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

By Andrew B Forbes

Understanding parasite biology and impact is essential when giving advice on parasite control in farm animals. In the first review devoted to parasites of domestic cattle and sheep alone, this book provides in-depth, focused advice which can be tailored to individual farms. It considers the impact of parasites, both as individual species and as co-infections, as well as epidemiological information, monitoring, and diagnostic procedures. Supported throughout by diagrams and photos to aid diagnosis, it also reviews the basis for control measures such as the responsible use of parasiticides, adaptive animal husbandry and other management practices.

This book:
Focuses on common parasites of domestic sheep and cattle;
Places emphasis on understanding host responses and epidemiology so that the impact and seasonality of parasitism can be incorporated into advice and decision making;
Highlights the fundamental importance of the individual farm and farmer in assessing endemic parasitism and tailoring control options accordingly;
Provides a comprehensive reference listing, including important historical citations, to underpin the content.

An important resource for students, veterinarians and researchers of farm animal health, this book maintains a focus on ruminant parasitology in order to deliver evidence-based advice and also context for the application of basic research.

• Language: English
• Publisher: CAB International
• Release date: Nov 17, 2020
• ISBN: 9781789245172

Andrew B Forbes

Andrew B Forbes - Royal (Dick) School of Veterinary Studies, University of Edinburgh, Scotland, 1971 BVM&S., Royal College of Veterinary Surgeons, UK, 1971 MRCVS. Certified Biologist, Member of the Royal Society of Biology, 2001 - CBiol.,MRSB. Foundation Diplomate of the European Veterinary Parasitology College, 2003 - DipEVPC. Doctor of Philosophy, University of Ghent, Belgium, 2008 - Ph.D. Past President of British Cattle Veterinary Association (BCVA) and British Association of Veterinary Parasitology (BAVP). Seven years general veterinary practice in Scotland, southern Africa and New Zealand. Thirty five years in Animal Health Industry in technical and research roles at national, European and global levels, predominantly focused on ruminant parasitology. Currently Honorary Professor, School of Veterinary Medicine, Glasgow University, involved with parasitology teaching and various related research projects. Independent Veterinary Parasitologist; mentor to post-graduate students at the universities of Dublin, Glasgow and Belfast; regular CPD provider to BCVA and ad hoc to other organisations. (Co-) author of over 65 papers on ruminant parasitology in peer-reviewed journals, including several, recent practitioner-oriented reviews in Livestock. I live on a small, 6 hectare, grass farm where we have kept sheep for ~20 years, so I also have a farmer's perspective on keeping livestock and controlling parasites.

Book preview

1The Origin and Evolution of Parasitism in Domestic Ruminants

Introduction

Parasitism is one of the most successful lifestyles in nature (Poulin and Morand, 2000) and, although it is impossible to know precisely how many parasite species exist (Poulin, 2014; Strona and Fattorini, 2014), it has been estimated that parasitic species considerably outnumber all the free-living species on Earth (Windsor, 1998). There are at least 50% more parasitic helminth species than vertebrate hosts, and among mammals, each individual animal can harbour two cestode, two trematode and four nematode species of parasite over its lifetime (Dobson et al., 2008).

There are several definitions of parasitism, all of which describe an association between one organism (the parasite) and another (the host) in which the parasite derives some benefits, whereas the host gains no advantage and may be harmed. Although there are a few parasites that can switch to a 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 helminths, comprising nematodes (roundworms), trematodes (flatworms) and cestodes (tapeworms); most ectoparasites are arthropods, either insects or arachnids. Strictly speaking, protozoa originally meant early (eukaryotic) life forms; however, in parasitology the word has become synonymous with 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 precise timing of events will inevitably change somewhat as new discoveries are made and new methodologies adopted.

Additional sources of useful information on parasites that transit the gastrointestinal (GI) tract are coprolites, which are fossilized dung and which can contain remnants of parasite eggs. Currently, the earliest fossil evidence for intestinal parasitism in vertebrates stretches back to the Triassic period 240 million years ago (MYA) when ascarid eggs were found in dinosaur coprolites (Poinar, 2015). Younger specimens of dinosaur coprolites from the Cretaceous period (130 MYA) yielded not only nematode eggs and protozoal remains but also trematode eggs, representing an early record of parasitic flatworms (Poinar and Boucot, 2006).

Fossil evidence points to the evolution of both chewing and sucking lice somewhat later than the helminths, probably around 77 MYA, coincident with the initial radiation of mammals (Johnson and Clayton, 2003; Light et al., 2010), though lice also parasitize birds, which diversified earlier. Free-living oribatid mites, which are the intermediate hosts for several species of tapeworms, for example Moniezia spp., have been found in fossils nearly 400 MYA (Arillo et al., 2012), but the obligate parasitic mites of vertebrates have a more recent history with fossil remains found in the Eocene period, ~50 MYA (Walter and Proctor, 2013).

Because of their chitinous exoskeletons, arthropods are preserved as fossils more readily than helminths and protozoa, while another rich source of insect and arachnid remains is amber (Nagler and Haug, 2015), which was formed from plant resins deposited from ~320 MYA. Amber with remains of arthropods currently dates from ~125 MYA, at which time parasitism among invertebrates is evident, for example, a fly parasitized by a Leptus spp. mite (Arillo et al., 2018). Some remarkably 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 evolutionary history of parasitic organisms, it is clear that by the end of the Cretaceous period and the mass extinction that followed ~65 MYA, predecessors of all the main classes of parasite were present in the world’s fauna. Potential intermediate hosts, such as snails, had also evolved from around 400 MYA onwards (Wanninger and Wollesen, 2019). By this time, other important links in the terrestrial food chain were also present, for example, dung beetles (Chin and Gill, 1996) and remnants of grass were found in coprolites from herbivorous dinosaurs in the late Cretaceous period, suggesting the possibility of early grazing mammals at that time (Prasad et al., 2005). Table 1.1 provides approximate evolutionary temporal relationships among the components that eventually led to parasitism in domestic ruminants (Dawkins, 2004; Lloyd, 2009).

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

The Ruminants

Following the Cretaceous extinctions of multiple species, notably the dinosaurs, and also many invertebrate and plant species (Macleod, 2013), the scene was set for the extensive radiation of flowering plants and mammals from their initial appearance ~200 MYA. The first ungulates (herbivorous, hoofed mammals) to make their presence felt were the perissodactyls (odd-toed ungulates, such as horses, rhinos and tapirs), species of which proliferated from ~55 MYA (Janis, 1976). The artiodactyls (even-toed ungulates, such as camels, pigs, hippos, deer, antelopes, sheep and cattle) evolved later; evidence of the earliest ruminants dates from ~40 MYA and from the late Miocene onwards (~10 MYA), the artiodactyls assumed numerical dominance over the perissodactyls (Janis, 1976).

A characteristic of these herbivores, which is well represented in the fossil record, is the presence of hypsodont teeth; these are large, high-crowned molars with hard enamel ridges that have evolved to grind down plant cell walls to release their contents and to reduce particle size to facilitate bacterial colonization and digestion in the alimentary tract (Janis and Fortelius, 1988). Hypsodont teeth are particularly important in grazing animals as many grass species have a high silicon content, which makes them particularly abrasive. In ruminants, these teeth are central to the efficiency of digestion when fibrous material is regurgitated, re-chewed, crushed and ground and then re-swallowed in the process known as rumination (Hofmann, 1989).

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

•Grazers, feeding predominantly on grass

•Browsers feeding on forbs, leaves and twigs and fruit

•Intermediate feeders, which are opportunist grazers or browsers

Fig. 1.1. Ruminant diversity: wildebeest and springbok.

Domestic cattle and sheep are grazers, while goats are intermediate feeders and their digestive systems are adapted to handle their feed. There are a number of challenges for ruminants living on a plant-based diet, which differ according to their chemical composition. For example:

•Grass and roughages are high in fibre, which has to be broken down by the rumen microflora and fauna, not only in order to digest the cellulose itself but in so doing to release soluble intracellular carbohydrates, proteins and other nutrients. Chewing the cud is required to reduce the particle size of plant material and increase its surface area so that the rumen microorganisms can access the substrate more efficiently.

•Browsers tend to eat young leaves and fruit, which are more easily digestible, particularly the latter, and therefore the breakdown of cellulose is less critical. However, many plants have chemical defences, such as tannins, to deter herbivorous insects and mammals and these phenolic 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).

Table 1.2. Comparative features of the digestive system of grazing and browsing ruminants.

Irrespective of their feeding strategy, ruminants have evolved to utilize plant material, including fibre, in a biologically efficient way that supports their requirements for maintenance, growth, mobility, reproduction and immune responses (Van Soest, 1994). Pivotal to this is the reticulorumen, which is a fermentation chamber hosting an array of microorganisms, including bacteria and ciliated protozoa (Oxford, 1955; Wolin, 1981), which can break down cellulose – a task that is beyond mammalian enzymes. Among the end products of microbial digestion in the rumen are volatile fatty acids (VFAs), notably acetic, butyric and propionic, which are absorbed through the rumen wall, facilitated by its large surface area, augmented by numerous papillae. Following metabolism, these VFAs are utilized as energy sources, for gluconeogenesis and lipid synthesis (Wolin, 1981).

The omasum appears to have a role in further absorption of VFAs, re-absorbing fluid and in regulating the outflow of digesta from the reticulorumen to the abomasum, in particular undigested, coarse fibrous material (Ehrlich et al., 2019). The digesta entering the abomasum comprises a sludge that includes rumen liquor, digested plant remains, undegraded dietary protein contents and bacteria. Rumen bacteria provide an important source of microbial protein for the host, and the enzyme profile of the ruminant abomasum reflects an important adaptation to this function through the presence of lysozymes (Jolles et al., 1984). Lysozymes have antibacterial properties, based on their ability to destroy cell walls of Gram-positive bacteria, which is the basis for their more common role in mammals as a defence mechanism against bacterial pathogens in other tissues (Dobson et al., 1984). Lysozymes are found in high concentrations in the fundic zone of the abomasal mucosa, where the digesta contents have a pH of ~6.5, at which lysozymes actively lyse bacteria; towards the pyloric zone of the abomasum, the hydrochloric acid (HCl) secretions from the gastric glands render the stomach contents acidic, with a pH that can fall to ~1.5. A low pH is required for the precursor pepsinogen to be converted into the proteolytic enzyme pepsin, which initiates protein digestion in the abomasum; however, bovine lysozyme is highly resistant to deactivation by pepsin (Dobson et al., 1984).

Grass and Grazing

Although there is evidence as long as 85 MYA, it was not until geological and climatic changes shaped the environment to favour grasses over forests that grasses came to assume a dominant position in the Earth’s vegetation types (Gibson, 2009). Grassland can now be found in agricultural settings and also in (semi-) natural habitats such as steppes, savannahs, prairies and pampas in various parts of the world. The spread and diversification of grasses coincided with climatic changes from around 30 MYA that resulted in greater aridity and some of the characteristics of grasses developed at this time as adaptations to grazing animals. For example, having the growing points at the base of the leaves at ground level allowed grasses to quickly regenerate and recover from grazing.

Ungulates diversified and coevolved, adapting to the changes in vegetation and the expansion of grasslands, the patterns differing somewhat over time and among ecosystems (Stebbins, 1981; Strömberg, 2011). Furthermore, there was a progressive change in the proportion of browsers compared with grazers as the dominant vegetation types evolved (Janis et al., 2000). Ruminant grazers tend to be more gregarious than browsers and hence are commonly found in groups that forage collectively throughout their territories (Estes, 1991).

Parasitism and Ruminant Grazers

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

The longevity of host–parasite relationships in grazing ruminants has been explored in gastrointestinal (GI) nematodes (GINs) of the family Trichostrongylidae, including the subfamilies Ostertagiinae and Haemonchinae (Hoberg and Lichtenfels, 1994). Taken in conjunction with the radiation of ruminants in the family Bovidae, which includes cattle, sheep and goats, from around 20 MYA and the evolution of nematode species from these subfamilies, it has been concluded that the bovids and their Ostertagia-like parasites have coevolved for 10–20 million years (Stear et al., 2011).

The gregarious nature of grazing ruminants may also have implications for ectoparasite infestations. Although some species of ticks, e.g. Rhipicephalus (Boophilus) microplus, remain on the same host for all the parasitic phases of the life cycle, many other species, e.g. Ixodes ricinus, only feed intermittently for a few days at each of the larval, nymph and adult stages, and for the rest of their lives, they live and develop in the vegetation. These parasites therefore are also reliant on their hosts returning to the sites where they dropped off the animal after a blood meal and re-locating potential ruminant hosts, a process that can be facilitated by the grazing behaviour of herds or flocks of mammals. Similar scenarios could apply to species of pest flies that lay their eggs off the host, but for obligate ectoparasites such as mange mites and lice, the close proximity of hosts within groups can facilitate spread through close contact.

Parasites in Wild and Feral Ruminants

Prior to the domestication of cattle, sheep, goats and buffalo, parasitism evolved in wild ruminants and other wildlife over millions of years, where they played an important role in ecology and population dynamics. Research into wildlife parasitism has shown many similarities and parallels with domestic animals; for example, a series of studies in wild African buffalo and other African bovids has shown the following:

•Nutritional status can influence the epidemiology and impact of GI nematodes ( Ezenwa, 2004b )

•Interactions between GI nematodes and bovine tuberculosis (BTb) ( Ezenwa et al ., 2010 )

•Reduction in mortality of buffalo from BTb following anthelmintic treatment ( Ezenwa and Jolles, 2015 )

•The importance of host behaviour in the epidemiology of parasitism ( Hawley et al ., 2011 )

•Anthelmintic treatment leads to increased daily foraging time in Grant’s gazelle ( Worsley-Tonks and Ezenwa, 2015 )

Additional examples of the impact of parasites in wild, feral and semi-domesticated ruminants in Europe include:

•Reduced body condition in red deer associated with low-level worm burdens ( Irvine et al ., 2006 )

•Increased mortality in Soay sheep on Hirta, the largest island in the St Kilda archipelago, associated with GIN, most marked during periods of malnutrition ( Gulland, 1992 )

•Depression of feed intake in reindeer with GIN infections ( Arneberg et al ., 1996 )

•Reduced fecundity in reindeer associated with abomasal parasite burdens ( Albon et al ., 2002 )

Domestication of Cattle and Sheep

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

The natural vegetation in this region at the time of domestication was oak/pistachio parkland, so it is likely that early domestic cattle and sheep combined grazing with some browsing and, though livestock are now commonly kept in fields with limited opportunities to browse, both cattle and sheep will readily browse on hedgerows and trees, and in some parts of Europe, cut branches are an important part of their diet, particularly over winter. There is renewed interest in silvopasture systems as a means to optimize land use from both productivity and environmental perspectives (Gabriel, 2018).

Controlled selection of cattle and sheep for various traits and their subsequent division into breeds and types is a relatively recent phenomenon, dating back only a few hundred years (Fig. 1.2). The objectives of selective breeding of ruminants were primarily focused on traits such as appearance, meat, milk and wool production, traction power and hardiness, all within a background of amenable behaviour in their interactions with man (Price, 1999; Mignon-Grasteau et al., 2005). Selection for resistance to parasites or resilience in the face of parasite challenge would have been incidental to the main breeding objectives and may have even been counterselected (Raberg et al., 2009). However, particularly in sheep, breeding programmes for resistance or resilience to parasitic gastroenteritis have been in place for several decades (Bisset and Morris, 1996; Morris et al., 1997) and there is growing interest in this practice as a means to help control parasites without dependence on parasiticides (Bisset et al., 2001; Stear et al., 2007).

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

Closing Remarks

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

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2Parasitic Gastroenteritis in Cattle

Introduction

More than 15 species of nematode that inhabit the gastrointestinal tract of cattle have been described (Rose, 1968; Taylor et al., 2007); however, in temperate farming regions, parasitic gastroenteritis (PGE) is predominantly associated with only two species:

•Ostertagia ostertagi in the abomasum

•Cooperia oncophora in the small intestine

Other species that occasionally can contribute to bovine PGE are Trichostrongylus axei and Nematodirus spp. In tropical and subtropical regions, Haemonchus spp. are the most common of the abomasal species and some other genera; for example Oesophagostomum spp. can assume greater importance. A characteristic of gastrointestinal nematodes in both cattle and sheep is that most species are host-specific and this opens up possibilities of grazing practices such as mixed or sequential grazing of cattle and sheep in order to reduce pasture larval populations. Notable exceptions to this general rule are T. axei, which can parasitize a variety of ungulates, including horses and pigs, and Nematodirus and Haemonchus spp.

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

Parasitic Gastritis, Ostertagiosis

O. ostertagi infections are acquired while grazing, when infective larvae, which are commonly present on the leaves of herbage, are ingested. Infective larvae exsheath in the rumen, a process that is stimulated by low pH, temperature and bicarbonate concentration (Hertzberg et al., 2002) and which occurs more quickly in grass-based diets (2 h), compared with those with a high proportion of grain (6 h) (DeRosa et al., 2005). The exsheathed third stage larvae, ~0.7 mm in length (Rose, 1969), pass into the abomasum where they enter the gastric glands within 2 days and moult to fourth stage larvae, which can be found from ~4 days onwards, when they measure ~1.1 mm; the majority of worms emerge from the glands into the abomasal lumen from day 16 onwards as fifth stage larvae or adults (Ritchie et al., 1966). Adult male O. ostertagi are on average 6.9 mm long, while females are 9.7 mm (Rose, 1969). Following copulation (Fig. 2.1), gravid females can be identified from day 16 onwards and most are laying eggs by 21 days post-infection, giving a typical pre-patent period of ~21 days (Ritchie et al., 1966; Rose, 1969). Male worms comprise ~45% of the adult population in the abomasum, females ~55% and the average fecundity per female is 284 eggs per day (Verschave et al., 2014a). Egg production is subject to density-dependent influences such that fecundity typically declines with increasing worm populations, resulting in a stereotypical pattern of egg output, irrespective of the size of the (female) worm burden; this is observed following experimental (Ross, 1963; Anderson et al., 1967; Michel, 1967, 1969c, 1969d) and natural infections (Michel, 1969b; Brunsdon, 1971).

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

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). Under experimental conditions, following a single infection, it can take 50–90 days for the abomasal mucosa to return to its normal appearance (Osborne et al., 1960; Ritchie et al., 1966), so lesions seen at necropsy may reflect the worm population over the previous 2–3 months. The abomasal lesions are essentially pathognomonic for nematode infections and are useful not only in diagnostic post-mortems but also for abattoir surveys, where abomasa can be examined in the ‘gut room’ without significant disruption to the line. Results of such surveys have shown that lesions of ostertagiosis are common in mature and adult cattle, being present in the great majority of animals, with 38–60% having in excess of 100 lesions (Larraillet et al., 2012; Bellet et al., 2016). The presence of significant pathological changes in mature cattle illustrates the fact that acquired immunity to O. ostertagi is incomplete and this in turn not only provides an explanation for the role that adult cattle can play in the epidemiology of ostertagiosis (Stromberg and Averbeck, 1999) but also may explain why adult cattle, as well as young stock, can experience production losses from parasitic gastritis (Stromberg and Corwin, 1993; Taylor et al., 1995; Charlier et al., 2009).

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

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

Clinical features of ostertagiosis type I

Following monospecific induced infections, clinical signs, including anorexia, diarrhoea and weight loss, typically occur from day 19 onwards, coincident with extensive damage to the abomasal mucosa and the establishment of adult worm populations. This disease is called ostertagiosis type I and is the typical presentation in FGS calves that have not been in an effective control programme (Armour, 1970), though it can also be seen in yearlings (Fig. 2.4) and adult cattle (Orpin, 1994).

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.

Hypobiosis

Infective larvae that are ingested towards the end of the grazing season are predisposed to undergo a period of hypobiosis in the gastric glands, thus greatly extending the pre-patent period. The stimulus for hypobiosis appears to be chilling (4°C) of the infective larvae on pasture in autumn as the ambient temperature declines (Armour and Bruce, 1974). The duration of inhibition is typically 16–18 weeks (Armour and Bruce, 1974), after which the larvae resume development and become adult worms. The precise mechanism for resumption of development is not known, but there is some evidence that small numbers of inhibited larvae resume development over the winter (Michel et al., 1976a; Smith, 1979), with a peak in February and March, which is consistent with larvae being ingested over several months prior to housing and having a fixed period of quiescence (Michel et al., 1976b).

The larvae of O. ostertagi inhibit as early fourth stage larvae in the gastric glands within 4 days of ingestion, when they measure ~1.1 mm (Armour and Duncan, 1987); in this state, although parasitized gastric glands can be recognized as 1–2 mm lesions in the abomasal mucosa (Ritchie et al., 1966), histological changes are minimal (Snider et al., 1988), and there is little evidence of parasite-associated alterations in biochemistry or immunobiology (Osborne et al., 1960). This is consistent with data from single infection experiments, which show that developing larvae are at least 16 days old before significant changes in pathophysiology and clinical signs are observed (Jennings et al., 1966; Ritchie et al., 1966). Larval inhibition is present in O. ostertagi populations not only in Europe and North America (Frank et al., 1988) but also in temperate regions of the southern hemisphere (Brunsdon, 1972), where the seasonality of hypobiosis is similar, but the months of the year are obviously different.

The significance of hypobiosis from an epidemiological perspective is that it provides another means of overwinter survival for O. ostertagi, in addition to infective larvae that persist in dung or on pasture to act as a source of infection in spring. From a clinical point of view, mass, simultaneous emergence of adult worms from the gastric glands in late winter can precipitate an acute, potentially fatal, abomasitis in a small proportion of infected animals. An early description of this disease, now known as ostertagiosis type II, appeared in the 1950s (Martin et al., 1957) and this syndrome can occur in heifers (Petrie et al., 1984) and adult cattle too (Wedderburn, 1970; Selman et al., 1976). Ostertagiosis type II is currently relatively uncommon in the UK (Mitchell, 2014) and there is strong circumstantial evidence that routine use of macrocyclic lactones (MLs) as housing treatments for the removal of gastrointestinal nematodes (including inhibited O. ostertagi larvae), lungworm and cryptic populations of lice and mange mites in (young) cattle has reduced the risk of this manifestation of ostertagiosis.

Pathophysiology

Normal gastric glands comprise a number of different types of cells (Banks, 1981), including:

•Mucus-producing neck cells, which may also synthesise and secrete lysozymes

•Parietal (oxyntic) cells that synthesise and secrete hydrochloric acid (HCl)

•Zymogen (chief) cells that synthesise and secrete pepsinogen (and prorennin in young animals)

•Enteroendocrine (enterochromaffin) cells that synthesise and secrete various hormones into the circulation, including gastrin (G cells)

Following invasion of gastric glands by the larvae of O. ostertagi, their subsequent development and emergence over a period of ~21 days and the direct and collateral damage to the gastric mucosa, several functional disorders can be observed. Changes in the concentration of various gastric secretions can contribute to the pathophysiology of ostertagiosis and its impact in infected cattle.

Mucus biosynthesis

Mucus provides a defensive mechanism against pathogens in the gastrointestinal tract (Miller, 1984); in ostertagiosis, changes in mucus synthesis are most marked following emergence of adult parasites from the gastric glands (Rinaldi et al., 2011). The main lesion is of hyperplasia of the mucus cells, accompanied by changes in the composition of the mucins synthesised and secreted; functionally, these responses are thought to play a role in the immune response to and elimination of the parasite (Mihi et al., 2014).

Pepsinogen

In a primary infection, coincident with the emergence of fifth stage larvae from the gastric glands at around 18 days, the pH in the abomasum increases rapidly. This is a consequence of damage to the parietal cells in the gastric glands by the parasite, which results in a reduction in the secretion of HCl. The pH of the normal, uninfected abomasum in calves averages 2.5 (Jennings et al., 1966; Murray, 1970; Stringfellow and Madden, 1979), ~3.5 in lightly infected animals (Ross et al., 1963) and 6.5–8.5 in clinical ostertagiosis; in subclinical ostertagiosis, the values are intermediate between these (Ross and Todd, 1965). At the higher pH values that tend towards neutrality or alkalinity, the abomasal contents contain very low concentrations of pepsin (Ross et al., 1963; Jennings et al., 1966), and this is because conversion of the precursor pepsinogen to pepsin is negligible at pH ~5.0 and above (Piper and Fenton, 1965; Jennings et al., 1966). Though changes in the milieu of the abomasal contents as a result of elevated pH and leakage through disrupted junctions between cells provide one explanation for pepsinogenaemia (Jennings et al., 1966), other mechanisms may be involved, for example direct secretion of pepsinogen from the zymogenic (chief) cells in damaged gastric glands into the circulation (Stringfellow and Madden, 1979; Baker et al., 1993). In addition, direct transplantation of adult O. ostertagi into normal abomasa results in an immediate increase in plasma pepsinogen (PP), in the absence of any abomasal pathology (McKellar et al., 1986). Furthermore, treatment of calves experimentally infected with O. ostertagi results in an immediate ~33% drop in PP, followed by a gradual decline in concentrations over the following 19 days (Hilderson et al., 1991), presumably reflecting the absence of stimuli from the adult worms and some resolution of the gastric gland lesions (Osborne et al., 1960).

Gastrin

Hypergastrinaemia is a feature of ostertagiosis (Fox et al., 1993). Gastrin is secreted by the G cells in the stomach in response to increasing pH in a feedback mechanism to stimulate the parietal cells to synthesise and secrete more HCl in order to restore the pH to its normal value of ~2.5 in the abomasal contents (Fox et al., 2006). The significance of gastrin in the pathogenesis of ostertagiosis is that it can suppress appetite, and a reduction in feed intake is a consistent and important feature of ostertagiosis; indeed, it has been shown that a loss of appetite accounts for 73% of the reduced growth rate that is commonly seen in young cattle (Fox et al., 1989a).

Lysozyme

The optimum pH for ruminant lysozymes is 5.0 (Dobson et al., 1984), so in theory, digestion of ruminal bacteria in the abomasum might be enhanced in ostertagiosis, though no experimental studies have been undertaken to explore this hypothesis. However, populations of both aerobic and anaerobic bacteria in the abomasum have been shown to increase in ostertagiosis in cattle (Jennings et al., 1966) and teladorsagiosis in sheep (Simcock et al., 1999), attributed by these authors to a loss of a bacteriostatic effect of acid in the stomach. Hence any effects of abomasal parasitism on the number and composition of bacterial populations seem to be more likely mediated by elevated pH per se, rather than through optimized lysozyme activity.

Examples of some pathophysiological consequences of ostertagiosis are as follows:

•Increase in abomasal pH ( Purewal et al ., 1997 )

•Increase in plasma pepsinogen ( Fox et al ., 1989b )

•Increase in plasma gastrin ( Fox et al ., 1989b )

•Increase in fundic (+96%) and pyloric (+31%) abomasal mass ( Purewal et al ., 1997 )

•Increase in gastrin mRNA in pyloric mucosa ( Purewal et al ., 1997 )

•Increase in the number of aerobic bacteria in abomasum ( Jennings et al ., 1966 )

•Reduction in nitrogen digestibility ( Fox et al ., 1989b )

•Hypoalbuminaemia ( Fox et al ., 1989b )

Host immune responses

A cellular response in the regional lymph nodes (LNs) associated with the abomasum is evident in induced O. ostertagi infections and this can be detected within 4 days; over the subsequent 28–35 days, LN mass can increase 20–30 times compared to uninfected animals and simultaneously lymphocytes are released into the circulation whence they reach and colonize the abomasal mucosa (Gasbarre, 1997). Parasite-specific lymphocytes in the abomasal LNs are responsible for the generation of immunoglobulins against O. ostertagi; these are mainly of the IgG1 class and appear to be associated with exposure rather than a protective immune response (Claerebout and Vercruysse, 2000). Following induced trickle infections in naïve calves with 5000 infective larvae (L3) per day, antibodies to O. ostertagi can be detected in serum from ~21 days onwards after which they continue to increase steadily; the response appears to be dose-dependent as 500 L3 per day fail to elicit a response (Berghen et al., 1993). These host responses help regulate parasite populations by reducing the size of the worm burden, decreasing the size of adult worms and reducing fecundity in female worms (Klesius, 1988). The sequence of events is typically as follows (Claerebout and Vercruysse, 2000):

•Decrease in fecundity

•Stunting of growth

•Retardation of development

•Expulsion of adult worms

•Limited establishment of infective larvae in gastric glands

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

Under field conditions, an example of the relative pathogenicity of C. oncophora and O. ostertagi was illustrated in a trial in which calves were vaccinated against C. oncophora and grazed on typical northern European pastures that were naturally contaminated with infective larvae of both species (Vlaminck et al., 2015). Calves were vaccinated and then turned out in May onto replicated pastures where they remained until the end of the grazing season in October. Over this period there was a ~60% reduction in cumulative faecal Cooperia egg counts, a ~65% reduction in infective C. oncophora larvae on pasture and an 82% reduction in worm burdens at housing, when numbers of Cooperia were also low (mean 3825) in the control calves, presumably because of naturally acquired immunity. However, there was no difference in live weight gain between the vaccinated calves and controls; furthermore, in all groups ostertagiosis was present at high levels, as indicated by high PP concentrations and clinical disease 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 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 subject 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 subclinical 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 therapeutic 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 reduction 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).

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.

In spring-born beef suckler calves, losses through subclinical PGE are limited while the calves are suckling their dams; when milk comprises a substantial 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 non-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. If SGS animals have not grazed previously, then they should be considered naïve 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.

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 demonstrated growth benefits from anthelmintic treatments 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 anthelmintic treatment have been observed (Stuedemann et al., 1989; Stromberg et al., 1997); these are generally 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 differences 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 depression in milk yield as a result of subclinical PGE, which is approximately 1 kg/day over a lactation (Charlier et al., 2009), are better understood. Longitudinal studies of abomasa in the abattoir have revealed not only that many cows harbour 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 hypergastrinaemia, 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.

Table 2.1. Summary of proven effects of subclinical parasitic gastroenteritis on performance of cattle.

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.

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.

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 development from egg to L3 under controlled conditions 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 development 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