Parasites of cattle and sheep a practical guide to their biology and control

Contents Preface vii Acknowledgements ix 1 The Origin and Evolution of Parasitism in Domestic Ruminants 1 3 Parasitic Gastroenteritis in Sheep: Teladorsagiosis and Trichostrongylosis 37

Parasites of Cattle and Sheep

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

CABI is a trading name of CAB International

© Andrew B Forbes, 2021 All rights reserved No part of this publication may be reproduced in any form

or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior 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 https://lccn.loc.gov/2020031633

LC ebook record available at https://lccn.loc.gov/2020031634

References to Internet websites (URLs) were accurate at the time of writing

ISBN-13: 9781789245158 (paperback)

9781789245165 (ePDF)

9781789245172 (ePub)

Commissioning Editor: Alexandra Lainsbury

Editorial Assistant: Lauren Davies

Production Editor: Marta Patiño

Typeset by SPi, Pondicherry, India

Printed and bound in the UK by Severn, Gloucester

Contents

Preface vii Acknowledgements ix

1 The Origin and Evolution of Parasitism in Domestic Ruminants 1

3 Parasitic Gastroenteritis in Sheep: Teladorsagiosis and Trichostrongylosis 37

4 Parasitic Gastritis in Sheep: Haemonchosis; and Parasitic Enteritis in Lambs: Nematodirosis 64

12 Obligate Ectoparasites of Cattle: Lice and Mange Mites 224

17 Grazing Management and Helminth Control on Stock Farms 312

19 Principles and Practical Implementation of Parasite Control on Livestock Farms 342 Index 351

Preface vii

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 rumi-nant 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 cov-ered 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 exper-tise 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 abor-tion and infertility

● Second, treatment and control of these protozoans generally require different products, vaccines and agement, appropriate to these organisms, whereas there is a lot of overlap in the epidemiology and control

man-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 bet-tered; 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 vari-ous 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

viii Preface

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 epi-demiology 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) nary-medicines-directorate and the National Office for Animal Health (NOAH) https://www.noah.co.uk/.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)

https://www.gov.uk/government/organisations/veteri-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 standing 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 knowl-edge and wisdom, and adapting and applying it to specific farm circumstances and the aspirations of indi-vidual 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

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 men-tion, 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

x Acknowledgements

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

1 The Origin and Evolution of

Parasitism in Domestic Ruminants

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

and Control (A.B Forbes).

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

har-bour two cestode, two trematode and four

nema-tode species of parasite over its lifetime (Dobson

et al., 2008).

There are several definitions of parasitism, all of

which describe an association between one

organ-ism (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

non-parasitic 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

hel-minths, comprising nematodes (roundworms),

trem-atodes (flatworms) and cestodes (tapeworms); most

ectoparasites are arthropods, either insects or

arach-nids Strictly speaking, protozoa originally meant

early (eukaryotic) life forms; however, in

parasitol-ogy the word has become synonymous with

single-celled 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 pre-cise timing of events will inevitably change some-what as new discoveries are made and new methodologies adopted

Additional sources of useful information on sites that transit the gastrointestinal (GI) tract are coprolites, which are fossilized dung and which can contain remnants of parasite eggs Currently, the earli-est fossil evidence for intestinal parasitism in verte-brates 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, repre-senting an early record of parasitic flatworms (Poinar and Boucot, 2006)

para-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

2 Parasites of Cattle and Sheep

(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,

arthro-pods are preserved as fossils more readily than

hel-minths 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

evi-dent, for example, a fly parasitized by a Leptus spp

mite (Arillo et  al., 2018) Some remarkably

well-preserved 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

evo-lutionary history of parasitic organisms, it is clear

that by the end of the Cretaceous period and the

mass extinction that followed ~65 MYA,

predeces-sors 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 para-sitism in domestic ruminants (Dawkins, 2004; Lloyd, 2009)

The Ruminants

Following the Cretaceous extinctions of multiple species, notably the dinosaurs, and also many inver-tebrate 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 mam-mals) to make their presence felt were the perisso-dactyls (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, ante-lopes, sheep and cattle) evolved later; evidence of the earliest ruminants dates from ~40 MYA and from the late Miocene onwards (~10 MYA), the artiodac-tyls assumed numerical dominance over the peris-sodactyls (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 Solar system, including Earth, formed

3.8 billion Bacteria and archaea (prokaryotes) appear

1.7 billion Single-celled organisms (eukaryotes) appear

700 million Multi-celled eukaryotic organisms appear

Evolutionary events relevant to parasitism in domestic sheep and cattle

400 million Devonian Mites, snails

320 million Carboniferous Ticks

130 million Cretaceous Trematodes

65 million Mass extinctions

50 million Tertiary, Eocene Parasitic mites Ungulates

Evolution of Parasitism in Domestic Ruminants 3

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

colo-nization and digestion in the alimentary tract (Janis

and Fortelius, 1988) Hypsodont teeth are

particu-larly 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

com-mon, there is quite a marked variation in their

diges-tive 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 browsersDomestic 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 com-position 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 intracellu-lar 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

4 Parasites of Cattle and Sheep

compounds 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,

repro-duction and immune responses (Van Soest, 1994)

Pivotal to this is the reticulorumen, which is a

fer-mentation chamber hosting an array of

microorgan-isms, 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

regu-lating 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,

unde-graded dietary protein contents and bacteria Rumen

bacteria provide an important source of microbial

protein for the host, and the enzyme profile of the

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 mecha-nism 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 pro-teolytic enzyme pepsin, which initiates protein diges-tion 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 cli-matic 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 pro-gressive change in the proportion of browsers compared with grazers as the dominant vegeta-

tion 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)

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)

Large (0.36% of bodyweight)Fermentation rate Slow Rapid

Rumen protozoa Numerous Sparse

Abomasum Thin mucosa,

lower hydrochloric acid (HCl) levels

Thick mucosa, higher HCl levels

(fermentation)

Evolution of Parasitism in Domestic Ruminants 5

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

trans-mitted 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

associ-ated 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

def-ecated (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 behav-iour of herds or flocks of mammals Similar scenar-ios 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 lowing anthelmintic treatment (Ezenwa and Jolles, 2015)

fol-● The importance of host behaviour in the

epide-miology 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, associ-ated 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)

6 Parasites of Cattle and Sheep

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

hir-cus) 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 ous 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 objec-tives of selective breeding of ruminants were pri-marily 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,

vari-1999; Mignon-Grasteau et al., 2005) Selection for

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

Evolution of Parasitism in Domestic Ruminants 7

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

parasiti-cides (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

verte-brates 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

asso-ciation 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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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

tem-perate 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

characteris-tic 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

sepa-rately 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

bicarbo-nate 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

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, giv-ing 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 ences such that fecundity typically declines with increasing worm populations, resulting in a stereo-typical pattern of egg output, irrespective of the size

influ-of the (female) worm burden; this is observed

fol-lowing 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)

Parasitic Gastroenteritis in Cattle 11

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

dis-ruption 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 immu-

nity 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

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

12 Parasites of Cattle and Sheep

loss, typically occur from day 19 onwards,

coinci-dent 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

stimu-lus for hypobiosis appears to be chilling (4°C) of the

infective larvae on pasture in autumn as the

ambi-ent 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

con-sistent 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 para-sitized 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

parasite-associated alterations in biochemistry or

immunobi-ology (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 epidemi-ological 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

Parasitic Gastroenteritis in Cattle 13

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

uncom-mon in the UK (Mitchell, 2014) and there is strong

circumstantial evidence that routine use of

macro-cyclic lactones (MLs) as housing treatments for the

removal of gastrointestinal nematodes (including

inhibited O ostertagi larvae), lungworm and

cryp-tic 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

differ-ent 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

path-ogens 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 gence 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 pari-etal cells in the gastric glands by the parasite, which results in a reduction in the secretion of HCl The

emer-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 con-tents 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 dis-rupted junctions between cells provide one expla-

nation 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 cir-culation (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 follow-

ing 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

14 Parasites of Cattle and Sheep

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

signifi-cance 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

conse-quences 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

unin-fected 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 immunoglob-

ulins 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 nạve 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 bur-den, decreasing the size of adult worms and reduc-ing 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 manifesta-tions of protective immunity in the animal It is evident from field observations that it takes expo-sure to infection over two grazing seasons to elicit

a protective response (Gasbarre, 1997), but tion 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

protec-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 clini- cal 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

Parasitic Gastroenteritis in Cattle 15

on pasture appears to be acquired irrespective of

control methods, for example the strategic use of

anthelmintics, and it is only following artificially

high challenge that significant differences in

protec-tion can be observed in cattle subject to different

levels of exposure to infective larvae (Claerebout

et al., 1998a,b).

Parasitic Enteritis, Cooperiosis

Species of the genus Cooperia are among the

com-monest gastrointestinal nematodes in young cattle

in both temperate and subtropical regions; C

oncophora is the most commonly encountered

spe-cies in temperate climates; Cooperia punctata and

Cooperia pectinata are typically found in warmer

climates (Reinecke, 1960; Chiejina and Fakae,

1989; Lima, 1998; Pfukenyi and Mukaratirwa,

2013) Even in calves, C oncophora is considered

to be of relatively low pathogenicity (Coop et al.,

1979; Satrija and Nansen, 1992) with transient

diarrhoea only occasionally reported in association

with high infection levels (Borgsteede and Hendriks,

1979), whereas C punctata and C pectinata have

been shown to be somewhat more pathogenic

(Alicata and Lynd, 1961; Herlich, 1965; Stromberg

et al., 2012) Under feedlot conditions, infection of

weaned beef calves ~6 months of age with 105

infective larvae of a ML-resistant isolate of C

punc-tata on days 0 and 14 resulted in a 5.4% reduction

in daily feed intake and a 7.5% reduction in daily

live weight gain (DLWG) (Stromberg et al., 2012)

At post-mortem, the small intestinal mucosa was

thickened and covered with excess mucus, while

the mesenteric LNs were enlarged, consistent with

histopathological changes in the small proximal

small intestine and a marked cellular infiltrate of

the mucosa (Rodrigues et al., 2004) The pre-patent

period for C punctata is 13 days and patent

infec-tions can persist for a mean of around 4 months,

reflecting a relatively rapid acquisition of immunity

(Leland, 1995)

Cooperia oncophora

C oncophora inhabits the small intestine, where it

plays an important role in PGE in FGS calves on

farms in temperate regions of the northern and

southern hemispheres There are two published

studies on experimental trickle infections with C

oncophora and the results are inconsistent in some

aspects Common features of infection in both

experiments are that the parasitic stages are located mainly in the duodenum and proximal jejunum and that immunity develops quite quickly (Coop

et al., 1979; Armour et al., 1987), within ~12 weeks,

which is consistent with field observations in FGS calves, which acquire immunity within the FGS (Bisset and Marshall, 1987; Armour, 1989) The clinical picture differs between the studies insofar

as in one, at daily larval doses of 5000–20,000, no clinical signs were seen and there were no effects on feed intake, though there was a reduction in growth rate of ~17% in the infected calves com-

pared with the uninfected controls (Coop et  al.,

1979) In contrast, in the other study, in which calves received 10,000 infective larvae per day, diarrhoea was seen around week 6, at which time appetite and growth rates also declined (Armour

et  al., 1987) Also in this experiment, there was

evidence that the worms were located in the tinal mucosa and villi were stunted and this was associated with impaired nitrogen retention, whereas in the former study, there was no evidence for mucosal colonization or damage

intes-Under field conditions, an example of the

rela-tive pathogenicity of C oncophora and O agi was illustrated in a trial in which calves were vaccinated against C oncophora and grazed on

ostert-typical northern European pastures that were urally contaminated with infective larvae of both

nat-species (Vlaminck et  al., 2015) Calves were

vac-cinated and then turned out in May onto cated pastures where they remained until the end

repli-of the grazing season in October Over this period there was a ~60% reduction in cumulative faecal

Cooperia egg counts, a ~65% reduction in tive C oncophora larvae on pasture and an 82%

infec-reduction in worm burdens at housing, when

num-bers of Cooperia were also low (mean 3825) in the

control calves, presumably because of naturally acquired immunity However, there was no differ-ence in live weight gain between the vaccinated calves and controls; furthermore, in all groups ostertagiosis was present at high levels, as indi-cated by high PP concentrations and clinical dis-ease in one of the vaccinated calves (Vlaminck

et al., 2015).

Experimental Coinfections With

O. ostertagi and C oncophora

While research using induced infections with either

O ostertagi or C oncophora is valuable in determining

16 Parasites of Cattle and Sheep

detailed aspects of their life cycle, pathogenicity and

population biology, under field conditions in young

grazing cattle, coinfections between both species

are common To complement field observations,

controlled experiments in calves infected with both

species could provide useful information; however,

of the few studies that have been published, the

results are somewhat equivocal A trial in which the

impact of singly or dually infected calves was

assessed, weight gain was significantly less in calves

with both C oncophora and O ostertagi burdens

when compared with calves infected with the same

infective dose of either parasite individually; all had

lower growth rates than the uninfected controls

(Kloosterman et  al., 1984) In contrast, when

trickle infections were used, there was no evidence

of any parasite interactions, though live weight

gain was not measured in this study (Satrija and

Nansen, 1993) Finally, a trickle infection in calves

of 2000 O ostertagi and 10,000 C oncophora

larvae per day over 42 days produced severe PGE

with inappetence, weight loss and diarrhoea; in

addition, digestive efficiency and nitrogen retention

were significantly reduced (Parkins et  al., 1990)

Although no direct comparisons were made, the

authors considered the clinical presentation to be

more severe than infections of this magnitude with

either nematode species individually, particularly

O ostertagi; a theory was proposed that the

mucosal damage in the small intestine associated

with C oncophora prevented host compensatory

responses aimed at retaining and reabsorbing

nutrients

Subclinical Parasitic Gastroenteritis

in Cattle in the Field

Though clinical parasitic gastroenteritis is not

uncommon in young cattle that have not been

sub-ject to effective control, by far the most common

expression of PGE is subclinical infections, which

are found widely in all ages of cattle

First grazing season calves

The largest evidence base for quantifying

subclini-cal losses is a meta-analysis of European studies in

autumn-born dairy calves subject to early season,

strategic control with anthelmintics (Shaw et  al.,

1998a,b) Over 2000 cattle were included in the

analyses of the 85 trials that were examined In 32

of the studies, there was no clinical disease in the

untreated control calves and the overall reduction

in DLWG in the controls compared with treated calves was 22% In the remaining 53 trials, in which the controls had clinical PGE, despite thera-peutic treatment with anthelmintics, their daily growth rate was 38% less than in strategically

treated animals (Shaw et al., 1998b).

The principle mechanism for poor growth in subclinical PGE appears to be a reduction in feed intake, though this is more difficult to measure in free-ranging animals on pasture than in confined animals In a study using jaw-movement recorders and ‘Graze’ software (Rutter, 2000), it has been shown that control calves graze for 105 min less per day compared with those treated with an

anthelmintic bolus (Forbes et al., 2000) The

reduc-tion in daily grazing time in the controls resulted in lower herbage intake, which was reflected in sward height and mass in the paddocks grazed by the animals (Fig 2.5), and reduced DLWG, which was

650 g/day in the controls and 800 g/day in the treated animals (Forbes, 2008)

In spring-born beef suckler calves, losses through subclinical PGE are limited while the calves are suckling their dams; when milk comprises a sub-stantial portion of their diet, nonetheless, calves, pre- and post-weaning, can show growth responses

of 6.5–10% to anthelmintic treatment (Forbes

et al., 2002; Hersom et al., 2011).

Second grazing season cattle (yearlings, stockers)

Because of differences in calving seasons, farm types and husbandry, second grazing season (SGS) cattle are more heterogeneous than other age groups and this is reflected in their PGE status and responses; nonetheless, the second year in the life

of cattle is important insofar as it is when breeding animals are expected to grow and reach target weights for sale and replacement heifers must reach their minimal mating weight by ~15 months of age if they are to calve at 2 years of age

non-If SGS animals have not grazed previously, then they should be considered nạve with respect to PGE, though there is some evidence for older, larger

cattle to be more resilient (Kloosterman et  al.,

1991) In SGS cattle that have grazed previously, their immune status affects their susceptibility to PGE; providing they have grazed for 3–6 months in the FGS, animals should be immune to cooperiosis and partially immune to ostertagiosis

Parasitic Gastroenteritis in Cattle 17

Yearling beef cattle that are born the previous

spring and not weaned till late in the year may have

had limited exposure to PGE while suckling and

hence incomplete immunity and this is reflected in

lower growth rates in the SGS, particularly in calves

born late the previous year (Guldenhaupt and

Burger, 1983; Taylor et al., 1995) A meta-analysis

of data from stocker calves in North America

dem-onstrated growth benefits from anthelmintic

treat-ments in this class of cattle, the mean response

being 50 g/day (Baltzell et  al., 2015) Beef heifer

replacements have also been shown to benefit from

anthelmintic treatments by growing faster, having

better fertility and rearing heavier calves (Loyacano

et  al., 2002) Control of PGE in dairy heifers has

also shown benefits in terms of growth rate and

onset of puberty (Mejia et al., 1999).

Adult cattle

Beef cows

Adult beef cows in extensive systems play an

important role in the epidemiology of PGE through

their role in contaminating pastures with nematode

eggs, particularly of O ostertagi (Stromberg and

Averbeck, 1999; Forbes, 2018), but they can

experience some losses themselves through the effects of subclinical PGE In several studies, improvements in cow fertility following anthelmin-tic treatment have been observed (Stuedemann

et al., 1989; Stromberg et al., 1997); these are

gen-erally attributed to improved energy balance and body condition In addition, beef cows treated with

an anthelmintic shortly after calving yielded 25% more milk per suckling compared with untreated cows (Stromberg and Corwin, 1993); these differ-ences in milk yield were reflected in calf weaning weights, which were 14–20 kg higher in calves from treated cows compared with untreated animals

Dairy cows

The scientific evidence base for the negative effects

of subclinical ostertagiosis on milk yield in dairy

cows is now quite extensive (Gross et  al., 1999; Sanchez et al., 2004; Charlier et al., 2009; Forbes,

2015); furthermore, the mechanisms for the sion in milk yield as a result of subclinical PGE, which is approximately 1 kg/day over a lactation

depres-(Charlier et  al., 2009), are better understood

Longitudinal studies of abomasa in the abattoir have revealed not only that many cows harbour

Grazed for 6.5 h/day Grazed for 7.7 h/day

Anthelmintic treated

DLWG 0.8 kg/day

Untreated DLWG 0.65 kg/day

6500 kg DM herbage/ha

4800 kg DM herbage/ha

Fig 2.5 Comparison of swards in adjacent paddocks; the left hand one has been grazed by anthelmintic-treated

calves and the right hand one by matched controls for 2 months Data from Forbes et al., 2000.

18 Parasites of Cattle and Sheep

burdens of O ostertagi (Burrows et  al., 1980a;

Vercruysse et  al., 1986; Agneessens et  al., 2000;

Borgsteede et  al., 2000) but also that abomasal

lesions, often extensive, are found in the majority

of adult cattle (Larraillet et al., 2012; Bellet et al.,

2016) Pathophysiological changes associated with

dysfunctional gastric glands, including

hypergastri-naemia, may be associated with the reduction in

daily grazing time of ~1 h in dairy cows, compared

with those treated with an anthelmintic (Forbes

et al., 2004) Thus, the adverse effects of subclinical

ostertagiosis in lactating dairy cows result from

responses including:

● Reduction in feed intake

● Impaired digestion

● Diversion of nutrients towards immune responses

As with beef cows, there is some evidence for

adverse effects of PGE on fertility in dairy cows too

in some studies (Sanchez et  al., 2002; Charlier

et  al., 2009) A summary of the main negative

effects of subclinical PGE in cattle is shown in

Table 2.1

Larval Ecology and the Epidemiology

of Parasitic Gastroenteritis in Cattle

The importance of an understanding of the biology

of free-living stages of parasitic nematodes in the

epidemiology and control of PGE was emphasized

many years ago, when it was stated that:

An enquiry into the detailed bionomics of the

free-living larvae of these parasitic worms

relative to the causes underlying the development

of parasitic gastritis concerns everything that

influences the hatching of the eggs of the

parasitic worms, their successful development

to the infective-larval stage, the longevity of the infective larvae in the pasture and the ultimate transmission of the larvae to the host animal (Taylor, 1938, p 1266)

Egg hatching and development to the

infective larval stage

Following a pre-patent period of ~21 days, worm eggs can be detected in faeces (Fig 2.6), and under natural pasture conditions, the eggs develop within the dung pats Providing the pats do not desiccate, hatching and the rate of development through the free-living larval stages is temperature-dependent (Rose, 1961, 1962, 1963); minimum development

times for O ostertagi and C oncophora are shown

in Table 2.2.The dynamics of the free-living stages of both

O ostertagi and C oncophora are very similar

and will be considered together (Rose, 1961,

1962, 1963) The minimum time taken for opment from egg to L3 under controlled condi-

devel-tions for both O ostertagi and C oncophora is

<1–3 weeks over a typical grazing season starting

in April and ending in October: development times on pasture during the winter months can range between 3 and 20 weeks (Rose, 1961, 1963) The optimum temperature for develop-ment for both species is ~25°C (Ciordia and Bizzell, 1963; Pandey, 1972) Once cattle are housed, development can still take place in the faeces if the bedding is conducive to maintaining suitable conditions of temperature and moisture; development of small strongyles to the infective larval stage has been demonstrated in stabled

horses (Love et  al., 2016) and cattle (Love,

2016) Nonetheless, there is currently no dence that cycling of gastrointestinal nematode infections occurs to any significant effect in housed cattle

evi-Survival of infective larvae

The L3 retains the cuticle of the L2 as a sheath that appears to confer some protection to the larvae as they are relatively resilient to fluctua-

tions in environmental conditions: O ostertagi and C oncophora L3 can be recovered from

herbage ~2 years after deposition in the dung (Rose, 1961, 1963) Intact dung pats that have

Table 2.1 Summary of proven effects of subclinical

parasitic gastroenteritis on performance of cattle

Class of stock Effect on performance

First grazing season Growth rate

Second grazing season Growth rate

Carcass yield and qualityPregnancy rate

Confined (feedlot) cattle Feed conversion ratio

Beef heifers Pregnancy rate

Dairy heifers and cows Milk yield

Calving to conceptionBeef cows Calf weaning weight

Pregnancy rate

Parasitic Gastroenteritis in Cattle 19

developed a crust provide a good habitat for

infective larvae (Fig 2.7), as long as sufficient

moisture is retained and they can act as a

reser-voir of infective larvae for several months (Rose,

1961) The importance of this reservoir is that,

following (heavy) rainfall, the crust is softened

and larvae are splashed out onto the surrounding

herbage where they can provide a high challenge

to grazing cattle; this probably explains

out-breaks of PGE in late summer/autumn following

a prolonged period of warm weather without rain

(Rose, 1961, 1962) The same mechanism

oper-ates in Mediterranean and subtropical countries

with more distinct dry and wet seasons, which

enables larvae to survive in faeces over periods of

drought, when mortality of larvae on herbage is

high (de Chaneet et al., 1981; Barger et al., 1984;

Fiel et  al., 2012; Knapp-Lawitzke et  al., 2014)

and there is a high risk of PGE once the rains

return (Chiejina and Fakae, 1989)

Development in faeces

Bovine dung pats are described as patchy, eral habitats insofar as they are deposited discreetly throughout cattle pastures and they are temporary, breaking down over time Disintegration of pats results from various perturbations, including rain-fall, mechanical disturbance through machinery, grazing animals, foraging birds or wild mammals and a suite of invertebrates, the best known of which are dung beetles (Putman, 1983) In tem-perate regions, flies and earthworms typically predominate in the dung fauna and the latter contribute most to the burial of dung, more so than insects (Holter, 1979) Disruption of the pat can have positive and negative effects on nema-tode larvae: if fragments are exposed to hot dry conditions, then dung becomes desiccated and larval mortality is high (Reinecke, 1960); con-versely, in wet conditions, larval survival is high and the scattered fragments of faeces can act as repositories for infective larvae over a large area

ephem-of pasture (Rose, 1962; Devaney et  al., 1990)

Dung beetle guilds include those that fragment

dung pats in situ (endocoprids/dwellers), which

are the most common in temperate zones; those that bury dung in tunnels below the pat (paraco-prids/tunnellers) and those that roll balls of dung away from the pat and bury them a distance away (telocoprids/rollers); these predominate in sub-tropical regions (Halffter and Edmonds, 1982) Different feeding behaviours can result in larvae

Fig 2.6 Strongyle eggs in faeces Courtesy of Dr S Rehbein, Kathrinenhof Research Centre, Rohrdorf

Table 2.2 Minimum development times of Ostertagia

ostertagi and Cooperia oncophora in bovine dung pats.

Development Minimum time in days

Egg to L3 O ostertagi C oncophora

20 Parasites of Cattle and Sheep

being buried in the soil inside dung balls or

exposed to the disruptive activities of beetles

within the pat and the consequences vary

accord-ingly The evidence for their role in nematode

transmission and the epidemiology of PGE is

equivocal because the outcomes are dependent on

several variables, including the functional guilds

of beetles present, seasonality and weather

condi-tions (Nichols and Gomez, 2014) Several studies,

mostly conducted in subtropical regions with

tun-nellers and rollers, have shown reductions in

infective larval populations in faeces or the

sur-rounding herbage in dung colonized by beetles

compared to insect-free pats (Reinecke, 1960;

Bryan, 1973, 1976; Gronvold et al., 1992) Only

two studies actually examined the consequences

of dung beetle activity in terms of acquisition of

infection, and in these, a lower uptake of larvae by

grazing calves was demonstrated (Fincher, 1973,

1975) In a study in a temperate region where

endocoprid Aphodius spp predominate, a

well-replicated, factorial trial that ran for 10 weeks

showed that effects on larval recovery varied by

time from deposition and rainfall, but overall

there was ~20% reduction in infective larvae in

pats with beetles compared with those with no

insect colonization (Sands et  al., 2017); it was

also noted that heavy rainfall could override

these effects However, in another study in Europe

with an Aphodius-dominant beetle fauna, larval

translocation was facilitated in the presence of

beetles (Chirico et  al., 2003), demonstrating the

variability of interactions between dung beetles

and the free-living stages of gastrointestinal

nematodes

Larval survival

The longevity of larvae on pasture is important from an epidemiological perspective, but there are two other areas of interest if cattle are housed:

● Survival of infective larvae in hay or silage fed to cattle is a potential risk factor for PGE

● The fate of worm eggs and larvae in manure and slurry from animals that did not receive a hous-ing treatment

Unfortunately, there is not a great deal of research

on these topics and some of it resides in relatively cessible journals, but a series of papers describing

inac-studies conducted with O ostertagi and C oncophora

in Sweden do provide some data In hay, ~50% of larvae survived for 3 days in the field after cutting; following storage in a barn and subject to drying with

a fan, survival declined to ~3% after 6 weeks, but a year later a few viable larvae could still be recovered (Persson, 1974d) In formic acid–treated grass silage with a pH of 4.2 and at a temperature of 33°C, 10%

of the larvae were viable after 40 days, but by 50 days

no live larvae could be found (Persson, 1974b) From this small data set, it can be concluded that infective larvae can survive in both hay and silage, but the num-bers decline during storage and it seems unlikely that these feeds would pose a significant risk of PGE in housed cattle, particularly older stock

Storage of manure, comprising dung, urine and bedding, can result in a core temperature of 40°C, which leads to the destruction of both nematode eggs and larvae; however, if manure is stored in smaller heaps and the internal temperature does not exceed 27°C, then most eggs and larvae survive (Persson, 1974c) Survival of eggs and larvae in slurry (liquid faeces) is temperature-dependent; at 20°C no viable eggs or larvae are present after 28 days, whereas at 3°C they live for 160–172 days (Persson, 1974a) These laboratory data supported field observations in which eggs and larvae survived

in slurry for 11–44 days during the summer, but for 3–5 months in autumn and winter; the latter num-ber is most relevant to commercial farms as it covers the period when cattle are normally housed Studies

in Ireland showed high numbers of worm eggs and larvae could be recovered from slurry derived from untreated, housed calves (Moore, 1979) and that the risk of PGE in calves grazing pastures on which slurry has been spread was higher than on a match-ing plot that had been dressed with an artificial nitrogenous fertilizer; pasture larval counts were higher on the slurry-treated paddock and calves

Fig 2.7 Dung pat with crust; a reservoir of infective

larvae

Parasitic Gastroenteritis in Cattle 21

exhibited signs of clinical PGE in June (Downey and

Moore, 1977) Similar results were seen in Danish

studies, in which spring (March) application of

slurry to calf pastures resulted in subclinical and

clinical PGE over the period between May and July

(Nansen et al., 1981) The same authors reported on

an outbreak of clinical PGE in housed calves that

were fed on freshly cut grass from a field that had

previously been fertilized with slurry

Translocation of infective larvae to herbage

The infective L3 are motile but appear to have

lim-ited capacity for active migration, in part due to the

fact that they do not feed and therefore have a finite,

non-renewable energy source Nevertheless, there is

some active movement within the dung as the

major-ity of L3 are eventually found in the top third of the

pat (Rose, 1961), presumably in readiness for

trans-location on to the surrounding herbage Transtrans-location

from the pat to the surrounding herbage requires

moisture to facilitate both active and passive

move-ment The ability of infective larvae to move actively

over distances of more than a few centimetres

appears to be limited Studies have shown that most

larvae move no more than ~5 cm horizontally from

the pat of origin (Rose, 1961) and their propensity to

travel vertically up the herbage appears to be equally

limited, with the majority of larvae being found in

the lower 5 cm of the sward (Silangwa and Todd,

1964; Williams and Bilkovich, 1973) However,

because guidelines for the continuous stocking

man-agement of cattle grazing temperate ryegrass swards

currently recommend that the sward height should

be maintained between 5 and 8 cm, there is ample

opportunity for such stock to ingest infective larvae,

particularly if they graze close to older dung pats

Infective larvae are typically found in higher

concen-trations in the herbage surrounding dung than in the

shorter, grazed turf (Gruner and Sauve, 1982)

Nevertheless, ruminants normally avoid grazing on

vegetation close to fresh dung, except when grazing

pressure is high (Bosker et al., 2002).

Passive mechanisms, however, can facilitate

disper-sal of infective larvae over greater distances from the

faecal pat Rainfall is known to be a very important

agent in facilitating passive movement of larvae away

from dung and onto pasture The mechanism involves

an initial wetting and softening of the dry crust,

which typically forms on pats after deposition,

fol-lowed by infective larvae close to the surface of the pat

being splashed out in droplets through the kinetic

energy of the falling rain (Rose, 1962; Gronvold, 1984b, 1987) Passive movement of larvae by this means can account for 90% of the translocation of larvae from the pat to the pasture, and larvae can be found up to 90 cm from the pat The trajectory of the droplets carrying infective larvae is normally at a height of 30 cm above ground, so, on landing on the herbage, they will initially be deposited on the upper leaves of the herbage and hence will be in the zone where they are likely to be ingested by grazing ani-mals (Gronvold and Hogh-Schmidt, 1989)

Spread of infective larvae beyond this range almost certainly takes place passively through trans-port hosts, including invertebrates such as earth-

worms (Gronvold, 1979), insects (Tod et al., 1971)

and vertebrates such as birds (Gronvold, 1984a) and livestock; viable infective L3 can be found in sam-ples of encrusted faeces on the feet and limbs of

grazing cattle (Hertzberg et  al., 1992) Farming

activities such as harrowing can also disperse dung along with any larvae present; indeed, this may be the main reason for carrying out this operation, though whether harrowing reduces or increases the risk of PGE is highly weather-dependent Although widely known to play an important role in the dis-persal of lungworm larvae, there is also evidence

that fungi of the genus Pilobolus, which commonly

grow on fresh cattle dung, can also disperse larvae of

Cooperia and Trichostrongylus spp when their

spo-rangia discharge spores (Bizzell and Ciordia, 1965)

The Epidemiology of Parasitic Gastroenteritis in Cattle

The majority of studies on epidemiology have been carried out with autumn-born, weaned, FGS calves, typically derived from dairy herds; in some studies, observations were continued into the animals’ SGS There have been some studies in beef suckler herds, looking at cow–calf pairs in spring calving herds, but few in adult dairy herds While some of the findings of this research can be relevant across all the different systems, from an applied point of view, it is preferable to consider them separately

Weaned, first grazing season calves on

permanent pasture

The first encounter with nematode parasitism in nạve, autumn-born calves, typically derived from the dairy herd, is after they are turned out in the spring on to pastures grazed by cattle the previous

22 Parasites of Cattle and Sheep

year The larvae of both O ostertagi and C

onco-phora can survive over winter; the number present

in spring depends on the larval populations present

in the previous autumn before cattle are housed

and the weather over winter Overwinter survival is

high if temperatures are low and in particular if

there is a covering of snow, as the larvae are in a

state of suspended animation and not utilizing

energy; conversely, if winters are warmer, the larvae

have a higher metabolic rate and their energy

reserves deplete more rapidly, shortening their

sur-vival In the absence of grazing cattle, larval

popu-lations typically decline exponentially until by

June/July few viable larvae remain on pasture

Calves ingest infective larvae immediately once

they start to graze, and the worms develop through

two more larval stages to become adult worms

within ~3 weeks; males and females mate and the

females commence laying eggs, which can be

detected in the calves’ faeces Following this

pre-patent period, the eggs are continually deposited in

the dung, where they develop into infective larvae

Given the temperature dependence of egg hatching

and larval development, it follows that eggs

depos-ited early in spring take considerably longer to

develop than those deposited later, when ambient

temperatures increase as summer approaches The net effect of this is that there is a concertina effect resulting in the simultaneous appearance of infec-tive larvae on pasture, typically from mid-July onwards (Fig 2.8) Though subject to some annual variation, this pattern is quite repeatable from year

to year in southern England (Michel, 1969a; Rose, 1970; Lancaster and Hong, 1987), Scotland

(Armour et al., 1979), continental Europe (Eysker

and van Miltenburg, 1988) and temperate zones in the southern hemisphere (Brunsdon, 1969; Suarez, 1990) The repeatable epidemiological patterns of PGE form the basis for several strategic approaches

to control PGE, for example:

● Strategic anthelmintic treatment of calves from turnout to ensure minimal further contamina-tion of pastures with worm eggs until mid-July, after which larval populations should remain low for the remainder of the grazing season, providing animals are kept on the same pasture

for the rest of the grazing season (Shaw et al.,

1998b)

● Tactical anthelmintic treatments from mid-July

to limit the impact of exposure to contaminated pasture (Steffan and Nansen, 1990)

Basis for strategic control of PGE

0Jan Feb

March Apri

lMay June July Aug Sept Oct Nov Dec

Weaned FGS calves turned out in April; Housed November; No treatment or moves

Main risk of disease

Fig 2.8 Diagram of epidemiology of parasitic gastroenteritis in weaned, first grazing season calves

Parasitic Gastroenteritis in Cattle 23

● Move calves to a low-risk pasture (e.g an

aftermath) in July, to avoid exposure to peak

larval populations (Michel, 1968a), with or

without anthelmintic treatment

(dose-and-move)

● Monitoring calves from ~2 months after

turn-out in order to identify and treat individuals

with (subclinical) PGE in a targeted selective

treatment (TST) approach (Merlin et  al.,

2018)

When exceptions to these patterns arise, calves

may be vulnerable to PGE at unexpected times; two

examples are:

● High populations of infective larvae survive over

winter, posing a risk to nạve calves immediately

after turnout and sometimes causing clinical

PGE The circumstances under which this can

occur are as follows:

 In temperate zones, following a very dry

summer the previous year, when pats fail to

disintegrate over winter, larvae survive in the

protected environment in the pat contents

and then, following the onset of warmer

tem-peratures and sufficient rainfall, larvae

trans-locate onto pasture in high numbers in spring

(Taylor et al., 1973)

 In Nordic countries and regions that

experi-ence low winter temperatures where snowfall

is common, larvae can survive in dung or on

pasture, protected from fluctuations in

tem-perature and humidity, and be present in

suf-ficient numbers to cause PGE in calves soon

after turnout (Smith and Archibald, 1968;

Helle and Tharaldsen, 1976; Oksanen and

Nikander, 1981)

 A combination of both a dry summer and

a cold winter provides good conditions for

larval survival in dung pats, which have

not disintegrated because of the lack of

rainfall and also low temperatures, which

diminish the activities of various

inverte-brates that facilitate decomposition of

dung, for example earthworms and

copro-philous insects (Holter, 1979) A study in

Denmark showed that in May at turnout

the pasture larval counts in grass tufts

within 200 mm of overwintered dung pats

were of the order 103–104, whereas those

on pasture >200 mm from pats were 102

(Nansen et al., 1989), providing strong evidence

that it was the recent translocation of tive larvae from the pats that was responsi-ble for the high challenge to the calves, resulting in clinical PGE within a month of turnout

infec-● Rather than experiencing the typical tial decline in overwintered larval populations

exponen-to low levels in July, high numbers are present

on fields that have not been grazed since the previous year, resulting in PGE in calves graz-

ing silage aftermaths (Bairden et  al., 1979; Armour et al., 1980) The most likely explana-

tion for these observations is that soil can act as

a reservoir for infective larvae and facilitate

their long-term survival (Al Saqur et al., 1982; Dimander et al., 1999; Knapp-Lawitzke et al.,

2016)

Cow–calf pairs in beef suckler herds

The most common type of husbandry in beef ler herds is for the animals to calve in spring (Gates, 2013) in order to take advantage of early grass to support lactation in the dams, thus optimizing growth in their offspring Suckler calves rarely suf-fer clinical PGE before weaning, though production

suck-losses can occur (Forbes et  al., 2002); there are

several reasons for this, including relative lack of exposure to infective larvae and the nutritional benefits of a milk-based diet, which can support high growth rates (>1 kg/day) The ratio of milk to forage in the diet of calves declines up to the age of

6 months, but even then, milk supplies ~50% of the

dry matter (DM) in the diet (Boggs et  al., 1980),

thus limiting the intake of infective larvae from pasture Furthermore, there appears to be a protec-

tive effect of milk in the diet against O ostertagi,

particularly in calves in which reticuloruminal

development is incomplete (Satrija et al., 1991).

The larval challenge to which suckler calves are exposed derives from overwintered larvae, though

by the time grass forms a significant part of their diet, these populations should be very small; how-ever, faecal contamination by the cows ensures that viable populations of infective larvae are present on pasture throughout the grazing season Contrary to some assumptions, cows are significant contribu-

tors to pasture larval populations of O ostertagi

because, despite their low faecal egg counts (FECs) (frequently <50 eggs per gram), each animal pro-duces a large volume of faeces each day (~25–30 kg/head) and this can result in thousands of worm

24 Parasites of Cattle and Sheep

eggs being deposited by each cow every day

(Stromberg and Averbeck, 1999) In spring-calving

herds, the month of calving also has an effect;

calves born early in the year suffer higher levels of

exposure and exhibit higher pepsinogen values

(reflecting ostertagiosis) compared with calves

born later in spring (Hưglund et al., 2013b).

Second grazing season cattle

By their SGS, most young cattle, irrespective of

their sex, type or destiny, will have been weaned

and will be entering a productive stage of their

lives, either as replacement heifers or as beef

ani-mals Assuming that they grazed naturally over

several months during their FGS, they should be

functionally immune to Cooperia spp and be partially

immune to O ostertagi so when they re-encounter

infective larvae on pasture following turnout, the

epidemiological pattern is similar to that in the

FGS, but larval populations on pasture will be

lower and comprise predominantly O ostertagi

Though clinical ostertagiosis has been observed in

yearlings and stockers (Taylor et  al., 1995),

sub-clinical disease poses the main threat as good live

weight gains are important for young cattle (Baltzell

et al., 2015), either to achieve target mating weight

by 15 months of age in replacement heifers

des-tined to calve at 2 years of age or to be marketed

economically at suitable weights for beef

Dairy herds

While most beef breeding herds have a seasonal

calving pattern with spring being the most common,

the picture is not so consistent in dairy farming

Although the basis of much of the research on PGE

in young cattle derives from studies conducted in

weaned, autumn-born calves from the dairy herd

(see above), this calving pattern appears to be

unu-sual now and many dairy herds currently run an

all-year-round (AYR) calving policy (Gates, 2013)

AYR calving provides a regular supply of milk

throughout the seasons and is preferable for

conti-nuity of supply to dairies and to ensure a regular

farm income that is not subject to seasonal

varia-tions AYR can also accommodate calving intervals

>365 days and allows a more flexible approach to

fertility management; in contrast strictly seasonally

calving herds require a sustainable, annual

intercalv-ing interval of ~365 days if the calvintercalv-ing season is not

to become too protracted and extend beyond ~2–3 months Spring-calving dairy farming predominates

in countries like Ireland and New Zealand, where dairying is based on optimal utilization of grassland

to support lactation in low-input systems

All-year-round calving dairy herds

The epidemiology of PGE in these different types of dairy farming has been less well studied than in autumn-calving herds and in particular, AYR herds

In theory, slightly less than 10% of calves are born each calendar month in AYR herds so that at any one time, cattle less than a year old (‘FGS calves’) comprise animals from 1 to 12 months of age with correspondingly different live weights and exposure

to infective larvae on pasture Indeed, on some farms, young cattle may not graze until they are over a year old, either because of farm policy or as

a result of their month of birth or a combination of both Furthermore, depending on age, calves may be turned out in spring, summer or autumn and will therefore encounter different challenge on pasture, depending on the previous grazing/cutting manage-ment of each field From a practical point of view at farm level, it is probably best to subdivide calves <1 year old into 2–4 cohorts of animals of roughly the same age, weight and grazing experience in order to manage PGE in each group in a rational way

Spring-calving dairy herds

Spring-calving herds typically start calving from late January through to April with a peak in February/March in the northern hemisphere (Ireland) and July to August in the southern hemi-sphere (New Zealand) In principle, if spring-born calves are kept inside until weaning at ~12 weeks

of age, then they could be turned out onto low-risk (fields that have not been grazed by cattle that year) pastures in mid-summer, by which time over-wintered larvae will normally have declined to very low concentrations However, current practices include early turnout onto pastures where calves are still fed milk until early weaning when they are

~6 weeks old Because of limitations of farm structure and the need to have calves close to the steading for close supervision and ease of manage-ment, the same paddocks may be used every year and thus there is a high risk of nạve calves encoun-tering infective larvae (and also coccidial oocysts) from an early age

infra-Parasitic Gastroenteritis in Cattle 25

Epidemiology of PGE on dairy cow pastures

Epidemiological studies on PGE in adult dairy

cows are rare, possibly because of the priority given

to grassland management for optimal milk

produc-tion on many farms and the lack of interacproduc-tions

between the milking herd and young stock There is

some evidence for a peri-parturient rise (PPR) in

worm egg counts in dairy heifers calving for the

first time (Borgsteede, 1978; Michel et  al., 1979)

and a ‘spring rise’ has also been reported in both

spring (PPR-associated) and non-seasonal calving

herds (Burrows et  al., 1980b; Hammerburg and

Lamm, 1980; Eysker and Van Meurs, 1982)

Generally speaking, adult dairy cows have low

FECs because:

● O ostertagi is the most common species present

in adult cattle and it has intrinsically low

fecun-dity (Burrows et al., 1980b)

● Acquired immunity reduces egg output

● For much of the year, especially over winter,

inhibited larval O ostertagi predominate in the

population

If the standard McMaster technique is used,

then individual FECs in cows are frequently below

the level of detection (50 eggs per gram (EPG))

(Forbes et  al., 2004); where more sensitive

tech-niques have been used, average egg counts are

typically in single figures (1–5 EPG) (Fox and

Jacobs, 1980; Eysker et  al., 2002; Fox et  al.,

2007) Though worm egg counts are low in dairy

cows, the same rationale applies as for beef cows

insofar as the large weight of faeces produced per

day (~30 kg), means that they can deposit

thou-sands of eggs daily, which after development to

infective larvae and translocation, can contribute

significantly to pasture contamination and

conse-quently increase the risk of PGE (in young stock)

Pasture larval counts in dairy cow fields typically

average ~250 L3/kg DM (Fox and Jacobs, 1980),

but with a range of 0–3500 L3/kg (Eysker et al.,

2002; Fox et  al., 2007) There are some

indica-tions that concentraindica-tions of infective larvae in

herbage have risen over a >20-year span (Fox

et  al., 2007); possible explanations include more

intensive grassland management, higher stocking

density and increase in Holstein genetics, but

these are all speculative From these observations

and using an average daily herbage intake of ~12

kg DM, it can be estimated that daily larval

intakes in grazing dairy cows range from 0 to 105

Diagnosis and Monitoring of Parasitic Gastroenteritis in Cattle

PGE in cattle essentially comprises coinfections

with O ostertagi and C oncophora in young

grazing cattle less than a year old and osis in adult cattle, with occasional contributions

ostertagi-from other nematode species such as Nematodirus and, in the tropics, Haemonchus placei In tem-

perate regions, the ubiquity of PGE means that identification of infection alone is inadequate and the goals of diagnosis and monitoring are to quantify the actual or potential impact of infec-tion on health and production Common prac-tices include:

● Regular observation of young cattle to detect clinical signs (scour) and ill-thrift

● Weighing of cattle to measure growth rates and compare with targets or expectations

● Monitoring milk yield for quantity, quality and unexplained fluctuations

● Bulk milk tank sampling for O ostertagi

anti-bodies

● Blood sampling for plasma pepsinogen

● Faecal sampling for nematode eggsThe first three are essentially part of good animal husbandry, but with a focus on any observations and trends that might be associated with PGE Milk yield

in dairy cattle can be influenced by numerous tors, so parasitism would not normally be the first factor to be considered; nonetheless, if yields during the grazing season are below expectations and there are no other obvious explanations, subclinical ostertagiosis is worth investigating Bulk tank milk

fac-samples can be tested for O ostertagi antibodies to

determine the level of exposure and likelihood that parasite-related losses are occurring

If nutrition is adequate and there are no other obvious causes of poor growth, then the most probable reason for young cattle having low DLWG is subclinical PGE; these observations and assumptions form the basis for TST in cattle

(Kenyon and Jackson, 2012; Höglund et  al.,

2013a) PP values are elevated when abomasal pathology is present and the most common cause

of this in groups of young cattle is ostertagiosis, hence testing for PP is useful in confirming infec-tion and also in differential diagnosis of ill-thrift

(Charlier et al., 2011).

FECs in cattle are not consistently associated with either the magnitude of worm burdens or

26 Parasites of Cattle and Sheep

adverse effects of PGE in cattle (Michel, 1968b;

Forbes, 2017), hence cannot be relied on for

diag-nosis, indeed FECs can be misleading as they are

commonly low even in clinical PGE (Fig 2.4;

Jackson, 2012) Coupled with weighing animals,

FECs can provide useful prognostic estimates of

negative impacts of PGE in weaned, FGS cattle

sampled ~2 months after turnout (Höglund et al.,

2009) Somewhat counterintuitively, in dairy

cows sampled at calving and using a sensitive

FEC technique, potential effects of PGE on milk

yield can be estimated (Mejia et  al., 2011;

Verschave et al., 2014b).

Control of Parasitic

Gastroenteritis in Cattle

The control of PGE in cattle can incorporate most

of the general elements of integrated parasite

management that are outlined in Chapter 19 (this

volume), but those that can be widely adopted on

most livestock farms are grazing management and

anthelmintic treatment Grazing management is

covered in Chapter 17 (this volume) and some of

the definitions and principles of anthelmintic use in

Chapter 18 (this volume); hence this section

focusses on the use of anthelmintics to control PGE

in cattle The main objective of PGE control in a

farm setting is to reduce the larval challenge to a

level that does not cause clinical disease and that

permits good performance This principle is

illus-trated in Fig 2.9, which shows the effect of

differ-ent daily doses of O ostertagi larvae on growth

performance in calves; as can be seen, a low challenge

of 200 larvae per day has little effect on mance (Michel, 1968a)

perfor-Anthelmintics

In most countries there are only three classes of spectrum anthelmintics licensed for use in cattle:

broad-● Benzimidazoles (BZDs)

 Albendazole, febantel, fenbendazole, oxfendazole

 Most formulations are oral, including drenches and long-acting boluses

 No persistent activity except as boluses

● Tetrahydropyrimidines

 Levamisole (LEV), morantel

 Can be formulated as oral, topical, injectable and boluses

 No persistent activity except as boluses

 No efficacy against larval O ostertagi,

including hypobiotic stages

of brands is enormous In addition, combinations among these classes and in association with other actives, notably flukicides, are common The selec-tion of appropriate products to treat cattle can be

0102030405060

Parasitic Gastroenteritis in Cattle 27

influenced by several factors, not only their efficacy

against target parasites, for example:

● Efficacy spectrum

● Resistance status of target and other endemic

parasites (if known)

● Formulation

 Different efficacy profiles

 Ease of administration

● Persistent efficacy

 Treatment intervals and frequency

● Therapeutic index (safety)

● Meat and milk withdrawal periods

● Environmental impact profile

● Pack/unit size (number of animals to be treated)

● Shelf-life

● Cost

Anthelmintics may only be available through

vet-erinary channels, but in many countries they can be

purchased from licensed retailers as well, so

guid-ance for farmers can come from disparate sources

that inevitably differ in their knowledge and

partial-ity In many regions of the world where cattle are

reared, the most commonly used products are the

MLs, and their popularity presumably derives from

their high levels of efficacy against a broad spectrum

of parasitic nematodes and arthropods, persistent

activity and ease of administration with the standard

topical and injectable products in cattle of all ages

Inevitably, ML resistance has developed in several

parasite species, notably and unsurprisingly in

Cooperia species, as these are dose-limiting

(Sutherland and Leathwick, 2011; Mederos et  al.,

2018) Responsible use of anthelmintics is not just a

glib mantra, but a necessity as long as treatment is

one of the keys to effective parasite control

Commonly used patterns of anthelmintics in

cat-tle are as follows:

● Therapeutic

 Treatment of individual, clinically affected animals

● Metaphylactic

 Treatment of all at-risk animals following

detec-tion of signal, clinical cases within a group

● Tactical

 Treatment of groups of animals when

moni-toring indicates subclinical infections and

loss of performance

● TST

 Treatment of individual animals when

moni-toring indicates subclinical infections and loss

of performance

● Strategic

 Treatment of groups of animals during ing or early in the grazing season to limit pas-ture contamination with worm eggs and hence the risk of parasitism

hous- Treatment of groups of animals when they move to low-risk fields in summer to limit contamination of the new pasture with worm eggs and hence the risk of parasitism (Dose-and-Move, see Chapter 17, this volume)

● Opportunistic

 Treatment of animals when they are being handled for other reasons, particularly in extensive systems where animals are gathered infrequently

Therapeutic and metaphylactic treatments are used on farms where the practice, policy or phi-losophy is to wait until something bad happens before acting in a reactive way If the level of stock-manship is good, these approaches can prevent the overt welfare problems associated with clinical parasitism, but by their nature, they allow animals

to become sick before acting and they ignore the negative effects of subclinical PGE These treat-ments are given in a high refugia environment and

so should not select strongly for resistance, although high-frequency treatment is a consistent risk factor for anthelmintic resistance, irrespective of the cir-

cumstances (Mederos et  al., 2012; Suarez and

Cristel, 2014)

The principles behind early season, strategic treatments of young stock have been outlined pre-viously and they are proven to prevent clinical disease and to enhance animal performance, even when the parasite challenge is relatively low (Shaw

et  al., 1998a,b) Strategic approaches are best

suited to autumn-born, weaned calves, but can be used in the SGS in any class of stock if required Proven regimens are based on:

● Administration of first anthelmintic treatment at turnout (for convenience) or within 3 weeks of turnout, before patent infections establish

● Treatments are repeated at intervals that mize faecal egg output (persistency efficacy + pre-patent period) up to mid-July (~January in the southern hemisphere)

mini- Non-persistent BZDs and LEV: 3 weeks

 Standard, persistent MLs: 5–8 weeks

● Long-acting boluses and injections: only one treatment needed

28 Parasites of Cattle and Sheep

Because strategic treatments are given when

refu-gia are low both in the animals and on the pasture,

there is potentially an increased risk of selection for

resistance, but currently there is little empirical

evidence that strategic programmes pose a greater

risk than other anthelmintic use practices (Mederos

et  al., 2018) Lack of acquired immunity to

O.  ostertagi and C oncophora, due to limited

exposure to infective larvae, has also been raised as

a potential issue with strategic treatment schedules,

but again, under typical farming conditions and

subject to natural challenge, there is little evidence

of a lack of functional immunity in SGS and adult

animals following FGS strategic treatments

(Claerebout et al., 1999).

Although early season strategic treatments are a

reliable way of controlling PGE in young cattle, they

do not fit well into some farming systems and are

inappropriate in others; furthermore, as the trend

towards fewer treatments and less reliance on

anthelmintics continues, other approaches are

gain-ing wider acceptance In fact, TST and tactical

prac-tices are variations on the same theme insofar as

they rely on monitoring, using thresholds for

treat-ment and focussing on outcomes; the main

differ-ence is simply whether control centres on groups of

cattle or individuals The two systems can converge

if, for example, the majority of animals in TST reach

their threshold for treatment at the same time, while

a proportion of animals are deliberately not treated

in a tactical plan, in order to enhance the refugia

Tactical treatments are well-suited to groups of

grazing cattle up to the age of 2 years, by which

time most will either have been sold or have

entered the breeding herd Regular (monthly if

pos-sible) weighing provides the most accurate measure

of growth rate, which is arguably the most

impor-tant criterion for all decision making in the

hus-bandry of young stock, as it can provide farmers

with objective, quantitative information on the

nutritional status and health of their animals For

most farm types, average daily gains of at least

0.7–0.8 kg/day are needed for young cattle to reach

breeding and marketing objectives, and if animals

are growing slower, then possible causes need to be

investigated If subclinical PGE is deemed to be the

most likely reason, then the group can be treated

with an appropriate anthelmintic To enhance the

refugia, it is possible to leave say 10% untreated;

these animals could be randomly selected or picked

on the basis of them having growth rates above the

threshold

TST has been shown to be an effective practice

in the control of PGE in young cattle and new nology, including automatic weighing (Segerkvista

tech-et al., 2020), can facilitate its adoption; most

stud-ies have used average DLWG as the threshold for treatment and found that less anthelmintic is used and performance is comparable with group-treated

cattle (Greer et  al., 2010; McAnulty et  al., 2011; Höglund et  al., 2013a; Jackson et  al., 2017)

Generally, the first weighing should take place

2 months after turnout as growth rates are too erratic within the first few weeks, while cattle

adjust to a grass diet (Höglund et al., 2009; Merlin

et al., 2018) If adult dairy cows are to be treated

for subclinical PGE, then TST based on samples collected at calving and examined for FEC and/or

O ostertagi antibodies can identify individual cows

that may respond favourably to treatment (Mejia

et al., 2011; Verschave et al., 2014b).

Closing Remarks

PGE is ubiquitous in all cattle that have access to pasture or herbage and it has an impact on animal health and productivity and hence is subject to con-trol on all grass-based livestock farms, irrespective

of their scale, intensity, economics or ethics (Charlier

et al., 2020) Because of the core role of PGE,

con-trol of other parasite infections is commonly carried out as an adjunct to the management of PGE; fur-thermore, PGE is the focus of many important aspects of ruminant parasitology, including:

● Grazing management to limit exposure to tive larvae and to mitigate the impact of PGE

infec-● Breeding programmes for resistance or tolerance

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