTERNATIONAL 2015; 2015:728321. [PMID: 26491683 PMCID: PMC4605230 DOI: 10.1155/2015/728321] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Received: 06/30/2015] [Revised: 08/21/2015] [Accepted: 09/16/2015] [Indexed: 11/17/2022]
Abstract
The cases of nine Polish patients with diagnosed cystic echinococcosis (CE) were examined. A total of nine isolates obtained postoperatively were investigated using PCR and sequencing. The mitochondrial region of nad1 gene was amplified. This PCR and sequencing analysis revealed the presence of Echinococcus canadensis G7 in seven patients and E. granulosus G1 in two patients. These data demonstrate that E. canadensis is the predominant causative agent of human cystic echinococcosis in Poland. E. granulosus G1 detection in Polish patients suggests that the parasite was imported; however it does not exclude the possibility that these cases could have been of Polish origin.
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Gori F, Armua-Fernandez MT, Milanesi P, Serafini M, Magi M, Deplazes P, Macchioni F. The occurrence of taeniids of wolves in Liguria (northern Italy). INTERNATIONAL JOURNAL FOR PARASITOLOGY-PARASITES AND WILDLIFE 2015; 4:252-5. [PMID: 26042204 PMCID: PMC4443502 DOI: 10.1016/j.ijppaw.2015.04.005] [Citation(s) in RCA: 22] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 03/16/2015] [Revised: 04/22/2015] [Accepted: 04/23/2015] [Indexed: 11/13/2022]
Abstract
Wolves are considered as definitive hosts for Echinococcus granulosus in Liguria, Italy. Scats were examinated and taeniid eggs isolated. Molecular species identification was performed through PCR analysis and sequencing. Taeniid species diagnosed document domestic, semi-domestic and wildlife cycles. Canids are definitive hosts of Taenia and Echinococcus species, which infect a variety of mammals as intermediate or accidental hosts including humans. Parasite transmission is based on domestic, semi-domestic and wildlife cycles; however, little is known of the epidemiological significance of wild large definitive hosts such as the wolf. In this study, 179 scats of wolves (Canis lupus italicus) collected throughout the Italian region of Liguria were analyzed for the detection of taeniid infection. Taeniid egg isolation was performed using a sieving/flotation technique, and the species level was identified by PCR (gene target: 12S rRNA and nad 1) followed by sequence analyses. Based on sequence homologies of ≥99%, Taenia hydatigena was identified in 19.6%, Taenia krabbei in 4.5%, Taenia ovis in 2.2%, Taenia crassiceps in 0.6%, Hydatigera taeniaeformis in 0.6% and Echinococcus granulosus in 5.6% of the samples. According to these results, Canis lupus italicus can be considered as involved in the wild (including cervids and rodents) and semi-domestic cycles (including sheep and goats) of taeniids in this area.
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Affiliation(s)
- Francesca Gori
- Department of Veterinary Science, Via Livornese (Lato Monte), 56122, San Piero a Grado Pisa, Italy ; Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland
| | | | - Pietro Milanesi
- Parco Naturale Regionale dell'Antola, Via XX Aprile 17, Villa Borzino, 16012, Busalla (GE), Italy
| | - Matteo Serafini
- Parco Naturale Regionale dell'Antola, Via XX Aprile 17, Villa Borzino, 16012, Busalla (GE), Italy
| | - Marta Magi
- Department of Veterinary Science, Via Livornese (Lato Monte), 56122, San Piero a Grado Pisa, Italy
| | - Peter Deplazes
- Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland
| | - Fabio Macchioni
- Department of Veterinary Science, Via Livornese (Lato Monte), 56122, San Piero a Grado Pisa, Italy
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Genetic characterization of human-derived hydatid cysts of Echinococcus granulosus sensu lato in Heilongjiang Province and the first report of G7 genotype of E. canadensis in humans in China. PLoS One 2014; 9:e109059. [PMID: 25329820 PMCID: PMC4199617 DOI: 10.1371/journal.pone.0109059] [Citation(s) in RCA: 30] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/13/2014] [Accepted: 08/29/2014] [Indexed: 12/21/2022] Open
Abstract
Cystic echinococcosis (CE) caused by the larval stage of Echinococcus granulosus sensu lato (s.l.) is one of the most important zoonotic parasitic diseases worldwide and 10 genotypes (G1–G10) have been reported. In China, almost all the epidemiological and genotyping studies of E. granulosus s.l. are from the west and northwest pasturing areas. However, in Heilongjiang Province of northeastern China, no molecular information is available on E. granulosus s.l. To understand and to speculate on possible transmission patterns of E. granulosus s.l., we molecularly identified and genotyped 10 hydatid cysts from hepatic CE patients in Heilongjiang Province based on mitochondrial cytochrome c oxidase subunit I (cox1), cytochrome b (cytb) and NADH dehydrogenase subunit 1 (nad1) genes. Two genotypes were identified, G1 genotype (n = 6) and G7 genotype (n = 4). All the six G1 genotype isolates were identical to each other at the cox1 locus; three and two different sequences were obtained at the cytb and nad1 loci, respectively, with two cytb gene sequences not being described previously. G7 genotype isolates were identical to each other at the cox1, cytb and nad1 loci; however, the cytb gene sequence was not described previously. This is the first report of G7 genotype in humans in China. Three new cytb gene sequences from G1 and G7 genotypes might reflect endemic genetic characterizations. Pigs might be the main intermediate hosts of G7 genotype in our investigated area by homology analysis. The results will aid in making more effective control strategies for the prevention of transmission of E. granulosus s.l.
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Molecular characterization and sequence analysis of Echinococcus granulosus from sheep isolates in East Azerbaijan province, northwest of Iran. J Parasit Dis 2014; 40:785-90. [PMID: 27605785 DOI: 10.1007/s12639-014-0579-3] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2014] [Accepted: 09/10/2014] [Indexed: 12/25/2022] Open
Abstract
Echinococcus granulosus as an etiologic agent of hydatid cyst is one of the most important zoonotic helminthes in the world that causing enormous economic and health losses. The aim of this study was to evaluate genotype of E. granulosus isolated from sheep using mitochondrial cytochrome c oxidase subunit 1 (cox1) gene and sequencing method in East Azerbaijan province, northwest of Iran. Nineteen sheep hydatid cyst samples were collected. Genomic DNA was extracted from protoscoleces using commercial DNA extraction kit. Mitochondrial cox1 region was amplified by polymerase chain reaction (PCR) and all isolates were sequenced. Afterward, sequences were analyzed for determination of genotypes by related software. G1 (94.73 %) and G3 (5.27 %) genotypes were identified from the isolates which out of 19 hydatid cysts, 17 samples were G1B, 1 sample G1D and the other one had G3 genotype. Results of this study indicate that common sheep strain (G1); especially G1B is the dominant subtype of E. granulosus in East Azerbaijan province.
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Umhang G, Chihai O, Boué F. Molecular characterization of Echinococcus granulosus in a hyperendemic European focus, the Republic of Moldova. Parasitol Res 2014; 113:4371-6. [DOI: 10.1007/s00436-014-4112-5] [Citation(s) in RCA: 22] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/02/2014] [Accepted: 08/26/2014] [Indexed: 11/30/2022]
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Boufana B, Lahmar S, Rebaï W, Ben Safta Z, Jebabli L, Ammar A, Kachti M, Aouadi S, Craig PS. Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Trans R Soc Trop Med Hyg 2014; 108:706-14. [DOI: 10.1093/trstmh/tru138] [Citation(s) in RCA: 61] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/15/2022] Open
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Umhang G, Richomme C, Hormaz V, Boucher JM, Boué F. Pigs and wild boar in Corsica harbor Echinococcus canadensis G6/7 at levels of concern for public health and local economy. Acta Trop 2014; 133:64-8. [PMID: 24556138 DOI: 10.1016/j.actatropica.2014.02.005] [Citation(s) in RCA: 29] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/31/2013] [Revised: 01/31/2014] [Accepted: 02/07/2014] [Indexed: 12/21/2022]
Abstract
Cystic echinococcosis (CE) is a parasitic zoonosis widespread in the Mediterranean area. The parasite is commonly maintained in a domestic cycle involving dogs and livestock species. As no new data have been made available for the last 15 years concerning the French Mediterranean island of Corsica, a cross-sectional survey at the slaughterhouse was conducted in 2009-2010 to describe the current presence of Echinococcus granulosus sensu lato in intermediate hosts. Only pig infections with the G6/7 genotype of Echinococcus canadensis were observed. No infection was detected in other breeding species but this should be interpreted with caution because 75% of the cows inspected during the survey were calves, and all sheep and goats were younger than two months old. In parallel four wild boars harvested during the 2010-2011 hunting season were also infected by the same genotype. These data constitute the first report of E. canadensis in France and the first molecular characterization of E. granulosus sensu lato in a wild species in France. The current prevalence observed in pigs (5.9%, n=2527) highlights the fact that CE is still of economic concern on Corsica, an island where certain regional products are produced using pig's liver ("Figatelli"). This prevalence, and the similar one observed in wild boars (4.0%, n=101), is a consequence of certain breeding practices and hunting practices which enable circulation of the parasite in the environment in close contact with humans.
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Echinococcus canadensis (G7) and Echinococcus granulosus sensu stricto (G1) in swine of southern Brazil. Vet Parasitol 2014; 202:335-8. [DOI: 10.1016/j.vetpar.2014.01.023] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2013] [Revised: 01/23/2014] [Accepted: 01/26/2014] [Indexed: 11/22/2022]
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42
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Molecular diagnosis of cystic echinococcosis in humans from central Poland. Parasitol Int 2013; 62:364-7. [DOI: 10.1016/j.parint.2013.03.005] [Citation(s) in RCA: 26] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2012] [Revised: 03/15/2013] [Accepted: 03/17/2013] [Indexed: 11/17/2022]
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43
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Echinococcus granulosus genotype G1 dominated in cattle and sheep during 2003-2006 in Buenos Aires province, an endemic area for cystic echinococcosis in Argentina. Acta Trop 2013; 127:136-42. [PMID: 23632259 DOI: 10.1016/j.actatropica.2013.04.008] [Citation(s) in RCA: 29] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2012] [Revised: 03/08/2013] [Accepted: 04/10/2013] [Indexed: 11/23/2022]
Abstract
Cystic echinococcosis (hydatidosis) is a severe and widespread disease, caused by the larval stage of the tapeworm Echinococcus granulosus; it affects large numbers of humans and farm animals annually, causing serious health and economic problems. Molecular studies have identified large genetic variation within the E. granulosus complex, with various hosts displaying different susceptibility to different genotypes. For the effective management of the disease, one of the most pressing tasks is to combine epidemiological and genetic data to better understand the role of different hosts and genotypes in the transmission of the parasite. The aim of the present study was to describe the epidemiology of cystic echinococcosis in cattle and sheep, and to characterise the genotypes of E. granulosus present in these farm animals. The study was carried out in the Pampa region of Argentina, with a particular focus on Buenos Aires province, where cystic echinococcosis represents an important human and veterinary health problem. Among 513 cattle and 792 sheep, 11.9% and 4.0%, respectively, were infected with E. granulosus. Genetic characterisation of 42 isolates from cattle and 34 isolates from sheep was carried out by sequencing mitochondrial cox1 and nad1 genes. The vast majority of isolates were identified as genotype G1, except for a single sheep isolate determined as genotype G2, and a single cattle isolate that corresponded to genotype G5. Genotype G1 has previously been found to be the most infectious genotype to humans. As G1 was also the genotype principally responsible for cystic echinococcosis in Buenos Aires province, these results have important implications for developing effective disease control programmes to improve human and animal healthcare in this region.
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Cardona GA, Carmena D. A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet Parasitol 2013; 192:10-32. [DOI: 10.1016/j.vetpar.2012.09.027] [Citation(s) in RCA: 146] [Impact Index Per Article: 12.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2012] [Revised: 08/31/2012] [Accepted: 09/18/2012] [Indexed: 11/29/2022]
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45
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Heath DD, Robinson C, Lightowlers MW. Maternal antibody parameters of cattle and calves receiving EG95 vaccine to protect against Echinococcus granulosus. Vaccine 2012; 30:7321-6. [DOI: 10.1016/j.vaccine.2012.08.076] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/02/2012] [Revised: 08/16/2012] [Accepted: 08/28/2012] [Indexed: 10/27/2022]
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46
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Prevalence and diversity of cystic echinococcosis in livestock in Maasailand, Kenya. Parasitol Res 2012; 111:2289-94. [DOI: 10.1007/s00436-012-3082-8] [Citation(s) in RCA: 47] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2012] [Accepted: 08/08/2012] [Indexed: 11/25/2022]
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47
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Grosso G, Gruttadauria S, Biondi A, Marventano S, Mistretta A. Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World J Gastroenterol 2012; 18:1425-37. [PMID: 22509074 PMCID: PMC3319938 DOI: 10.3748/wjg.v18.i13.1425] [Citation(s) in RCA: 195] [Impact Index Per Article: 15.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/02/2011] [Revised: 09/17/2011] [Accepted: 10/14/2011] [Indexed: 02/06/2023] Open
Abstract
The worldwide incidence and prevalence of cystic echinococcosis have fallen dramatically over the past several decades. Nonetheless, infection with Echinococcus granulosus (E. granulosus) remains a major public health issue in several countries and regions, even in places where it was previously at low levels, as a result of a reduction of control programmes due to economic problems and lack of resources. Geographic distribution differs by country and region depending on the presence in that country of large numbers of nomadic or semi-nomadic sheep and goat flocks that represent the intermediate host of the parasite, and their close contact with the final host, the dog, which mostly provides the transmission of infection to humans. The greatest prevalence of cystic echinococcosis in human and animal hosts is found in countries of the temperate zones, including several parts of Eurasia (the Mediterranean regions, southern and central parts of Russia, central Asia, China), Australia, some parts of America (especially South America) and north and east Africa. Echinococcosis is currently considered an endemic zoonotic disease in the Mediterranean region. The most frequent strain associated with human cystic echinococcosis appears to be the common sheep strain (G1). This strain appears to be widely distributed in all continents. The purpose of this review is to examine the distribution of E. granulosus and the epidemiology of a re-emerging disease such as cystic echinococcosis.
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48
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Sánchez E, Cáceres O, Náquira C, Miranda E, Samudio F, Fernandes O. Echinococcus granulosus genotypes circulating in alpacas (Lama pacos) and pigs (Sus scrofa) from an endemic region in Peru. Mem Inst Oswaldo Cruz 2012; 107:275-8. [DOI: 10.1590/s0074-02762012000200019] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/15/2011] [Accepted: 10/18/2011] [Indexed: 11/22/2022] Open
Affiliation(s)
| | | | - César Náquira
- Instituto Nacional de Salud, Peru; Universidad Nacional Mayor de San Marcos, Peru
| | | | - Franklyn Samudio
- Instituto Conmemorativo Gorgas de Estúdio de la Salud, Panamá; Fioruz, Brasil
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Hosseinzadeh S, Fazeli M, Hosseini A, Shahram Shekarforoush S. Molecular Characterization of <i>Echinococcus granulosus</i> in South of Iran. ACTA ACUST UNITED AC 2012. [DOI: 10.4236/ojvm.2012.24032] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022]
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50
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Varcasia A, Tanda B, Giobbe M, Solinas C, Pipia A, Malgor R, Carmona C, Garippa G, Scala A. Cystic Echinococcosis in Sardinia: Farmers’ knowledge and dog infection in sheep farms. Vet Parasitol 2011; 181:335-40. [DOI: 10.1016/j.vetpar.2011.05.006] [Citation(s) in RCA: 61] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/06/2010] [Revised: 04/30/2011] [Accepted: 05/05/2011] [Indexed: 10/18/2022]
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