|
1
|
Tukeni KN, Abadiko EA, Woyimo TG, Muleta GD. Cardiac Hydatid Cyst in a 34-Year-Old Ethiopian Woman With Heart Failure. JACC Case Rep 2025; 30:103105. [PMID: 40054956 PMCID: PMC11911885 DOI: 10.1016/j.jaccas.2024.103105] [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: 09/03/2024] [Revised: 10/21/2024] [Accepted: 10/29/2024] [Indexed: 03/20/2025]
Abstract
Although the majority of hydatid cysts are found in the liver and lungs, cardiac hydatid cysts, particularly those in the left ventricle and interventricular septum, pose unique challenges because of their extremely rare manifestation of cystic echinococcosis, critical location, and potential for serious complications. Although uncommon, a hydatic cyst of the heart should be investigated in a patient with an intracardiac mass-particularly if it is cystic-and in a patient with symptoms of heart failure caused by a mass shown in imaging examinations. We present a case of left ventricular hydatid cyst in a 34-year-old woman who had been complaining of worsening dyspnea, shortness of breath, orthopnea, and cough for 3 weeks.
Collapse
Affiliation(s)
- Kedir Negesso Tukeni
- Department of Internal Medicine, Division of Cardiology, Jimma University, Jimma, Ethiopia.
| | - Elias Ababulgu Abadiko
- Department of Internal Medicine, Division of Cardiology, Jimma University, Jimma, Ethiopia
| | - Tamirat Godebo Woyimo
- Department of Internal Medicine, Division of Cardiology, Jimma University, Jimma, Ethiopia
| | - Gaddisa Dessu Muleta
- Department of Internal Medicine, Division of Cardiology, Jimma University, Jimma, Ethiopia
| |
Collapse
|
|
2
|
Calu V, Enciu O, Toma EA, Pârvuleţu R, Pîrîianu DC, Miron A. Complicated Liver Cystic Echinococcosis-A Comprehensive Literature Review and a Tale of Two Extreme Cases. Tomography 2024; 10:922-934. [PMID: 38921947 PMCID: PMC11209078 DOI: 10.3390/tomography10060070] [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: 04/26/2024] [Revised: 06/02/2024] [Accepted: 06/07/2024] [Indexed: 06/27/2024] Open
Abstract
Cystic echinococcosis is a zoonotic parasitic disease that affects the liver in more than 70% of cases, and there is still an underestimated incidence in endemic areas. With a peculiar clinical presentation that ranges from paucisymptomatic illness to severe and possibly fatal complications, quality imaging and serological studies are required for diagnosis. The mainstay of treatment to date is surgery combined with antiparasitic agents. The surgical armamentarium consists of open and laparoscopic procedures for selected cases with growing confidence in parenchyma-sparing interventions. Endoscopic retrograde cholangiopancreatography (ERCP) is extremely useful for the diagnosis and treatment of biliary fistulas. Recent relevant studies in the literature are reviewed, and two complex cases are presented. The first patient underwent open surgery to treat 11 liver cysts, and during the follow-up, a right pulmonary cyst was diagnosed that was treated by minimally invasive surgery. The second case is represented by the peritoneal rupture of a giant liver cyst in a young woman who underwent laparoscopic surgery. Both patients developed biliary fistulas that were managed by ERCP. Both patients exhibited a non-specific clinical presentation and underwent several surgical procedures combined with antiparasitic agents, highlighting the necessity of customized treatment in order to decrease complications and successfully cure the disease.
Collapse
Affiliation(s)
- Valentin Calu
- Elias University Emergency Hospital, 011461 Bucharest, Romania; (V.C.); (E.-A.T.); (R.P.); (A.M.)
- Department of Surgery, Carol Davila University of Medicine and Pharmacy, 020021 Bucharest, Romania
| | - Octavian Enciu
- Elias University Emergency Hospital, 011461 Bucharest, Romania; (V.C.); (E.-A.T.); (R.P.); (A.M.)
- Department of Surgery, Carol Davila University of Medicine and Pharmacy, 020021 Bucharest, Romania
| | - Elena-Adelina Toma
- Elias University Emergency Hospital, 011461 Bucharest, Romania; (V.C.); (E.-A.T.); (R.P.); (A.M.)
- Department of Surgery, Carol Davila University of Medicine and Pharmacy, 020021 Bucharest, Romania
| | - Radu Pârvuleţu
- Elias University Emergency Hospital, 011461 Bucharest, Romania; (V.C.); (E.-A.T.); (R.P.); (A.M.)
| | - Dumitru Cătălin Pîrîianu
- Elias University Emergency Hospital, 011461 Bucharest, Romania; (V.C.); (E.-A.T.); (R.P.); (A.M.)
- Department of Surgery, Carol Davila University of Medicine and Pharmacy, 020021 Bucharest, Romania
| | - Adrian Miron
- Elias University Emergency Hospital, 011461 Bucharest, Romania; (V.C.); (E.-A.T.); (R.P.); (A.M.)
- Department of Surgery, Carol Davila University of Medicine and Pharmacy, 020021 Bucharest, Romania
| |
Collapse
|
|
3
|
Lucas JR, Cabrera M, Falcón N, Lucas O, Rodríguez A, Ramos D, Gavidia C. The role of cattle in the transmission of cystic echinococcosis in a highly endemic area of the Peruvian Andes. Vet Parasitol Reg Stud Reports 2024; 51:101021. [PMID: 38772638 DOI: 10.1016/j.vprsr.2024.101021] [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: 01/25/2024] [Revised: 04/07/2024] [Accepted: 04/10/2024] [Indexed: 05/23/2024]
Abstract
Cystic echinococcosis (CE) causes significant losses in Andean livestock production and affects Andean food security. However, more studies are needed to understand the epidemiology of the disease. In addition, the potential contribution of Andean cattle to the transmission of Echinococcus granulosus sensu lato needs to be known. This study aimed to determine the CE-prevalence and its association with risk factors, such as age and sex of the animals, the parasite load (number of cysts/organ) of condemned organs, and the viability and fertility of Echinococcus cysts from cattle in the Andes. The prevalence was examined in 348 cattle from an authorized slaughterhouse of Huancayo at 3300 m altitude. Cyst burden was determined by extracting all cysts from the total of the CE-infected organs. Cyst fertility and protoscolices viability were analysed from 90 randomly selected CE-infected organs. The CE prevalence was 35.6% (124/348; 95% CI: 30.6%-40.6%). There was no significant effect of age and sex on CE prevalence. CE was significantly more prevalent (p < 0.05) in lungs than livers, 34.8% (121/348; 95% CI: 29.8%-39.8%) vs 8.9% (31/348; 95% CI: 5.9%-11.9%). Most (75%) infected organs had one to five cysts. The mean cyst burden was significantly (p = 0.018) higher in the lungs than livers, 6.4 ± 4.9 vs 3.7 ± 2.9. Cyst fertility was 1.6% (10/608; 95% CI: 0.6%-2.6%). Despite the high CE prevalence, infected organs from Andean cattle play a minor role in CE transmission to dogs in the central Peruvian Andes.
Collapse
Affiliation(s)
- J Raúl Lucas
- Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Peru.
| | - Miguel Cabrera
- Facultad de Medicina Veterinaria y Zootecnia, Universidad Peruana Cayetano Heredia, Lima, Peru
| | - Néstor Falcón
- Facultad de Medicina Veterinaria y Zootecnia, Universidad Peruana Cayetano Heredia, Lima, Peru
| | - Orlando Lucas
- Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Peru
| | | | - Daphne Ramos
- Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Peru
| | - Cesar Gavidia
- Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Peru
| |
Collapse
|
|
4
|
Alvi MA, Ali RMA, Khan S, Saqib M, Qamar W, Li L, Fu BQ, Yan HB, Jia WZ. Past and Present of Diagnosis of Echinococcosis: A Review (1999-2021). Acta Trop 2023; 243:106925. [PMID: 37080264 DOI: 10.1016/j.actatropica.2023.106925] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/18/2023] [Revised: 03/17/2023] [Accepted: 04/08/2023] [Indexed: 04/22/2023]
Abstract
The larval forms of taeniid cestodes belonging to the genus Echinococcus are the source of the zoonotic infection known as echinococcosis. Alveolar and cystic echinococcosis are caused by Echinococcus multilocularis and Echinococcus granulosus (s. s) respectively. It is endemic in several regions of the world. In this systematic review, we describe diagnosis, and the species (human, canids, livestock, and small rodents) affected by cystic (CE) and alveolar echinococcosis (AE). From 1999 to 2021, we searched the online directory through PubMed, SCOPUS, Web of Science, and google scholar. Among the 37,700 records found in the online databases, 187 publications met our eligibility requirements. The majority of investigations employed a range of diagnostic methods, such as ELISA, imaging, copro-PCR, necropsy or arecoline hydrobromide purgation, morphological cestode confirmation, and fecal sieving/flotation to detect and confirm Echinococcus infection. ELISA was the most commonly used method followed by PCR, and imaging. The research team retrieved data describing the incidence or assessment of the diagnostic test for E. multilocularis in humans (N = 99), canids (N = 63), small ruminants (N = 13), large ruminants (N= 3), camel (N= 2), pigs (N=2) and small mammals (N= 5). This study was conducted to explore the diagnostic tools applied to detect echinococcosis in humans as well as animals in prevalent countries, and to report the characteristic of new diagnostic tests for disease surveillance. This systematic review revealed that ELISA (alone or in combination) was the most common method used for disease diagnosis and diagnostic efficacy and prevalence rate increased when recombinant antigens were used. It is highly recommended to use combination protcols such as serological with molecular and imaging technique to diagnose disease. Our study identified scarcity of data of reporting echinococcosis in humans/ animals in low-income or developing countries particularly central Asian countries. Study reports in small rodents indicate their role in disease dissemination but real situation in these host is not refected due to limited number of studies. Even though echinococcosis affects both public health and the domestic animal sector, therefore, it is important to devise new and strengthe implementation of the existing monitoring, judging, and control measures in this estimate.
Collapse
Affiliation(s)
- Mughees Aizaz Alvi
- State Key Laboratory of Veterinary Etiological Biology, 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
| | - Rana Muhammad Athar Ali
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | - Sadiq Khan
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | - Muhammad Saqib
- Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Pakistan
| | - Warda Qamar
- Department of Parasitology, University of Agriculture, Faisalabad, Pakistan
| | - Li Li
- State Key Laboratory of Veterinary Etiological Biology, College of Veterinary Medicine, Lanzhou University, National Para-reference Laboratory for Animal Echinococcosis, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China
| | - Bao-Quan Fu
- State Key Laboratory of Veterinary Etiological Biology, 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 of Veterinary Etiological Biology, 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 of Veterinary Etiological Biology, 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 Diseases and Zoonoses, Yangzhou, China.
| |
Collapse
|
|
5
|
Mutwiri T, Muigai AWT, Magambo J, Mulinge E, Gitau L, Muinde P, Bettridge JM, Rogan M, Fèvre EM, Falzon LC. The potential role of roaming dogs in establishing a geographically novel life cycle of taeniids (Echinococcus spp. and Taenia spp.) in a non-endemic area. Vet Parasitol Reg Stud Reports 2023; 38:100829. [PMID: 36725161 DOI: 10.1016/j.vprsr.2022.100829] [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: 08/28/2022] [Revised: 12/07/2022] [Accepted: 12/26/2022] [Indexed: 12/31/2022]
Abstract
INTRODUCTION Cystic Echinococcosis (CE) is endemic in humans and livestock in many pastoral communities in Kenya. The distribution of the disease is enhanced by several factors, including livestock trade, which has allowed for the spread of CE to non-endemic areas such as western Kenya. Dogs' roaming behaviour, with consequent contamination of the environment with intestinal parasites, could then lead to parasite establishment. This study examined dogs' infection levels with taeniid eggs and their potential role in contaminating the environment with intestinal parasites. METHODOLOGY We selected sixteen ruminant slaughterhouses in Busia and Bungoma Counties, and around each slaughterhouse we identified ten homesteads owning free-roaming dogs. We administered a questionnaire on dog management practices to the homestead owner and collected a faecal sample from the dog's rectum. In homesteads around 8 of the 16 slaughterhouses, we collared dogs with a GPS tracker to assess their movement patterns. The faecal samples were examined microscopically following zinc-chloride sieving-floatation technique for the presence of taeniid eggs and other canine intestinal parasites. Polymerase Chain Reaction - Restriction Fragment Length Polymorphism of NADH dehydrogenase subunit 1 gene and sequencing were used to confirm taeniid eggs identified during microscopy. Additionally, the Coproantigen-ELISA was used to detect the presence of taeniid antigen in a sub-set of the faecal samples. RESULTS Helminths detected in the 155 dogs sampled included hookworms (n = 92; 59.4%), ascarids (n = 15; 9.7%), and taeniids (n = 1; 0.6%). Through Copro-PCR, 13 eggs extracted from the sample of the only taeniid infected dog were sequenced and identified as E. canadensis (G6/7) [n = 1], Taenia multiceps [n = 1], and Taenia serialis [n = 6]; the remaining were indeterminate. Of the 77 faecal samples tested for E. granulosus sensu lato (s. l.) with the Copro-ELISA, 64 (83.1%) were negative, 12 (15.6%) were positive, while 1 (1.3%) was suspicious. The dogs travelled a median of 13.5 km daily, and 28 dogs visited the slaughterhouses during the 5-day recording period. CONCLUSION The results indicate a relatively high carriage of zoonotic parasites by free-roaming domestic dogs in western Kenya, which poses a risk to human and livestock populations. We report for the first time a domestic lifecycle of Echinococcus canadensis and Taenia multiceps in western Kenya, as well as a presumptive sylvatic cycle of coenurosis by T. serialis. We recommend an extensive and ongoing Copro-antigen survey of dog faeces, broader assessment of dog parasites with zoonotic potential, adherence to slaughterhouse management practices, and dog-ownership programmes to highlight the importance of deworming and restricted dog movements.
Collapse
Affiliation(s)
- Titus Mutwiri
- Jomo Kenyatta University of Agriculture and Technology, P.O. Box 60200, 00200 Nairobi, Kenya; International Livestock Research Institute, P.O. Box 30709, 00100 Nairobi, Kenya; Kenya Methodist University, P.O. Box 45240, 00100 Nairobi, Kenya.
| | - Anne W T Muigai
- Jomo Kenyatta University of Agriculture and Technology, P.O. Box 60200, 00200 Nairobi, Kenya
| | - Japhet Magambo
- Meru University of Science and Technology, P.O. Box 972, 60200 Meru, Kenya
| | - Erastus Mulinge
- Kenya Medical Research Institute, P.O. Box 54840, 00200 Nairobi, Kenya
| | - Lucy Gitau
- Kenya Medical Research Institute, P.O. Box 54840, 00200 Nairobi, Kenya
| | - Patrick Muinde
- International Livestock Research Institute, P.O. Box 30709, 00100 Nairobi, Kenya; World Animal Protection, P.O. Box 66580, 00800 Nairobi, Kenya
| | - Judy M Bettridge
- International Livestock Research Institute, P.O. Box 30709, 00100 Nairobi, Kenya; Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, United Kingdom; Natural Resources Institute, University of Greenwich, Chatham Maritime, United Kingdom
| | - Mike Rogan
- School of Science, Engineering, and Environment, University of Salford, United Kingdom
| | - Eric M Fèvre
- International Livestock Research Institute, P.O. Box 30709, 00100 Nairobi, Kenya; Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, United Kingdom.
| | - Laura C Falzon
- International Livestock Research Institute, P.O. Box 30709, 00100 Nairobi, Kenya; Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, United Kingdom
| |
Collapse
|
|
6
|
Manciulli T, Enríquez-Laurente R, Tamarozzi F, Lissandrin R, Elizalde M, Sedano C, Bardales K, Vola A, De Silvestri A, Tinelli C, Brunetti E, Santivanez S, Mariconti M. Field Performance of a Rapid Diagnostic Test for the Serodiagnosis of Abdominal Cystic Echinococcosis in the Peruvian Highlands. Am J Trop Med Hyg 2021; 105:181-187. [PMID: 34029208 PMCID: PMC8274789 DOI: 10.4269/ajtmh.21-0045] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2021] [Accepted: 02/11/2021] [Indexed: 11/07/2022] Open
Abstract
We evaluated the performance of a commercial rapid diagnostic test (RDT) in a field setting for the diagnosis of abdominal cystic echinococcosis (CE) using sera collected during an ultrasound population screening in a highly endemic region of the Peruvian Andes. Abdominal CE was investigated by ultrasonography. Sera collected from individuals with abdominal CE (cases) and age- and gender-matched volunteers with no abdominal CE (controls) were tested independently in two laboratories (Peru and Italy) using the VIRapid® HYDATIDOSIS RDT and RIDASCREEN® Echinococcus IgG enzyme-linked immunosorbent assay. Performance indexes of single and serially combined tests were calculated and applied to hypothetical screening and clinical scenarios. Test concordance was also evaluated. Prevalence of abdominal CE was 6.00% (33 of 546) by ultrasound. Serum was obtained from 33 cases and 81 controls. The VIRapid test showed similar sensitivity (76% versus 74%) and lower specificity (79% versus 96%) than results obtained in a hospital setting. RDTs showed better performance when excluding subjects reporting surgery for CE and if weak bands were considered negative. Concordance between tests was moderate to very good. In hypothetical screening scenarios, ultrasound alone or confirmed by RDTs provided more reliable prevalence figures than serology alone, which overestimated it by 5 to 20 times. In a simulation of case diagnosis with pre-test probability of CE of 50%, positive and negative post-test probabilities of the VIRapid test were 78% and 22%, respectively. The application of the VIRapid test alone would not be reliable for the assessment of population prevalence of CE, but could help clinical decision making in resource-limited settings.
Collapse
Affiliation(s)
- Tommaso Manciulli
- PhD School of Experimental Medicine, University of Pavia, Pavia, Italy
- Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
| | | | - Francesca Tamarozzi
- Department of Infectious-Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, Negrar, Verona, Italy
| | - Raffaella Lissandrin
- Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
| | - Maira Elizalde
- Instituto Peruano de Parasitologia Clinica y Experimental, Lima, Peru
| | - Cesar Sedano
- Instituto Peruano de Parasitologia Clinica y Experimental, Lima, Peru
| | - Karina Bardales
- Instituto Peruano de Parasitologia Clinica y Experimental, Lima, Peru
| | - Ambra Vola
- Unit of Infectious and Tropical Diseases, IRCCS San Matteo Hospital Foundation, Pavia, Italy
| | - Annalisa De Silvestri
- Unit of Epidemiology and Biostatistics, IRCCS San Matteo Hospital Foundation, Pavia, Italy
| | - Carmine Tinelli
- Unit of Epidemiology and Biostatistics, IRCCS San Matteo Hospital Foundation, Pavia, Italy
| | - Enrico Brunetti
- Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
- Unit of Infectious and Tropical Diseases, IRCCS San Matteo Hospital Foundation, Pavia, Italy
| | - Saul Santivanez
- Instituto Peruano de Parasitologia Clinica y Experimental, Lima, Peru
| | - Mara Mariconti
- Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
| |
Collapse
|
|
7
|
Tamarozzi F, Longoni SS, Vola A, Degani M, Tais S, Rizzi E, Prato M, Scarso S, Silva R, Brunetti E, Bisoffi Z, Perandin F. Evaluation of Nine Commercial Serological Tests for the Diagnosis of Human Hepatic Cyst Echinococcosis and the Differential Diagnosis with Other Focal Liver Lesions: A Diagnostic Accuracy Study. Diagnostics (Basel) 2021; 11:diagnostics11020167. [PMID: 33503986 PMCID: PMC7911993 DOI: 10.3390/diagnostics11020167] [Citation(s) in RCA: 21] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/05/2021] [Revised: 01/19/2021] [Accepted: 01/21/2021] [Indexed: 12/19/2022] Open
Abstract
The differential diagnosis of hepatic cystic echinococcosis (CE) may be challenging. When imaging is insufficient, serology can be applied, but no consensus diagnostic algorithm exists. We evaluated the performances of nine serological tests commercialized in Europe for the diagnosis of “echinococcosis”. We performed a diagnostic accuracy study using a panel of sera from patients with hepatic CE (n = 45 “liquid” content stages, n = 25 “solid” content stages) and non-CE focal liver lesions (n = 54 with “liquid” content, n = 11 with “solid” content). The diagnosis and staging of CE were based on ultrasound (gold standard). Nine commercial seroassays (5 ELISA, 2 WB, 1 Chemiluminescence Immunoassay [CLIA] and 1 Immunochromatographic test [ICT]) were the index tests. Sensitivity (Se) ranged from 43 to 94% and from 31 to 87%, and specificity (Sp) from 68 to 100% and from 94 to 100%, when borderline results were considered positive or negative, respectively. Three seroassays (2 ELISA, 1 WB) were excluded from further analyses due to poor performances. When tests were combined, Sp was 98–100%. The best results were obtained using the WB-LDBIO alone (Se 83%) or as a third test after two non-WB tests (Se 67–86%). A validated WB or two non-WB tests, read with stringent criteria (borderline = negative and considered positive only if concordant positive), possibly confirmed by the WB, appear sensible approaches.
Collapse
Affiliation(s)
- Francesca Tamarozzi
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
- Correspondence: ; Tel.: +39-0456013226
| | - Silvia Stefania Longoni
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Ambra Vola
- Department of Medical Sciences and Infectious Diseases, IRCCS San Matteo Hospital Foundation, 27100 Pavia, Italy; (A.V.); (E.B.)
| | - Monica Degani
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Stefano Tais
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Eleonora Rizzi
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Marco Prato
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Salvatore Scarso
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Ronaldo Silva
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| | - Enrico Brunetti
- Department of Medical Sciences and Infectious Diseases, IRCCS San Matteo Hospital Foundation, 27100 Pavia, Italy; (A.V.); (E.B.)
- Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, 27100 Pavia, Italy
| | - Zeno Bisoffi
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
- Department of Diagnostics and Public Health, University of Verona, 37129 Verona, Italy
| | - Francesca Perandin
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, 37024 Verona, Italy; (S.S.L.); (M.D.); (S.T.); (E.R.); (M.P.); (S.S.); (R.S.); (Z.B.); (F.P.)
| |
Collapse
|
|
8
|
Echinococcus granulosus sensu lato and Echinococcus multilocularis: A review. Res Vet Sci 2020; 135:517-522. [PMID: 33246571 DOI: 10.1016/j.rvsc.2020.11.010] [Citation(s) in RCA: 79] [Impact Index Per Article: 15.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/14/2020] [Revised: 11/12/2020] [Accepted: 11/17/2020] [Indexed: 12/12/2022]
Abstract
Echinococcus spp. have a global distribution and are found on every continent except Antarctica. Infections with these parasites are considered extremely serious, contributing to significant morbidity and mortality in addition to substantial economic losses to the livestock industry. Echinococcus granulosus sensu lato (s.l.) and Echinococcus multilocularis, causing cystic echinococcosis (CE) and alveolar echinococcosis (AE) respectively, are the two main species of interest from a human and veterinary perspective. This review collates the current state-of-the-art understanding of these two parasites within four key areas of relevance to human and veterinary professionals: transmission and epidemiology, clinical signs and pathogenesis, diagnosis, and treatment and prevention. This review should serve as a broad introduction to the most important Echinococcus spp. The reader is advised to seek out specific literature on individual diseases and their causative parasites for a deeper understanding.
Collapse
|
|
9
|
Dudha M, Shaikh Z, Bhaiyat M, Wadiwala IJ, Bhaiyat ZT. A Case of Echinococcal Cyst of the Lung. Respir Med Case Rep 2018; 25:286-292. [PMID: 30364676 PMCID: PMC6197673 DOI: 10.1016/j.rmcr.2018.10.007] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/21/2018] [Revised: 10/05/2018] [Accepted: 10/08/2018] [Indexed: 11/04/2022] Open
Abstract
Echinococcosis, also known as Hydatid disease, is caused by the larvae of the tapeworm Echinococcus. It is globally prevalent and is a major clinical health concern. It is endemic in most underdeveloped regions including Asia, the Mediterranean, South America and Africa. There are four species within the genus Echinococcus, with E. granulosus and E. multilocularis being the most common, causing Cystic Echinococcosis (CE) and Alveolar Echinococcosis (AE). The clinical presentation of the disease is non-specific. It commonly involves the liver, lungs, brain and adrenal glands. Pulmonary disease is significant for its propensity to affect children and young adults. This young population accounts for ∼50% of pulmonary hydatid cysts [1]. Cysts are known to grow extensively in size. Many patients are asymptomatic and have only a solitary cyst. Symptoms arise from enlargement of the cyst and from eroding and pressure applied by the cyst to blood vessels and organs. If rupture of the cyst occurs it can lead to immunologic reactions such as asthma and anaphylaxis. Echinococcus in the lung can pose diagnostic dilemmas, as their homogeneous density and tendency to occur alone may cause them to be confused with squamous cell carcinoma, adenocarcinoma, solitary metastasis, and abscess [2]. Our case is of such a patient who was found to have a 6 cm mass in the right middle lobe (RML) found on a chest X-ray during evaluation of back pain. Echinococcus should always be included in a differential diagnosis of any mass lesions especially in immigrant populations from endemic countries.
Collapse
Affiliation(s)
| | - Zakir Shaikh
- Surat Municipal Institute of Medical Education and Research, Surat, Gujarat, India
| | - Mohammed Bhaiyat
- Surat Municipal Institute of Medical Education and Research, Surat, Gujarat, India
| | - Ishaq J Wadiwala
- Surat Municipal Institute of Medical Education and Research, Surat, Gujarat, India
| | | |
Collapse
|
|
10
|
Brik K, Hassouni T, Youssir S, Baroud S, Elkharrim K, Belghyti D. Epidemiological study of Echinococcus granulosus in sheep in the Gharb plain (North-West of Morocco). J Parasit Dis 2018; 42:505-510. [PMID: 30538347 DOI: 10.1007/s12639-018-1026-7] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/16/2018] [Accepted: 08/09/2018] [Indexed: 12/20/2022] Open
Abstract
Hydatidosis is considered endemic in Morocco and caused serious health problems in ruminants. The aim of this research is to present an epidemiological study on echinococcosis in sheep. The study was carried out between April 2016 and May 2017. A total number of 1600 sheeps was examined via autopsy for Echinococcus granulosus in various slaughterhouses in the Gharb plain of Morocco. The Results of the study showed that the prevalence of cystic echinococcosis was 7.63%. The infection was not significant among sheep which age is < 1 year (2.67%), while it increases among those which age is from 1 to 3 years old (8.63%). It also grows significantly among sheep which age is over 3 years old (11.71%). Parasitized at 62%, the liver is the most affected organ followed by the lungs (38%). Protoscoleces are only found in liquid cysts and contribute to their fertility which is estimated at 66.66% in the liver and 57.74% in the lungs. In addition, the prevalence of calcified cysts is 12.24% in the liver and 21.11% in the lungs. Examination of the fertile cysts revealed a high level of Protoscoleces viability, whether it's in the liver (65.93%) or in the lungs (59.30%). This study also shows how the evolution of echinococcosis is closely linked to sex and age.
Collapse
Affiliation(s)
- Kamal Brik
- 1Laboratory of Agro-physiology, Biotechnology, Environment and Quality, Faculty of Sciences, Ibn Tofail University, BOX 133, 14000 Kenitra, Morocco
| | - Taoufik Hassouni
- Regional Center of the Trades of Education and Training, Team of Biology and Pedagogical Innovation, Meknes, Morocco
| | - Sanaa Youssir
- 1Laboratory of Agro-physiology, Biotechnology, Environment and Quality, Faculty of Sciences, Ibn Tofail University, BOX 133, 14000 Kenitra, Morocco
| | - Samir Baroud
- 1Laboratory of Agro-physiology, Biotechnology, Environment and Quality, Faculty of Sciences, Ibn Tofail University, BOX 133, 14000 Kenitra, Morocco
| | - Khadija Elkharrim
- 1Laboratory of Agro-physiology, Biotechnology, Environment and Quality, Faculty of Sciences, Ibn Tofail University, BOX 133, 14000 Kenitra, Morocco
| | - Driss Belghyti
- 1Laboratory of Agro-physiology, Biotechnology, Environment and Quality, Faculty of Sciences, Ibn Tofail University, BOX 133, 14000 Kenitra, Morocco
| |
Collapse
|
|
11
|
Tamarozzi F, Hou A, Morales ML, Giordani MT, Vilca F, Mozo K, Bascope R, White AC, Brunetti E, Chen L, Cabada MM. Prevalence and Risk Factors for Human Cystic Echinococcosis in the Cusco Region of the Peruvian Highlands Diagnosed Using Focused Abdominal Ultrasound. Am J Trop Med Hyg 2017; 96:1472-1477. [PMID: 28719254 DOI: 10.4269/ajtmh.16-0882] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/07/2022] Open
Abstract
AbstractLatin America is among the highly endemic regions for cystic echinococcosis (CE). In Peru, an estimated 1,139 disability-adjusted life years are lost annually from surgical treatment of CE. This is comparable with the combined total for Argentina, Brazil, Uruguay, and Chile. The prevalence of human infection has been investigated in the central Peruvian Andes, but there are no community-based screening data from other regions of Peru. We carried out a population survey in January 2015 using abdominal ultrasound to estimate the prevalence of abdominal CE in the Canas and Canchis provinces, in the Cusco region of Peru. Among 1,351 subjects screened, 41 (3%) had CE. There was significant variation between communities with similar socioeconomic features in a small geographical area. A history of CE was reported by 4.1% of the screened subjects, among whom 30.3% still had CE on ultrasound. Among patients reporting previous CE treatment, 14.9% had CE in active stages. Limited education, community of residence, and knowing people with CE in the community were associated with CE. These results demonstrate a significant burden of CE in the region and suggest the need for further investigations, control activities, and optimization of clinical management for CE in this area.
Collapse
Affiliation(s)
- Francesca Tamarozzi
- WHO Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy.,Department of Clinical Surgical Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
| | - Amy Hou
- Department of Medicine, Mount Auburn Hospital, Cambridge, Massachusetts
| | - Maria Luisa Morales
- Universidad Peruana Cayetano Heredia and University of Texas Medical Branch Collaborative Research Center in Cusco, Cusco, Peru
| | | | - Freddy Vilca
- Hospital Alfredo Callo Rodriguez de Sicuani, Cusco, Peru
| | - Karen Mozo
- Universidad Peruana Cayetano Heredia and University of Texas Medical Branch Collaborative Research Center in Cusco, Cusco, Peru
| | - Ruben Bascope
- Programa de Control de Enfermedades Zoonoticas, Direccion Regional de Salud Cusco, Cusco, Peru
| | - A Clinton White
- Division of Infectious Diseases, Department of Medicine, University of Texas Medical Branch, Galveston, Texas
| | - Enrico Brunetti
- Department of Clinical Surgical Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy.,WHO Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy.,Division of Infectious and Tropical Diseases, San Matteo Hospital Foundation, Pavia, Italy
| | - Lin Chen
- Travel Medicine Center, Mount Auburn Hospital, Cambridge, Massachusetts.,Harvard Medical School, Boston, Massachusetts
| | - Miguel M Cabada
- Division of Infectious Diseases, Department of Medicine, University of Texas Medical Branch, Galveston, Texas.,Universidad Peruana Cayetano Heredia and University of Texas Medical Branch Collaborative Research Center in Cusco, Cusco, Peru
| |
Collapse
|
|
12
|
Merino V, Falcón N, Morel N, González G. Detección de coproantígenos de Echinococcus granulosus en canes de trabajadores de camales y comercializadores de vísceras en Lima metropolitana. Rev Panam Salud Publica 2017. [PMID: 28443998 PMCID: PMC6645243 DOI: 10.26633/rpsp.2017.10] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/24/2022] Open
Abstract
Objetivo. Demostrar la presencia de Echinoccocus granulosus en el hospedero definitivo en la ciudad de Lima, Perú, mediante la detección de antígenos del parásito en heces de canes pertenecientes a trabajadores y comercializadores de vísceras de centros de beneficio autorizados en Lima metropolitana.
Métodos. Se recolectaron muestras de heces de 58 canes, que fueron evaluadas utilizando la técnica coproELISA para detectar antígenos secretorio/excretorio de E. granulosus. Mediante una encuesta se obtuvo información sobre las prácticas de alimentación y el manejo de las mascotas.
Resultados. El 13,8% (8/58) de canes fue positivo a E. granulosus. En 27,8% (5/18) de los hogares se encontró al menos un animal positivo y se estimó que en las familias que tenían más de cuatro canes las posibilidades de encontrar al menos uno positivo eran mayores. En todos los hogares con al menos un can positivo sus mascotas se alimentaban con vísceras. El 94,4% (17) de los participantes no tenía conocimiento de las formas de contagio de la equinococosis.
Conclusiones. Los resultados muestran la presencia de hospederos definitivos en la zona urbana de Lima y subrayan la necesidad de aumentar la difusión de las prácticas para evitar la transmisión del parasito.
Collapse
Affiliation(s)
- Veronika Merino
- Facultad de Medicina Veterinaria y Zootecnia, Universidad Peruana Cayetano Heredia, Lima, Perú
| | | | - Noelia Morel
- Comisión Nacional de Zoonosis, Ministerio de Salud Pública, Montevideo, Uruguay
| | - Gualberto González
- Cátedra de Inmunología de la Facultad de Química, Instituto de Higiene, Universidad de la República, Montevideo, Uruguay
| |
Collapse
|
|
13
|
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: 626] [Impact Index Per Article: 78.3] [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.
Collapse
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
| |
Collapse
|
|
14
|
Abstract
Echinococcosis, caused by the zoonotic cestodes Echinococcus granulosus (sensu lato) and Echinococcus multilocularis, is highly endemic in the Central Asian Republic of Kyrgyzstan, and is being identified increasingly as a public health problem, especially amongst pastoral communities. As domestic dogs are considered to be the main source of human infection, the identification of potential transmission pathways is of relevance when considering implementing an echinococcosis control scheme. The current report describes the results of an analytical study of canine Echinococcus coproantigen enzyme-linked immunosorbent assay (ELISA) prevalence in the Alay valley of southern Kyrgyzstan prior to the commencement of regular praziquantel dosing of dogs. A logistic regression model using a form of Bayes modal estimation was used to identify possible risk factors for coproantigen positivity, and the output was interpreted in a Bayesian context (posterior distributions of the coefficients of interest). The study found that sheepdogs had lower odds of coproantigen positivity, as did dogs in households with donkeys, where owners had knowledge of echinococcosis, and households which engaged in home slaughtering. Surprisingly, there was no evidence of an association between free roaming or previous praziquantel dosing and coproantigen positivity, as has been found in previous studies. Possible reasons for these findings are discussed in the context of the epidemiology of echinococcosis and potential intervention approaches.
Collapse
|
|
15
|
Iraqi W. Diagnostic value of semi-purified antigens of hydatid cyst fluid in human cystic echinococcosis. Acta Parasitol 2016; 61:144-50. [PMID: 26751885 DOI: 10.1515/ap-2016-0019] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/07/2015] [Accepted: 10/07/2015] [Indexed: 11/15/2022]
Abstract
Cystic Echinococcosis (CE) is an infection caused by the larval stage of Echinococcus granulosus. The diagnosis of this disease has been problematic. Serological tests detecting antibodies against E. granulosus are the most popular and mainly use the crude Hydatid Cyst Fluid (HCF) or its components, Ag 5 and B. However, the diagnostic value of these tests is limited by the problems of specificity and/or sensitivity. The use of purified HCF antigens could be more helpful in the serodiagnosis of CE compared to the whole HCF. In the present study, we have evaluated the diagnostic value of semi-purified antigens using ELISA tests. Our results have shown that the 53 KDa antigen gave the best specificity (97.5%) and sensitivity (80%). We have also used Western Blot technique to analyze the serological profile against HCF. The results have confirmed that the most immunogenic component of HCF is the Ag 5.
Collapse
|
|
16
|
Arce MA, Limaylla H, Valcarcel M, Garcia HH, Santivañez SJ. Primary Giant Splenic Echinococcal Cyst Treated by Laparoscopy. Am J Trop Med Hyg 2016; 94:161-165. [PMID: 26556833 PMCID: PMC4710423 DOI: 10.4269/ajtmh.13-0505] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/02/2013] [Accepted: 09/30/2015] [Indexed: 12/28/2022] Open
Abstract
Cystic echinococcosis (CE) is a zoonosis caused by the larval stage of the dog tapeworm Echinococcus granulosus. Liver and lungs are the most commonly affected organs whereas splenic infection is rarer and its primary involvement occurs in less than 2% of abdominal CE. We report a case of primary giant splenic hydatid cyst in a 75-year-old Peruvian woman that was laparoscopically removed without any complications, perioperative prophylactic chemotherapy with albendazole 400 mg twice a day 5 days before, and 7 days after the surgical procedure was administered, postoperative recovery was uneventful, and; at her 3-month follow-up the patient remains asymptomatic and an abdominal computed tomography scan demonstrated a cystic cavity of 15 cm diameter with no daughter vesicles, neither other abdominal organ involvement. This case is in line with the existing literature on laparoscopical treatment of splenic cystic hydatid disease, suggesting that laparoscopical treatment is a safe and effective approach for large splenic hydatid cysts to be preferred to open surgical techniques.
Collapse
Affiliation(s)
- Maira A Arce
- Instituto Peruano de Parasitologia Clinica y Experimental (INPPACE), Lima, Perú; Department of Surgery, Hospital Nacional Dos de Mayo, Lima, Perú; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Perú; Center for Global Health, Tumbes, Universidad Peruana Cayetano Heredia, Lima, Perú; Cysticercosis Unit, Instituto Nacional de Ciencias Neurologicas, Lima, Perú
| | - Himerón Limaylla
- Instituto Peruano de Parasitologia Clinica y Experimental (INPPACE), Lima, Perú; Department of Surgery, Hospital Nacional Dos de Mayo, Lima, Perú; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Perú; Center for Global Health, Tumbes, Universidad Peruana Cayetano Heredia, Lima, Perú; Cysticercosis Unit, Instituto Nacional de Ciencias Neurologicas, Lima, Perú
| | - Maria Valcarcel
- Instituto Peruano de Parasitologia Clinica y Experimental (INPPACE), Lima, Perú; Department of Surgery, Hospital Nacional Dos de Mayo, Lima, Perú; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Perú; Center for Global Health, Tumbes, Universidad Peruana Cayetano Heredia, Lima, Perú; Cysticercosis Unit, Instituto Nacional de Ciencias Neurologicas, Lima, Perú
| | - Hector H Garcia
- Instituto Peruano de Parasitologia Clinica y Experimental (INPPACE), Lima, Perú; Department of Surgery, Hospital Nacional Dos de Mayo, Lima, Perú; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Perú; Center for Global Health, Tumbes, Universidad Peruana Cayetano Heredia, Lima, Perú; Cysticercosis Unit, Instituto Nacional de Ciencias Neurologicas, Lima, Perú
| | - Saul J Santivañez
- Instituto Peruano de Parasitologia Clinica y Experimental (INPPACE), Lima, Perú; Department of Surgery, Hospital Nacional Dos de Mayo, Lima, Perú; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Perú; Center for Global Health, Tumbes, Universidad Peruana Cayetano Heredia, Lima, Perú; Cysticercosis Unit, Instituto Nacional de Ciencias Neurologicas, Lima, Perú
| |
Collapse
|
|
17
|
Abstract
Diagnosis and detection of Echinococcus granulosus (sensu lato) infection in animals is a prerequisite for epidemiological studies and surveillance of echinococcosis in endemic, re-emergent or emergent transmission zones. Advances in diagnostic approaches for definitive hosts and livestock, however, have not progressed equally over the last 20 years. Development of laboratory based diagnostics for canids using coproantigen ELISA and also coproPCR, have had a huge impact on epidemiological studies and more recently on surveillance during hydatid control programmes. In contrast, diagnosis of cystic echinococcosis (CE) in livestock still relies largely on conventional post-mortem inspection, despite a relatively low diagnostic sensitivity especially in early infections, as current serodiagnostics do not provide a sufficiently specific and sensitive practical pre-mortem alternative. As a result, testing of dog faecal samples by coproantigen ELISA, often combined with mass ultrasound screening programmes for human CE, has been the preferred approach for monitoring and surveillance in resource-poor endemic areas and during control schemes. In this article we review the current options and approaches for diagnosis of E. granulosus infection in definitive and animal intermediate hosts (including applications in non-domesticated species) and make conclusions and recommendations for further improvements in diagnosis for use in epidemiological studies and surveillance schemes.
Collapse
|
|
18
|
Stewart BT, Jacob J, Finn T, Lado M, Napoleon R, Brooker S, Sidhu PS, Kolaczinski J. Cystic echinococcosis in Mundari tribe-members of South Sudan. Pathog Glob Health 2013; 107:293-8. [PMID: 24139620 DOI: 10.1179/2047773213y.0000000111] [Citation(s) in RCA: 10] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/31/2022] Open
Abstract
Many neglected tropical diseases, including the zoonotic disease cystic echinococcosis (hydatidosis), are endemic to East Africa. However, their geographical distribution is heterogenous and incompletely characterized. The aim of this study was to determine if Mundari pastoralists harbor endemic human hydatidosis. The survey was conducted in cattle camps randomly selected from accessible sites provided by officials in Terekeka, South Sudan. Following informed consent, a questionnaire collected demographic data and hydatid exposure risk. A systematic sonographic abdominal exam was performed using General Electric's LOGIQ Book XP with a 3C-RS 2-5 MHz curvilinear transducer. Six hundred and ten individuals were screened from 13 camps. Four infections were identified, all in women. The prevalence of abdominal hydatid disease in the Mundari tribe-members in cattle camps was 0·7% and all individuals reporting at least one high-risk exposure to hydatid disease. Cystic echinococcosis is endemic among Mundari pastoralists; however, it would appear to be less endemic than in neighboring tribes.
Collapse
|
|
19
|
Otero-Abad B, Torgerson PR. A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis 2013; 7:e2249. [PMID: 23755310 PMCID: PMC3674998 DOI: 10.1371/journal.pntd.0002249] [Citation(s) in RCA: 185] [Impact Index Per Article: 15.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/17/2012] [Accepted: 04/23/2013] [Indexed: 12/12/2022] Open
Abstract
BACKGROUND Human echinococcosis is a neglected zoonosis caused by parasites of the genus Echinococcus. The most frequent clinical forms of echinococcosis, cystic echinococcosis (CE) and alveolar echinococcosis (AE), are responsible for a substantial health and economic burden, particularly to low-income societies. Quantitative epidemiology can provide important information to improve the understanding of parasite transmission and hence is an important part of efforts to control this disease. The purpose of this review is to give an insight on factors associated with echinococcosis in animal hosts by summarising significant results reported from epidemiological studies identified through a systematic search. METHODOLOGY AND PRINCIPAL FINDINGS The systematic search was conducted mainly in electronic databases but a few additional records were obtained from other sources. Retrieved entries were examined in order to identify available peer-reviewed epidemiological studies that found significant risk factors for infection using associative statistical methods. One hundred studies met the eligibility criteria and were suitable for data extraction. Epidemiological factors associated with increased risk of E. granulosus infection in dogs included feeding with raw viscera, possibility of scavenging dead animals, lack of anthelmintic treatment and owners' poor health education and indicators of poverty. Key factors associated with E. granulosus infection in intermediate hosts were related to the hosts' age and the intensity of environmental contamination with parasite eggs. E. multilocularis transmission dynamics in animal hosts depended on the interaction of several ecological factors, such as hosts' population densities, host-prey interactions, landscape characteristics, climate conditions and human-related activities. CONCLUSIONS/SIGNIFICANCE Results derived from epidemiological studies provide a better understanding of the behavioural, biological and ecological factors involved in the transmission of this parasite and hence can aid in the design of more effective control strategies.
Collapse
Affiliation(s)
- Belen Otero-Abad
- Vetsuisse-Faculty, University of Zurich, Section for Veterinary Epidemiology, Zurich, Switzerland
| | - Paul R. Torgerson
- Vetsuisse-Faculty, University of Zurich, Section for Veterinary Epidemiology, Zurich, Switzerland
| |
Collapse
|
|
20
|
Budke CM, Carabin H, Ndimubanzi PC, Nguyen H, Rainwater E, Dickey M, Bhattarai R, Zeziulin O, Qian MB. A systematic review of the literature on cystic echinococcosis frequency worldwide and its associated clinical manifestations. Am J Trop Med Hyg 2013; 88:1011-27. [PMID: 23546806 DOI: 10.4269/ajtmh.12-0692] [Citation(s) in RCA: 120] [Impact Index Per Article: 10.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022] Open
Abstract
A systematic literature review of cystic echinoccocosis (CE) frequency and symptoms was conducted. Studies without denominators, original data, or using one serological test were excluded. Random-effect log-binomial models were run for CE frequency and proportion of reported symptoms where appropriate. A total of 45 and 25 articles on CE frequency and symptoms met all inclusion criteria. Prevalence of CE ranged from 1% to 7% in community-based studies and incidence rates ranged from 0 to 32 cases per 100,000 in hospital-based studies. The CE prevalence was higher in females (Prevalence Proportion Ratio: 1.35 [95% Bayesian Credible Interval: 1.16-1.53]) and increased with age. The most common manifestations of hepatic and pulmonary CE were abdominal pain (57.3% [95% confidence interval [CI]: 37.3-76.1%]) and cough (51.3% [95% CI: 35.7-66.7%]), respectively. The results are limited by the small number of unbiased studies. Nonetheless, the age/gender prevalence differences could be used to inform future models of CE burden.
Collapse
Affiliation(s)
- Christine M Budke
- Department of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, TX 77843, USA.
| | | | | | | | | | | | | | | | | |
Collapse
|
|
21
|
Salant H, Abbasi I, Hamburger J. The development of a loop-mediated isothermal amplification method (LAMP) for Echinococcus granulosus [corrected] coprodetection. Am J Trop Med Hyg 2012; 87:883-7. [PMID: 22987649 DOI: 10.4269/ajtmh.2012.12-0184] [Citation(s) in RCA: 36] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/28/2022] Open
Abstract
We have previously developed a polymerase chain reaction (PCR) assay for detection of Echinococcus granulosus infection, which proved very sensitive and specific for identification of infected dogs. We have now developed a loop-mediated isothermal amplification (LAMP) assay, which amplifies the same genomic repeated sequences of E. granulosus for coprodetection. This assay enabled detection of a single egg in fecal samples and showed high species specificity for E. granulosus with no cross-amplification of DNA from closely related helminths, including Echinococcus multilocularis. Because the method does not require thermocycling for DNA amplification, or electrophoresis for amplicon detection, it can potentially be used for premortem identification of E. granulosus-infected dogs to enable large-scale surveys in endemic countries where highly specialized equipment to undertake PCR analysis is rare.
Collapse
Affiliation(s)
- Harold Salant
- Department of Molecular Genetics, Hebrew University-Hadassah Medical School, Jerusalem, Israel.
| | | | | |
Collapse
|
|
22
|
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.
Collapse
|
|
23
|
Abstract
Background Cystic echinococcosis (CE) constitutes an important public health problem in Peru. However, no studies have attempted to estimate the monetary and non-monetary impact of CE in Peruvian society. Methods We used official and published sources of epidemiological and economic information to estimate direct and indirect costs associated with livestock production losses and human disease in addition to surgical CE-associated disability adjusted life years (DALYs) lost. Findings The total estimated cost of human CE in Peru was U.S.$2,420,348 (95% CI:1,118,384–4,812,722) per year. Total estimated livestock-associated costs due to CE ranged from U.S.$196,681 (95% CI:141,641–251,629) if only direct losses (i.e., cattle and sheep liver destruction) were taken into consideration to U.S.$3,846,754 (95% CI:2,676,181–4,911,383) if additional production losses (liver condemnation, decreased carcass weight, wool losses, decreased milk production) were accounted for. An estimated 1,139 (95% CI: 861–1,489) DALYs were also lost due to surgical cases of CE. Conclusions This preliminary and conservative assessment of the socio-economic impact of CE on Peru, which is based largely on official sources of information, very likely underestimates the true extent of the problem. Nevertheless, these estimates illustrate the negative economic impact of CE in Peru. Cystic echinococcosis (CE), caused by infection with the larval stage of the cestode Echinococcus granulosus, constitutes an important public health problem in Peru. Despite its high prevalence in endemic communities no studies have attempted to estimate the economic impact of CE in Peruvian society. We used official and published sources of epidemiological and economic information to estimate direct and indirect costs associated with livestock production losses and human disease. We also used disability adjusted life years (DALYs) which is an overall measure of disease burden, expressed as number of years lost due to ill-health, disability or early death due to CE. We found that the total estimated cost of human CE in Peru was U.S.$2,420,348 per year. Total estimated livestock-associated costs due to CE ranged from U.S.$196,681 to U.S.$3,846,754. An estimated 1,139 DALYs were also lost due to surgical cases of CE which is comparable to DALY losses from Amebiasis or Malaria in Peru. This conservative assessment found significant economic losses caused by this CE in Peruvian society. The findings of this study are important as these data can serve to prioritize those areas that may need to be targeted in a control program.
Collapse
|
|
24
|
Sutherland JE, Sutphin D, Redican K, Rawlins F. Telesonography: foundations and future directions. JOURNAL OF ULTRASOUND IN MEDICINE : OFFICIAL JOURNAL OF THE AMERICAN INSTITUTE OF ULTRASOUND IN MEDICINE 2011; 30:517-522. [PMID: 21460152 DOI: 10.7863/jum.2011.30.4.517] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/30/2023]
Abstract
The practice of telesonography has yielded promising results in several domestic and international projects aimed at providing basic sonography services. Common themes that recur within telesonography-based research include the quality of transmitted images, clinical applications, and technical and nontechnical barriers to implementation. The research base continues to grow in concert with expanding telecommunications capabilities and refinement of small portable sonographic devices. Persistent barriers to the deployment of telesonography systems include a lack of telecommunications access, a lack of standard training and operational protocols, and a paucity of research regarding the long-term health impact of telesonography within target communities. Telesonography may be used directly to improve the standard of care within a given community; however, limited resources and interest may prevent sustained operations. Future projects may use telesonography to supplement the training of health care providers in remote locations in an effort to establish permanent sonography services for their respective communities.
Collapse
Affiliation(s)
- James E Sutherland
- Edward Via Virginia College of Osteopathic Medicine, Virginia Polytechnic Institute, Blacksburg, Virginia, USA.
| | | | | | | |
Collapse
|
|
25
|
Sutherland JE, Sutphin HD, Rawlins F, Redican K, Burton J. A comparison of telesonography with standard ultrasound care in a rural Dominican clinic. J Telemed Telecare 2009; 15:191-5. [PMID: 19471031 DOI: 10.1258/jtt.2009.080909] [Citation(s) in RCA: 13] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
Abstract
We compared telesonography to usual patient care in a rural clinic in the Dominican Republic. A total of 108 low-income Dominican and Haitian patients volunteered to participate. The patients were randomly assigned to either telesonography or control groups. Patients in the telesonography group were scanned and sonographic images and Request for Interpretation (RFI) forms were sent by email to six volunteer radiologists in the USA. Completed RFI forms were transmitted back to the clinic at the radiologists' earliest convenience. Patients in the control group received an ordinary ultrasound referral, which required travel to a tertiary medical centre where their scans were completed by a local sonographer. Sonographic reports from the control group were hand delivered to the referring physician at patient follow-up. The telesonography system provided a four-fold increase in the proportion of patient follow-ups and a six-fold increase in the proportion of returned radiological reports. In the telemedicine group, the median total elapsed time from referral to report return was 17.8 h (interquartile range, IQR 12.2-27.1) and the median time to patient follow-up was 67.1 h (IQR 45.9-113.7). The latter was similar in the control group, where the median total elapsed time was 76.7 h (IQR 65.8-144.7). The pilot study demonstrated that store-and-forward telesonography reduced time to diagnosis and increased the continuity of care compared to the usual ultrasound referral system in the region of the Dominican Republic which was studied.
Collapse
Affiliation(s)
- James Eric Sutherland
- Department of International and Appalachian Outreach, Edward Via Virginia College of Osteopathic Medicine, Blacksburg, Virginia, USA.
| | | | | | | | | |
Collapse
|
|
26
|
Torgerson PR, Deplazes P. Echinococcosis: diagnosis and diagnostic interpretation in population studies. Trends Parasitol 2009; 25:164-70. [PMID: 19269248 DOI: 10.1016/j.pt.2008.12.008] [Citation(s) in RCA: 82] [Impact Index Per Article: 5.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/25/2008] [Revised: 12/10/2008] [Accepted: 12/16/2008] [Indexed: 12/13/2022]
Abstract
Diagnosis is a basic component of population studies on echinococcosis. Other than careful necropsy in animals, there is no perfect gold standard. In the definitive host, techniques for direct parasite identification include copro-antigen and copro-DNA detection. In intermediate hosts, necropsy is typically used. In humans, diagnostic imaging and serology are both widely employed. The use of multiple parallel testing or an additional confirmatory test (or tests) in a diagnostic strategy can overcome the lack of a perfect gold standard. This will yield valuable information at population and individual levels, providing the study is well designed and any shortcomings of the tests are incorporated into the analysis. Here, we discuss analytical approaches to population studies of echinococcosis.
Collapse
Affiliation(s)
- Paul R Torgerson
- Institute of Parasitology, University of Zurich, CH-8057, Zurich, Switzerland.
| | | |
Collapse
|
|
27
|
Gavidia CM, Gonzalez AE, Zhang W, McManus DP, Lopera L, Ninaquispe B, Garcia HH, Rodríguez S, Verastegui M, Calderon C, Pan WKY, Gilman RH. Diagnosis of cystic echinococcosis, central Peruvian Highlands. Emerg Infect Dis 2008; 14:260-6. [PMID: 18258119 PMCID: PMC2600205 DOI: 10.3201/eid1402.061101] [Citation(s) in RCA: 51] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/28/2022] Open
Abstract
High prevalence was confirmed by ultrasonography, radiography, and 2 serologic tests, although usefulness of serologic testing in the field was limited. We evaluated prevalence of cystic echinococcosis (CE) in a central Peruvian Highland district by using 4 diagnostic methods: ultrasonography for 949 persons, radiography for 829, and 2 serologic tests for 929 (2 immunoblot formats using bovine hydatid cyst fluid [IBCF] and recombinant EpC1 glutathione S-transferase [rEpC1-GST] antigens). For the IBCF and rEpC1-GST testing, prevalence of liver and pulmonary CE was 4.7% and 1.1% and seropositivity was 8.9% and 19.7%, respectively. Frequency of seropositive results for IBCF and rEpC1-GST testing was 35.7% and 16.7% (all hepatic cysts), 47.1% and 29.4% (hepatic calcifications excluded), and 22.2% and 33.3% (lung cysts), respectively. Weak immune response against lung cysts, calcified cysts, small cysts, and cysts in sites other than lung and liver might explain the poor performance of the serodiagnostic tests. We confirm that CE is highly endemic to Peru and emphasize the limited performance of available serologic assays in the field.
Collapse
Affiliation(s)
- Cesar M Gavidia
- Universidad Nacional Mayor de San Marcos, San Borja, Lima, Peru.
| | | | | | | | | | | | | | | | | | | | | | | |
Collapse
|
|
28
|
Moro PL, Cavero CA, Tambini M, Briceño Y, Jiménez R, Cabrera L. Identification of risk factors for cystic echinococcosis in a peri-urban population of Peru. Trans R Soc Trop Med Hyg 2007; 102:75-8. [PMID: 17949765 DOI: 10.1016/j.trstmh.2007.09.010] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2007] [Revised: 09/18/2007] [Accepted: 09/18/2007] [Indexed: 02/08/2023] Open
Abstract
We conducted a questionnaire-based case-control study to identify risk factors for cystic echinococcosis (CE) in Lima, Peru during July-December 2005. Data were obtained from 32 cases and 64 controls. Multivariate conditional logistic regression showed that having owned > or =10 dogs [adjusted odds ratio (AOR) 8.7, 95% CI 1.3-57.5) and raising sheep (AOR 5.9, 95% CI 1.2-28.1) were independently associated with CE. The belief that CE could be transmitted by food (AOR 0.1, 95% CI 0.01-0.7) and breeding goats (AOR 0.02, 95% CI 0.001-0.6) were protective factors against CE transmission. Our results suggest that preventive measures to decrease the transmission of echinococcosis to humans in Peru should include limiting the number of dogs owned and encouraging owners to restrict dogs' access to food and water used for human consumption.
Collapse
Affiliation(s)
- Pedro L Moro
- Immunization Safety Office, Centers for Disease Control and Prevention, 1600 Clifton Road MS-D26, Atlanta, GA 30333, USA.
| | | | | | | | | | | |
Collapse
|
|
29
|
Gatti A, Alvarez AR, Araya D, Mancini S, Herrero E, Santillan G, Larrieu E. Ovine echinococcosis. Vet Parasitol 2007; 143:112-21. [PMID: 16979823 DOI: 10.1016/j.vetpar.2006.08.022] [Citation(s) in RCA: 33] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/05/2006] [Revised: 07/25/2006] [Accepted: 08/03/2006] [Indexed: 11/25/2022]
Abstract
Immunodiagnosis in sheep presents problems of sensitivity and specificity, limiting its applicability in surveillance systems. The objective of this study was to develop a sensitive, specific and accessible technique for diagnosing cystic echinococcosis in naturally infected sheep and to evaluate the validity of necropsy as a reference test. A total of 247 sheep were studied at slaughterhouses, confirming the parasitological diagnosis with histology. Serum was processed with enzyme immunoassay (EIA) using three antigen preparations: total hydatid liquid (LHT), purified fraction of LHT (S2B) and purified lipoprotein (B). Western Blot (WB) was used as a control. EIA proved effective for differentiating Echinococcus granulosus from larval stage of Taenia hydatigena and intestinal cestodes in all three antigen preparations. Serums from macroscopically negative sheep were reactive to EIA and positive with WB. In the whole flock, sensitivity was 89.2% for LHT, 80.0% for S2B and 86.4% for B. Sensitivity in lambs was 78.6% for LHT, 75.0% for S2B and 64.3% for B. Macroscopic diagnosis at the time of slaughter was found to have limitations as a reference test for immunodiagnosis of cystic equinococcosis in sheep, so it was necessary to include histology and WB as reference tests. LHT was the antigen preparation of greatest value and EIA proved to be a sensitive and specific technique, adequate for surveillance systems and for evaluating control programmes.
Collapse
|
|
30
|
Craig PS, Larrieu E. Control of cystic echinococcosis/hydatidosis: 1863-2002. ADVANCES IN PARASITOLOGY 2006; 61:443-508. [PMID: 16735171 DOI: 10.1016/s0065-308x(05)61011-1] [Citation(s) in RCA: 151] [Impact Index Per Article: 7.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
Abstract
Echinococcosis/hydatidosis, caused by Echinococcus granulosus, is a chronic and debilitating zoonotic larval cestode infection in humans, which is principally transmitted between dogs and domestic livestock, particularly sheep. Human hydatid disease occurs in almost all pastoral communities and rangeland areas of the underdeveloped and developed world. Control programmes against hydatidosis have been implemented in several endemic countries, states, provinces, districts or regions to reduce or eliminate cystic echinococcosis (CE) as a public health problem. This review assesses the impact of 13 of the hydatid control programmes implemented, since the first was introduced in Iceland in 1863. Five island-based control programmes (Iceland, New Zealand, Tasmania, Falklands and Cyprus) resulted, over various intervention periods (from <15 to >50 years), in successful control of transmission as evidenced by major reduction in incidence rates of human CE, and prevalence levels in sheep and dogs. By 2002, two countries, Iceland and New Zealand, and one island-state, Tasmania, had already declared that hydatid disease had been eliminated from their territories. Other hydatid programmes implemented in South America (Argentina, Chile, Uruguay), in Europe (mid-Wales, Sardinia) and in East Africa (northwest Kenya), showed varying degrees of success, but some were considered as having failed. Reasons for the eventual success of certain hydatid control programmes and the problems encountered in others are analysed and discussed, and recommendations for likely optimal approaches considered. The application of new control tools, including use of a hydatid vaccine, are also considered.
Collapse
Affiliation(s)
- P S Craig
- Cestode Zoonoses Research Group, Biomedical Sciences Institute & School of Environment and Life Sciences, University of Salford, Salford, Greater Manchester M5 4WT, UK
| | | |
Collapse
|
|
31
|
Romani ELS, Rodrigues-Silva R, Maldonado A, Machado-Silva JR, Gomes DC. Notes on human cases of cystic echinococcosis in Peru. Mem Inst Oswaldo Cruz 2006; 101:335-7. [PMID: 16862333 DOI: 10.1590/s0074-02762006000300020] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2005] [Accepted: 04/12/2006] [Indexed: 11/22/2022] Open
Abstract
Cystic echinococcosis (CE) is a high prevalent zoonosis in the central and southern Peruvian Andes. Serum samples (n50)from patients presenting presumptive clinical and radiological diagnosis of CE (group 1), were tested for antibodies against Echinococcus granulosus metacestode using Arc-5 double diffusion assay (DD5), immunoelectrophoresis (IEF), and immunoelectrotransfer blot (EITB) techniques. Serum samples (n18) from patients presenting other parasite infections (paragonomiasis, cysticercosis, and fascioliasis) or healthy blood donors (n15), were designated as control groups. The overall sensitivity of the tests was of 94% (DD5 and IEF tests) or 96% (EITB test). Only patients from group 1 were seropositive for CE. Polypeptides of 21, 31, and 48 kDa were considered positive for CE. Based on these results, this study demonstrates that CE also occurs in other coastal departments (Piura, Ancash, Ica, Arequipa, and Tacna) besides Lima.
Collapse
|
|
32
|
Abstract
Echinococcus granulosus and related genotypic variants, the agents of cystic hydatid disease, occur widely in the American continents from Alaska and Northern Canada in North America to Tierra del Fuego in South America. Here we review the historical and current distribution and prevalence of these infections throughout the American countries and the results of programs to control or eliminate the infection.
Collapse
Affiliation(s)
- Pedro Moro
- Immunization Safety Office, Office of the Director, Centers for Disease Control and Prevention, Atlanta, Georgia 30341, USA
| | | |
Collapse
|
|
33
|
Abstract
The application of modern immunodiagnostic or molecular diagnostic techniques has improved the diagnosis of the taeniid cestode infections, echinococcosis and taeniasis. One particularly promising approach is the detection of parasite-specific antigens in faeces (coproantigens). This approach has been applied to both Echinoccocus and Taenia species and it has gained increasingly widespread use. Taeniid coproantigen tests are based on either monoclonal or polyclonal antibodies raised against adult tapeworm antigens. These tests have the following common characteristics; they are largely genus-specific, specificity is high (>95%), parasite antigen can be detected in faeces weeks prior to patency, levels of coproantigen are independent of egg output, coproantigen is stable for days at a range of temperatures (-80 degrees C to 35 degrees C), for several months in formalin-fixed faecal samples, and coproantigen levels drop rapidly (1-5 days) following successful treatment. In the genus Taenia, most work has been done on Taenia solium and coproantigen tests have reliably detected many more tapeworm carriers than microscopy. For Echinococcus species, there is a broad positive correlation between test sensitivity and worm burden with a reliable threshold level for the test of >50 worms. Characterisation of taeniid coproantigens in order to further improve the tests is ongoing. Studies indicate taeniid coproantigens to include high molecular weight (>150 kDa), heavily glycosylated molecules with carbohydrate moieties contributing substantially to the levels of antigen detected in faeces. Application of the existing coproantigen tests in epidemiological and control programmes for Echinococcus and Taenia species infection has begun to contribute to an improved understanding of transmission and of surveillance of these important zoonotic cestodes.
Collapse
Affiliation(s)
- James C Allan
- Cestode Zoonoses Research Group, Bioscience Research Institute University of Salford, UK.
| | | |
Collapse
|
|
34
|
Moro PL, Lopera L, Bonifacio N, Gonzales A, Gilman RH, Moro MH. Risk factors for canine echinococcosis in an endemic area of Peru. Vet Parasitol 2005; 130:99-104. [PMID: 15893076 DOI: 10.1016/j.vetpar.2005.03.015] [Citation(s) in RCA: 18] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 03/10/2005] [Indexed: 10/25/2022]
Abstract
An epidemiological study was conducted in a highland rural community in Peru to determine risk factors for canine echinococcosis caused by Echinococcus granulosus. Dogs were diagnosed using a coproantigen enzyme-linked immunosorbent assay (ELISA). Dog owners were interviewed prior to stool collection and asked for attitudes, practices and beliefs likely to be associated with local patterns of E. granulosus transmission. Univariate and multivariate analysis were used to determine odds ratios (OR) and their 95% confidence intervals (CI). The main risk factors found to be significantly associated with canine echinococcosis by univariate analysis were dog age (3-25 months) (OR, 5.14; CI, 1.7-15.7), female sex (OR, 4.3; CI, 1.4-13.3) and having been fed hydatid infected offal (OR, 2.9; 95% CI, 1.0-8.6). There was complete lack of knowledge about echinococcosis transmission. In addition to periodic dog treatment, control programs need to emphasize education of the human population to increase knowledge of parasite transmission and to change human practices associated with high rates of infection.
Collapse
|
|
35
|
Moro PL, Garcia HH, Gonzales AE, Bonilla JJ, Verastegui M, Gilman RH. Screening for cystic echinococcosis in an endemic region of Peru using portable ultrasonography and the enzyme-linked immunoelectrotransfer blot (EITB) assay. Parasitol Res 2005; 96:242-6. [PMID: 15875215 DOI: 10.1007/s00436-005-1350-6] [Citation(s) in RCA: 36] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/07/2004] [Accepted: 03/10/2005] [Indexed: 10/25/2022]
Abstract
Cystic echinococcosis (CE) caused by the larval form of Echinococcus granulosus is a major public health problem in sheep-raising regions of the World. This study compared portable ultrasound with the enzyme-linked immunoelectrotransfer blot (EITB) assay as screening methods to estimate the prevalence of human CE in a remote village in the Peruvian Andes. Three hundred eighty-nine villagers were examined by portable ultrasound and blood samples were drawn by venipuncture. Sera were collected and tested for antibodies against CE using an EITB assay. Cystic lesions were classified based on their ultrasound morphologic characteristics. The prevalence of human CE using portable ultrasound and the EITB assay were 4.9% and 2.6%, respectively. Fifty-three percent of subjects with CE were EITB positive. Portable ultrasound was well received by the community, augmented CE detection and allowed a faster estimate of human infection than the EITB assay.
Collapse
Affiliation(s)
- Pedro L Moro
- National Immunization Program, Centers for Disease Control and Prevention, 1600 Clifton Rd, 61, Atlanta, GA, USA.
| | | | | | | | | | | |
Collapse
|
|
36
|
Cavagión L, Perez A, Santillan G, Zanini F, Jensen O, Saldía L, Diaz M, Cantoni G, Herrero E, Costa MT, Volpe M, Araya D, Rubianes NA, Aguado C, Meglia G, Guarnera E, Larrieu E. Diagnosis of cystic echinococcosis on sheep farms in the south of Argentina: areas with a control program. Vet Parasitol 2005; 128:73-81. [PMID: 15725535 DOI: 10.1016/j.vetpar.2004.11.006] [Citation(s) in RCA: 15] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 11/04/2004] [Indexed: 11/25/2022]
Abstract
In 2000 Guarnera et al. proposed using ELISA in canine faeces collected from the ground to detect dogs infected with Echinococcus granulosus, thus determining sheep farms with active transmission. The objective was to evaluate the prevalence of E. granulosus infection in sheep farms of the Patagonia. Sheep farms were randomly selected in the Provinces of Río Negro, Chubut, Neuquén, Santa Cruz and Tierra del Fuego (areas with control programs) and La Pampa (comparison area). From one to three samples of fecal matter were obtained for each sheep farm, which were processed by means of copro-ELISA test with confirmation of positive samples by copro-Western blot. A total of 1042 samples were obtained from 352 sheep farms, 26 (7.3%) proving positive. Of these 5 (6.3%) were from La Pampa, 9 (13.8%) from Neuquén, 4 (4.7%) from Río Negro, 2 (2.9%) from Chubut, 1 (5.9%) from Santa Cruz and 5 (13.9%) from Tierra del Fuego. The identification of parasitized dogs is an essential activity upon which rests the strategy of control and surveillance. Arecoline tests or coproantigen test with fecal matter obtained directly from the dog contribute information on individual prevalence, while the use of coproantigens detected in ground-collected samples transfers the dog unit of observation to units of greater epidemiological value. In the present experience, the technique employed seems promising for its application in systems of epidemiological surveillance of cystic echinococcosis and in drawing a baseline on which to measure the progress of control programs in the Argentine Patagonia in subsequent years.
Collapse
Affiliation(s)
- Laura Cavagión
- School of Veterinary Sciences, National University of La Pampa, Argentina
| | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | |
Collapse
|
|
37
|
Simsek S, Koroglu E. Evaluation of enzyme-linked immunosorbent assay (ELISA) and enzyme-linked immunoelectrotransfer blot (EITB) for immunodiagnosis of hydatid diseases in sheep. Acta Trop 2004; 92:17-24. [PMID: 15301971 DOI: 10.1016/j.actatropica.2004.04.006] [Citation(s) in RCA: 20] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2003] [Revised: 03/26/2004] [Accepted: 04/06/2004] [Indexed: 10/26/2022]
Abstract
This study was undertaken to investigate antigenic characteristics of hydatid cyst fluid in sheep by SDS-PAGE method, to evaluate sensitivity and specificity of Enzyme-linked immunosorbent assay (ELISA) and Enzyme-linked immunoelectrotransfer blot (EITB) assay for diagnosis of sheep hydatidosis, and to determine seroprevalance of hydatidosis in sheep population in Elazig, Turkey. SDS-PAGE analysis of hydatid cyst fluids indicated that 6 specific-protein bands were detected at molecular weights of 29, 45, 58, 68, 98 and 116 kDa. EITB analysis showed presence of 29, 38, 42, 58, 62, 68, 98, 116, 120, 150 and 205 kDa bands in positive sheep sera, while 38, 58, 62, 68, 116 and 205 kDa bands were detected in negative sheep sera. Therefore, it was concluded that the 116 kDa band was specific for diagnosis of sheep hydatid disease by EITB assay. Sensitivity and specificity of EITB assay were determined as 88% and 84%, respectively, whereas corresponding rates for ELISA were 60% and 94%, respectively. Sensitivity of ELISA was 47.3% in hepatic cysts, 60% in pulmonary cysts, 69.2% in hepato-pulmonar cysts. Sensitivity ratios of ELISA were 67.8%, 75%, and 38.4% for fertile, sterile, and under-growth cysts, respectively. Sensitivity of EITB was found 84.2% in hepatic cysts, 80% in pulmonary cysts, and 92.3% in hepato-pulmonar cysts. Corresponding ratios for sensitivity of EITB for fertile, sterile, calcified, and under growth cysts were 92.8%, 75%, 100%, and 84.6%, respectively. In addition, seroprevalance of hydatidosis in sheep was found as 62% by ELISA and 66.4% by EITB in Elazig, Turkey and seroprevalance increased by age.
Collapse
Affiliation(s)
- S Simsek
- Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119 Elazig, Turkey.
| | | |
Collapse
|
|
38
|
Abstract
Echinococcosis is one of the world's most geographically widespread parasitic zoonoses, with transmission occurring in tropical, temperate and arctic biomes. Most human infections are due to Echinococcus granulosus transmitted between domestic dogs and livestock, but this cosmopolitan species also cycles between wild carnivores (principally canids) and wild ungulates. The other species with significant zoonotic potential is E. multilocularis that occurs naturally in fox definitive hosts and small mammal intermediate hosts. These two species cause human cystic or alveolar echinococcosis respectively, which may be considered serious public health problems in several regions including developed countries. This review provides an introductory overview to the Supplement and summarises the biology and epidemiology of these two related cestodes with an emphasis on applied aspects relating to detection, diagnosis and surveillance in animal and human populations, and includes aspects of transmission ecology, and also considers aspects of community epidemiology and potential for control.
Collapse
|
|
39
|
Lopera L, Moro PL, Chavez A, Montes G, Gonzales A, Gilman RH. Field evaluation of a coproantigen enzyme-linked immunosorbent assay for diagnosis of canine echinococcosis in a rural Andean village in Peru. Vet Parasitol 2004; 117:37-42. [PMID: 14597277 DOI: 10.1016/j.vetpar.2003.07.019] [Citation(s) in RCA: 13] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/23/2022]
Abstract
One hundred and six dogs (61 males and 45 females) were examined for Echinococcus granulosus infection in a farming cooperative in the central highlands of Peru during November 1998. Canine echinococcosis was diagnosed using direct microscopic examinations of purged feces following arecoline purging and a coproantigen-detection enzyme-linked immunosorbent assay (ELISA) for E. granulosus. Mean age was 2 years with a range of 3 months to 9 years. The overall prevalence of canine echinococcosis using the ELISA test was 79% (84/106). Seventy-four dogs were successfully purged with arecoline. The frequency of canine echinococcosis was 82 (61/74) and 34% (25/74) by the coproantigen ELISA test and arecoline purging, respectively. The sensitivity and specificity of the coproantigen ELISA test was 88 and 95%, respectively. We found this assay to be especially advantageous in remote geographical areas. In future control programs against echinococcosis in Peru and other areas where E. granulosus is endemic the coproantigen ELISA should be used for the surveillance of the dog population.
Collapse
|
|
40
|
Dueger EL, Verastegui M, Gilman RH. Evaluation of the enzyme-linked immunoelectrotransfer blot (EITB) for ovine hydatidosis relative to age and cyst characteristics in naturally infected sheep. Vet Parasitol 2003; 114:285-93. [PMID: 12809754 DOI: 10.1016/s0304-4017(03)00128-6] [Citation(s) in RCA: 13] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
Abstract
An enzyme-linked immunoelectrotransfer blot (EITB) for ovine echinococcosis was evaluated in an endemic area of the Peruvian central sierra. An overall test sensitivity of 91.4% was determined for 199 sheep. EITB sensitivity reached a plateau of nearly 100% at 3 years of age, while the prevalence of cystic disease peaked at 95% in sheep >/=6 years of age. In this highly endemic area, 61.7% of sheep without detectable cystic disease at necropsy (n=47) had positive EITB results. Relationships between EITB sensitivity, age, and cyst location, size, number, type, fertility, and viability were evaluated with logistic regression models. EITB sensitivity increased 14-fold in sheep with calcified cysts and 4-fold for each 1cm increase in pulmonary cyst size.
Collapse
Affiliation(s)
- Erica L Dueger
- Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USA.
| | | | | |
Collapse
|
|
41
|
Moro PL, Lopera L, Bonifacio N, Gilman RH, Silva B, Verastegui M, Gonzales A, Garcia HH, Cabrera L. Taenia solium infection in a rural community in the Peruvian Andes. ANNALS OF TROPICAL MEDICINE AND PARASITOLOGY 2003; 97:373-9. [PMID: 12831523 DOI: 10.1179/000349803235002371] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/28/2022]
Abstract
An epidemiological study was conducted in a highland, rural community in Peru, to determine the seroprevalences of human and porcine infection with Taenia solium and the risk factors associated with human infection. The seroprevalences, determined using an assay based on enzyme-linked-immuno-electrotransfer blots (EITB), were 21% (66/316) in the humans and 65% (32/49) in the pigs. The human subjects aged <30 years were more likely to be positive for anti-T. solium antibodies than the older subjects (P < 0.001). The risk factors associated with human seropositivity were lack of education beyond the elementary level [odds ratio (OR)=2.69; 95% confidence interval (CI)=1.09-6.65] and pig-raising (OR=1.68; CI=0.96-2.92). Curiously, sheep-raising was inversely associated with human T. solium infection (OR=0.50; CI=0.28-0.90). The study site appears to be a new endemic focus for T. solium in the central Peruvian Andes. Although, in earlier studies, the seroprevalence of T. solium infection has generally been found to increase with age, the opposite trend was observed in the present study. The results of follow-up studies should help determine if the relatively high seroprevalence in the young subjects of the present study is the result of a transient antibody response.
Collapse
Affiliation(s)
- P L Moro
- Asociacion Benefica PRISMA, C Gonzalez 251, Maranga, San Miguel, Lima, Peru.
| | | | | | | | | | | | | | | | | |
Collapse
|
|
42
|
Umur S. Prevalence and economic importance of cystic echinococcosis in slaughtered ruminants in Burdur, Turkey. JOURNAL OF VETERINARY MEDICINE. B, INFECTIOUS DISEASES AND VETERINARY PUBLIC HEALTH 2003; 50:247-52. [PMID: 12864901 DOI: 10.1046/j.1439-0450.2003.00667.x] [Citation(s) in RCA: 40] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
This study was conducted between April 2000 and March 2001, in 12-month period. During the study, local slaughterhouses were visited periodically for 1 year to examine the internal organs (livers, lungs, spleens and hearts) for the presence of cysts and total 1355 cattle, 218 sheep and 104 goats were examined for the cystic echinococcosis (CE). It was found that 13.5% of cattle, 26.6% of sheep and 22.1% of goats were infected with this disease. While cysts in cattle (P < 0.001) and goats (P > 0.05) were found mostly in lungs (88.5 and 82.6%, respectively), but they were mostly found in livers (P > 0.05) in sheep. In addition to this, three spleens and one heart in cattle were infected with CE. In this study, the prevalence of CE and the number of cysts in ruminants were found different when the cattle, sheep and goats examined were stratified based on age. The prevalence and the number of cysts increased with age approaching an asymptotic prevalence of one in the oldest animals (P < 0.05). The number of cysts in cattle, sheep and goats were increasing at a rate of 0.31, 0.63 and 0.42/year, respectively. The economic decrease in the value of the carcasses because of the discarded liver and lung as a result of CE was estimated as 1.1% (7.5 US dollars per cattle) for cattle, 4.37% (3.2 US dollars per sheep) for sheep and 4.26% (2.9 US dollars per goat) for goats. The minimum total loss for all infected animals was determined to be 583 US dollars in infected animals, based on the market prices in the year 2002.
Collapse
Affiliation(s)
- S Umur
- Department of Parasitology, Faculty of Veterinary Medicine, Akdeniz University, 15100, Burdur, Turkey.
| |
Collapse
|
|
43
|
Moro PL, Moro RN, Poggi L, Gilman RH. Cystic echinococcosis in a rural Peruvian family. ANNALS OF TROPICAL MEDICINE AND PARASITOLOGY 2002; 96:219-22. [PMID: 12080984 DOI: 10.1179/000349802125000709] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/28/2022]
Affiliation(s)
- P L Moro
- Department of International Health, The Johns Hopkins University School of Hygiene and Public Health, Baltimore, MD 21205, USA.
| | | | | | | |
Collapse
|
|
44
|
Dueger EL, Gilman RH. Prevalence, intensity, and fertility of ovine cystic echinococcosis in the central Peruvian Andes. Trans R Soc Trop Med Hyg 2001; 95:379-83. [PMID: 11579878 DOI: 10.1016/s0035-9203(01)90188-9] [Citation(s) in RCA: 34] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/29/2022] Open
Abstract
An abattoir survey of 212 sheep of different ages was undertaken to determine the local epidemiological transmission patterns of Echinococcus granulosus in the central Peruvian Andes. Overall prevalence of the disease in sheep in this survey (which ended in July 1996) was 77.4%, with 96% of sheep aged > or = 6 years being infected. Of 1165 cysts examined, 41.1% were fertile with a mean protoscolex viability of 73.2%. A logistic regression model for the distribution of cyst fertility and type by age, location and size is described. Mathematical modelling also determined that infection pressure on sheep was 0.44 infections per year and that the mean number of cysts increased linearly by 1.28 cysts per year. These data suggest that E. granulosus is in an endemic state in this area and control measures could drive the disease towards extinction.
Collapse
Affiliation(s)
- E L Dueger
- Department of International Health, Johns Hopkins School of Hygiene and Public Health, Baltimore, MD 21205, USA.
| | | |
Collapse
|
|
45
|
Abstract
Understanding the epidemiology of zoonotic parasitic infections is dependent upon the availability of accurate and sensitive diagnostic techniques. The development of molecular diagnostic methods, particularly those utilising PCR for the detection of zoonoses will contribute greatly to the identification and control of these pathogens, by increasing the speed of diagnosis, specificity and sensitivity, reproducibility and ease of interpretation. Molecular characterisation studies allow us to distinguish between closely related infectious agents and to document the patterns of transmission of 'strains' and species within populations. This will allow precise determinations to be made about the aetiological agent, its characteristics and the source of infection. This review focuses on recent detection and characterisation techniques for both emerging and re-emerging parasite zoonoses.
Collapse
Affiliation(s)
- U M Morgan
- World Health Organization Collaborating Centre for the Molecular Epidemiology of Parasitic Infections and State Agricultural Biotechnology Centre, Division of Veterinary and Biomedical Sciences, Murdoch University, Western Australia 6150, Australia
| |
Collapse
|