John wiley sons medicina bioquimica 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


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

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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
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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)
1. 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

1

History of Parasitology
G. C. Cook

2

Parasite Epidemiology
D. A. P. Bundy and E. Michael

21

3

Malaria
B.-A. Biggs and G. V. Brown

53

4

Babesiosis
Je€rey A. Gelfand and
Debra D. Poutsiaka

99

5

Toxoplasmosis
Joseph D. Schwartzman

113

6

Cryptosporidiosis and Isosporiasis
Cynthia L. Sears and
Beth D. Kirkpatrick

139

Cyclospora
Richard L. Guerrant and
Theodore S. Steiner

165

8

Microsporidia
E. U. Canning

171

9

Amebas
197
Upinder Singh and William A. Petri Jr

7

12

1

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

Je€rey A. Gelfand International Medical A€airs
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, 4 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 do Rio Grande do 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 do 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, 1
Medical Center Drive, Lebanon, NH 03756, USA

D. J. Stenzel Analytical Electron Microscopy

Facility, Queensland University of Technology,
Garden Point Campus, 2 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 su€ering 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,
e€ective 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


648

INDEX

albendazole treatment
cutaneous larva migrans 539
cystic echinococcosis 604±5
cysticercosis 627
deworming randomized trial 36, 37
giardiasis 231, 232
intestinal nematode infection 578
loiasis 448
lymphatic ®lariasis 443
microsporidiosis 190
multivesicular/alveolar echinococcosis 605±6
strongyloidiasis 492
taeniasis 626
toxocariasis 515
trichinellosis 530, 531
alveolar hydatid growth 594
amastigotes

Leishmania spp. 288, 290, 291, 294
detection 304
pathogenesis 291, 292
Trypanosoma cruzi 336, 337, 338
amebapores 201
amebas
taxonomy 270±1
see also speci®c species
amebic dysentery/colitis 206±7, 210, 211
amebic liver abscesses 205, 207±8
diagnosis 208, 209, 210, 211
management 211
amebic meningoencephalitis see primary amebic meningoencephalitis
ameboid form, Blastocystis hominis 359
American trypanosomiasis see Chagas' disease
aminosidine see paromomycin
amocarzine 472
amphotericin B 281, 306, 307, 308
Ancyclostoma caninum/A. braziliense 535±7
epidemiology 538
life-cycle 537±8
pathogenesis 538, 570
see also cutaneous larva migrans; eosinophilic enteritis
Ancyclostoma duodenale 569, 570, 571
AndreÂ, Nicholas 2
anemia
in babesiosis 103
in hookworm infection 571
in malaria 62, 79
in schistosomiasis 384, 390

angiostrongyliasis
Angiostrongylus/angiostrongyliasis 536, 543
A. cantonensis 543
A. costaricensis 543
clinical features 545
epidemiology 543, 544
laboratory diagnosis 545
life-cycle 544

pathogenesis 544±5
treatment 545±6
anion-exchange centrifugation technique 328
Annesley, James 12
annual transmission potential (ATP) 464
Anopheles mosquitoes 55
control 87
house screening against 88
insecticide resistance 87
microsporidia in 187
in Plasmodium life-cycle 56
prevention of bites 88
variation and malaria transmission 67
anticoagulants, hookworm 538, 570
antigen detection tests
Angiostrongylus spp. 545
Echinococcus spp. 603, 604
Entamoeba histolytica 209±10
Giardia lamblia 229
Schistosoma spp. 394
Strongyloides stercoralis 492

Taenia spp. 625
Toxocara spp. 514
Trichomonas vaginalis 254
Trypanosoma brucei 329
Wuchereria bancrofti 441
antigenic variation, mechanisms in Trypanosoma
brucei 323, 324±5
antimalarial antibodies 64
antimalarial drug resistance 69, 78
chloroquine 54, 75, 76±7, p.vi
countries a€ected 89, p.vi
mis-diagnosed babesiosis 106
pyrimethamine±sulfadioxine 84
quinine 77
tests for 69, 74
antimalarial drugs 81±6
see also speci®c drugs
antimony dimercaptosuccinate 371
ants 421
apicoplasts 114
appendicitis and Enterobius infections 574
arecoline 603
artemesinin 77, 81, 85
artemether 81, 85
artesunate 77, 81, 85
Ascaris lumbricoides
adult 567
classi®cation 566±7
clinical features of ascariasis 568
control program, cost-e€ectiveness analysis 32±4

child-targeted treatment 34±5
eggs 567
epidemiology
genetic predisposition 568
transmission 567±8


INDEX
history 566
see also intestinal nematodes
asthma and toxocariasis 513
astrocytes 321
atovaquone 109
atovaquone±proguanil 75, 85, 90
autoantibody production in trypanosomiasis
autoimmunity in Chagas' disease 339
autoinfection
capillariasis 575
strongyloidiasis 485
avacuolar form, Blastocystis hominis 358
axostyles 244, 256, 258
azithromycin 154, 231

321

Babesia spp.
description 99±101
epidemiology 105±6
life cycle 101±3
mechanisms of injury 103±4

tick vectors 101
babesiosis
clinical features 106±9
clinical management 109±10
history 14, 99
immunology 104
cell-mediated immunity 105
humoral immunity 104±5
phagocytosis 105
laboratory diagnosis 108±9
organisms see Babesia spp.
prevention and control 110
bacitracin zinc 232
bacterial infections
Dracunculus medinensis tracks 557
in malaria 79
Baermann method 490
Balamuthia mandrillaris
culture 274
epidemiology 276
history 269
life cycle 271, 272±3
taxonomy 270, 271
see also granulomatous amebic encephalitis
bancroftian ®lariasis see lymphatic ®lariasis: bancroftian
®lariasis
basic reproductive number (R0) 22
estimation for microparasites 24
for macroparasite infections 27
and vaccination levels to eradicate diseases 24±5

Bastianelli, Giuseppe 14, 16
Bavay, A. 479
Baylisascaris procyonis 536, 548
diagnosis 548±9
treatment 549
Bayluscide 371

649

beef tapeworm see Taenia spp: T. saginata
behaviour changes in toxocariasis 510±11, 512
bentonite ¯occulation test 530
benzimidazole treatment
intestinal nematode infections 578±9
Trichinella larvae elimination 530±1
see also albendazole treatment; mebendazole treatment; thiabendazole treatment
benznidazole 347, 348
Bignami, Amico 14, 16, 53
Bilharz, Theodore 11, 369
biliary tract Cryptosporidium infection 150, 152±3
Biomphalaria snails 376
birds
migration and cyclosporiasis outbreaks 167
pet, in Encephalitozoon hellem infections 186
bis(glucathionyl)spermidine metabolism 317±18
bithionol 419, 420, 429, 642
black¯ies as onchocerciasis vectors 458, 459
blood meals 466
control 472±3
dispersal and migration 466

geographical distribution of vector species 465
infective density determination 463±4
life-cycle 465±6
seasonality 466
Blacklock, D.B. 458
blackwater fever 63
bladder cancer and urinary schistosomiasis 383, 391
Blastocystis hominis
clinical features of infection 362
clinical management of infection 364
chemotherapy 364
diet 364±5
epidemiology 361
history 355
immunology 361
laboratory diagnosis
culture 363
microscopy 362±3, p.vii
serology, not yet available 363
life-cycle 359±60
molecular biology and biochemistry 360
morphological forms 356, p.vii
ameboid 359
avacuolar 358
cyst 358±9
granular 357
multivacuolar 358
vacuolar 356±7
pathogenesis 360±1
prevention and control 365

taxonomy 355±6
Blastocystis spp. with animal hosts 356
blindness
from onchocerciasis 467, 468
from toxocariasis 511±12


650

INDEX

blood concentration methods 327±8
blood smears
acute Chagas' disease diagnosis 345
African trypanosomiasis diagnosis 327±8
babesiosis diagnosis 108
malaria diagnosis 71±3
Plasmodium falciparum/Babesia di€erentiation 100,
108
blood transfusion
babesiosis transmission 106, 110
Chagas' disease transmission 340, 341±2, 349
blood-borne ®larial parasites 433, 434
see also Loa loa; lymphatic ®lariae; Mansonella
ozzardi; Mansonella perstans
blood-stage malarial vaccines 91±2
Borrelia burgdorferi/Babesia microti co-infection 106,
108, 109±10
bottled water, safety 155
bovine anti-Cryptosporidium hyperimmune colostrum

154
Brachiola spp. 178±9, 187
life-cycles 172, 173, 180
pathogenesis 181, 182
bradyzoites 114, 115, 116, 122
brain calci®cation in neurocysticercosis 623
breast feeding, protective against Giardia 225
broad ®sh tapeworm see Diphyllobothrium latum
brood capsules, Echinococcus spp. 590, 591, 592
Bruce, David 17, 18
Brugia malayi 434, 436, 441
Brugia timori 434±5, 441
brugian ®lariasis 434, 436, 438
Bulinus snails 376
burden of disease estimation 28, 30±1
bush yaws 298
Calabar swellings 446
Calco¯uor M2R stain 187
cancer risk with schistosomiasis 391
Capillaria philippinensis 575
clinical features of infection 575±6
epidemiology 575
laboratory diagnosis 576
life-cycle 575
pathogenesis 575
treatment 576
see also intestinal nematodes
capsule, ®brous of Echinococcus granulosus 593, 594,
598
card agglutination tests for trypanosomiasis 329

cardiovascular trichinellosis 527
Carneophallus brevicaeca 637, 645
Castellani, Aldo 18
cats
ownership and toxocariasis risk 509
Toxocara cati life-cycle in 502, 503, 504
in Toxoplasma gondii transmission 115, 116, 133

CD4+ cells, in Cryptosporidium parvum immunity
146, 150
cell detaching factor (CDF) 247
cercariae
intestinal trematodes 635, 637, 638, 641, 643
Schistosoma spp. 372±3, 374, 377
cerebral gnathostomiasis 542
cerebral infection, microsporidia 176±7, 182, p.iv, p.v
cerebral malaria 61±2, 64, 70, 71, 79
cerebrospinal ¯uid (CSF) examination
African trypanosomiasis 328
granulomatous amebic encephalitis 280
primary amebic meningitis 280
cervical cancer and Trichomonas vaginalis 248
cestodes 613
history 9±10
see also Diphyllobothrium latum; Echinococcus spp;
Hymenolepis nana; Taenia spp.
Chagas, Carlos 18, 336
Chagas' disease
clinical features
acute disease 342

chronic gastrointestinal disease 343±4
chronic heart disease 343
in immunosuppressed patients 344
indeterminate phase 342±3
clinical management 347±8
antiparasitic drugs 346±7
heart transplantation 348
history 18, 335±6
immunology 339±40
laboratory diagnosis
acute disease 344±5
chronic disease 345
PCR 346
recombinant assays 346
organism see Trypanosoma cruzi
prevention and control 348±9
chagoma 337, 338, 342
chaos in measles epidemics 23
chicle ulcers 298
child-targeted treatment, cost-bene®t analysis 34±5
Chinese medicinal herbs, Blastocystis hominis treatment
364
chlorination of Cryptosporidium oocysts 155
chlorination of water
giardiasis prevention 233, 234
primary amebic meningoencephalitis prevention 282
chlorine resistance
Blastocystis hominis cysts 365
Cyclospora oocysts 167
Giardia cysts 226

chloroquine 54, 76, 82
for amebic liver abscesses 211
prophylaxis 89, 90
resistance 54, 74±5, 77, p.vi


INDEX
for severe malaria 81
cholangiocarcinoma 410, 413
chondroitin sulphate A 59
chromotrope stain 187, p.iv, p.v
chronic trichinellosis 528
chyluria 439, 444
ciliary tufts, detached 254
cinchonism 82
cipro¯oxacin 158
circumsporozoite protein (CSP) repeat 91
clindamycin 109, 131, 132±3
clonorchiasis 412
clinical features
acute infection 411
cholangiocarcinoma 413
chronic infection 411, 412
obstructive biliary disease 412
recurrent pyogenic cholangitis 412±13
control 414
laboratory diagnosis 413
organism see Clonorchis silensis
treatment 413±14
Clonorchis sinensis 407, 409±10

epidemiology 410, 411
immunology 410
life cycle 408, 410
pathogenesis 410
Cobbold, Thomas Spencer 3, 5, 11, 369
Cochrane Parasitic Diseases Group 38
cognitive impairment and intestinal nematode infection 562
colitis, amebic 206±7, 210, 211
colon cancer risk in schistosomiasis 381, 391
colonic mucins 200
colonic polyposis 389
colonoscopy, amebic dysentery diagnosis 210
colpitis macularis 253
common variable hypogammaglobulinemia, predisposition to giardiasis 225
community micro®larial load 469, 470
complement
evasion by Entamoeba histolytica 200±1
killing of trichomonads 249
role in Babesia infection 103
complex lymphedema therapy 444
computed tomography (CT) scans
amebic liver abscesses 210, 211
fascioliasis 419
granulomatous amebic encephalitis 281
neurocysticercosis 623, 626
primary amebic meningoencephalitis 280
toxoplasmosis 126, 127, 128
congenital toxoplasmosis 123±4, 125, 132
contact-mediated cytotoxicity 247
copper sulphate 371

coproantigen detection in strongyloidiasis 492

coracidia 629, 630
corticosteroids 132, 516, 531
cost±e€ectiveness analysis 31
dynamic models 32
age-structured 34
Ascaris lumbricoides control program 32±4
cost per DALY 36
coverage and frequency of treatment 34±5
static models 31±2
cost per DALY 35
cost±utility analysis 35±6
costae 243, 244
covert toxocariasis 502, 512
CpABC 144
creeping eruption see cutaneous larva migrans
crustaceans see cyclops; snail hosts
cryptosporidiosis
clinical features 149±51
in immunocompetent patients 149±50
in immunocompromised patients 150
relapsing diarrhea 150
repeated infections 150
in young children 151
clinical management 153
di€erential diagnosis 151
history 139
immunology 145
cell-mediated immunity 145±7

humoral immunity 147
laboratory diagnosis 151
PCR 152, 153
serology 153
stains 152
organism see Cryptosporidium parvum
prevention and control 154±5
treatment 153±4
Cryptosporidium parvum 139
classi®cation 139±40, 142
epidemiology
infection and outbreak potential 148
prevalence 148
transmission 147±8, 149
future studies 155
genotypes 140, 142
life-cycle 141, 142
pathogenesis 142±5
crypts of Lieberkuhn 587, 595, 615
culture media
Blastocystis hominis 363
free-living amebae 274
cutaneous amebiasis 208
cutaneous larva migrans
clinical features 538±9
diagnosis 539
pathogenesis 538
treatment 539

651

652
cutaneous leishmaniasis see leishmaniasis, cutaneous
cyclops 541, 555, 558
cyclosporiasis
clinical features 167±8
clinical management 168
Cyclospora spp. 165±6
epidemiology 166±7
history 165
immunology 166
laboratory diagnosis 168
prevention and control 168±9
cyst wall proteins 223, 229
cystic echinococcosis
clinical features 602
clinical management 604±5
diagnosis 603±4
pathogenesis 595±6
see also Echinococcus spp.
cysticercosis 620±1
clinical manifestations 624
diagnosis 624±5, 626
organism see Taenia spp: T. solium
pathology 621±4
prevention 627±8
treatment 626
see also taeniasis
cysts

Acanthamoeba spp. 272, 275, 279, 281
Balamuthia mandrillaris 273, 275, 280
Blastocystis hominis 358±9, 362, 365, p.vii
in cysticercosis pathology 621±4
Endolimax nana 214
Entamoeba spp. 199, 213, 214
Giardia lamblia 220±1, 223, 226, 229, 234
Naegleria fowleri 271, 272
Paragonimus spp. 421, 422
Toxoplasma gondii 114, 115, 122, 127, 128
Trichinella spp. 521, 523
see also hydatid cysts
cytoadherence
babesiosis 103
falciparum malaria 59
cytokine mimicry 416
DALYs see disability-adjusted life years
Davaine, Casimir 3, 6
DDT
black¯y control 472±3
mosquito control 87
sand ¯y control 308
DEC see diethylcarbamazine citrate (DEC) treatment
DEET see N,N-diethylmetatoluamide
Demarquay, Jean 8
dendritic cells 121
dermatolymphangioadenitis, acute (ADLA) 443
deworming, randomized trial 36±7

INDEX

dexamethasone 627
diarrhea
of Cochin China 479, 480
relapsing 150
Dicrocoelium spp. 420±1
Dientamoeba fragilis 260
clinical features of infection 262
clinical management of infection 263
description 260±1
epidemiology 262
history 260
immunology 261±2
laboratory diagnosis
culture 263
microscopy 262±3
pathogenesis 261
prevention and control 263±4
see also other trichomonads
dietary management of Blastocystis hominis 364±5
diethylcarbamazine citrate (DEC) treatment
loiasis 448
lymphatic ®lariasis 439, 443, 444, 445
Mansonella ozzardi infections 450
in the Mazzotti test 470
onchocerciasis 471
perstans ®lariasis 449
N,N-diethylmetatoluamide (DEET) 88, 90, 110, 309
di€erential agglutination test 130±1
diiodohydroxyquin 263
diloxanide furoate 211, 214

Diphyllobothrium latum
clinical features of infection 629
diagnosis and treatment 630
epidemiology 629±30
life-cycle 629
directly transmitted infections, R0 estimation 24
Diro®laria spp. 536
clinical features of infection 547
diagnosis 547±8
life-cycle 547
treatment 548
disability-adjusted life years (DALYs) 28, 30±1
in cost-utility analyses 35±6
in intestinal nematode infections 564
disease mapping see epidemiology: emerging
technologies
disseminated strongyloidiasis 486, 489±90
Distomum buski see Fasciolopsis buski
diurnal temperature di€erence maps 48±9
DNA vaccines, malaria 92
dog hookworms see Ancylostoma caninum/A. braziliense
dogs
Diro®laria immitis infection 547
Echinococcus spp. hosts 600, 601, 603, 606
Encephalitozoon cuniculi transmission 186
in leishmaniasis control 309


INDEX
Metorchis conjunctus infection 420

Toxocara canis infection 503±4, 509, 510, 515
Toxoplasma gondii transmission 117
DonneÂ, Alfred 12
Donovan, Charles 19, 287
doxycycline treatment 85
contraindicated in pregnancy 81
prophylaxis 76, 89, 90
severe malaria 81
uncomplicated malaria 75, 77
dracunculiasis
clinical features 556±7
clinical management 557
history 553
laboratory diagnosis 557
organism see Dracunculus medinensis
prevention and control 557±8
seasonality 556
Dracunculus medinensis 553
epidemiology 556
history 6±7
immunology 555
life cycle 555, 556
pathogenesis 553±5
drug resistance
metronidazole in Trichomonas vaginalis 255
nitroimidazole in Giardia lamblia 231
oxamniquine in schistosomes 396
praziquantel in schistosomes 395
see also antimalarial drug resistance
Dujardin, FeÂlix 3

duodenal sampling for Fasciola hepatica 419
Dutton, Joseph 17
dysentery, amebic see amebic dysentery/colitis
echinococcosis
cystic echinococcosis see cystic echinococcosis
history 585±6
immunology
de®nitive host 598
intermediate host 597±8
laboratory diagnosis
humans 603±4
non-humans 602±3
multivesicular/alveolar echinococcosis see multivesicular/alveolar echinococcosis
organisms see Echinococcus spp.
prevention and control 606
Echinococcus spp.
control
E. granulosus 606±7
E. multilocularis 607
problem of strain variation 607
vaccination 607±8
development
in the de®nitive host 590

653

E. granulosus 591±4
E. multilocularis 592, 593, 594
E. vogeli/E. oligarthrus 594±5
in the intermediate host 590±1

epidemiology 598
geographical distribution 588, 598±9
life-cycles and transmission patterns 599±601
molecular techniques 601±2
life-cycle 587
pathogenesis
adult tapeworms 595
E. granulosus larvae 595±6
E. multilocularis larvae 596
E. vogeli/E. oligarthrus larvae 596
strain/species di€erences 596±7
taxonomy 586, 588±9
Echinostoma spp. 636
clinical features of infection 638, 641±2
description 639, 640±1
epidemiology 641
laboratory diagnosis 642
life cycle 637, 641
pathogenesis 641
prevention and control 643
taxonomy 640
treatment of infection 642±3
e€ective reproductive number (R) 22, 26
e¯ornithine 330
egg granulomas, Schistosoma spp. 376, 380, 381
in hepatosplenic pathology 381±2
immune responses to 385±7
in intestinal pathology 381
in neuroschistosomiasis 383
in pulmonary ®brosis 382±3

eggs
Ascaris lumbricoides 567, 568
Capillaria philippinensis 575
Diphyllobothrium latum 629, 630
Echinococcus spp. 587, 590
Echinostoma spp. 641
Enterobius vermicularis 573, 574
Fasciola hepatica 408, 415, 418, 419
Fasciolopsis buski 638, 640, 641
Gnathostoma spinigerum 540, 541
Heterophyes heterophyes 643
hookworm 535, 537, 569
Hymenolepis nana 628, 629
identi®cation of intestinal nematode 577±8
Metagonimus yokogawai 641, 643
Opisthorchis and Clonorchis spp. 408, 409, 410, 413
Paragonimus spp. 408, 421, 427, 428
Schistosoma spp. 372, 373, 374, 375
detection 392±4
granulomas see egg granulomas, Schistosoma spp.
hatching techniques 393
release 376


654

INDEX

eggs (cont)
Strongyloides fulleborni 495

Strongyloides stercoralis 482, 484
Taenia spp. 614±15, 616, 617, 621, 625
Toxocara spp. 502, 503, 504, 509±10
Trichuris trichiura 572
elephantiasis 8, 438, 440, 443±4
ELISA detection
Blastocystis hominis antibodies 363
cryptosporidiosis 153
Encephalitozoon spp. antibodies 185
giardiasis 229
opisthorchiasis 413
strongyloidiasis 491
toxocariasis 514
toxoplasmosis 130
trichinellosis 530
visceral leishmaniasis 305
emetine 198, 419, 420
encephalitis in loiasis 446±7, 448
Encephalitozoon spp. see microsporidia: Encephalitozoon spp.
encystation, Giardia lamblia 223
endemic hemoptysis see paragonimiasis
endemicity of malaria 67
Endolimax nana 214
endoscopic retrograde cholangiopancreatography
(ERCP) 153
endoscopy for giardiasis diagnosis 230
Entamoeba coli 213
Entamoeba dispar 198, 212
epidemiology 213
laboratory diagnosis 213

molecular biology 212±13
pathogenesis 212
Entamoeba histolytica
clinical features of infection 205
asymptomatic colonization 205±6
cutaneous amebiasis 208
dysentery 206±7
liver abscess 207±8
diagnosis
antigen detection 209±10
colonoscopy 210
imaging 210±11
microscopy 208, 209
PCR 210
serology 210
epidemiology 204±5
history 12, 14, 197±8
immunology 201±2
life-cycle 199
management of infection 211
molecular biology 202±4
pathogenesis 200±1
prevention and control 211±12

taxonomy 198
Entamoeba polecki 214
Enterobius vermicularis
clinical features of infection 574
description 573
Dientamoeba fragilis transmission in eggs 262

life-cycle 573±4
management of infection 574
pathogenesis 574
see also intestinal nematodes
Enterocytozoon bieneusi see microsporidia: E. bieneusi
eosinophilic enteritis 538, 539
epidemic dynamics 22±3
epidemic malaria 67±8
epidemiology
burden of disease estimation 28, 30±1
classical
meta-analyses, examples 38±44
randomized trials, example 36±7
cost±e€ectiveness analysis see cost±e€ectiveness
analysis
emerging technologies 44±5
applied to African trypanosomiasis 45±6, p.i,
p.ii, p.iii
applied to lymphatic ®lariasis 46±9
population dynamics see population dynamics
see also speci®c parasites
epilepsy
in neurocysticercosis 624
and Toxocara titres 512, 513
epimastigotes
Trypanosoma brucei 318, 319, 320
Trypanosoma cruzi 336, 337
eradication therapy, malarias 75, 76
erythrocytes
Babesia infection 100, 103

Plasmodium infection 55, 56, 57, 59, 60
espundia 288, 298, 301
estrogen, role in neonatal trichomoniasis 246, 252
exchange transfusions 79, 109
excretory±secretory (ES) antigens
hookworms 571
Toxocara canis 505, 506
Trichuris trichiura 572
excystation, Giardia lamblia 223
expression sites (ESs) in vsg genes 323
eyeworm 446
failure to thrive, giardiasis 228
Fairley, Neil Hamilton 16
falciparum malaria 70
see also Plasmodium falciparum
Fasciola gigantica 420
Fasciola hepatica 414
description 415
epidemiology 416, 417


INDEX
history 10±11, 414±15
immunology 416
life-cycle 408, 415
pathogenesis 415, 416
fascioliasis
clinical features 417
acute hepatic phase 417
chronic obstructive biliary phase 417, 418

ectopic manifestations 418
laboratory diagnosis 418
radiology 419
serology 418±19
stool analysis 418
laboratory features 417, 418
organism see Fasciola hepatica
treatment 419±20
Fasciolopsis buski 636
clinical features of infection 638, 640
description 635, 638, 639
epidemiology 638
laboratory diagnosis 640
life cycle 637, 638
pathogenesis 638
prevention and control 640
treatment of infection 640
fatty acid binding protein Sm-14 397
fenbendazole 515
Fibricola seoulensis 637, 645
®laria dance sign 442
®larial fever 437
®larial granulomata 439
®lariform larvae
hookworms 537±8, 569
Strongyloides stercoralis 483±4, 485, 488
®lter paper culture of Strongyloides stercoralis
490
®ltration of drinking water
cryptosporidiosis prevention 155

dracunculiasis prevention 558
giardiasis prevention 234
®sh
Capillaria philippinensis transmission 575
Gnathostoma spp. transmission 541, 543
intestinal trematode transmission 636, 637, 641,
644, 645
Metorchis conjunctus transmission 420
Opisthorchis and Clonorchis spp. transmission 408,
410
¯agellate form, Naegleria fowleri 271, 272
¯otation techniques 577
food-borne transmission
cryptosporidiosis 149
cyclosporiasis 165, 166±7
giardiasis 226
see also speci®c foods
formol±ether technique 490, 577

655

free-living amebas
taxonomy 270±1
see also Acanthamoeba spp; Balamuthia mandrillaris;
Naegleria fowleri
free-living forms of Strongyloides stercoralis 481±2,
484
Fujii, Y. 370
fumagillin 189±90
fungi, microsporidia related to 174, 184

furazolidone 231, 232, 364
GAE see granulomatous amebic encephalitis
Gal/GalNAc lectin, Entamoeba histolytica 200±1,
202, 204, 210, 212
gametocytes, malarial 55, 56, 78, 92
Gastrodiscoides hominis 637, 639, 641, 645
gastrointestinal disease
Blastocystis hominis 360±1, 362
chronic Chagas' disease 339, 341, 343±4
strongyloidiasis 489
gelatin particle agglutination test 491
gene expression, Entamoeba histolytica 203±4
gene sequencing, microsporidia 184
genetic predisposition and Ascaris burden 568
genitourinary schistosomiasis 390±1
genome, Entamoeba histolytica 203
genotypes of Cryptosporidium parvum 140, 142
geographical information systems (GISs) 44±5, 49
geophagia 504, 509, 511, 512
Giardia lamblia/giardiasis
antigenic variation 222±3
clinical features 227±8
chronic giardiasis 228
description 219±22
encystation and excystation 223
growth requirements 222
history 219
immune response 224±5
laboratory diagnosis
antigen detection assays 229

culture 230
drug sensitivity testing 230±1
duodenal sampling 229
ova and parasite examination 229
serology 230
management 231±3
asymptomatic infections 232±3
drugs 231±2
in pregnancy 233
resistance and relapse 233
pathogenesis
cytokine response 224
di€erences between isolates 223±4
trophozoite adherence to intestinal mucosa 224
predisposition to 225
prevention and control 233±4
in day care centres 234


656

INDEX

Giardia lamblia/giardiasis (cont.)
species 222
transmission 225±6
cross-species 227
food-borne 226
person-to-person 226
travelers 226±7

water-borne 226
trophozoite analysis 222
Giardia-speci®c antigen 65 (GSA 65) 229
gliding motility, Toxoplasma gondii 118, 119
Glossina spp. 45±6, 323, 325, 326, 327
glucose-6-phosphate dehydrogenase (G-6-PD) de®ciency
63, 64
primaquine therapy 76, 83
glutathione-S-transferases
hookworm 570±1
Sm-28 397
Gnathostoma spinigerum 536, 539±40
epidemiology 541
life-cycle 540±1
gnathostomiasis 541
clinical features 541
cerebral disease 542
visceral disease 541±2
diagnosis 542
management 542
organism see Gnathostoma spinigerum
prevention and control 543
Golgi, Camillo 14, 53
GoÈze, Johann 2, 9, 10, 585
GP63 293, 297
granular form, Blastocystis hominis 357, 359
granulomas, egg see egg granulomas
granulomatous amebic encephalitis (GAE) 277
clinical management 281±2
clinical signs and symptoms 277

laboratory diagnosis 280±1
organisms see Acanthamoeba spp; Balamuthia mandrillaris
pathogenesis 274±5
pathological features 278±80
Grassi, Battista 16, 479, 480
growth retardation see stunting
GSA 65 (Giardia-speci®c antigen 65) 229
guinea worm see Dracunculus medinensis
gynecophoral canal, Schistosoma spp. 371, 373
halofantrine 77, 81, 84
halzoun 418
Haplorchis spp. 636
description and life cycle 637, 643
epidemiology 644
treatment of infection 644
Harada±Mori method 490
heart disease, chagastic 338±9, 341, 343, 347, 348

helminths
cognitive impairment and infection with 562
global prevalences 30, 564
population dynamics 27±8
sex bias in infection levels, meta analysis 38±41
see also speci®c parasites
hematoxylin and eosin stain 187, p.iv, p.v
hemoglobin S 64
hemozoin 62, 108
hepatitis B vaccine interference 387
hepatitis/schistosome co-infections 387, 391
hepatobiliary ¯ukes 407, 411

Dicrocoelium spp. 420±1
Metorchis conjunctus 420
see also Fasciola hepatica; Opisthorchis spp; Clonorchis
silensis
hepatocellular carcinoma risk in schistosomiasis 382
Heterophyes heterophyes 636
description and life cycle 637, 639, 643
epidemiology 644
treatment of infection 642, 644
heterophyidiasis
clinical features 638, 644
laboratory diagnosis 644
organisms see Haplorchis spp; Heterophyes heterophyes; Metagonimus yokogawai
treatment 644
Hippocrates 53
history of parasitology
belief in spontaneous generation 1±2
chemotherapeutic agents 19
development of protozoology 12
establishment of the discipline 19
nineteenth century 2±3
Casimir Davaine 3, 6
early texts 3, 4
Thomas Spencer Cobbold 3, 5
origins of the discipline 2
see also speci®c organisms
HIV/AIDS see AIDS/HIV infection
HLA antigens and cysticercosis 621
HMS (hyper-reactive malarial splenomegaly) 61
homosexual males, Entamoeba infection 206, 213

hookworm platelet inhibitor 571
hookworms
classi®cation 569
clinical features of infection 571
di€erentiation from Strongyloides stercoralis 482,
483
history 7±8, 568
immunology 570±1
life-cycle 569
skin penetration 569±70
pathogenesis 570
see also Ancylostoma caninum/A. braziliense
hormonal in¯uence on Trichomonas vaginalis 246


INDEX
horse meat 526, 531
host mediators in babesiosis injury 104
host-adapted Echinococcus spp. 588, 589
household clusters of strongyloidiasis 489, 493
HSP70 genes 184
hydatid cysts 587, 588
chemotherapy for 604±5
detection 603, 604
Echinococcus granulosus 591±4, 595±6, 602
Echinococcus multilocularis 592, 593, 594, 596
Echinococcus vogeli/E. oligarthrus 594±5, 596
history 10, 585
protection from host immunity 597±8
surgical removal 604, 605

hydatid disease see echinococcosis
hydroceles 43, 438±9, 444
hydrogenosomes 245±6, 258, 260
Hymenolepis nana
diagnosis and treatment 629
epidemiology 628
life-cycle 627±8
hyper-reactive malarial splenomegaly (HMS) 61
hypnozoites 54, 55, 75
hypoglycemia in malaria 63, 70, 79
IFNg see interferon gamma
IgA response
giardiasis 225
strongyloidiasis 487
trichinellosis 524
IgE assays
Toxocara spp. 514
Toxoplasma gondii 130
IgE response
schistosome reinfection 388
strongyloidiasis 487
IgG response, strongyloidiasis 486±7
IgG4 assays, ®larial infections 442, 462
IgM assays
Toxoplasma gondii 123, 130, 131
see also serological diagnosis
IgM response
African trypanosomiasis 321
strongyloidiasis 487
imidocarb 109

immune evasion
Fasciola hepatica 416
hookworms 571
Paragonimus spp. 422±3
Schistosoma spp. 384±5
disrupted by praziquantel 395
immune modulation, chronic schistosomiasis 381, 386
immune suppression
by Onchocerca volvulus 462
by Trypanosoma brucei 321
by Trypanosoma cruzi 339±40

657

immune tolerance
in cysticercosis 621
in onchocerciasis 462, 463
in strongyloidiasis 487
immunocompromised patients
cryptosporidiosis in 150, 154
granulomatous amebic encephalitis in 274±5
microsporidial infections in 180, 181, 189, 191
reactivation of Trypanosoma cruzi 344, 348
Strongyloides stercoralis hyperinfection 485±6
toxoplasmosis in 124±6, 132±3
transfusion-associated Chagas' disease in 342
see also AIDS/HIV infection
immunotherapy for leishmaniasis 308
imported malaria 68, 69
incremental cost±e€ectiveness ratios 33±4

in¯ammatory response, cysticercosis 621, 624
innate resistance to malaria 64
insecticidal control
black¯ies 472±3
mosquitoes 54, 87
impregnated bednets 87±8
sand ¯ies 308±9
tsetse ¯ies 331
insecticide resistance 473
intensity of infection, intestinal nematodes 27, 28, 565±6
interferon gamma (IFNg)
in cryptosporidiosis immunity 146
in leishmaniasis immunity 293, 294, 295, 296
mediation of Trypanosoma brucei immune suppression 321
in microsporidiosis immunity 183
recombinant
Chagas' disease treatment 347
leishmaniasis treatment 306±7, 308
response to Entamoeba histolytica 202
stimulation of trypanosomal growth 321±2
in toxoplasmosis immunity 120, 121
in Trypanosoma cruzi immunity 339
interleukin 1 (IL-1) 295
interleukin 2 (IL-2) 295, 296, 339, 462
interleukin 4 (IL-4) 295, 296, 462
interleukin 5 (IL-5) 295, 296, 462, 463, 524
interleukin 6 (IL-6) 462, 470
interleukin 8 (IL-8) 152
interleukin 10 (IL-10) 295, 296, 340, 462, 463
interleukin 12 (IL-12) 121, 146, 295, 488

intestinal ascariasis 568
intestinal disease pathogenesis
Cryptosporidium parvum 142±5
microsporidia 181, p.iv, p.v
intestinal nematodes
entry to the host 566
epidemiology
global disease burden 564
infection intensity and transmission 565±6


658

INDEX

intestinal nematodes (cont)
history 561
laboratory diagnosis
egg identi®cation 577±8
¯otation techniques 577
formol±ether concentration 577
Kato±Katz technique 577
larval identi®cation 578
simple fecal smears 576±7
specimen handling 576
life-cycles 566
pathogenesis
cognitive impairment 562
morbidity 563±4
prevention and control 580

species associated with human intestines 562, 563
treatment 578±80
see also speci®c organisms
intestinal obstruction with Ascaris lumbricoides 568
intestinal trematodes 635, 639
infecting humans 636±7, 638
life-cycles 635, 637
see also speci®c organisms
intradermal test for paragonimiasis 427, 428
iodination of water 234
iodoquinol 211, 364
ipecac bark 198
iron
e€ects on Trichomonas vaginalis 247, 249
loss in hookworm infection 570
irradiated cercarial vaccines 387
isosporiasis
clinical features 157
clinical management 157±8
epidemiology 156±7
history 156
Isospora belli 156
laboratory diagnosis 157
pathogenesis and immunology 156
prevention and control 158±9
ivermectin treatment
adverse reactions in loiasis 448, 472
cutaneous larva migrans 539
lymphatic ®lariasis 443
Mansonella ozzardi infections 450

onchocerciasis 471
adverse reactions 472
mass treatment campaigns 474
strongyloidiasis 492
Ixodes scapularis life-cycle 101
kala-azar 301±3
Kartulis, Staphanos 12
karyotypic analyses, Blastocystis hominis
Katayama fever 370, 388±9
Kato±Katz technique 392, 577

360

Katsurada, Fujiro 11, 370
keyhole limpet antibodies 394
kinetoplasts
Leishmania spp. 288, 289, 297
Trypanosoma brucei 316, 318, 322, 330
Trypanosoma cruzi 336, 346
kissing bugs see triatomine vectors
knob-associated histidine-rich protein (KAHRP) 62
knock-out mice, egg granuloma studies 385, 386
lactoferrin 152
lactose malabsorption 228
laminated layer, Echinococcus spp. 591, 593, 594,
598, 604
Landsat Thematic Mapper 45
larva currens 489
larvae
Dracunculus medinensis 553, 555, 556, 557

Echinococcus spp. see hydatid cysts
Gnathostoma spinigerum 541
hookworm 537±8, 569
intestinal nematode 566, 578
lymphatic ®lariae 434
Onchocerca volvulus 458, 459
Sparganum mansoni 546
Strongyloides stercoralis 482±4
Taenia spp. see metacestodes: Taenia spp.
Toxocara spp. 502, 503, 504, 505
Trichinella spp. 522, 523
larvicidal control of black¯ies 472±3
latent microsporidial infections 183
Laveran, Alphonse 14, 53, 479
Leeuwenhoek, Anthony van 1±2, 10, 12, 13, 219
Leidy, Joseph 19, 521
Leishman, William 19, 287
Leishmania spp. 288, 289
of the Americas
L. (L.) amazonensis 298
L. (L.) chagasi 296, 298±9, 302
L. (L.) mexicana 298
L. (V.) braziliensis 296, 298
L. (V.) guyanensis 298
L. (V.) panamensis 298
L. (V.) peruviana 298
biochemistry 297
classi®cation 288
cultivation 290, 291, 304
epidemiology 288, 297±8

immunology 293
interactions with macrophages 293±4
mouse models of cell-mediated immunity 294±6
life-cycle 290
molecular biology 297
morphological forms 288, 289, 291, 292
of the Old World
L. (L.) aethiopica 299


INDEX
L. (L.) donovani 294±5, 296
L. (L.) dovani 299±300
L. (L.) major 295, 299
L. (L.) tropica 299
L. (L.) infantum 299±300
pathogenesis 291
cutaneous disease 291, 292±3
visceral disease 293
vectors 289, 290
leishmaniasis
cutaneous
di€use 292, 301
immune response to 296
simple 300±1
treatment 307±8
diagnosis
leishmanin skin test 305
parasite identi®cation and culture 304±5
serology 305

drug therapy 305±7
history 18±19, 287±8
immunology 296±7
leishmaniasis recidiva 292±3, 299, 301
mucosal 301, 302
treatment 308
organisms see Leishmania spp.
post-kala-azar dermal leishmaniasis 304
prevention 308±9
visceral 301±3
in AIDS/HIV infection 203
immune response to 296
treatment 307
viscerotropic 303±4
leishmanin skin test 305
leopard skin 467, 468
Leuckart, R. 457, 480, 585±6
leukovorin 131, 132, 133
levamisole 449, 579
Linnaeus, Carl 10
lipophosphoglycan (LPG) 293, 297
liposome-encapsulated amphotericin B 306, 307
liver abscesses, Entamoeba histolytica see amebic liver
abscesses
liver function in malaria 63
liver infection
Fasciola hepatica 415, 416
microsporidia 183
Paragonimus spp. 422, 425
liver-trapping phenomenon 507

Livingstone, David 17
Loa loa 434
epidemiology 445±6
life-cycle 445
loiasis 445
clinical manifestations 446
complications 446±7

659

diagnosis 441, 447
organism see Loa loa
prevention 448
treatment 448
Looss, Arthur 7, 11
lovastatin 109
Low, George Carmichael 9, 16, 18
LPG (lipophosphoglycan) 293, 297
lumbar puncture 74
lung ¯ukes see pulmonary ¯ukes
Lyme disease concurrent with babesiosis 106, 108,
109±10
lymphatic ®lariae
epidemiology
Brugia malayi and B. timori 434±5
Wucheria bancrofti 435
life-cycle 434
lymphatic ®lariasis 433±4
acute manifestations 436±7
asymptomatic micro®laremia 436

bancroftian ®lariasis 434, 436
lymphedema of the limbs 438
male genital disease 438±9
brugian ®lariasis 434, 436, 438
chronic manifestations 437±8
adenopathy 440
chyluria 439
®larial granulomata 439
hydroceles 438±9
lymphedema of the genitalia 439
lymphedema of the limbs 438
tropical pulmonary eosinophilia (TPE) 439
diagnosis 440
antigen detection 441
imaging studies 442
microscopical detection and speciation 440±1
PCR 442
serology 441±2
disease mapping 46
at global and regional levels 46±8
at village level 48±9
history 8±9
micro®laraemia and chronic disease, meta-analysis
41±4
in movers to endemic areas 440
organisms see lymphatic ®lariae
pathology 435
prevention and control 445
treatment
acute manifestations 443

asymptomatic micro®laremia 442±3
chronic manifestations 443±5
dosage of DEC 445
lymphoscintigraphy 442
macrophage in¯ammatory protein-1a

296


660

INDEX

macrophages, in immunity to Leishmania spp.
293±6
magnetic resonance imaging (MRI)
granulomatous amebic encephalitis 281
neurocysticercosis 622, 626
primary amebic meningoencephalitis 280
toxoplasmosis 126, 127
malaria
airport 68
antimalarial drugs 81±6
cerebral 60, 79
clinical examination 74
clinical features 69
in children 71
falciparum malaria 70
Plasmodium vivax/P. ovale/P. malariae malarias
70±1

in pregnancy 71
clinical management, in pregnancy 81
clinical management, severe malaria 78
anemia 79
bacterial infections 79
cerebral malaria 79
chemotherapy 80±1
circulatory collapse 79
exchange transfusion 79±80
follow-up 81
hydration 78
hypoglycemia 79
renal function 78
clinical management, uncomplicated malaria 74,
77±8
drug dosages 76
eradication therapy, Plasmodium vivax/P. ovale
malarias 75±6
Plasmodium falciparum malaria 75, 76±7
Plasmodium vivax/P. ovale/P. malariae malarias
74±5
control 86±7
chemoprophylaxis in endemic areas 87
early treatment 86±7
vector control 87±8
epidemiology
Anopheles mosquito variation 67
drug resistance 69, p.vi
geographic distribution 66±7, p.vi
patterns of clinical disease 68±9

prevalence 66
resurgence 66
transmission modes 67±8
history 14±16, 53±4
immunity 63
clinical, in endemic areas 64±5
innate resistance 64
non-speci®c 64
speci®c (acquired) 63±4

laboratory diagnosis 71
microscopy 71±3
PCR 73
rapid antigen tests 73, 74
serology 73, 74
organisms see Plasmodium spp; speci®c Plasmodia
pathology of clinical syndromes 61
anemia 62
cerebral malaria 61±2
hypoglycemia 63
pregnancy 63
renal failure 62±3
respiratory distress 62
thrombocytopenia and coagulation 62
prevention in travelers 88
chemoprophylaxis 88±90
presumptive treatment 90
role of the spleen 60, 61
splenectomized patients 71
vaccine development 25, 91

blood stage vaccines 91±2
DNA vaccines 92
pre-erythrocytic vaccines 91
transmission-blocking vaccines 92
Malarone1 76, 78, 86, 89, 90
Manson, Patrick 6, 8, 9, 11, 16
Mansonella ozzardi 434
epidemiology 450
life-cycle 441, 450, 461
Mansonella perstans 434
epidemiology 449
life-cycle 441, 449, 461
MAP-4 397
mast cells in Trichinella expulsion 524
Mazzotti test 470
mebendazole treatment
clonorchiasis and opisthorchiasis 414
cystic echinococcosis 605
eosinophilic enteritis 539
intestinal nematode infections 578
perstans ®lariasis 449
strongyloidiasis 492
toxocariasis 515
trichinellosis 530
me¯oquine treatment 82±3
prophylaxis 76, 89, 90
severe malaria 81
uncomplicated malaria 75, 77
megadisease 339, 341, 343±4, 347±8
meglumine antimonate 306, 307

Melanesian ovalocytosis 64
melarsoprol 330±1
meningeal cysticercosis 624, 627
mepacrine hydrochloride 54
merogony, microsporidia 173, 174, 176, 178, 180
meronts
Cryptosporidium parvum 141, 142


INDEX
Cyclospora spp. 166
microsporidia 172, 173, 174±5, 176±7, 178±9
merozoites
Babesia spp. 100, 103
Cryptosporidium parvum 141, 142, 147
Plasmodium spp. 54, 55, 56, 58, 92
meta-analyses 37±8, 44
examples 38±44
metacercariae, intestinal trematodes 635, 637, 638,
641, 643
metacestodes
Echinococcus spp. see hydatid cysts
Taenia spp. 614, 615, 616, 617, 622
Metagonimus yokogawai 636
description and life-cycle 637, 639, 643
epidemiology 644
treatment of infection 642, 644
Metorchis conjunctus 420
metrifonate 396
metronidazole treatment

Blastocystis hominis infections 364
Dientamoeba fragilis infections 263
Entamoeba polecki infections 214
giardiasis 231, 232, 233
invasive amebiasis 211
trichomoniasis 254±5
miconazole 281
micro®lariae
Diro®laria spp. 547
Loa loa 445, 446, 448
lymphatic ®lariae 433, 434
detection and speciation 440±1
killing with DEC 443, 444, 445
micro®laremia 436
Mansonella ozzardi 441, 450, 461
Mansonella perstans 441, 449, 461
Onchocerca volvulus 459, 460±1, 464
detection 468, 469, 470
microsporidia
aniso®lar polar tube group 174±5, 176, 177, 178, 179
diplokaryotic group 174±5, 178, 179, 180
Encephalitozoon spp. 171, 174±6, p.iv, p.v
Enterocytozoon bieneusi 171, 174, 175, p.iv, p.v
epidemiology
Encephalitozoon spp. 185±6
Enterocytozoon bieneusi 185
other species 186±7
questions 185
transmission 184±5
genera and species, listed 171±2

life-cycles 172, 173
molecular biology 184
phylogeny 172, 174
spores see spores: microsporidia
microsporidioses 171±95
clinical management 189

661

albendazole 190
fumagillin 189±90
other drugs 190±1
TNP-470 190
history 171
immunology 183±4
laboratory diagnosis
microscopy 187, p.iv, p.v
PCR 188±9
serology 187±8
organisms see microsporidia
pathogenesis 180±3
Microsporidium spp. 176±7, 178, 181, 182
migrating worms 535, 536
see also speci®c species
miltefosine 307
miracidia
Fasciola hepatica 408, 415
intestinal trematodes 635, 637, 638, 641, 643
Opisthorchis and Clonorchis spp. 408, 410
Paragonimus spp. 408, 421

Schistosoma spp. 372, 373, 374
miracil 371
molecular karyotypes of microsporidia 184
molecular taxonomy see phylogenetic analysis
molluscicides 371
monocyte chemoattractant protein-1 296
monthly biting rate (MBR)/transmission potential
(MTP) calculations 464
mosquitoes
control 87
in Diro®laria immitis life-cycle 547
lymphatic ®lariae transmission 434, 435
microsporidia infections in 186±7
see also Anopheles mosquitoes
mouse models
Giardia infection 224
leishmaniasis cell-mediated immunity 294±6
schistosomal egg granuloma induction 385±6
toxocariasis 510±11, 512
trichinellosis immunity 523±4
mucins, colonic 200
mucosal leishmaniasis 301, 302
multivacuolar form, Blastocystis hominis 358, 359, p.vii
multivesicular/alveolar echinococcosis (MAE)
clinical features 602
clinical management 605±6
diagnosis 603, 604
pathogenesis 596
see also Echinococcus spp.
muscle biopsy for trichinellosis diagnosis 529

muscle cysticercosis 624
myocardial infection, microsporidia 182, p.iv, p.v
myosins 118
Nabarro, David 18


662

INDEX

Naegleria fowleri
culture 273±4
epidemiology 276, 277
history 269
immunology 275, 276
life-cycle 271, 272
molecular biology 276
taxonomy 270
see also primary amebic meningoencephalitis (PAM)
nagana 17, 335
Nanophyetes salmincola 637, 645
natural-resistance-associated macrophage protein
(Nramp) 294±5
Necator americanus 569, 570, 571
neonatal trichomoniasis 246, 252
neural paragonimiasis 424, 425, 429
neurocysticercosis (NC) 617
clinical features 624
diagnosis 626
epidemiology 619±20

pathology 621±3
see also cysticercosis
neuroschistosomiasis 383
neurotrichinellosis 527
neutral thiol protease (NTP) 423
neutrophil inhibitory factor, hookworm 570
neutrophils in Trichomonas vaginalis infection 249
niclofan 429
niclosamide 629, 640, 642, 644
nifurtimox 346±7, 348
nitazoxanide 154
nitric oxide 120, 121, 202, 294, 321
nitroimidazole treatment
Blastocystis hominis 364
giardiasis 230±2
trichomoniasis 254±5
see also speci®c drugs
nitrosamines 413
normalized di€erence vegetation index (NDVI) 45,
46
Normand, Louis 479
Nosema ocularum 173, 180, 181
Nramp (natural-resistance-associated macrophage protein) 294±5
nurse cells 523
nutrient malabsorption, chronic giardiasis 228
obstructive biliary disease 412, 417, 418
occupational risk of schistosomiasis 379
ocular disease
cysticercosis 624, 627
diro®lariasis 548

gnathosomiasis 542
microsporidiosis 182
onchocerciasis 461±2, 467
toxocariasis see ocular larva migrans

toxoplasmosis 124, 125
trichinellosis 527
ocular larva migrans
clinical features 511±12
epidemiology 510
history 501±2
laboratory diagnosis 514±15
treatment 515±16
odds ratios 41
Onchocerca volvulus
life-cycle 458, 459
adult worms 458, 459±60
micro®lariae 459, 460±1
strain di€erences 464
taxonomy 458
onchocerciasis
clinical features 466±8
clinical management
amocarzine 472
historical 470±1
ivermectin 471±2
epidemiology 463
entomology 465±6
geographical variation 464
infective vector density 463±4

history 457, 458
immunology 462±3
laboratory diagnosis
Mazzotti test 470
skin snips 468±70
slit lamp examination 470
organism see Onchocerca volvulus
pathogenesis 461±2
prevention and control 472
mass ivermectin treatment 474
nodulectomy campaigns 474
vaccine development 475
vector control 472±3
Onchocerciasis Control Programme 473
onchocercomata see subcutaneous nodules: in onchocerciasis
Oncomelania snails 376
oncospheres
Echinococcus spp. 587, 590±1, 597
Taenia spp. 614, 615, 616, 617
O'Neill, J. 457
oocysts
Cryptosporidium parvum 139
elimination in drinking water 155
infection potential 148
in life-cycle 141, 142
PCR detection 152, 153
viability determination 153
virulence 145
visualization 151, 152
Cyclospora spp. 165, 166, 168