Handbook of Equine Parasite Control

Handbook of Equine Parasite Control

Second Edition

Martin K. Nielsen, DVM, PhD, Dipl. ACVMAssociate Professor and Schlaikjer Professor Department of Veterinary ScienceM.H. Gluck Equine Research CenterUniversity of KentuckyLexington, Kentucky, USA

Craig R. Reinemeyer, DVM, PhD, Dipl. ACVMPresident, East Tennessee Clinical ResearchRockwood, Tennessee, USA

This edition first published 2018© 2018 John Wiley & Sons, Inc.

Edition HistoryJohn Wiley & Sons (1e, 2012)

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The right of Martin K. Nielsen and Craig R. Reinemeyer to be identified as the authors of this work has been asserted in accordance with law.

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Limit of Liability/Disclaimer of WarrantyThe contents of this work are intended to further general scientific research, understanding, and discussion only and are not intended and should not be relied upon as recommending or promoting scientific method, diagnosis, or treatment by veterinarians for any particular patient. In view of ongoing research, equipment modifications, changes in governmental regulations, and the constant flow of information relating to the use of medicines, equipment, and devices, the reader is urged to review and evaluate the information provided in the package insert or instructions for each medicine, equipment, or device for, among other things, any changes in the instructions or indication of usage and for added warnings and precautions. While the publisher and authors have used their best efforts in preparing this work, they make no representations or warranties with respect to the accuracy or completeness of the contents of this work and specifically disclaim all warranties, including without limitation any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives, written sales materials or promotional statements for this work. The fact that an organization, website, or product is referred to in this work as a citation and/or potential source of further information does not mean that the publisher and authors endorse the information or services the organization, website, or product may provide or recommendations it may make. This work is sold with the understanding that the publisher is not engaged in rendering professional services. The advice and strategies contained herein may not be suitable for your situation. You should consult with a specialist where appropriate. Further, readers should be aware that websites listed in this work may have changed or disappeared between when this work was written and when it is read. Neither the publisher nor authors shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages.

Library of Congress Cataloging‐in‐Publication Data

Names: Nielsen, Martin Krarup, 1972–, author | Reinemeyer, Craig Robert, 1952–, authorTitle: Handbook of equine parasite control / Martin K. Nielsen, Craig R. Reinemeyer.Description: Second edition. | Hoboken, NJ : John Wiley & Sons, Inc., 2018. | Craig R. Reinemeyer’s

name appears first in the previous edition. | Includes bibliographical references and index. | Identifiers: LCCN 2018000457 (print) | LCCN 2018001338 (ebook) | ISBN 9781119382805 (pdf) |

ISBN 9781119382812 (epub) | ISBN 9781119382782 (cloth)Subjects: | MESH: Horse Diseases–therapy | Parasitic Diseases, Animal–prevention & controlClassification: LCC SF959.P37 (ebook) | LCC SF959.P37 (print) | NLM SF 959.P37 | DDC 636.1–dc23LC record available at https://lccn.loc.gov/2018000457

Cover design: Martin K NielsenCover images: Top: Parascaris spp. eggs obtained from a single female worm (Photo courtesy: Maci Stephens).Middle: Icelandic colts on pasture (Photo courtesy: Shaila Sigsgaard).Bottom: Anoplocephala perfoliata eggs recovered from a gravid proglottid (Photo courtesy: Jamie Norris).

Set in 10/12pt Warnock by SPi Global, Pondicherry, India

10 9 8 7 6 5 4 3 2 1

Dedication

We dedicate this second edition to Dr. Eugene T. Lyons and his career-long assistant Ms. Sharon C. Tolliver, who both passed away shortly before this second edition went into print. They were passionate equine parasitologists, good friends, and highly respected by colleagues around the world. They both worked at the University of Kentucky for over 50 years and their contributions to equine parasitology are unmatched. They are by far the most cited authors in this book. Dr. Lyons described the life cycles of Strongyloides westeri, Thelazia lacrymalis, and Strongylus vulgaris. He virtually tested and evaluated every single anthelmintic product that ever made it to the equine market, and he diligently documented the progression of anthelmintic resistance in equine parasites. He published over 300 research articles. Sharon was his right and left hands through all of this. She was one of the world’s few experts on identifying equine helminth specimens, and she herself contributed to over 200 seminal publications in equine parasitology. It was a privilege to know and work with the two of them. They were both equine parasitologists par excellence and their passing really marks the end of an era. The discipline of veterinary parasitology is diminished by their absence, but their spirits and contributions linger on – as evidenced by this book.

vii

List of Contributors ixPreface to the First Edition xiPreface to the Second Edition xiiiAcknowledgements xv

Section I Internal Parasites and Factors Affecting Their Transmission 1

1 Biology and Life Cycles of Equine Parasites 3

2 Pathology of Parasitism and Impact on Performance 25

3 Environmental Factors Affecting Parasite Transmission 45Contributing authors: Dave Leathwick and Christian Sauermann

4 Host Factors Affecting Parasite Transmission 55

5 Parasite Factors Affecting Parasite Transmission 61

Section II Principles of Equine Parasite Control 69

6 Decreasing Parasite Transmission by Non‐chemical Means 71

7 Pharmaceutical Approaches to Parasite Control 81Contributing authors: Dave Leathwick and Christian Sauermann

8 Anthelmintic Resistance 99

Section III Diagnosis and Assessment of Parasitologic Information 111

9 Diagnostic Techniques 113

10 Detection of Anthelmintic Resistance 141

11 Evaluating Historical Information 149

12 Synopsis of Evidence‐Based Parasite Control 155

Contents

Contentsviii

Section IV Case Histories 163

Case 1: Mystery Drug 165

Case 2: Pyrantel Efficacy Evaluation 167

Case 3: Egg Count Results from Yearlings 169

Case 4: Peritonitis and Parasites 173

Case 5: Confinement after Deworming 177

Case 6: Abdominal Distress in a Foal 179

Case 7: Quarantining Advice 181

Case 8: Diarrhea and Colic 183

Case 9: Foal Diarrhea 187

Case 10: Oral Lesion 191

Case 11: Skin Lesion 193

Case 12: Legal Case 197

Case 13: Repeated Egg Counts 199

Case 14: Repeated Colic 201

Case 15: Ivermectin Efficacy 205

Case 16: Anthelmintic Treatments in Foals 207

Case 17: Ivermectin Egg Reappearance 209

Case 18: Name That Worm 211

Case 19: Parasite Control for Yearlings 213

Case 20: Reaction to Treatment 215

Case 21: Anthelmintic Toxicosis? 217

Case 22: Deworming Program Adjustment? 219

Glossary 221

Index 225

ix

Dave Leathwick PhDAgResearch GrasslandsPalmerston NorthNew Zealand

Christian Sauermann PhDAgResearch GrasslandsPalmerston NorthNew Zealand

List of Contributors

xi

This book was conceived through the authors’ realization that equine practi­tioners were not likely to achieve compe­tence in evidence‐based parasite control (EBPC) by reading journal‐length articles or by attending a few hours of continuing education. Like any clinical skill set, par­asite control must be grounded solidly in theory, practiced with thoughtful applica­tion, and continuously assessed and improved. Most new clinical skills, such as surgical procedures or diagnostic algo­rithms, represent variations of basic pro­ficiencies or knowledge already held by practitioners, who can also turn to local mentors for advice and support. In con­trast, the private sector harbors few, if any, experts in equine parasitology who can impart mastery of the principles of EBPC.

Evidence‐based parasite control is a rel­atively new development in equine medi­cine, but similar principles have been applied for  decades by small ruminant practitioners in Europe and the southern hemisphere. In  these locales, parasitic challenges to indigenous livestock are prevalent and extreme. Near‐total anthel­mintic resistance by certain parasites (e.g., Haemonchus contortus) has rendered practical control of these highly patho­genic nematodes nearly impossible, with severe economic consequences for the sheep and goat industries on multiple continents. In comparison, equine cyathostomins (small strongyles) have demonstrated resistance to one or more anthelmintic classes for nearly four

decades, but these nematodes are modest pathogens under most circumstances. The authors and other veterinary parasi­tologists have been disseminating EBPC recommendations for many years, but equine practitioners have been relatively unreceptive to these messages until very recently. The impetus for this changed attitude is uncertain, but it seems to be associated with the contemporary detec­tion of anthelmintic resistance in some populations of Parascaris equorum. Mere demonstration of resistance in a second group of equine parasites is not likely the major threat perceived by practitioners. Rather, it could be the hard evidence that macrocyclic lactone anthelmintics, previ­ously considered bullet‐proof panaceas in horses, are also vulnerable to nema­tode resistance.

Regardless of the motivation, equine practitioners now seem uniquely recep­tive to EBPC, and this book represents our attempt to address that interest and to fill the need with practical advice and logical recommendations. Most veteri­nary textbooks organize and discuss related facts, and then present recom­mendations for the logical application of that knowledge in clinical situations. This handbook has an additional objective that is far more daunting. The authors face the challenge of changing a mindset; of over­coming four decades of tradition, literally tens of millions of episodes of implemen­tation, and competing recommendations from the marketing departments of every

Preface to the First Edition

Preface to the First Editionxii

pharmaceutical company with a horse in the race. Change is painful but necessary, and progress in parasite control will be measured one practitioner and one horse owner at a time. As Darwin famously observed, “It is not the strongest of the spe­cies that survives, nor the most intelligent that survives. It is the one that is the most adaptable to change.” The worms have been changing since the dawn of effective anthelmintic therapy; now it’s our turn.

We have not included an exhaustive col­lection of references in this book, because busy practitioners have neither the time nor the means to delve deeper into rele­vant literature. In addition, we readily acknowledge the irony that many of our “evidence‐based” recommendations have minimal scientific support at present.

So  until more definitive proof is pub­lished, some practices clearly represent “stop digging” advice. (This term is derived from the adage that when you find yourself in a hole, the first thing to do is stop digging.) It is often a greater manage­ment challenge to convince people to stop doing the wrong thing than it is for them to adopt correct measures.

Our primary goal is to teach, and we believe that training in EBPC is best done by vet‐side mentors. Accordingly, we beg the reader’s indulgence whenever our tone becomes informal or even casual. This merely reflects our teaching styles.

Martin K. NielsenOctober, 2012 Craig R. Reinemeyer

xiii

“Parasite control is confusing.” “There are so many opinions out there.” “What’s wrong with continuing to follow our his­torical practices?” Statements like these are commonly made by people who reach out to us with questions about this topic. While we understand these frustrations, they are really unnecessary and they are the main reasons for writing this book, which now emerges in its Second Edition. Equine parasitology is a very small research field with a limited number of scientists involved across the world. One would not expect a lot of new information to be developed in just a handful of years. Nonetheless, a substantial amount of new knowledge has been generated and rele­vant technology has emerged since the First Edition of this book was published in 2013. Thus, we found it timely to update the contents and publish a Second Edition.

It has been our ambition from the very beginning to make this a practical book, written in straightforward language, and we have attempted to retain this style in the Second Edition. The case scenarios near the end of the book serve as a testa­ment to this ambition. Having said that, we realize that the text may appear some­what academic to some, and we make extensive use of scientific‐style references throughout. Although the majority of readers are unlikely to look up references and read scientific papers, we know from experience with the First Edition that a proportion will do this. Therefore, we

have expanded the reference lists with papers published within the last five years.  Veterinarians who are members of  American Association of Equine Practitioners (AAEP) or British Equine Veterinary Association (BEVA) will notice that the authors have published several review papers in the journal Equine Veterinary Education, which is distributed to the membership of both associa­tions. Thus, there is direct access to more in‐depth information there. We consider the citation of published references as a healthy and objective exercise, which helps us to avoid making unsupported and sometimes misleading assumptions. In a world where any kind of information can be disseminated globally in a matter of seconds, we believe that basing recom­mendations on credible and peer‐reviewed evidence is the only responsible approach for a publication such as this. Veterinary textbooks and the scientific lit­erature are full of examples of statements that are repeated through generations. In the end, no one remembers where the statement originated or why a specific practice was initiated. When the litera­ture is searched meticulously, it is often found that a statement has been miscon­strued or that it was never based on objec­tive data to begin with. Along those lines, revisiting the literature helped us to iden­tify some misleading and even erroneous content that appeared in the First Edition. Yes, we are also guilty of making unsubstantiated assumptions.

Preface to the Second Edition

xiv Preface to the Second Edition

While we have not experienced the launch of a new anthelmintic class for equines since the First Edition was published, we have enjoyed remarkable advances on the diagnostic frontier. As a result, the diagnostic chapter (Chapter 9) has grown more than any other portion of this book. A parasitologist cannot imagine a world without our beloved fecal egg counts, and despite their old school nature, we can conclude that they are here to stay. In fact, they remain the foundation of good evidence‐based parasite control. The diagnostic chapter contains an expanded discussion of interpretation of fecal egg counts, with special emphasis on accuracy and preci­sion. Furthermore, this edition has devoted an entire chapter to anthel­mintic resistance. We continue to see more  and more resistance across the world, and this chapter features two sets  of heat maps summarizing all reported findings of anthelmintic resist­ance in  cyathostomin and Parascaris spp. parasites.

Some exciting developments have evolved since 2013. One of these is the use of computer modeling to predict the dynamics of equine parasite infections and  anthelmintic resistance development. These tools allow us to investigate the principles of these complicated biological phenomena without the  need to involve

live animals in tedious, expensive, and frequently inconclusive research. This book also includes contributions from two leading scientists in the field of computer modeling: Dr. Dave Leathwick and Dr. Christian Sauermann from AgResearch, New Zealand. They have generously pro­vided model simulation outputs which illustrate important biological principles in equine parasitology.

Other unique features in this Second Edition include the addition of new clini­cal case scenarios near the end of the book. These are all based on actual cases that we have encountered through the years. The book also features a glossary of technical and scientific terms that appear in the book. Hopefully, this glossary will increase the understanding of readers who are not veterinarians or parasitolo­gists. Finally, a large number of new images have been added.

We realize that we just represent another opinion about parasitology; we might even be adding to the confusion about these top­ics. Nonetheless, our ambition is the exact opposite, and our opinions at least are based on the best possible evidence availa­ble at this time. Undoubtedly, we will need to revise some of the content again in a few years. Until then, enjoy.

Martin K. Nielsen June, 2018 Craig R. Reinemeyer

xv

We are deeply grateful to fellow scientists, veterinarians, horse owners, and farm man-agers from all over the world for asking us challenging questions about equine parasite control. They serve as an invaluable source of inspiration for this book. Sincere thanks to our friends, colleagues, and collaborators in  New Zealand, Drs Dave Leathwick and Christian Sauermann, for their insightful contributions to several chapters. We warmly acknowledge Dr. Tetiana Kuzmina,

Dr. Stine Jacobsen, Dr. Paul Slusarewicz, Dr. Alan Loynachan, Ms. Shaila Sigsgaard, Ms. Holli Gravatte, Mr. Jamie Norris, Ms.  Maci Stephens, Ms. Faith Miller, Ms. Jennifer Bellaw, Ms. Maria Rhod, and Ms. Tina Roust for providing high quality photo-graphs. Last, but not least, we are deeply indebted to Mr. Jamie Norris, a scientific illustrator in the making, for preparing beautiful life cycle figures and for his tireless help with digitally optimizing image quality.

Acknowledgements

1

Section I

Internal Parasites and Factors Affecting Their Transmission

3

Handbook of Equine Parasite Control, Second Edition. Martin K. Nielsen and Craig R. Reinemeyer. © 2018 John Wiley & Sons, Inc. Published 2018 by John Wiley & Sons, Inc.

Life cycles are the road maps that guide parasites to their ultimate goal – propagating a subsequent generation. Some parasites follow a single, direct path to grandma’s house, while yet others may travel by con­voluted routes, sojourn for protracted peri­ods at some wayside convenience, or even pick up a passenger or two. These differ­ences represent alternate strategies for coping with the vagaries of the environ­ment and of their eventual hosts.

A thorough knowledge of life cycles is not emphasized merely to torment veterinary students. Rather, life cycle details reveal opportunities to control parasites through chemical or management interventions, to exploit unfavorable environmental condi­tions, or to promote natural enemies that might act as agents of biological control. Taking advantage of these potential control opportunities will be emphasized in indi­vidual chapters in this volume.

At the root of all life cycles is a funda­mental principle that distinguishes hel­minth parasites from other infectious agents such as viruses, bacteria, fungi, and protozoa. Through various types of clonal expansion, the latter can all amplify their numbers within a host animal. Literally millions of individual organisms may arise from infective burdens that are orders of magnitude smaller. The reproductive products of nearly all helminths, however, are required to leave the host and undergo essential change in a different location. Defecation is the most common means by

which reproductive products exit the host, but a notable exception includes immature parasitic stages that are ingested by blood‐sucking arthropods (e.g., Onchocerca, Setaria). Most parasitic products can become infective in the environment, whereas others require intermediate hosts or vectors. Regardless, all of these essential transformations occur “outside the defini­tive host”. Indeed, dramatic biological change is mandatory before a parasitic organism is capable of infecting a new host animal or of reinfecting the original host.

Compared to those organisms that amplify their numbers through clonal expansion, helminth disease is a numbers game. Simply put, as the number of invad­ing parasites increases, greater tissue damage or nutrient loss results, and the range and severity of clinical signs become more extensive.

In this chapter, we propose to describe the basic life cycles of the major helminth parasites of equids. Specific control opportunities may be mentioned in this overview, but these will be discussed more fully elsewhere in the volume.

Nematodes

Superfamily Strongyloidea

The members of the Strongyloidea (“strongyles”) are moderately sized, stout worms with substantial buccal capsules.

1

Biology and Life Cycles of Equine Parasites

Internal Parasites and Factors Affecting Their Transmission4

The males have a copulatory bursa at the  posterior end and females of all spe­cies produce eggs that are similar in appear­ance. Eggs of small strongyles cannot be differentiated microscopically from those of large strongyles, and the only practi­cal method of differentiation (other than

molecular approaches) is through coproc­ulture. The strongyloids of horses all have direct life cycles; intermediate or paratenic hosts are never used (Figure 1.1).

Strongyloid eggs pass in feces and hatch in favorable environmental condi­tions of moisture, temperature, and

L4 Adult

L2 L1

Morula egg

L3, infective stageEmbroyonated egg

Figure 1.1 Strongyle life cycle. The life cycle of strongyle parasites. Parasitic stages can be seen above the horse and preparasitic stages below it. Fertilized eggs are shed by adult females in the cecum and colon, and excreted to the environment in the feces. Here, the eggs hatch and a first‐stage larva (L1) emerges. The L1 then molts to L2 in the feces. Another molt gives rise to the L3, which retains its L2 cuticle and thus has a double‐layered sheath. The L3 leaves the fecal pat and migrates on to forage, where it is ingested by a horse. Inside the horse, the L3 exsheathes and invades the mucosa of the large intestine. Large strongyles (Strongylus spp.) undergo extensive migration in various organs of the horse, while cyathostomins encyst in the mucosal lining of the large intestine. After returning to the large intestinal lumen, the worms reach sexual maturity and start shedding eggs.

Biology and Life Cycles of Equine Parasites 5

oxygenation. All species exhibit three sequential larval stages, first (L1), second (L2), and third (L3). The L1 and L2 stages feed on organic material in the environ­ment, but the third stage develops within the sheath of the L2. This protective cover­ing helps L3s to resistant environmental conditions, but it has no oral opening, so third stage larvae are unable to ingest nutrients. The L3 is the infective stage for all strongyloid nematodes of equids. Infection invariably occurs through inadvertent ingestion, whether while grazing or via oral contact with elements of the environment.

Apparently, horses never develop abso­lute immunity to strongyloids, so these are often the sole nematode parasites recovered from well‐managed, mature equids. The Strongyloidea of horses are comprised of two distinct subfamilies, the Strongylinae and the Cyathostominae.

Strongylinae (large strongyles)Members of the subclass Strongylinae tend to be larger, on average, than most genera that comprise the Cyathostominae. In addition, Strongylinae have large buc­cal capsules, adapted for attachment to, and even ingestion of, the gut mucosa. The larval stages of at least one strongylin genus undergo extensive, albeit stereo­typic, migration within the host prior to returning to the gut to mature and begin reproduction.

Strongylus vulgarisStrongylus vulgaris is widely acknowl­edged as the single most pathogenic nem­atode parasite of horses. Adult worms measure about 1.5–2.5 cm in length and the females are larger than the males. Adults are usually found attached to the mucosa of the cecum and the ventral colon (Figure  1.2). After ingestion from the environment, third stage larvae invade the mucosa of the distal small intestine, cecum, and colon. Here, they molt to the fourth stage (L4) before penetrating local

arterioles and migrating proximally beneath the intimal layer of local blood vessels. Migrating S. vulgaris L4s leave subintimal tracts in their wake and con­gregate near the root of the cranial mes­enteric artery. A portion of the infecting larvae may continue to migrate, even to the root of the aorta near the left ventricle. Migrating L4s have been found in numer­ous vessels arising from the aorta, includ­ing the celiac artery, the renal arteries, and external and internal iliac arteries. The pathologic characteristics and conse­quences of these arterial lesions will be discussed in Chapter 2.

Larvae reach the cranial mesenteric artery about two weeks post‐infection. Here, they reside for about four months before returning to the large intestine. The final molt to the L5 stage occurs about 90 days after infection, while larvae are still present in the artery. These L5s (essen­tially young adults) characteristically retain their L4 cuticle and thus appear with a double‐layered cuticle just like the infective L3 (Figure  1.3). Beginning approximately 120 days after infection, young adults migrate within the blood stream to the large intestine, where they are found within pea‐sized nodules in the

Figure 1.2 Adult Strongylus vulgaris attached to the cecal mucosa. (Source: Photograph courtesy of Dr. Tetiana Kuzmina).

Internal Parasites and Factors Affecting Their Transmission6

submucosa of the ventral colon and cecum. Adult worms eventually emerge from these nodules and mature in the intestinal lumen for an additional 6 weeks. Females begin to lay eggs from 5.5 to 7 months after infection (Ogbourne and Duncan, 1985).

Strongylus edentatusStrongylus edentatus is a larger worm than S.  vulgaris, measuring about 2.5–4.5 cm in length, and apparently is also more prevalent. Adults are usually attached to the mucosa of the base of the cecum and the proximal ventral colon. The larvae undergo a complex and fasci­nating migratory route. Following inges­tion of infective L3 stages from the environment, larvae are carried by the portal system to the liver, where they molt to the fourth stage. Following migra­tion within the parenchyma, larvae leave the liver via the hepatorenal ligament and  migrate beneath the peritoneum to

various locations in the flanks and ven­tral abdominal wall (hence, the common term, “flank worm”). Larvae are also commonly found in the perirenal fat. The majority of larvae are found on the right side of the body (i.e., in the right ventral abdominal wall and around the right kid­ney), probably because the hepatorenal ligament attaches on the right side of the ventral midline (see Chapter 2).

The final molt to the fifth stage occurs within retroperitoneal nodules about four months post‐infection. Young adults migrate back to the large intestinal walls (primarily the ventral colon), where puru­lent nodules form and eventually rupture to release adult worms into the lumen. Altogether, this extensive migration results in a prepatent period of up to one year (McCraw and Slocombe, 1978).

Strongylus equinusStrongylus equinus is another large strongyle with a prolonged life cycle and a prepatent period of 8–9 months from infection to egg production. The adult worms are of about the same size as S. edentatus. Larvae molt to the L4 stage upon invading the mucosa of the  cae­cum and colon. They then migrate across the abdominal cavity and through the pancreas to finally reach the liver, where they wander for several weeks. On the way back to the large intestine, larvae again migrate through the pan­creas and large L4s and L5s can be found free in the peritoneal cavity (McCraw and Slocombe, 1984). The third stage larvae of S. equinus are very distinctive in coproculture. This nematode species has become exceedingly rare in domestic herds and is not detected in  managed and regularly dewormed horses. S. equi­nus can be highly prevalent and abun­dant in feral horses, however, and has been reported in prevalence surveys of working equids in South America (Kyvsgaard et al., 2011).

Figure 1.3 Strongylus vulgaris L5 pre‐adult collected from the cranial mesenteric artery. Note that this specimen characteristically has retained its L4 cuticle.

Biology and Life Cycles of Equine Parasites 7

Strongylus asiniStrongylus asini is a common internal par­asite of zebras and donkeys in Africa. It resembles S. vulgaris in many ways but genetically is more closely related to S. edentatus and S.  equinus (Hung et  al., 1996). Adults occur in the cecum and colon, but larvae are found attached to the lining of hepatic and portal veins (Malan et  al., 1982). Fourth stage larvae migrate within the liver and hepatic cysts are reportedly found in zebras.

Triodontophorus spp.Although they are technically “large stron­gyles”, the several species of Triodontophorus are non‐migratory. The larvae encyst within the lining of the large intestine and eventu­ally emerge to become adults. The prepatent period is thought to be approximately 2–3 months (Round, 1969). Triodontophorus brevicauda and T. serratus are probably the most prevalent species of large strongyles in managed horses, presumably because of a shorter life cycle than Strongylus species. One study of naturally infected horses found that the presence of Triodontophorus larvae  in coproculture was independent of  the presence of Strongylus spp. (Cao, Vidyashankar, and Nielsen, 2013). This find­ing was attributed to a shorter life cycle, which is more similar in duration to that of cyathostomins.

Triodontophorus females apparently pro­duce eggs that are significantly larger than those of the other strongylin and cyathos­tomin genera (Figure 1.4).

Other strongylinaeCraterostomum acuticaudatum, Oesophagodontus robustus, and Bidentostomum ivaschkiniThese species have non‐migratory life cycles and are only classified as Strongylinae on the basis of their large buccal capsules (see Table 1.1). The larvae derived by coproculture can be differenti­ated, but as the species prevalences are so

Figure 1.4 Most strongyle eggs are relatively uniform in size and shape. One exception is the eggs of Triodontophorus spp. (right), which are about twice the size of a typical strongyle egg. (Source: Photograph courtesy of Tina Roust and Maria Rhod).

Table 1.1 Examples of predilection sites of common cyathostomin species. Information from Tolliver (2000).

Cecum

Coronocyclus coronatusCyathostomum alveatumCylicocyclus elongatusCylicostephanus calicatusPetrovinema poculatum

Ventral colon

Coronocyclus labiatus, Cor. labratus,Cyathostomum catinatum, Cya. pateratum (also dorsal colon), Cya. tetracanthum,Cylicocyclus auriculatus, Cyc. brevicapsulatus, Cyc. radiatus, Cyc. leptostomum Cyc. nassatus, Cyc. ashworthi, Cyc. ultrajectinus (also dorsal colon)Cylicodontophorus bicoronatusCylicostephanus asymetricus, Cys. minutus

Dorsal colon

Cyathostomum pateratum (also ventral colon)Cylicocyclus insigne, Cyc. ultrajectinus (also ventral colon)Cylicostephanus goldi, Cys. longibursatusParapoteriostomum euproctus, Par. mettamiPoteriostomum imparidentum, Pot. ratzii