Parasites of Cattle and Sheep

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Parasites of Cattle and Sheep
A Practical Guide to their Biology
and Control

by

Andrew B. Forbes
Scottish Centre for Production Animal Health and Food Safety
School of Veterinary Medicine
University of Glasgow
UK

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© Andrew B. Forbes, 2021. All rights reserved. No part of this publication may be reproduced in any form
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permission of the copyright owners.
A catalogue record for this book is available from the British Library, London, UK.
Library of Congress Cataloging-in-Publication Data
Names: Forbes, Andrew B., author.
Title: Parasites of cattle and sheep : a practical guide to their biology and control / by Andrew B. Forbes,
Scottish Centre for Production Animal Health and Food Safety, School of Veterinary Medicine, University
of Glasgow.
Description: Wallingford, Oxfordshire ; Boston, MA : CAB International, [2021] | Includes bibliographical
references and index. | Summary: "This book provides the first review devoted to parasites of domestic
cattle and sheep. It considers the impact of parasites, both as individual species and as co-infections,
as well as epidemiological information, monitoring, diagnostic procedures, and implementing control
measures such as the responsible use of parasiticides"-- Provided by publisher.
Identifiers: LCCN 2020031633 (print) | LCCN 2020031634 (ebook) | ISBN 9781789245158 (paperback) |

  ISBN 9781789245165 (ebook) | ISBN 9781789245172 (epub)
Subjects: LCSH: Cattle--Parasites. | Sheep--Parasites.
Classification: LCC SF967.P3 F67 2021 (print) | LCC SF967.P3 (ebook) | DDC 636.2/089633--dc23
LC record available at />LC ebook record available at />References to Internet websites (URLs) were accurate at the time of writing.
ISBN-13: 9781789245158 (paperback)
9781789245165 (ePDF)
9781789245172 (ePub)
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Contents

Prefacevii
Acknowledgementsix
1  The Origin and Evolution of Parasitism in Domestic Ruminants

1

2  Parasitic Gastroenteritis in Cattle

10

3  Parasitic Gastroenteritis in Sheep: Teladorsagiosis and Trichostrongylosis


37

4  Parasitic Gastritis in Sheep: Haemonchosis; and Parasitic Enteritis in Lambs: Nematodirosis

64

5  Tapeworm Infections

88

6  Parasitic Enteritis: Coccidiosis

102

7  Lungworm Infections in Cattle

116

8  Lungworm Infections in Sheep

139

9  Liver Fluke

149

10  Rumen Fluke

201


11  The Lancet or Lanceolate Fluke

217

12  Obligate Ectoparasites of Cattle: Lice and Mange Mites

224

13  Ectoparasites in Cattle: Flies

244

14  Ectoparasites of Sheep: Sheep Mange Mites

267

15  Sheep Ectoparasites: Insects

275

16  Ticks and Tick-borne Disease

295

17  Grazing Management and Helminth Control on Stock Farms

312

18  Responsible Use of Parasiticides


331

19  Principles and Practical Implementation of Parasite Control on Livestock Farms

342

Index351

v

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Preface

There are several excellent general textbooks on veterinary parasitology and also many that cover individual
parasite groups or parasitism in particular host species; however, to date, no single volume is devoted to the
common parasites of sheep and cattle. This book seeks to fill that gap; the rationale for including both ruminant species is that cattle and sheep are kept together on many livestock farms, and while some parasites are
quite species-specific and restricted to cattle or sheep, several are generalists and can infect both. The species
specificity of different parasites is an important component in approaches to control, some of which can be
used to advantage; for example, mixed grazing to help control parasitic gastroenteritis in both sheep and
cattle, whereas the control of liver fluke, which can infect both hosts and indeed other animals, can be more
challenging when more than one host is present.
The scope of this book is the common parasites of cattle and sheep, with emphasis on those occurring in
the temperate regions of the northern and southern hemispheres. The reason for focusing on parasites that
are frequently encountered is to acknowledge the old adage that ‘common things occur commonly’, and when
it comes to control, which ultimately has to be incorporated into livestock farm management of all types, it

is preferable to focus on the everyday rather than the exotic. Although parasite species that are important in
the tropics and sub-tropics are not explicitly excluded from this book – haemonchosis, for example, is covered in some detail – several very important parasitic diseases, particularly those that are vector-borne, have
not been included. Though I have worked in some of these regions, to do justice to these topics, local expertise is required, and this can be found in various textbooks and the scientific literature, to which readers are
directed.
Not all protozoal diseases are addressed here; the reasons are threefold:
● First, although they are parasitic in nature, some species are more logically dealt with in a systems approach,
thus cryptosporidiosis in the neonatal diarrhoea complex and toxoplasmosis and neosporosis within abortion and infertility.
● Second, treatment and control of these protozoans generally require different products, vaccines and management, appropriate to these organisms, whereas there is a lot of overlap in the epidemiology and control
of many helminths and some ectoparasites, so they can be considered together at farm level.
● Third, because I have little personal experience of some of these and other protozoan diseases such as
besnoitiosis, there seems little point in merely regurgitating what can be found in review papers or text
books.
I am fortunate in that I have worked to a greater or lesser extent on virtually all the other parasites in this
book, through my early career as a veterinary surgeon in practice, in the animal health industry, as an advisor
and researcher, as a teacher and through running a small sheep farm at our home.
While this book is not intended as a bibliographic review, each chapter has an extensive list of references
that support the factual content, guide the opinions given and provide readers with sources of additional
information, should they wish to pursue subjects further. Several papers were published many years ago; a
few are more than one hundred years old. The reasons for including them are various, but include the fact
that many contain observations and descriptions of parasites and parasitism that have simply not been bettered; I also think it is important to track down original references so that they can be cited accurately. It is
fortunate that many journals have archives that go back to their origins and papers can be accessed via various websites: a boon for researchers and writers. For papers that are not available electronically, hard copies
of journals need to be tracked down in libraries.
There is an acknowledged bias in the literature cited, as I have focused on those written in English, which
has become the most widely used language in scientific writing, meaning that some papers in other languages
Preface 

vii

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have not been cited. This is another reason for citing the older literature, as the authors of that era were far
more conscientious in tracking the literature in all languages, including German and Russian, in which much
was written.
Although I have been lucky enough to work in several different parts of the world, my origins and current
domicile in Britain are reflected to some extent in the content of this book, particularly in some of the epidemiology in relation to farming practices. However, given the background information provided, it is hoped
that reasonable extrapolations can be made to other regions and different farming systems.
It would be a monumental task to try and provide up-to-date, accurate information on the multitude of
antiparasitic products available worldwide and local differences in formulations, claims, recommendations
and restrictions, so most of the information provided on parasiticides and vaccines in this book is based on
those available in the UK at the time of writing. Primary sources of information on licensed products in the
UK are the Veterinary Medicines Directorate (VMD) and the National Office for Animal Health (NOAH) />The layout adopted in this book is to provide quite detailed descriptions of the main groups of parasites,
how they affect farm livestock and approaches to control. Given my somewhat pessimistic view that there
will be few meaningful developments in large animal parasiticides in the short-term future, it is crucial that
all other options for control are explored, and this requires a good understanding of the biology behind the
diseases. The framework that I have adopted has proved useful in teaching and it does place emphasis on
building a complete picture of parasitism before contemplating treatment and control (Fig. 1).
I frequently recall a statement made by a prominent livestock farmer, which was ‘farmers in the main want
to know what to do; very few, if any, want to know why’. At the time I was somewhat taken aback as it
seemed to undermine much of what I believe insofar as advice and actions based on knowledge and understanding should be superior to those made randomly or intuitively, without a substantial evidence base, but
then I realized that I have precisely the same approach to many subjects, from cars to computers. Nonetheless,
while not ignoring such views, the control of parasites ultimately is a filtering of accumulated general knowledge and wisdom, and adapting and applying it to specific farm circumstances and the aspirations of individual farmers. Ultimately, everyone wants to see healthy, well-performing livestock and contented farmers,
and a sound understanding of parasitism, its impact and management is central to achieving these aims.
Andrew B. Forbes

Pathology
Pathophysiology

Diagnostics
Impact


Host–parasite
interactions
Immunity

Control

Epidemiology
Free-living stages

Risk & patterns
of exposure

Monitoring

Fig. 1.  Flow diagram of accumulation of knowledge leading to rational approaches to the control of helminth
infections.

viii

Preface

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Acknowledgements

Although I am the sole author of this book, numerous people have knowingly or unknowingly helped and
inspired me, and this is the time to pay tribute to some of those groups and individuals.
The expertise and scientific literature emanating from institutions such as the Central Veterinary

Laboratory in Weybridge, the Moredun and the University of Glasgow, during what were, arguably, some of
the halcyon days of discovery in ruminant parasitology from the 1950s to the 1980s, have been a great
inspiration to me long before and during the writing of this book.
Much of my career was spent in technical services and research and development in the animal health
industry, and during that time, I received support and encouragement from colleagues too numerous to mention, but including: Alexandra Batard, Dietrich Barth, David Biland, Edson Bordin, Cédric Dezier, Fiona
MacGillivray, Jean-Jacques Pravieux, John Preston, Steffen Rehbein, Steve Rochester, Dieter Schillinger, Mark
Soll, Marie-Pascale Tiberghien, Sioned Tmothy and Roddy Webster. More recently, it has been a pleasure and
a privilege to work with students and colleagues at the University of Glasgow; to name but a few: Valentina
Busin, Kathryn Ellis, Kim Hamer, Abi Jackson, James McGoldrick, Jane Orr and Mike Stear.
The University of Ghent has been important in several respects, but not least for fostering my ambitions
to get a PhD, and among numerous people there, I worked particularly closely with Jozef Vercruysse and
Johannes Charlier. Much of the research that contributed towards my thesis was carried out at what was
then called the Institute of Grassland and Environmental Research in Devon, where I had invaluable support
from Malcolm Gibb, Chris Huckle and Andrew Rook; I also had the pleasure of working with Christina
Marley at the sister organization in Aberystwyth. Mark Fox of the University of London has always been a
valued colleague and provided much helpful advice.
Among many in other universities and research establishments, I would like to mention Christina Strube,
the late Thomas Schnieder and Georg von Samson-Himmelstjerna of the University of Hanover; Dave
Bartlett, Frank Jackson, Fiona Kenyon and Philip Skuce of the Moredun; Eric Morgan and Richard Wall
from the University of Bristol; Clarke Scholtz from the University of Pretoria; Ilias Kyriazakis of the
University of Newcastle; Diana Williams from the University of Liverpool; Dermot O'Brien and Grace
Mulcahy, Dublin; Ian Fairweather of the University of Belfast; Rob Kelly and Neil Sargison, University of
Edinburgh; Giuseppe Cringoli and Laura Rinaldi, University of Naples Federico II; Johan Höglund, Swedish
University of Agricultural Sciences; Georgina Grell, UK-Vet Livestock; Heinz Strobel, Schafpraxis, Germany;
Sinclair Stammers, MicroMacro; and Dave Leathwick, AgResearch in New Zealand.
Collectively many people from various other organizations have been the source of information and ideas,
including the World Association for Veterinary Parasitology (WAAVP), British Association of Veterinary
Parasitology (BAVP), British Cattle Veterinary Association (BCVA), Sheep Veterinary Society (SVS), British
Grassland Society (BGS), British Society of Animal Science (BSAS), Scottish Agricultural College (SAC), and
Agriculture and Horticulture Development Board (AHDB) Beef and Lamb.

I particularly thank those who have allowed me to use some of the photographs to illustrate this book:
Karol Racka (Slovakia), Chris Watson (Gloucester), Kat Bazeley (Dorset), Kathryn Ellis, Richard Irvine and
Gordon Robertson (Glasgow) and Steffen Rehbein (Germany). As is convention, I absolve all the above and
many others that I have not mentioned of blame for any mistakes I have made in this manuscript. Neither
does their being named imply that they agree with my views on some of the more contentious subjects, for
example, the merits of faecal egg counting, environmental risk assessments and dose-and-move practices to
control nematode parasitism.
My publishers at CAB International have been patient and accommodating in the extreme, having missed
several deadlines and created a monster several times bigger than planned or intended. So thank you Alex
Lainsbury and Ali Thompson, and I hope the effort proves worthwhile.
ix

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Needless to say, those that have had their tolerance stretched to the limit during the writing of this book
have been my family, in particular my wife, Tricia, who has had to put up with my frequent absences in various
rooms in the house where I have camped and progressively filled with more and more papers and books.
Thank you to one and all.

xAcknowledgements

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1



The Origin and Evolution of

Parasitism in Domestic Ruminants
Introduction

Parasitism is one of the most successful lifestyles in
nature (Poulin and Morand, 2000) and, although it
is impossible to know precisely how many parasite
species exist (Poulin, 2014; Strona and Fattorini,
2014), it has been estimated that parasitic species
considerably outnumber all the free-living species on
Earth (Windsor, 1998). There are at least 50% more
parasitic helminth species than vertebrate hosts, and
among mammals, each individual animal can harbour two cestode, two trematode and four nematode species of parasite over its lifetime (Dobson
et al., 2008).
There are several definitions of parasitism, all of
which describe an association between one organism (the parasite) and another (the host) in which
the parasite derives some benefits, whereas the host
gains no advantage and may be harmed. Although
there are a few parasites that can switch to a nonparasitic life cycle, for example, the threadworms,
Strongyloides spp. and blowflies, which can feed on
non-living substrates such as carrion, the vast
majority of parasite species are dependent on their
hosts for all or part of their life cycle (Smyth,
1962).

Parasites
Parasites can be subdivided into those species that
are found inside the host (endoparasites) and those
that live in or on the skin (ectoparasites). While there
are some exceptions, endoparasites are typically helminths, comprising nematodes (roundworms), trematodes (flatworms) and cestodes (tapeworms); most
ectoparasites are arthropods, either insects or arachnids. Strictly speaking, protozoa originally meant

early (eukaryotic) life forms; however, in parasitology the word has become synonymous with singlecelled organisms. Bacteria (prokaryotes), archaea and
viruses are the domain of microbiologists, while fungal
diseases of animals, though sometimes included

within parasitology (Euzéby et  al., 2005), are now
usually considered separately.

Evolution of Parasitism
Parasitism has evolved multiple times from free-­
living invertebrates belonging to diverse phyla that
had been present on Earth for millennia (Dorris et al.,
1999; Nagler and Haug, 2015). The evidence for the
origin and evolution of parasites comes largely from
fossils; however, there are obvious limitations of the
fossil record for small, soft-bodied organisms that
leave little or no direct evidence of their existence.
Nonetheless, through the fossil record and adoption
of newer molecular biology techniques (Donoghue
and Benton, 2007), a more complete picture of the
chronology of parasitism is possible, albeit the precise timing of events will inevitably change somewhat as new discoveries are made and new
methodologies adopted.
Additional sources of useful information on parasites that transit the gastrointestinal (GI) tract are
coprolites, which are fossilized dung and which can
contain remnants of parasite eggs. Currently, the earliest fossil evidence for intestinal parasitism in vertebrates stretches back to the Triassic period 240
million years ago (MYA) when ascarid eggs were
found in dinosaur coprolites (Poinar, 2015). Younger
specimens of dinosaur coprolites from the Cretaceous
period (130 MYA) yielded not only nematode eggs
and protozoal remains but also trematode eggs, representing an early record of parasitic flatworms
(Poinar and Boucot, 2006).

Fossil evidence points to the evolution of both
chewing and sucking lice somewhat later than the
helminths, probably around 77 MYA, coincident
with the initial radiation of mammals (Johnson and
Clayton, 2003; Light et al., 2010), though lice also
parasitize birds, which diversified earlier. Free-living
oribatid mites, which are the intermediate hosts for
several species of tapeworms, for example Moniezia
spp., have been found in fossils nearly 400 MYA

© Andrew B. Forbes, 2021. Parasites of Cattle and Sheep: A Practical Guide to their Biology 
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1


(Arillo et al., 2012), but the obligate parasitic mites
of vertebrates have a more recent history with fossil
remains found in the Eocene period, ~50 MYA
(Walter and Proctor, 2013).
Because of their chitinous exoskeletons, arthropods are preserved as fossils more readily than helminths and protozoa, while another rich source of
insect and arachnid remains is amber (Nagler and
Haug, 2015), which was formed from plant resins
deposited from ~320 MYA. Amber with remains of
arthropods currently dates from ~125 MYA, at
which time parasitism among invertebrates is evident, for example, a fly parasitized by a Leptus spp.
mite (Arillo et  al., 2018). Some remarkably wellpreserved specimens in amber have shown that ticks
parasitized animals 99 MYA (Peñalver et al., 2017),

though it has been estimated that ticks may have
been present much earlier as parasites of dinosaurs,
around 320 MYA (Klompen et  al., 1996; Barker
et al., 2014).
From this very brief review of some of the evolutionary history of parasitic organisms, it is clear
that by the end of the Cretaceous period and the
mass extinction that followed ~65 MYA, predecessors of all the main classes of parasite were present
in the world’s fauna. Potential intermediate hosts,
such as snails, had also evolved from around 400
MYA onwards (Wanninger and Wollesen, 2019).
By this time, other important links in the terrestrial

food chain were also present, for example, dung
beetles (Chin and Gill, 1996) and remnants of
grass were found in coprolites from herbivorous
dinosaurs in the late Cretaceous period, suggesting
the possibility of early grazing mammals at that
time (Prasad et  al., 2005). Table 1.1 provides
approximate evolutionary temporal relationships
among the components that eventually led to parasitism in domestic ruminants (Dawkins, 2004;
Lloyd, 2009).

The Ruminants
Following the Cretaceous extinctions of multiple
species, notably the dinosaurs, and also many invertebrate and plant species (Macleod, 2013), the scene
was set for the extensive radiation of flowering plants
and mammals from their initial appearance ~200
MYA. The first ungulates (herbivorous, hoofed mammals) to make their presence felt were the perissodactyls (odd-toed ungulates, such as horses, rhinos
and tapirs), species of which proliferated from ~55
MYA (Janis, 1976). The artiodactyls (even-toed

ungulates, such as camels, pigs, hippos, deer, antelopes, sheep and cattle) evolved later; evidence of the
earliest ruminants dates from ~40 MYA and from
the late Miocene onwards (~10 MYA), the artiodactyls assumed numerical dominance over the perissodactyls (Janis, 1976).

Table 1.1.  Chronology of evolutionary events relevant to parasitism in domestic sheep and cattle.
Years ago

Major milestones in the natural history of planet Earth

4.6 billion
3.8 billion
1.7 billion
700 million

Solar system, including Earth, formed
Bacteria and archaea (prokaryotes) appear
Single-celled organisms (eukaryotes) appear
Multi-celled eukaryotic organisms appear
Evolutionary events relevant to parasitism in domestic sheep and cattle
Period

Invertebrates

400 million
320 million
240 million
150 million
130 million
77 million


Devonian
Carboniferous
Triassic
Jurassic
Cretaceous
Cretaceous

Mites, snails
Ticks
Nematodes

65 million

Mass extinctions

50 million
30 million
10,000

Tertiary, Eocene
Tertiary, Miocene
Quaternary, Holocene

Vertebrates

Plants

Dinosaurs
Mammals


Flowering plants

Trematodes
Lice

Parasitic mites

2

Ungulates
Ruminants
Domestication

Grass

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A characteristic of these herbivores, which is well
represented in the fossil record, is the presence of
hypsodont teeth; these are large, high-crowned
molars with hard enamel ridges that have evolved to
grind down plant cell walls to release their contents
and to reduce particle size to facilitate bacterial colonization and digestion in the alimentary tract (Janis
and Fortelius, 1988). Hypsodont teeth are particularly important in grazing animals as many grass
species have a high silicon content, which makes them
particularly abrasive. In ruminants, these teeth are
central to the efficiency of digestion when fibrous

material is regurgitated, re-chewed, crushed and
ground and then re-swallowed in the process known
as rumination (Hofmann, 1989).
There are around 200 extant or recently extinct
species of ruminant (Fig. 1.1), the largest family of
which is the Bovidae (bovids), comprising ~137 species
of cattle, sheep, goats and antelopes; the next largest
family is the Cervidae (deer) with ~47 species
(Hernandez Fernandez and Vrba, 2005). The ~150
living ruminant species range in size from <10 kg to
>1 t and, although they have several features in common, there is quite a marked variation in their digestive tracts, which reflects adaptation to different
diets. Feeding patterns can be categorized as
(Hofmann, 1989; Clauss et al., 2010):

● Grazers, feeding predominantly on grass
● Browsers feeding on forbs, leaves and twigs and
fruit
● Intermediate feeders, which are opportunist grazers
or browsers
Domestic cattle and sheep are grazers, while goats
are intermediate feeders and their digestive systems
are adapted to handle their feed. There are a number of
challenges for ruminants living on a plant-based
diet, which differ according to their chemical composition. For example:
● Grass and roughages are high in fibre, which has
to be broken down by the rumen microflora and
fauna, not only in order to digest the cellulose
itself but in so doing to release soluble intracellular carbohydrates, proteins and other nutrients.
Chewing the cud is required to reduce the particle
size of plant material and increase its surface area

so that the rumen microorganisms can access the
substrate more efficiently.
● Browsers tend to eat young leaves and fruit,
which are more easily digestible, particularly the
latter, and therefore the breakdown of cellulose is
less critical. However, many plants have chemical
defences, such as tannins, to deter herbivorous
insects and mammals and these phenolic

Fig. 1.1.  Ruminant diversity: wildebeest and springbok.

Evolution of Parasitism in Domestic Ruminants

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c­ ompounds can have negative effects on cellulase
activity (Hofmann, 1989).
Adaptations between these two feeding strategies
are given in Table 1.2 (Clauss et al., 2010).
Irrespective of their feeding strategy, ruminants
have evolved to utilize plant material, including fibre, in
a biologically efficient way that supports their
requirements for maintenance, growth, mobility, reproduction and immune responses (Van Soest, 1994).
Pivotal to this is the reticulorumen, which is a fermentation chamber hosting an array of microorganisms, including bacteria and ciliated protozoa (Oxford,
1955; Wolin, 1981), which can break down cellulose –
a task that is beyond mammalian enzymes. Among the
end products of microbial digestion in the rumen are

volatile fatty acids (VFAs), notably acetic, butyric and
propionic, which are absorbed through the rumen wall,
facilitated by its large surface area, augmented by
numerous papillae. Following metabolism, these VFAs
are utilized as energy sources, for gluconeogenesis and
lipid synthesis (Wolin, 1981).
The omasum appears to have a role in further
absorption of VFAs, re-absorbing fluid and in regulating the outflow of digesta from the reticulorumen
to the abomasum, in particular undigested, coarse
fibrous material (Ehrlich et  al., 2019). The digesta
entering the abomasum comprises a sludge that
includes rumen liquor, digested plant remains, undegraded dietary protein contents and bacteria. Rumen
bacteria provide an important source of microbial
protein for the host, and the enzyme profile of the
Table 1.2.  Comparative features of the digestive
­system of grazing and browsing ruminants.
Digestive system

Grazers

Browsers

Salivary glands

Small (0.18% of
bodyweight)
Slow
Large
Numerous
Large

Thin mucosa,
lower
hydrochloric
acid (HCl)
levels
Small
Short
Small

Large (0.36% of
bodyweight)
Rapid
Small
Sparse
Small
Thick mucosa,
higher HCl
levels

Fermentation rate
Rumen
Rumen protozoa
Omasum
Abomasum

Liver
Intestine
Hindgut

Large

Long
Large
(fermentation)

ruminant abomasum reflects an important adaptation
to this function through the presence of lysozymes
(Jolles et  al., 1984). Lysozymes have antibacterial
properties, based on their ability to destroy cell walls of
Gram-positive bacteria, which is the basis for their
more common role in mammals as a defence mechanism against bacterial pathogens in other tissues
(Dobson et al., 1984). Lysozymes are found in high
concentrations in the fundic zone of the abomasal
mucosa, where the digesta contents have a pH of
~6.5, at which lysozymes actively lyse bacteria;
towards the pyloric zone of the abomasum, the
hydrochloric acid (HCl) secretions from the gastric
glands render the stomach contents acidic, with a
pH that can fall to ~1.5. A low pH is required for the
precursor pepsinogen to be converted into the proteolytic enzyme pepsin, which initiates protein digestion in the abomasum; however, bovine lysozyme is
highly resistant to deactivation by pepsin (Dobson
et al., 1984).

Grass and Grazing
Although there is evidence that grasses evolved as
long as 85 MYA, it was not until geological and
climatic changes shaped the environment to favour
grasses over forests that grasses came to assume a
dominant position in the Earth’s vegetation types
(Gibson, 2009). Grassland can now be found in
agricultural settings and also in (semi-) natural

habitats such as steppes, savannahs, prairies and
pampas in various parts of the world. The spread
and diversification of grasses coincided with climatic changes from around 30 MYA that resulted
in greater aridity and some of the characteristics of
grasses developed at this time as adaptations to
grazing animals. For example, having the growing
points at the base of the leaves at ground level
allowed grasses to quickly regenerate and recover
from grazing.
Ungulates diversified and coevolved, adapting
to the changes in vegetation and the expansion of
grasslands, the patterns differing somewhat over
time and among ecosystems (Stebbins, 1981;
Strömberg, 2011). Furthermore, there was a progressive change in the proportion of browsers
compared with grazers as the dominant vegetation types evolved (Janis et al., 2000). Ruminant
grazers tend to be more gregarious than browsers
and hence are commonly found in groups that
forage collectively throughout their territories
(Estes, 1991).

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Parasitism and Ruminant Grazers
There are features of ruminant feeding ecology and
behaviour that may have favoured the adaptation

and evolution of parasitism. Parasites that are transmitted by the so-called faecal–oral route rely on their
hosts ingesting infective stages while grazing.
Infections are acquired when infective nematode
larvae and trematode metacercariae that are associated with or attached to grass leaves or stems are
eaten while animals are grazing. Oribatid mites, the
intermediate hosts of several species of tapeworms,
and sporulated coccidial oocysts are normally found
in the vegetation mat or soil surface, but are ingested
when grazing, particularly on short swards. Because
grazing ruminants are aggregated in groups and,
apart from highly migratory species, are typically
confined to territories, their grazing patterns ensure
that they will return to previously grazed areas,
where they will also have rested, ruminated and defecated (Ezenwa, 2004a). During the intervening
period between successive grazing on a patch, the
free-living stages of nematode larvae and coccidia
can develop to infective stages, subject to fluctuations
in temperature and rainfall and so be present when
the animals return (Ezenwa, 2004a). Similarly, those
parasites with invertebrate, intermediate hosts, such
as trematodes (liver and rumen fluke) and cestodes
(tapeworms) will have time to complete this stage in
their life cycles so that infective stages are present
when the host ruminant species return to feed in the
same area later.
The longevity of host–parasite relationships in
grazing ruminants has been explored in gastrointestinal
(GI) nematodes (GINs) of the family Trichostrongylidae,
including the subfamilies Ostertagiinae and
Haemonchinae (Hoberg and Lichtenfels, 1994).

Taken in conjunction with the radiation of ruminants
in the family Bovidae, which includes cattle, sheep
and goats, from around 20 MYA and the evolution of
nematode species from these subfamilies, it has been
concluded that the bovids and their Ostertagia-like
parasites have coevolved for 10–20 million years
(Stear et al., 2011).
The gregarious nature of grazing ruminants may
also have implications for ectoparasite infestations.
Although some species of ticks, e.g. Rhipicephalus
(Boophilus) microplus, remain on the same host for
all the parasitic phases of the life cycle, many other
species, e.g. Ixodes ricinus, only feed intermittently
for a few days at each of the larval, nymph and adult
stages, and for the rest of their lives, they live and

develop in the vegetation. These parasites therefore
are also reliant on their hosts returning to the sites
where they dropped off the animal after a blood
meal and re-locating potential ruminant hosts, a
process that can be facilitated by the grazing behaviour of herds or flocks of mammals. Similar scenarios could apply to species of pest flies that lay their
eggs off the host, but for obligate ectoparasites such
as mange mites and lice, the close proximity of hosts
within groups can facilitate spread through close
contact.

Parasites in Wild and Feral Ruminants
Prior to the domestication of cattle, sheep, goats and
buffalo, parasitism evolved in wild ruminants and
other wildlife over millions of years, where they

played an important role in ecology and population
dynamics. Research into wildlife parasitism has
shown many similarities and parallels with domestic
animals; for example, a series of studies in wild
African buffalo and other African bovids has shown
the following:
● Nutritional status can influence the epidemiology
and impact of GI nematodes (Ezenwa, 2004b)
● Interactions between GI nematodes and bovine
tuberculosis (BTb) (Ezenwa et al., 2010)
● Reduction in mortality of buffalo from BTb following anthelmintic treatment (Ezenwa and
Jolles, 2015)
● The importance of host behaviour in the epidemiology of parasitism (Hawley et al., 2011)
● Anthelmintic treatment leads to increased daily
foraging time in Grant’s gazelle (Worsley-Tonks
and Ezenwa, 2015)
Additional examples of the impact of parasites in
wild, feral and semi-domesticated ruminants in
Europe include:
● Reduced body condition in red deer associated
with low-level worm burdens (Irvine et  al.,
2006)
● Increased mortality in Soay sheep on Hirta, the
largest island in the St Kilda archipelago, associated with GIN, most marked during periods of
malnutrition (Gulland, 1992)
● Depression of feed intake in reindeer with GIN
infections (Arneberg et al., 1996)
● Reduced fecundity in reindeer associated with
abomasal parasite burdens (Albon et  al.,
2002)


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Domestication of Cattle and Sheep
Although agriculture may have evolved separately in
different parts of the world, such as South America
and Asia, the best studied and documented evidence
for the domestication of crops and animals comes
from the so-called Fertile Crescent in the Near East.
Evidence for the domestication of cattle, sheep and
goats dates from 11,000 to 10,000 years before
present and is centred on the northern arc of the
Crescent, encompassing the present-day countries of
Iraq and Turkey (Zeder, 2008). The wild ancestors of
domestic cattle (Bos taurus) are the aurochs (Bos
primigenius primigenius), of sheep (Ovis aries) the
mouflon (Ovis orientalis) and of goats (Capra hircus) the wild species, bezoar (Capra aegagrus)
(Driscoll et al., 2009).
The natural vegetation in this region at the time of
domestication was oak/pistachio parkland, so it is
likely that early domestic cattle and sheep combined

grazing with some browsing and, though livestock
are now commonly kept in fields with limited
opportunities to browse, both cattle and sheep will

readily browse on hedgerows and trees, and in some
parts of Europe, cut branches are an important part
of their diet, particularly over winter. There is
renewed interest in silvopasture systems as a means
to optimize land use from both productivity and
environmental perspectives (Gabriel, 2018).
Controlled selection of cattle and sheep for various traits and their subsequent division into breeds
and types is a relatively recent phenomenon, dating
back only a few hundred years (Fig. 1.2). The objectives of selective breeding of ruminants were primarily focused on traits such as appearance, meat,
milk and wool production, traction power and
hardiness, all within a background of amenable
behaviour in their interactions with man (Price,
1999; Mignon-Grasteau et al., 2005). Selection for

Fig. 1.2.  Longhorn cattle – the result of domestication and selective breeding.

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resistance to parasites or resilience in the face of
parasite challenge would have been incidental to the
main breeding objectives and may have even been
counterselected (Raberg et  al., 2009). However,
particularly in sheep, breeding programmes for
resistance or resilience to parasitic gastroenteritis
have been in place for several decades (Bisset and

Morris, 1996; Morris et  al., 1997) and there is
growing interest in this practice as a means to help
control parasites without dependence on parasiticides (Bisset et al., 2001; Stear et al., 2007).

Closing Remarks
The purpose of this introductory chapter is to provide
a brief ecological, evolutionary and historic perspective
on parasitism in domestic ruminants. Non-parasitic
invertebrates have been present on Earth for hundreds
of millions of years, preceding the emergence of vertebrates in the world’s fauna. Evidence of parasitism in
dinosaurs dates from ~250 MYA and coevolution of
parasites and their hosts continued over the millennia
and continues to this day. Of particular relevance to
this book is the appearance of grasses and grazing
mammals in terrestrial ecosystems over the last ~20
million years. Parasitism in ruminants has a lineage
that stretches back for millions of years, but this association has changed since domestication of sheep and
cattle, because, while natural evolutionary mechanisms
continue, some selection is directly influenced by
humans.

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2



Parasitic Gastroenteritis in Cattle

Introduction
More than 15 species of nematode that inhabit the
gastrointestinal tract of cattle have been described
(Rose, 1968; Taylor et al., 2007); however, in temperate farming regions, parasitic gastroenteritis (PGE)
is predominantly associated with only two species:
● Ostertagia ostertagi in the abomasum
● Cooperia oncophora in the small intestine
Other species that occasionally can contribute to bovine
PGE are Trichostrongylus axei and Nematodirus
spp. In tropical and subtropical regions, Haemonchus
spp. are the most common of the abomasal species and
some other genera; for example Oesophagostomum
spp. can assume greater importance. A characteristic of gastrointestinal nematodes in both cattle and
sheep is that most species are host-specific and this
opens up possibilities of grazing practices such as
mixed or sequential grazing of cattle and sheep in
order to reduce pasture larval populations. Notable
exceptions to this general rule are T. axei, which can
parasitize a variety of ungulates, including horses

and pigs, and Nematodirus and Haemonchus spp.
In young cattle in their first grazing season (FGS)
in temperate climates, coinfections comprising both
O. ostertagi and C. oncophora are the norm, but
host–parasite interactions will be considered separately for each species before considering PGE as
an entity.

Parasitic Gastritis, Ostertagiosis
O. ostertagi infections are acquired while grazing,
when infective larvae, which are commonly present
on the leaves of herbage, are ingested. Infective
larvae exsheath in the rumen, a process that is
stimulated by low pH, temperature and bicarbonate concentration (Hertzberg et  al., 2002) and
which occurs more quickly in grass-based diets (2 h),
compared with those with a high proportion of
grain (6 h) (DeRosa et al., 2005). The exsheathed

10

third stage larvae, ~0.7 mm in length (Rose, 1969),
pass into the abomasum where they enter the gastric
glands within 2 days and moult to fourth stage
larvae, which can be found from ~4 days onwards,
when they measure ~1.1 mm; the majority of worms
emerge from the glands into the abomasal lumen
from day 16 onwards as fifth stage larvae or adults
(Ritchie et  al., 1966). Adult male O. ostertagi are
on average 6.9 mm long, while females are 9.7 mm
(Rose, 1969). Following copulation (Fig. 2.1), gravid
females can be identified from day 16 onwards and

most are laying eggs by 21 days post-infection, giving a typical pre-patent period of ~21 days (Ritchie
et  al., 1966; Rose, 1969). Male worms comprise
~45% of the adult population in the abomasum,
females ~55% and the average fecundity per female
is 284 eggs per day (Verschave et al., 2014a). Egg
production is subject to density-dependent influences such that fecundity typically declines with
increasing worm populations, resulting in a stereotypical pattern of egg output, irrespective of the size
of the (female) worm burden; this is observed following experimental (Ross, 1963; Anderson et al.,
1967; Michel, 1967, 1969c, 1969d) and natural
infections (Michel, 1969b; Brunsdon, 1971).

Pathology
By 16–21 days, parasitized gastric glands have
increased in size and have become undifferentiated,
hyperplastic and dysfunctional. Gastric glands from
which mature worms have emerged are easily visible
on the abomasal mucosa, particularly on the folds of
the fundus (anterior aspect of the abomasum) as
slightly raised circular, pale lesions ~4–5 mm in
diameter, with a central orifice, marking the site of
exit of the worm (Fig. 2.2). In heavy infections, the
lesions can coalesce (Fig. 2.3), resulting in a more
diffuse thickening of the mucosa, and the abomasum
is noticeably larger and heavier than in lightly
infected or uninfected animals (Michel, 1968a).

© Andrew B. Forbes, 2021. Parasites of Cattle and Sheep: A Practical Guide to their Biology
and Control (A.B. Forbes).

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Fig. 2.1.  Male and female Ostertagia ostertagi copulating. Courtesy of Dr S. Rehbein, Kathrinenhof Research Centre,
Rohrdorf.

Fig. 2.2.  Discrete abomasal lesions associated with
Ostertagia ostertagi.

Fig. 2.3.  Coalescent parasitized gastric glands in the
abomasum.

Under experimental conditions, following a single
infection, it can take 50–90 days for the abomasal
mucosa to return to its normal appearance (Osborne
et al., 1960; Ritchie et al., 1966), so lesions seen at
necropsy may reflect the worm population over the
previous 2–3 months. The abomasal lesions are
essentially pathognomonic for nematode infections
and are useful not only in diagnostic post-mortems
but also for abattoir surveys, where abomasa can be
examined in the ‘gut room’ without significant disruption to the line. Results of such surveys have
shown that lesions of ostertagiosis are common in
mature and adult cattle, being present in the great
majority of animals, with 38–60% having in excess
of 100 lesions (Larraillet et al., 2012; Bellet et al., 2016).

The presence of significant pathological changes in
mature cattle illustrates the fact that acquired immunity to O. ostertagi is incomplete and this in turn not
only provides an explanation for the role that adult
cattle can play in the epidemiology of ostertagiosis

(Stromberg and Averbeck, 1999) but also may
explain why adult cattle, as well as young stock, can
experience production losses from parasitic gastritis
(Stromberg and Corwin, 1993; Taylor et al., 1995;
Charlier et al., 2009).
Clinical features of ostertagiosis type I
Following monospecific induced infections, clinical
signs, including anorexia, diarrhoea and weight

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loss, typically occur from day 19 onwards, coincident with extensive damage to the abomasal mucosa
and the establishment of adult worm populations.
This disease is called ostertagiosis type I and is the
typical presentation in FGS calves that have not
been in an effective control programme (Armour,
1970), though it can also be seen in yearlings (Fig. 2.4)
and adult cattle (Orpin, 1994).
Hypobiosis
Infective larvae that are ingested towards the end of
the grazing season are predisposed to undergo a
period of hypobiosis in the gastric glands, thus
greatly extending the pre-patent period. The stimulus for hypobiosis appears to be chilling (4°C) of the
infective larvae on pasture in autumn as the ambient temperature declines (Armour and Bruce, 1974).
The duration of inhibition is typically 16–18 weeks

(Armour and Bruce, 1974), after which the larvae
resume development and become adult worms. The
precise mechanism for resumption of development
is not known, but there is some evidence that small
numbers of inhibited larvae resume development
over the winter (Michel et al., 1976a; Smith, 1979),
with a peak in February and March, which is consistent with larvae being ingested over several

months prior to housing and having a fixed period
of quiescence (Michel et al., 1976b).
The larvae of O. ostertagi inhibit as early fourth
stage larvae in the gastric glands within 4 days of
ingestion, when they measure ~1.1 mm (Armour
and Duncan, 1987); in this state, although parasitized gastric glands can be recognized as 1–2 mm
lesions in the abomasal mucosa (Ritchie et  al.,
1966), histological changes are minimal (Snider
et al., 1988), and there is little evidence of parasiteassociated alterations in biochemistry or immunobiology (Osborne et al., 1960). This is consistent with
data from single infection experiments, which show
that developing larvae are at least 16 days old before
significant changes in pathophysiology and clinical
signs are observed (Jennings et  al., 1966; Ritchie
et  al., 1966). Larval inhibition is present in O.
ostertagi populations not only in Europe and North
America (Frank et al., 1988) but also in temperate
regions of the southern hemisphere (Brunsdon,
1972), where the seasonality of hypobiosis is similar,
but the months of the year are obviously different.
The significance of hypobiosis from an epidemiological perspective is that it provides another
means of overwinter survival for O. ostertagi, in
addition to infective larvae that persist in dung or

on pasture to act as a source of infection in spring.

Fig. 2.4.  Clinical ostertagiosis in yearling with a faecal egg count of 50 EPG and plasma pepsinogen value of 4.2 IU.
Courtesy of K. Ellis, Glasgow.

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From a clinical point of view, mass, simultaneous
emergence of adult worms from the gastric glands
in late winter can precipitate an acute, potentially
fatal, abomasitis in a small proportion of infected
animals. An early description of this disease, now
known as ostertagiosis type II, appeared in the
1950s (Martin et al., 1957) and this syndrome can
occur in heifers (Petrie et al., 1984) and adult cattle
too (Wedderburn, 1970; Selman et  al., 1976).
Ostertagiosis type II is currently relatively uncommon in the UK (Mitchell, 2014) and there is strong
circumstantial evidence that routine use of macrocyclic lactones (MLs) as housing treatments for the
removal of gastrointestinal nematodes (including
inhibited O. ostertagi larvae), lungworm and cryptic populations of lice and mange mites in (young)
cattle has reduced the risk of this manifestation of
ostertagiosis.
Pathophysiology
Normal gastric glands comprise a number of different types of cells (Banks, 1981), including:
● Mucus-producing neck cells, which may also

synthesise and secrete lysozymes
●Parietal (oxyntic) cells that synthesise and
secrete hydrochloric acid (HCl)
● Zymogen (chief) cells that synthesise and secrete
pepsinogen (and prorennin in young animals)
● Enteroendocrine (enterochromaffin) cells that
synthesise and secrete various hormones into the
circulation, including gastrin (G cells)
Following invasion of gastric glands by the larvae
of O. ostertagi, their subsequent development and
emergence over a period of ~21 days and the direct
and collateral damage to the gastric mucosa, several
functional disorders can be observed. Changes in
the concentration of various gastric secretions can
contribute to the pathophysiology of ostertagiosis
and its impact in infected cattle.
Mucus biosynthesis
Mucus provides a defensive mechanism against pathogens in the gastrointestinal tract (Miller, 1984); in
ostertagiosis, changes in mucus synthesis are most
marked following emergence of adult parasites
from the gastric glands (Rinaldi et al., 2011). The
main lesion is of hyperplasia of the mucus cells,
accompanied by changes in the composition of the
mucins synthesised and secreted; functionally, these

responses are thought to play a role in the immune
response to and elimination of the parasite (Mihi
et al., 2014).
Pepsinogen
In a primary infection, coincident with the emergence of fifth stage larvae from the gastric glands at

around 18 days, the pH in the abomasum increases
rapidly. This is a consequence of damage to the parietal cells in the gastric glands by the parasite, which
results in a reduction in the secretion of HCl. The
pH of the normal, uninfected abomasum in calves
averages 2.5 (Jennings et al., 1966; Murray, 1970;
Stringfellow and Madden, 1979), ~3.5 in lightly
infected animals (Ross et al., 1963) and 6.5–8.5 in
clinical ostertagiosis; in subclinical ostertagiosis,
the values are intermediate between these (Ross
and Todd, 1965). At the higher pH values that tend
towards neutrality or alkalinity, the abomasal contents contain very low concentrations of pepsin
(Ross et al., 1963; Jennings et al., 1966), and this is
because conversion of the precursor pepsinogen to
pepsin is negligible at pH ~5.0 and above (Piper
and Fenton, 1965; Jennings et  al., 1966). Though
changes in the milieu of the abomasal contents as a
result of elevated pH and leakage through disrupted junctions between cells provide one explanation for pepsinogenaemia (Jennings et al., 1966),
other mechanisms may be involved, for example
direct secretion of pepsinogen from the zymogenic
(chief) cells in damaged gastric glands into the circulation (Stringfellow and Madden, 1979; Baker
et al., 1993). In addition, direct transplantation of
adult O. ostertagi into normal abomasa results in
an immediate increase in plasma pepsinogen (PP),
in the absence of any abomasal pathology (McKellar
et  al., 1986). Furthermore, treatment of calves
experimentally infected with O. ostertagi results in
an immediate ~33% drop in PP, followed by a
gradual decline in concentrations over the following 19 days (Hilderson et  al., 1991), presumably
reflecting the absence of stimuli from the adult
worms and some resolution of the gastric gland

lesions (Osborne et al., 1960).
Gastrin
Hypergastrinaemia is a feature of ostertagiosis
(Fox et al., 1993). Gastrin is secreted by the G cells
in the stomach in response to increasing pH in a
feedback mechanism to stimulate the parietal cells

Parasitic Gastroenteritis in Cattle

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to synthesise and secrete more HCl in order to
restore the pH to its normal value of ~2.5 in the
abomasal contents (Fox et  al., 2006). The significance of gastrin in the pathogenesis of ostertagiosis
is that it can suppress appetite, and a reduction in
feed intake is a consistent and important feature of
ostertagiosis; indeed, it has been shown that a loss
of appetite accounts for 73% of the reduced
growth rate that is commonly seen in young cattle
(Fox et al., 1989a).
Lysozyme
The optimum pH for ruminant lysozymes is 5.0
(Dobson et  al., 1984), so in theory, digestion of
ruminal bacteria in the abomasum might be
enhanced in ostertagiosis, though no experimental
studies have been undertaken to explore this
hypothesis. However, populations of both aerobic

and anaerobic bacteria in the abomasum have been
shown to increase in ostertagiosis in cattle (Jennings
et al., 1966) and teladorsagiosis in sheep (Simcock
et al., 1999), attributed by these authors to a loss of
a bacteriostatic effect of acid in the stomach. Hence
any effects of abomasal parasitism on the number
and composition of bacterial populations seem to
be more likely mediated by elevated pH per se,
rather than through optimized lysozyme activity.
Examples of some pathophysiological consequences of ostertagiosis are as follows:
Increase in abomasal pH (Purewal et al., 1997)
Increase in plasma pepsinogen (Fox et al., 1989b)
Increase in plasma gastrin (Fox et al., 1989b)
Increase in fundic (+96%) and pyloric (+31%)
abomasal mass (Purewal et al., 1997)
● Increase in gastrin mRNA in pyloric mucosa
(Purewal et al., 1997)
● Increase in the number of aerobic bacteria in
abomasum (Jennings et al., 1966)
● Reduction in nitrogen digestibility (Fox et  al.,
1989b)
● Hypoalbuminaemia (Fox et al., 1989b)
●
●
●
●

Host immune responses
A cellular response in the regional lymph nodes (LNs)
associated with the abomasum is evident in induced

O. ostertagi infections and this can be detected
within 4 days; over the subsequent 28–35 days, LN
mass can increase 20–30 times compared to uninfected animals and simultaneously lymphocytes are

released into the circulation whence they reach and
colonize the abomasal mucosa (Gasbarre, 1997).
Parasite-specific lymphocytes in the abomasal LNs
are responsible for the generation of immunoglobulins against O. ostertagi; these are mainly of the
IgG1 class and appear to be associated with exposure
rather than a protective immune response (Claerebout
and Vercruysse, 2000). Following induced trickle
infections in naïve calves with 5000 infective larvae
(L3) per day, antibodies to O. ostertagi can be
detected in serum from ~21 days onwards after
which they continue to increase steadily; the
response appears to be dose-dependent as 500 L3
per day fail to elicit a response (Berghen et  al.,
1993). These host responses help regulate parasite
populations by reducing the size of the worm burden, decreasing the size of adult worms and reducing fecundity in female worms (Klesius, 1988). The
sequence of events is typically as follows (Claerebout
and Vercruysse, 2000):
●
●
●
●
●

Decrease in fecundity
Stunting of growth
Retardation of development

Expulsion of adult worms
Limited establishment of infective larvae in gastric
glands

Although there has been a massive research
effort over several decades into the immunobiology
of ostertagiosis, much of it driven by the pursuit of
helminth vaccines (Meeusen and Piedrafita, 2003),
there is surprisingly little focus on the manifestations of protective immunity in the animal. It is
evident from field observations that it takes exposure to infection over two grazing seasons to elicit
a protective response (Gasbarre, 1997), but protection from infection, pathological changes, depressed
production and clinical disease is incomplete
(Armour and Ogbourne, 1982). Studies in adult
cattle provide many examples that testify to the
presence of O. ostertagi infection (Burrows et  al.,
1980a; Agneessens et  al., 2000; Borgsteede et  al.,
2000), abomasal pathology (Larraillet et al., 2012),
changes in grazing behaviour (Forbes et al., 2004),
production losses (Charlier et al., 2009) and clinical disease (Selman et al., 1977; Orpin, 1994). The
acquisition of immunity can be influenced by the
level and duration of exposure to infective larvae
(Claerebout et al., 1998b), an obvious example of
lack of exposure being cattle that are housed for
long periods of time (Claerebout et  al., 1997).
Immunity to O. ostertagi under natural exposure

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Parasites of Cattle and Sheep


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