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Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Principles and Practice of Clinical Parasitology Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Principles and Practice of Clinical Parasitology Edited by Stephen H Gillespie Royal Free Hospital and School of Medicine and Richard D Pearson University of Virginia Health Sciences Center, Charlottesville, Virginia, USA JOHN WILEY & SONS, LTD Chichester New York Weinheim Brisbane Singapore Toronto Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Copyright # 2001 by John Wiley & Sons Ltd, Bans Lane, Chichester, West Sussex PO19 1UD, England National 01243 779777 International (+44) 1243 779777 e-mail (for orders and customer service enquiries): cs-books@wiley.co.uk Visit our Home Page on: http://www.wiley.co.uk or http://www.wiley.com All Rights Reserved No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, scanning or otherwise, except under the terms of the Copyright, Designs and Patents Act 1988 or under the terms of a licence issued by the Copyright Licensing Agency Ltd, 90 Tottenham Court Road, London W1P 0LP, UK, without the permission in writing of the publisher Chapter 19b is in the public domain Other Wiley Editorial Oces John Wiley & Sons, Inc., 605 Third Avenue, New York, NY 10158-0012, USA WILEY-VCH Verlag GmbH, Pappelallee 3, D-69469 Weinheim, Germany John Wiley & Sons Australia Ltd, 33 Park Road, Milton, Queensland 4064, Australia John Wiley & Sons (Asia) Pte, Ltd, Clementi Loop #02-01, Jin Xing Distripark, Singapore 129809 John Wiley & Sons (Canada) Ltd, 22 Worcester Road, Rexdale, Ontario M9W 1L1, Canada Library of Congress Cataloging-in-Publication Data Principles and practice of clinical parasitology / edited by Stephen Gillespie, Richard D Pearson p cm Includes bibliographical references and index ISBN 0-471-97729-2 (cased) Medical parasitology I Gillespie, S H II Pearson, Richard D QR251 P775 2001 616.90 6Ðdc21 00-047755 British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN 0-471-97729-2 Typeset in 10/12pt Times from authors' disks by Dobbie Typesetting Limited, Tavistock, Devon Printed and bound in Great Britain by Antony Rowe Ltd, Chippenham, Wiltshire This book is printed on acid-free paper responsibly manufactured from sustainable forestry, in which at least two trees are planted for each one used for paper production Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Contents List of Contributors vii Preface ix History of Parasitology G C Cook Parasite Epidemiology D A P Bundy and E Michael 21 Malaria B.-A Biggs and G V Brown 53 Babesiosis Jerey A Gelfand and Debra D Poutsiaka 99 Toxoplasmosis Joseph D Schwartzman 113 Cryptosporidiosis and Isosporiasis Cynthia L Sears and Beth D Kirkpatrick 139 Cyclospora Richard L Guerrant and Theodore S Steiner 165 Microsporidia E U Canning 171 Amebas 197 Upinder Singh and William A Petri Jr 12 10 Giardia lamblia David R Hill 219 11 Trichomonads J P Ackers 243 13 Pathogenic and Opportunistic Free-living Amebas: Naegleria fowleri, Acanthamoeba spp and Balamuthia mandrillaris Augusto Julio MartõÂnez and Govinda S Visvesvara Leishmaniasis Richard D Pearson, Selma M B Jeronimo and Anastacio de Q Sousa 14a African Trypanosomiasis I Balakrishnan and A Zumla 269 287 315 14b American Trypanosomiasis (Chagas' Disease) Louis V Kirchho 335 15 Blastocystis D J Stenzel and R E Boreham 355 16 Schistosomiasis G Richard Olds and Srinivasan Dasarathy 369 17 Hepatobiliary and Pulmonary Flukes: Opisthorchis, Clonorchis, Fasciola and Paragonimus Species Thomas R Hawn and Elaine C Jong 18a Blood-borne Filarial Infections: Wuchereria bancrofti, Brugia malayi, Brugia timori, Loa loa, Mansonella perstans and Mansonella ozzardi Thomas B Nutman 18b Onchocerciasis J Whitworth 407 433 457 vi CONTENTS 18c Strongyloides stercoralis and S fulleborni John F Lindo and Michael G Lee 479 19a Toxocariasis 501 M R H Taylor and Celia V Holland 19b Trichinellosis Peter M Schantz and Vance Dietz 521 19c Migrating Worms Stephen H Gillespie 535 20 553 Dracunculiasis Ralph Muller 21 Intestinal Nematodes Stephen H Gillespie 561 22 Echinococcosis R C A Thompson 585 23 Cestodes Kaethe Willms and Julio Sotelo 613 24 Intestinal Trematodes Thomas R Hawn and Elaine C Jong 635 Index 647 Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Contributors J P Ackers Department of Infections and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK Jerey A Gelfand International Medical Aairs Partners, Healthcare System, Massachusetts General Hospital, 50 Stanford Street, Suite 801, Boston, MA 02114-2517, USA S I Balakrishnan Department of Medical Microbiology, Royal Free & University College Medical School, Rowland Hill Street, London NW3 2PF, UK Stephen H Gillespie Department of Medical Microbiology, Royal Free and University College Hospital Medical School, Pond Street, London NW3 2QG, UK B.-A Biggs Division of Infectious Diseases, Department of Medicine, The Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital, Victoria 3050, Australia Richard L Guerrant Division of Geographic and International Medicine, Box 801379, University of Virginia School of Medicine, Charlottesville, VA 22908, USA R E Boreham PO Box 1246, Toowong, Queensland 4066, Australia Thomas R Hawn Division of Allergy and Infectious Diseases, Department of Medicine, University of Washington Medical Center, The Institute for Systems Biology, Suite 200, 4225 Roosevelt Way NE, Seattle, WA 98105, USA Graham Brown Division of Infectious Diseases, Department of Medicine, The Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital, Victoria 3050, Australia D A P Bundy The World Bank, 1818 H Street NW, Washington, DC 20433, USA E Canning Department of Biology, Imperial College of Science, Technology and Medicine, London SW7 2AZ, UK G C Cook The Wellcome Trust Centre for the History of Medicine at UCL, 183 Euston Road, London NW1 2BE, UK Srinivasan Dasarathy MetroHealth Medical Center, Case Western Reserve University, 2500 MetroHealth Drive, Cleveland OH 44109-1998, USA Vance Dietz OrganizacioÂn Panamericana de Salud, Marcelo T de Alvear 684, Piso, 1395 Buenos Aires, Argentina David R Hill Division of Infectious Diseases, University of Connecticut Health Center, Farmington, CT 06030-3212, USA Celia V Holland Department of Zoology, Trinity College, Dublin 2, Ireland Selma M B Jeronimo Department of Biochemistry, Universidade Federal Rio Grande Norte, Natal, Brazil Elaine C Jong University of Washington, Hall Health Primary Care Center, Box 354410, Seattle, WA 98195-4410, USA Michael G Lee Department of Medicine, University of the West Indies, Mona, Kingston 7, Jamaica Louis V Kirchho University of Iowa, Department of Internal Medicine, 300G EMRB, Iowa City, IA 52242, USA viii CONTRIBUTORS Beth D Kirkpatrick Division of Infectious Diseases, Department of Medicine, University of Vermont School of Medicine, Burlington, VT, USA John F Lindo Department of Microbiology, University of the West Indies, Mona, Kingston 7, Jamaica Augusto Julio MartõÂ nez University of Pittsburgh School of Medicine, Department of Pathology, Division of Neuropathology, 200 Lothrop Street, Pittsburgh, PA 15213-2582, USA Cynthia L Sears Department of Medicine, Division of Infectious Diseases and Gastroenterology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA Upinder Singh University of Viginia School of Medicine, 300 Park Place, Charlottesville, VA 22908, USA Anastacio de Q Sousa Department of Internal Medicine, Universidade Federal Ceata, Fortaleza, Brazil E Michael Department of Infectious Disease Epidemiology, Imperial College School of Medicine, Norfolk Place, London W2 1PG, UK Julio Sotelo Instituto Nacional de NeurologõÂa y NeurocirugõÂa, Insurgentes Sur 3877, Mexico City 14269, Mexico Ralph Muller International Institute of Parasitology, 22 Cranbrook Drive, St Albans, Hertfordshire AL4 0SS, UK Theodore S Steiner Division of Geographic and International Medicine, Box 801379, University of Virginia School of Medicine, Charlottesville, VA 22908, USA Thomas B Nutman Helminth Immunology Section and Clinical Parasitology Unit, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Building 4, Room B1-03, Bethesda, MD 20892-0425, USA G Richard Olds Medical College of Wisconsin, Department of Medicine, 9200 W Wisconsin Avenue, Suite 4186, Milwaukee, WI 53226, USA Richard D Pearson University of Virginia School of Medicine, Department of Medicine & Pathology, Box 801379, Charlottesville, VA 22908, USA William A Petri Jr University of Virginia Health Sciences Center, 300 Park Place, MR4 Building, Room 2115, Charlottesville, VA 22908, USA Debra D Poutsiaka New England Medical Center, 750 Washington Street, Boston, MA 02111, USA Peter M Schantz Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway, Atlanta, GA 30341-3724, USA Joseph D Schwartzman Department of Pathology, Dartmouth-Hitchcock Medical Center, Medical Center Drive, Lebanon, NH 03756, USA D J Stenzel Analytical Electron Microscopy Facility, Queensland University of Technology, Garden Point Campus, George Street, GPO Box 2434, Brisbane, Queensland 4001, Australia M R H Taylor Department of Paediatrics, Trinity College, Dublin 2, and National Children's Hospital, Harcourt Street, Dublin 2, Ireland R C A Thompson Department of Veterinary Studies, Murdoch University, Murdoch, WA 6150, Australia J Whitworth Medical Research Council, Uganda Virus Research Institute, PO Box 49, Entebbe, Uganda Kaethe Willms Department of Microbiology and Parasitology, Facultad de Medicine, Universidad Nacional AutoÂnoma de MeÂxico, Mexico City, Mexico Govinda S Visvesvara Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA A Zumla Centre for Infectious Diseases, University College London, Royal Free and University College Medical School, Rowland Hill Street, London NW3 2PF, UK Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Preface In the 1970s and 1980s, in an attempt to focus world attention on parasitic diseases, the World Health Organization formed the Tropical Diseases Research Group Their target was six major infections that damaged the health of individuals in developing countries, and ®ve of these six were parasitic diseases The Rockefeller Foundation also identi®ed parasitic infections as a major target for health improvement for the world community They formed a research network to develop new drugs and vaccines by understanding the pathogenesis of diseases Its title `The Great Neglected Diseases Network' emphasised that, in the post-colonial world, parasitic diseases were no longer identi®ed by governments and pharmaceutical companies as important subjects for medical research Despite the success of these two ventures in developing our understanding of the immunology, molecular biology and potential for vaccines and drugs, the position of parasitic diseases in the world is, if anything, worse than it was 30 years ago The territories in which malaria is endemic have expanded and the number of cases with it Malaria causes more than a million child deaths in Africa every year The number of individuals suering from intestinal helminth infections has more than doubled in the last 50 years and the prevalence of schistosomiasis is rising Urbanisation in Brazil, where more than 80% of the population live in cities, has resulted in large peri-urban epidemics of Chagas' disease and epidemics of visceral leishmaniasis This general global deterioration has occurred in a context where, for many countries, endemic parasitic diseases are a thing of the past In epidemiological terms, parasitic infections are over-dispersed or, in more everyday terms, focused in the poorest sector of the world community Globalisation has changed the spectrum of parasitic infection in clinical medical practice Not only has the incidence of disease worldwide risen, but frequency of travel, migration and population dispersal due to war has resulted in individuals presenting with parasitic infections in locations where these diseases have become rare Patients with malaria and intestinal protozoan and helminth infections are now an everyday occurrence in family practice throughout the world The diagnosis of parasitic diseases has also become an everyday component of medical laboratory practice worldwide The HIV pandemic has also had a potent in¯uence on the spectrum of parasitic infections A number of organisms that cause disease rarely have become commonplace The HIV epidemic itself was identi®ed through an apparent epidemic of Pneumocystis carinii infection, at that time considered to be a protozoan and now considered to be a fungus Intractable cryptosporidiosis and isosporiasis, and the recognition of microsporidium infections and cerebral toxoplasmosis, have all been consequences of severe immunocompromise secondary to HIV infection Visceral leishmaniasis, too, has been recognised as a major opportunistic disease in HIV-infected individuals in Southern France and Italy New technologies have increased our ability to investigate parasitic diseases and to understand the biology of the organisms and the hosts' immune response to them Developments in immunology and molecular biology have enabled diagnostic laboratories to improve the diagnosis of parasitic infections through enzyme-immunoassays and DNA ampli®cation techniques Genome sequence programmes are under way for parasites, including malaria, Leishmania and x PREFACE amoebas and these may lead to the identi®cation of new virulence determinants, or targets for chemotherapy or vaccine development Although new treatments and vaccines have progressed more slowly than in other infection disciplines, eective chemotherapy is now available for almost all parasitic infections An international panel of authors have drawn together their experience and understanding of parasitic infections The chapters contain a clinically orientated overview of all the major parasitic infections in medical practice The editors hope that those who read and use this book will develop their clinical diagnostic and therapeutic skills, and that these skills will be used for the bene®t of those who most need themÐthe people who are often the poorest in the world community Stephen H Gillespie Richard D Pearson Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Index Numbers in italics indicate ®gures; those in bold indicate tables Plates are denoted by `p' abdominal angiostrongyliasis 545 Acanthamoeba keratitis 281 clinical management 282 diagnosis 281 prevention 282 Acanthamoeba spp culture 273±4 epidemiology 276±7 history 269 immunology 275±6 life cycle 271, 272, 273 molecular biology 276 taxonomy 270±1 see also granulomatous amebic encephalitis acanthopodia 272, 273 acetylcholinesterases 570 acid-fast stains 152, 157, 168, 187 acidosis 62, 78 acquired immunity and helminth vaccination 28 acridine orange 73, 254 actin rearrangement on invasion by Cryptosporidium parvum 143±4 in Toxoplasma gondii motility 119 acute dermatolymphangioadenitis (ADLA) 443 acute necrotizing colitis 207 adenolymphangitis (ADL) 436, 437 adenopathy 440 adhesins, Trichomonas vaginalis 247, 249 adventitial layer, Echinococcus granulosus 593, 594, 598 a¯atoxins 413 African Programme for Onchocerciasis Control (APOC) 474 African trypanosomiasis clinical features 327 clinical management 329 hemolymphatic stage 329±30 meningoencephalitic stage 330 history 17±18, 315, 335 immunology 320±1 immunopathology 321±2 laboratory diagnosis antibody tests 329 antigen tests 329 parasite detection 327±8 organism see Trypanosoma brucei prevention and control disease suppression 331±2 vaccination 332 vector control 331 WHO recommendations 315 agar plate culture of Strongyloides stercoralis 490 age at ®rst infection related to R0 26 optimum for helminth vaccination, mathematical models 27±8, 29 age prevalences cryptosporidiosis 148 Entamoeba infections 202, 204 intestinal nematode infections 565 malaria 68 schistosomiasis 377, 379 strongyloidiasis 488±9 toxocariasis 508 Trichomonas tenax infections 257 age-structured dynamic cost±bene®t analysis model 34±5 AIDS/HIV infection cryptosporidiosis in 140, 147, 148, 150, 153±4 cyclosporiasis treatment 168 giardiasis in 225 granulomatous amebic encephalitis in 278, 279 isosporiasis in 156, 157, 158 microsporidioses in 181, 185, 186, 190, 191 toxoplasmosis in 114, 125±6, 132±3 trichomoniasis and transmission risk of 248 Trypanosoma cruzi brain abscesses in 344 visceral leishmaniasis in 293, 294, 303, 307 airport malaria 68 Alaria americana 536, 549, 637, 645 CESTODES ACKNOWLEDGEMENTS The 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saginata Goeze 1792 Onderstepoort J Vet Res 38 (1): 63±4 Von Bonsdor B, Bylund G (1992) The ecology of Diphyllobothrium latum Ecology Dis 1: 21 Wadia N, Desai S, Bhatt M (1988) Disseminated cysticercosis New observations, including CT scan ®ndings and experience with treatment by praziquantel Brain 111: 597±614 Watanabe N, Nawa Y, Okamoto K et al (1994) Expulsion of Hymenolepis nana from mice with congenital de®ciencies of IgE production or of mast cell development Parasite Immunol 16: 137 Willms K (1998) Cestodes (tapeworms) In Gorbach SL, Bartlett JG, Blacklow NR (eds), Infectious Diseases, 2nd edn WB Saunders: Philadelphia; 2481±99 Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 24 Intestinal Trematodes Thomas R Hawn and Elaine C Jong University of Washington Medical Center, Seattle, WA, USA GENERAL CONSIDERATIONS Although there are over 40 000 documented species of digenetic trematodes, only a limited number are capable of causing infection in humans (Malek, 1980) Approximately 50 of these species are intestinal trematodes, which occur worldwide and usually cause asymptomatic or benign infections (Table 24.1) (Bunnag and Harinasuta, 1989; Bunnag et al., 1991; Chai and Lee, 1991; Chung and Soh, 1991; Waikagul, 1991; Waikagul et al., 1997) These trematodes have not been intensively studied, possibly due to the mild nature of the majority of the infections The life cycles of these ¯ukes are similar and involve a de®nitive host and two intermediate hosts (Figure 24.1) The adult worm lives in the de®nitive host, where it secretes eggs that are released in feces The ova hatch into miracidia, which infect the ®rst intermediate host, which is often a mollusc The miracidia transform into sporocysts, which successively transform into mother and daughter rediae and then into cercariae, which leave the snail in freshwater The cercariae then infect a second intermediate host, where they encyst as metacercariae Second intermediate hosts are variable and include ®sh, snails, tadpoles, shrimp, dragon¯y naiads and aquatic vegetation The de®nitive host ingests the metacercariae, which then develop into adult worms to complete the life cycle Although there are many dierent species of intestinal trematodes with numerous variations of life cycles and hosts, the clinical features of infection, diagnosis and therapeutic options are not complicated (Table 24.2) Most of the infections are asymptomatic or only involve mild gastrointestinal symptoms (with exceptions noted below) While stool microscopy is the central tool for diagnosis, distinguishing the ova of various species is dicult and accurate identi®cation often requires collecting the adult worm The drug of choice for treating many intestinal trematode infections is praziquantel, although the US Food & Drug Administration considers its use investigational for these infections (Medical Letter, 1998) None of the intestinal ¯ukes is known to be resistant to praziquantel but ecacy data are not available for most of them This chapter will describe the organisms, epidemiology, pathogenesis, clinical features and treatment of some of the most important of these ¯uke infections FASCIOLOPSIS BUSKI DESCRIPTION OF THE ORGANISM Fasciolopsis buski is one of the largest trematodes, with some organisms reaching 75 mm in Principles and Practice of Clinical Parasitology Edited by Stephen Gillespie and Richard D Pearson length and 20 mm in width (Table 24.1) (Malek, 1980) This ¯uke belongs to the Family Fasciolidae, which also contains the hepatobiliary ¯ukes Fasciola hepatica and F gigantica It was & 2001 John Wiley & Sons Ltd 636 PRINCIPLES AND PRACTICE OF CLINICAL PARASITOLOGY Table 24.1 Intestinal trematodes in human infection: geographic location, hosts and source of infection* Species Family Fasciolidae Fasciolopsis buski Family Echinostomatidae Echinostoma ilocanum E hortense E lindoense ( E echinatum) E malayanum E revolutum ( E caproni) E jassyense ( E melis) E cinetorchis Echinochasmus japonicus Echinochasmus perfoliatus Paryphostomum sufrartyfex Hypoderaeum conoideum Episthmium caninum Himasthla muehlensi Echynoparyphium recurvatum Family Heterophyidae Metagonimus yokogawai Geographic location Non-human definitive hosts Source of infection China, Taiwan, Thailand, Laos, Bangladesh Pig, dog Water plants Indonesia, Philippines, Thailand, China Korea, Japan Indonesia, Brazil Indonesia, China, Thailand, Philippines, Malaysia, Singapore Thailand, Indonesia, Taiwan Dog, rat, mice Dog, rat Rodent, birds Rat Snail Fish Snail Snail, tadpole, ®sh Chicken, goose, duck, rodent Unknown Rat Cat, dog, rodent, chicken Cat, dog, pig, fox, rat Snail, tadpole Tadpole Tadpole Fish Fish Pig Duck, fowl Dog Gulls, bird Bird, rat, mammals Snail Snail, tadpole Fish Clam Tadpole frog Cat, dog, pig, pelican Fish Cat, dog, rat, fowl ? Mammals, birds Fish Fish Fish Cat, dog, rat Cat, dog Dog Cat, dog, rat Cat, dog Fish Fish Fish ? Fish Cat, dog Fish Cat, dog ? Cat, dog, night heron Cat, dog, rat, fox, rabbit Bird, cat, dog, rat Cat, dog, rat, mouse, rabbit, heron Rat Cat, dog, rat, chicken, duck ? Rat, chicken ? Cat, bird Cat, dog Cat, bird Fish Fish Fish Fish Fish Fish China, Romania Japan, Korea, Indonesia China, Korea Japan, Italy, Romania, Russia, Egypt, Taiwan India Thailand Thailand Germany Indonesia, Japan H taichui H vanissumus H pumilio Apophallus donicus Pygidiopsis summa Centrocestus armatus China, Japan, Korea, Balkans, Russia, Spain, Taiwan, Philippines Korea Taiwan Egypt, Korea, China, Taiwan, Philippines, Mediterranean, Africa, Japan Japan Korea Korea, Japan, China Greenland Philippines, Thailand, Hawaii, Japan, Korea Taiwan, Philippines, Thailand, Indonesia, South China Taiwan, Philippines, Thailand, Pakistan, Philippines Taiwan, Philippines, Thailand, Egypt USA Korea Korea, Japan C canimus C formosanus Thailand, Taiwan Taiwan, South China, Philippines C kurokawai C cuspidatus C longus Stictodora fuscatum Procerovuom calderoni P varium Japan Egypt, Taiwan Taiwan Korea, Japan Philippines Japan M takahashii M minutus Heterophyes heterophyes H nocens H dispar Heterophyopsis continua Cryptocotyle lingua Stellantchasmus falcatus Haplorchis yokogawai Fish Fish, frog Fish Fish ? ®sh Fish Fish Continued INTESTINAL TREMATODES 637 Table 24.1 Continued Species Geographic location Non-human definitive hosts Source of infection Family Lecithodendriidae Phaneropsolus bonnei Prosthodendrium molenkampi Indonesia, Thailand Indonesia, Thailand Bat, monkey Bat, monkey, rat Dragon¯y naiads Dragon¯y naiads Family Plagiorchiidae Plagiorchis harinasutai P javensis P philippinensis P muris Thailand Indonesia Philippines Japan ? Bird, bat Bird, rat Bird, dog, rat ? Larval insects ?Larval insects ?Snails, aquatic insects Family Paramphistomatidae Watsonius watsoni Gastrodiscoides hominis South-west Africa South-east Asia, Kazakstan Baboon, monkey Pig, rats, monkey ?Water plants Aquatic vegetation Philippines Bird Shrimp Family Diplostomatidae Fibricola seoulensis Alaria americana Korea North America Rats Wild carnivores Snake, frog, tadpole Tadpoles, frogs Family Nanophyetidae Nanophyetis salmincola salmincola N salmincola schikhobalowi North America Siberia Dogs, foxes, coyote Dogs, foxes, coyote Salmon and trout Fish Family Microphallidae Spelotrema brevicaeca ( Carneophallus brevicaeca) *Table adapted from Bunnag and Harinasuta (1989), Bunnag et al (1991), Chai and Lee (1991), Chung and Soh (1991) and Waikagul (1991) Fig 24.1 Generalized life-cycle of intestinal trematodes Each intestinal trematode life cycle stage is highlighted in bold letters with its accompanying host where indicated 638 PRINCIPLES AND PRACTICE OF CLINICAL PARASITOLOGY Table 24.2 Major intestinal trematode infections in humans: clinical features, organism size and treament Trematode Fasciolopsis buski Echinostoma spp Heterophyes heterophyes Metagonimus yokogawai Clinical features Average size Asymptomatic or mild GI symptoms Can be severe, more often in children Asymptomatic or mild GI symptoms Asymptomatic or mild GI symptoms Occasional disseminated disease Asymptomatic or mild GI symptoms Occasional disseminated disease Treatment Adult (mm) Egg (mm) 50615 135680 Praziquantel* 1061 1.460.4 110670 29616 Praziquantel* Praziquantel* 1.560.6 29615 Praziquantel* GI, gastrointestinal; *considered investigational for this use discovered by Busk in 1843 at an autopsy where the worms were found in the duodenum, and was originally named Distomum buski The adult worm varies in length from 20 to 75 mm, with a width of 8±20 mm and a thickness of mm (Figure 24.2) It contains testes which are highly branched, ovaries, a ventral sucker, an intestinal cecum and an excretory bladder An average of 10 worms infect each human host and excrete approximately 10 000±20 000 eggs/day (Malek, 1980; Rahman et al., 1981) The eggs are ovoid, operculated, have a thin shell and average 130± 140 mm in length and 80±85 mm in width (Figure 24.3) They are excreted in the feces of humans or pigs, where they mature into miracidia over 3±7 weeks in freshwater The miracidia hatch from the egg and infect the snail intermediate host (Segmentina hemisphaerula and Hippeutis cantori ) where sporocyst, rediae and then cercariae develop after approximately weeks The cercariae encyst and form metacercariae on various water plants, including water caltrop, chestnut, morning glory, lotus and water hyacinth (Manning et al., 1971) The metacercariae, which are visible with an average size of 2±4 mm, are ingested by the de®nitive host and excyst in the duodenum, where they mature over months into adult ¯ukes (Malek, 1980) infection with over 400 adult worms, the mucosa of the stomach and intestines was hyperemic without ulceration There were also hemorrhagic lesions in the lungs (Viranuvatti et al., 1953) IMMUNOLOGY AND MOLECULAR BIOLOGY There are few substantive studies on the immunology and molecular biology of F buski In one study, the peak prevalence of infection was in the 10±15 year-old group, with very few cases in old age (Manning et al., 1971) Elderly individuals continued to ingest metacercariae even though they had lower infection rates, which suggests that humans may acquire resistance EPIDEMIOLOGY F buski is found in China and south-east Asia in areas where animal feces (mainly from pigs) contaminates water sources that contain aquatic vegetation that is consumed by humans CLINICAL FEATURES PATHOGENESIS In animal models, intestinal pathology includes small foci of petechial hemorrhage with mucusal edema and in¯ammation at the sites of attachment In an autopsy study of a fatal human While F buski has been associated with severe illness, the majority of infections are mild or asymptomatic Diarrhea, abdominal pain and even death have been attributed to infection with heavy worm burdens In one of the few controlled trials, 28 Thai individuals with F buski INTESTINAL TREMATODES 639 Fig 24.2 Adult intestinal trematodes (A) Fasciolopsis buski, average size 20±7568±20 mm (B) Echinostoma malayanum, average size 2±2061±1.5 mm (C) Heterophyes heterophyes, average size 1±1.760.3±0.4 mm (D) Metagonimus yokogawai, average size 1± 2.560.4±0.75 mm (E) Gastrodiscoides spp., average size 1065 mm Photographs courtesy of Professor Prayong Radomyos, Faculty of Allied Health Sciences, Thammasat University, Thailand 640 PRINCIPLES AND PRACTICE OF CLINICAL PARASITOLOGY infection were compared to an uninfected group (Plaut et al., 1969) Gastrointestinal symptoms such as nausea, vomiting, anorexia, abdominal pain, diarrhea, melena and weight loss were present in 89% of infected subjects, but also in 82% of controls No symptoms distinguish F buski infection in the majority of individuals While symptoms are generally mild, clinical manifestations may be more severe in children with heavy worm burdens Shah et al (1973) described an outbreak of F buski in India, where 11 of 34 children died The children who died had heavier infestations and suered from diarrhea, anorexia, edema and emesis of ¯ukes While there are potential confounding causes of death in this study, it does appear that F buski can occasionally cause signi®cant morbidity and mortality (Shah et al., 1973) LABORATORY DIAGNOSIS Examination of stool for eggs or adult worms is the only available diagnostic tool The eggs are large in comparison to other helminth eggs and must be distinguished from Fasciola spp., as well as from Paragonimus, Echinostoma and Gastrodiscoides spp CLINICAL MANAGEMENT Praziquantel is the drug of choice for treating F buski Bunnag et al (1983) treated 85 individuals with praziquantel at 15, 25 or 40 mg/kg in a single dose and had 100% cure rates, with stool studies followed up to 56 days (Table 24.3) There was no control group for comparative cure rates in untreated individuals Alternative treatment options are limited Tetrachloroethylene is a suboptimal alternative, with lower ecacy and signi®cant side eects In one study, tetrachloroethylene was eective in eradicating worms in of 11 subjects, with follow-up at and weeks (Plaut et al., 1969) In a separate study, severe allergic reactions with tetrachloroethylene were observed in four of six children who were not pre-treated with antihistamines (Rabbani et al., 1985) Niclosamide has also been tested and has minimal ecacy, with a 10±12% cure in one study compared to 77% for tetrachloroethylene (n 40 patients) (Suntharasamai et al., 1974) Tetrachloroethylene also had severe side eects in this study, with nausea (85%), vomiting (70%) and vertigo (31%) Thiabendazole, mebendazole, levamisole and pyrantel palmoate were ineective in one study (Rabbani et al., 1985) Overall, praziquantel is the most eective and best tolerated of all available medications While tetrachloroethylene is eective, it has signi®cant toxicity and is not routinely available PREVENTION AND CONTROL Individuals should avoid ingestion of uncooked water plants in endemic areas Since pigs are the main reservoir, water resource planning to avoid contamination by pigs may decrease transmission The metacercariae are destroyed by drying, so interruption of the life cycle is not dicult ECHINOSTOMA SPP Echinostoma species (echinos spine, stoma mouth) are predominantly found in animal reservoirs, with occasional infections of humans The taxonomy of this genus is confusing, with reported numbers of species ranging from 61 to 114 with ongoing revision of classi®cation schemes (Human and Fried, 1990) While the majority of species are found in birds and rodents, several species have been found in humans (Table 24.1) (Carney, 1991) There is a signi®cant body of literature on experimental Echinostoma infections, due to the ease with which it can be maintained in the laboratory DESCRIPTION OF THE ORGANISM Echinostomes are small elongated ¯ukes, 2± 20 mm in length and 1.0±1.5 mm in width (Figure 24.2) (Carney, 1991) The `spiny mouth' is the INTESTINAL TREMATODES 641 most characteristic feature and refers to one or two collars of spines surrounding the oral sucker The number of spines varies from 24 to 49, with many species belonging to the 37-collared-spine group The adult also contains testes, ovaries and a ventral sucker The adult secretes eggs into the host's intestinal lumen which are then passed in the feces The eggs are large, ovoid, operculated, have a thin shell and vary in length (88±130 mm) and width (53±90 mm) depending on the species (Figure 24.3) (Malek, 1980) After approximately 10 days a miracidium is formed, which hatches and infects a snail intermediate host, where it develops into a sporocyst, two generations of rediae and then cercariae This stage then encysts as metacercariae in a variety of second intermediate hosts, including snails, ®sh, bivalves or tadpoles The de®nitive host then ingests the metacercariae to complete the life cycle Development in the de®nitive host from a metacercariae to an egg-secreting adult worm can be as rapid as weeks (Malek, 1980) PATHOGENESIS, IMMUNOLOGY AND MOLECULAR BIOLOGY In animal models, Echinostoma species cause in¯ammatory changes in the intestine, including edema, mucosal destruction and lymphocytic in®ltrates (Human and Fried, 1990) While there have not been any signi®cant studies on the immunology or pathology of human echinostomiasis, E caproni has been intensively studied in animal laboratory models Molecular studies are available for speciation and phylogenetic analysis (Fried and Human, 1996) Fig 24.3 Intestinal trematode eggs (A) Fasciolopsis buski, average size 130±140680±85 mm (B) Echinostoma malayanum, average size 120±130680±90 mm (C) Metagonimus yokogawai, average size 27±28616±17 mm (D) Gastrodiscoides spp., average size 127±160660±75 mm Photographs courtesy of Professor Prayong Radomyos, Faculty of Allied Health Sciences, Thammasat University, Thailand EPIDEMIOLOGY rates of less than 1%, there are hyperendemic areas with rates of over 50% (Carney, 1991) The majority of cases of echinostomiasis in humans occur in Asia, including Indonesia, Thailand, The Philippines, Taiwan, Japan, Korea, China, Malaysia and Singapore (Table 24.1) In addition, there have been reports of infection from Africa, Brazil, Romania, Russia, Italy and Egypt Ingestion of molluscs, ®sh, clams or amphibians is the major risk factor While most areas surveyed have low infection CLINICAL FEATURES There are few descriptions of the clinical features of echinostomiasis Most infections are asymptomatic, with no long-term morbidity In human volunteers who were given 30 metacercariae orally, eggs were discharged from the feces on days 16±106 and peripheral eosinophilia was 642 PRINCIPLES AND PRACTICE OF CLINICAL PARASITOLOGY Table 24.3 Treatment of intestinal trematode infections* Drug Dose (mg/ kg)6duration{ Fasciolopsis buski Praziquantel 15 qd61 25 qd61 40 qd61 TCE ?mg qd61 N Efficacy (%) Reference Side effects 29 28 28 13 100 100 100 77 Bunnag et al (1983) Frequent: malaise, headache, dizziness Suntharasami et al (1974) Suntharasami et al (1974) Rabbani et al (1985) Severe allergic reactions, nausea, vomiting, vertigo Minimal Niclosamide TCE 43±160 qd61 0.1 qd61 27 66 TCE 0.2 ml qd61 11 11 99% Lower egg counts 82 Heterophyes heterophyes Praziquantel 40 tid61 25 tid61 40 qd61 20 qd61 10 qd61 Niclosamide g qod63 Niclosamide g qd62 Piperazine 100 qd61 15 18 20 15 15 40 40 22 100 100 100 100 60 78 72 55 El-Hawy et al (1988) Metagonimus yokogawai Praziquantel 10 qd61 20 qd61 20 qd62 Niclosamide 100 qd61 100 qd62 Bithionol 30 qd62 20 50 10 10 12 24 85 88 100 30 67 38 Rim et al (1978) Plaut et al (1969) Sheir (1970) Occasional GI discomfort and urticaria Photosensitivity, vomiting, diarrhea, abdominal pain, urticaria Rare: leukopenia, hepatitis *None of the listed drugs are approved by the US Food & Drug Administration for these uses { Duration in number of days; TCE, tetrachloroethylene; qd, once a day; tid, three times a day; qod, every other day; GI, gastrointestinal noted (Human and Fried, 1990) While heavier infections may cause abdominal discomfort, diarrhea and anorexia, there have been no controlled studies to examine this issue (Maji et al., 1993; Radomyos et al., 1982) A potential outbreak of echinostomiasis was described in 19 American tourists visiting Kenya and Tanzania (Poland et al., 1985) The eggs most closely resembled echinostomes, although no adult worms were recovered to make an unequivocal diagnosis Symptoms included moderately severe abdominal cramps (12/18), diarrhea (10/18) and epigastric pain (7/18) The incubation period ranged from to 62 days and eosinophilia was a common ®nding Praziquantel provided rapid relief of symptoms LABORATORY DIAGNOSIS Diagnosis is by identi®cation of eggs in feces The unembryonated, operculated eggs of echinostomes can be dicult to distinguish from those of Fasciola hepatica and Paragonimus westermani Identi®cation at the species level requires recovery of the adult worm, which may be passed after anthelminthic treatment CLINICAL MANAGEMENT While praziquantel is the recommended drug for treating echinostomiasis, there is minimal INTESTINAL TREMATODES evidence regarding its ecacy (Maji et al., 1993; Pungpak et al., 1998; Radomyos et al., 1982) Mebendazole and albendazole may also be eective (Cross and Basaca-Sevilla, 1986; Pungpak et al., 1984) PREVENTION AND CONTROL Infection with echinostomes can be prevented by avoiding raw or undercooked molluscs, ®sh, 643 clams and amphibians While control programs are probably not necessary due to the mild nature of the infection, such measures would likely to be eective Echinostomiasis was unintentionally controlled in an area of Indonesia that had previously had high infection rates (24±96%; Carney et al., 1990) when a non-indigenous ®sh was introduced to a lake in the area that had echinostome-infected mussels, which were serving as the second intermediate host The ®sh eliminated the mussels and human echinostomiasis disappeared as well HETEROPHYIDIASIS The Family Heterophyidae contains several species of intestinal trematodes, including Heterophyes heterophyes, Metagonimus yokogawai, Stellantchasmus falcatus and several Haplorchis species (Table 24.1) H heterophyes (heteros dierent; phye shape) was discovered in Cairo by Bilharz in 1851, M yokogawai (meta posterior; gonimus genitalia) was found by Kobayshi in 1908, and Haplorchis (haploos single; orchis testis) was described by Loos in 1896 (Grove, 1990) The majority of infections are mild or asymptomatic, although disseminated disease can occur with M yokogawai and H heterophyes DESCRIPTION OF THE ORGANISM H heterophyes is a minute trematode with the adult worm, 1±1.7 mm in length60.3±0.4 mm in width (Figure 24.2) (Malek, 1980) The body is covered with tegumentary scales The eggs are operculated, ovoid, light brown and measure 28± 30 mm615±17 mm The adult M yokogawai varies in length (1.0±2.5 mm) and width (0.4±0.75 mm) and is also covered with scale-like spines (Figures 24.2 and 24.3) The egg is similar to that of H heterophyes and measures 27±28 mm616±17 mm The adult Haplorchis yokogawai measures 0.5± 0.9 mm long60.3 mm wide and also has scales The eggs measure 28±30 mm614±16 mm The adult ¯ukes reside in the intestine, where they secrete eggs that are passed in human feces The eggs are ingested by the intermediate snail host, where they hatch into miracidia and then develop into sporocysts and then rediae This latter stage produces cercariae which encyst in various ®sh and develop into metacercariae Mammalian and avian hosts acquire infection by ingesting raw or undercooked ®sh Even metacercariae soaked in brine or wine remain infective for several days These ¯ukes are probably able to live for up to a year in their hosts, with reservoirs of infection in dogs, cats, foxes and some birds (Malek, 1980) PATHOGENESIS Heterophyid ¯ukes live attached to the intestinal mucosa, where they cause a mild in¯ammatory reaction with some necrosis In one case of metagonimiasis, the worms were both free in the lumen and impacted in the villous spaces (Chi et al., 1988) The lesions contained lymphocytes, plasma cells and eosinophils, with erosions, goblet cell depletion and edema The worms are capable of invading into the submucosa, where the eggs may gain access to the bloodstream and cause disseminated disease IMMUNOLOGY AND MOLECULAR BIOLOGY No information is available on the immunology and molecular biology of these infections 644 PRINCIPLES AND PRACTICE OF CLINICAL PARASITOLOGY EPIDEMIOLOGY Heterophyid infections are found worldwide (Table 24.1) H heterophyes is found in Egypt, Korea, China, Taiwan, Africa, Japan, The Philippines and the Mediterranean M yokogawai is found in China, Japan, Korea, Russia, Spain, Taiwan, the Balkans and The Philippines Various Haplorchis species are found in Taiwan, Thailand and The Philippines The ¯ukes are present where there are ®sh-eating mammals and birds CLINICAL FEATURES The majority of infections are mild and asymptomatic, with heavier infestations possibly causing chronic diarrhea, abdominal discomfort, nausea and malaise (Goldsmith, 1978) Occasionally, intestinal infection can simulate an acute abdomen or appendicitis (Tantachamrun and Kliks, 1978) When heterophyid eggs disseminate hematogenously, visceral complications can ensue (Malek, 1980) Eggs can be found in the heart, brain, spinal cord, liver, lungs and spleen Lesions in the myocardium led to heart failure in some patients, while brain involvement has been reported to cause seizures LABORATORY DIAGNOSIS Stool microscopy remains the cornerstone of diagnosis It is dicult to distinguish the small, operculated ova of the dierent heterophyids from each other and also from Clonorchis sinensis and Opisthorchis spp Recovery of adult worms is necessary for more precise identi®cation CLINICAL MANAGEMENT Praziquantel is the ®rst-line drug for heterophyid infections, although there are only data available for treating some of the species In Egypt, cure rates of 100% were achieved for H heterophyes at most doses tested (Table 24.3) (El-Hawy et al., 1988) At least 20 mg/kg in one dose should be administered, since a dose of 10 mg/kg only had a cure rate of 60% Other drugs that have been used for H heterophyes include niclosamide (72% cure rate, 40 patients) and piperazine (55% cure rate, 22 patients) (Sheir, 1970) Praziquantel's ecacy against Haplorchis taichui and Haplorchis yokogawai was demonstrated by the presence of these ¯ukes in stool during a trial of treatment for Opisthorchis (Pungpak et al., 1980) M yokogawai is also susceptible to praziquantel, with high cure rates ranging from 85% (10 mg/kg for dose) to 100% (20 mg/kg for doses over days) (Rim et al., 1978) PREVENTION AND CONTROL This is similar to measures used for other intestinal trematodes Heterophyid infections can be prevented by avoiding the ingestion of raw or undercooked ®sh OTHER INTESTINAL TREMATODES FAMILY LECITHODENDRIIDAE The Family Lecithodendriidae contains Phaneropsolus bonnei and Prosthodendrium molenkampi, which are endemic in Thailand and Indonesia (Table 24.1) Many cases have been detected after examining stool of patients with opisthorchiasis who were treated with praziquantel (Radomyos et al., 1994, 1998) The capacity for these organisms to cause symptoms in humans is not known One interesting feature of the life cycle is that insects (dragon¯y and damsel¯y naiads) serve as the second intermediate host The eggs of these two species can be dicult to distinguish from other small trematode eggs, including P viverrini, Haplorchis taichui and H pumilio (Tesana et al., 1991) FAMILY PLAGIORCHIIDAE Three species of Plagiorchis have been reported in humans in south-east Asia and include P harinasutai, P javensis, and P philippinensis INTESTINAL TREMATODES (Table 24.1) These parasites have been detected after the examination of stool in patients that were treated with praziquantel for opisthorchiasis It is not known whether any of the Plagiorchis spp cause signi®cant disease in humans (Radomyos et al., 1994, 1998) FAMILY PARAMPHISTOMATIDAE Gastrodiscoides hominis is present in south-east Asia, where it can infect humans It attaches to the cecum and may cause diarrhea (Table 24.1) The adult worm averages 10 mm in length and mm in width (Figures 24.2 and 24.3) Other de®nitive hosts include rodents, monkeys and pigs Ingestion is probably from metacercariae on aquatic vegetation, although the details of the life cycle have not been completely elucidated (Waikagul, 1991) FAMILY MICROPHALLIDAE Spelotrema brevicaeca (also known as Carneophallus brevicaeca) have rarely been associated with human infection in The Philippines, where the second intermediate host is a shrimp (Table 24.1) No other species in this family causes infection in humans FAMILY DIPLOSTOMATIDAE This family contains two species capable of causing infection in humans (Table 24.1) Fibricola seoulensis was found in the intestine of rats in Seoul in 1964, and later in a patient with abdominal pain and fever who had eaten raw snake days previously The presence of metacercariae in snakes has subsequently been veri®ed and additional human infections have occurred in individuals who have eaten raw snake (Chai and Lee, 1991) A total of 26 human cases have been documented (Chung and Soh, 1991) The second species in this family of human signi®cance is Alaria americana, which is endemic in North America, where its usual de®nitive host is a wild carnivore The life cycle involves snail and frog intermediate hosts Humans acquire 645 infection by ingestion of mesocercariae, which are migratory larval forms that develop in tadpoles and frogs While de®nitive hosts include canids and felids, other mammals can serve as paratenic or transport hosts in which the mesocercariae not develop further A fatal human case with disseminated organisms was reported from Canada in a young man who died within days of acquiring the infection Hundreds of mesocercariae were found in his liver, heart, kidney, brain, spleen, spinal cord and peritoneal ¯uid (Freeman et al., 1976) Intraocular infections have also been reported The route of infection may be via oral ingestion and migration to the eye or via direct penetration through the conjunctiva (McDonald et al., 1994) FAMILY NANOPHYETIDAE Two subspecies within the Family Nanophyetidae are capable of causing infection in humans (Table 24.1) Nanophyetes salmincola schikhobalowi is endemic in Siberia, where infection rates exceed 90% in some villages The second subspecies is N salmincola salmincola, which is endemic in the Paci®c north-west of the USA Both subspecies are acquired from ingestion of undercooked, infected ®sh, including salmon and trout (Fritsche et al., 1989) There has also been a case report of infection acquired from handling ®sh (Harrell and Deardor, 1990) Symptoms range from an asymptomatic state to various gastrointestinal complaints, including abdominal pain, diarrhea, bloating, nausea and vomiting Praziquantel appeared to be eective in alleviating these symptoms and eradicating the infection N salmincola is also responsible for a fatal canine infection known as salmon-poisoning disease The trematode serves as a transmission vector for Neorickettsia helminthoeca, which causes a rickettsial illness There has been no evidence that this organism can be transmitted to humans REFERENCES Bunnag D, Harinasuta K (1989) Liver, lung and intestinal trematode diseases In Goldsmith R, Heyneman D (eds), Medicine and Parasitology, pp 459±83 East Norwalk, NJ: Appleton and Lange 646 PRINCIPLES AND PRACTICE OF CLINICAL PARASITOLOGY Bunnag D, Radomyos P, Harinasuta K (1983) Field trial on the treatment of fasciolopsiasis with praziquantel SE Asian J Trop Med Publ Health 14: 216±19 Bunnag T, Bunnag D, Goldsmith R (1991) Intestinal ¯uke infections In Strickland G (ed.), Tropical Medicine, pp 809± 18 Philadelphia, PA: WB Saunders Carney W (1991) Echinostomiasis-snail-borne intestinal trematode zoonosis SE Asian J Trop Med Publ Health 22S: 206±11 Carney W, Sudomo M, Purnomo (1980) Echinostomiasis: a disease that disappeared Trop Geogr Med 32: 101±5 Chai J, Lee S (1991) Intestinal trematodes infecting humans in Korea SE Asian J Trop Med Publ Health 22(suppl): 163±70 Chi J, Kim C, Kim J et al (1988) Intestinal pathology in human metagonimiasis with ultrastructural observations of parasites J Kor Med Sci 3: 171±7 Chung P, Soh C (1991) Snail-borne parasitic zoonoses in Korea SE Asian J Trop Med Publ Health 22(suppl): 391±5 Cross J, Basaca-Sevilla V (1986) Studies on Echinostoma ilocanum in The Philippines SE Asian J Trop Med Pub Health 17: 23±7 El-Hawy A, El-Nasr M, Rahman M (1988) The cure rates of patients infected with heterophyiasis and treated with praziquantel versus niclosamide J Egypt Soc Parasitol 18: 437±42 Freeman R, Stuart P, Cullen J et al (1976) Fatal human infection with mesocercariae of the trematode Alaria americana Am J Trop Med Hyg 25: 803±7 Fried B, Human J (1996) The biology of the intestinal trematode Echinostoma caproni Adv Parasitol 38: 311±68 Fritsche T, Eastburn R, Wiggins L et al (1989) Praziquantel for treatment of human Nanophyetus salmincola (Troglotrema salmincola) infection J Infect Dis 160: 896±9 Goldsmith R (1978) Chronic diarrhea in returning travelers: intestinal parasitic infection with the ¯uke Metagonimus yokogawai South Med J 71: 1513±15 Grove D (1990) In A History of Human Helminthology Oxford, UK: CAB International Harrell L, Deardor T (1990) Human nanophyetiasis: transmission by handling naturally infected Coho salmon (Oncorhynchus kisutch) J Infect Dis 161: 146±8 Human J, Fried B (1990) Echinostoma and echinostomiasis Adv Parasitol 29: 215±69 Maji A, Bera D, Manna B et al (1993) First record of human infection with Echinostoma malayanum in India Trans R Soc Trop Med Hyg 87: 673 Malek EA (1980) In Snail-transmitted Parasitic Diseases Boca Raton, FL: CRC Press Manning G, Brockelman W, Viyanant V (1971) An analysis of the prevalence of Fasciolopsis buski in central Thailand using catalytic models Am J Epidemiol 93: 354±60 McDonald H, Kazacos K, Schatz H et al (1994) Two cases of intraocular infection with Alaria mesocaria (Trematoda) Am J Ophthalmol 117: 447±55 Medical Letter, Inc (1998) Drugs for parasitic infections The Medical Letter 40: 1±12 Plaut A, Kampanart-Sanyakorn C, Manning G (1969) A clinical study of Fasciolopsis buski infection in Thailand Trans R Soc Trop Med Hyg 63: 470±8 Poland G, Navin T, Sarosi G (1985) Outbreak of parasitic gastroenteritis among travelers returning from Africa Arch Intern Med 145: 2220±21 Pungpak S, Bunnag D, Harinasuta T (1984) Albendazole in the treatment of opisthorchiasis and concomitant intestinal helminthic infections SE Asian J Trop Med Publ Health 15: 46±50 Pungpak S, Radomyos P, Radomyos B et al (1998) Treatment of Opisthorchis viverrini and intestinal ¯uke infections with praziquantel SE Asian J Trop Med Publ Health 29: 246±9 Rabbani G, Gilman R, Kabir I et al (1985) The treatment of Fasciolopsis buski infection in children: a comparison of thiabendazole, mebendazole, levamisole, pyrantel pamoate, hexylresorcinol and tetrachloroethylene Trans R Soc Top Med Hyg 79: 513±15 Radomyos B, Wongsaroj T, Wilairatana P et al (1998) Opisthorchiasis and intestinal ¯uke infections in Northern Thailand SE Asian J Trop Med Publ Health 29: 123±7 Radomyos P, Bunnag D, Harinasuta T (1982) Echinostoma ilocanum (Garrison, 1908) Odhner, 1911, infection in man in Thailand SE Asian J Trop Med Publ Health 13: 265±9 Radomyos P, Radomyos B, Tungtrongchitr A (1994) Multiinfection with helminths in adults from north-east Thailand as determined by post-treatment fecal examination of adult worms Trop Med Parasitol 45: 133±5 Rahman K, Idris M, Khan A (1981) A study of fasciolopsiasis in Bangladesh J Trop Med Hyg 84: 81±6 Rim H, Chu D, Lee J et al (1978) Antihelminthic eects of various drugs against metagonimiasis Kor J Parasitol 16: 117±22 Shah P, Udani P, Manjarumkar P et al (1973) Fasciolopsis buski infestation in children Ind Pediat 10: 721±4 Sheir Z (1970) Demographic, clinical, and therapeutic appraisal of heterophyasis J Trop Med Hyg 73: 148±52 Suntharasamai P, Bunnag D, Tejavanij S et al (1974) Comparative clinical trials of niclosamide and tetrachloroethylene in the treatment of Fasciolopsis buski infection SE Asian J Trop Med Publ Health 5: 556±9 Tantachamrun T, Kliks M (1978) Heterophyid infection in human ileum: report of three cases SE Asian J Trop Med Publ Health 9: 228±31 Tesana S, Srisawangwonk T, Kaewkes S et al (1991) Eggshell morphology of the small eggs of human trematodes in Thailand SE Asian J Trop Med Publ Health 22: 631±6 Viranuvatti V, Stitnimankarn T, Tansurat P (1953) A fatal case of infection with Fasciolopsis buski in Thailand Ann Trop Med Parasitol 47: 132±3 Waikagul J (1991) Intestinal ¯uke infections in south-east Asia SE Asian J Trop Med Publ Health 22(suppl): 158±62 Waikagul J, Wongsaroj T, Radomyos P et al (1997) Human infection of Centrocestus caninus in Thailand SE Asian J Trop Med Publ Health 28: 831±5 .. .Principles and Practice of Clinical Parasitology Edited by S Gillespie & Richard D Pearson Copyright & 2001 John Wiley & Sons Ltd Print ISBN 0-471-97729-2 Online ISBN 0-470-84250-4 Principles. .. 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