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Overview of Gastrointestinal Parasites of Ruminants


The clinical signs associated with GI parasitisms are shared by many diseases and conditions; however, a presumptive diagnosis based on signs, grazing history, and season is often justified. Infection usually can be confirmed by demonstrating nematode eggs or tapeworm segments on fecal examination. However, in clinical evaluation of fecal examinations, two points should be remembered 1) a fecal worm egg count (number of worm eggs per gram (EPG) of feces is not always an accurate indication of the number of adult worms present; and 2) specific identification of certain nematode eggs (eg, “strongyles”) is impractical except in specialized laboratories. EPG counts can be negative or deceptively low in the presence of large numbers of immature worms; even when many adult parasites are present, the count can be low if egg production has been suppressed by host immune reaction or recent anthelmintic treatment. Variations in the egg-producing capability of different worms (significantly lower for Trichostrongylus, Ostertagia, and Nematodirus than for Haemonchus) may also distort the true picture. The ova of Nematodirus, Bunostomum, Strongyloides, and Trichuris are distinctive, but reliable differentiation of the more common species of ruminant strongyle ova is difficult. Fecal culture of strongyle eggs can produce distinctive third-stage larvae if differentiation is important premortem.

The advent of safe and effective broad-spectrum anthelmintics has largely reduced the need to differentiate the genera and species of these parasites. In areas where Ostertagia spp predominate, the analysis of sera for increased plasma pepsinogen levels is a useful diagnostic aid. Generally, increased levels of pepsinogen activity (tyrosine levels >3 IU) are associated with clinical abomasal parasitism. Problems of interpretation may arise in immune animals under challenge, in which there are no clinical signs but the pepsinogen levels may be increased because of a hypersensitivity-type reaction in the abomasal mucosa. Where Haemonchus spp predominate, the traditional estimation of blood packed cell volume (PCV) as an indicator of anemia has been largely replaced by use of the FAMACHA test (see below). In some countries, serologic diagnosis (ELISA) of important species, such as Ostertagia in cattle, is also used and based on antibody titers in bulk tank milk samples in dairy herds. Such information is used as an indicator of pasture challenge at a herd level, as an indirect indicator of productivity, and is linked with the effectiveness of parasite control strategies.

In many management situations, high levels of infection can be expected, particularly after favorable temperature and rainfall conditions. “Diagnostic drenching” may be recommended when eggs are few or absent, yet history and signs suggest infections, although care should be taken not to treat animals indiscriminately to minimize the risk of anthelmintic resistance developing.

Routine postmortem examinations can provide valuable parasitologic data about the status of the rest of the herd or flock. On necropsy, Haemonchus, Bunostomum, Oesophagostomum, Trichuris, and Chabertia adults (or advanced immature worms) can be seen easily. Ostertagia, Trichostrongylus, Cooperia, and Nematodirus are difficult to see except by their movement in fluid digesta, and clinically important infections are easily overlooked. In such cases, the total contents and all washings should be combined to a known volume, and a worm count established to evaluate the severity of the infection. The number of worms found in aliquots of the gut contents and scrapings of the mucosa will enable the total worm count to be calculated. However, the smaller nematodes may be difficult to see against a background of digesta, so they can be stained (5 min) with a strong iodine solution. Once the digesta and any tissue have been decolorized with 5% sodium thiosulfate, the iodine-stained worms can be seen easily. The significance of the numbers of worms present varies according to worm and host species. For example, only 100 Haemonchus are of clinical significance in lambs, whereas 5,000–10,000 Ostertagia are typically required before clinical signs are seen. If the animals have been diarrheic for a few days, worms may have been expelled and so the location, type, and severity of gross lesions may also be of considerable diagnostic value.

Mixed parasite infections should be considered when evaluating clinical, laboratory, and necropsy findings, because grazing animals rarely have mono-specific infections in the field.

The diagnosis of ostertagiosis in cattle during the period of larval inhibition (aka arrested development, hypobiosis, diapause) presents technical problems, particularly for the feedlot industry in the USA. Fecal egg counts and plasma pepsinogen analysis do not provide useful information because inhibition occurs within a few days of larval ingestion, before either the egg-laying adult stage has been reached or plasma pepsinogen levels increase. Predisposing factors for inhibition of larvae include age and geographic source of cattle, time of year or season of arrival, previous grazing history and management, weather conditions prevailing during the last grazing period, and prevalence of Ostertagia ostertagi in the source region.

Information on such factors is not usually available for feedlot cattle. If cattle have arrived after spring grazing in the south of the USA or fall grazing in the north, they could have heavy burdens of inhibited larvae. Lighter calves from areas where prevalence of parasites is high may also have such a problem. It is becoming more widely accepted that a significant cause of clinical disease or feed efficiency problems in feedlot cattle is parasitism, possibly ostertagiosis. When cattle are brought in from a suspect area and at a suspect time of year, it may be advisable to treat the new arrivals promptly with an anthelmintic effective against inhibited larvae.

Effective worm control cannot always be achieved by drugs alone; however, anthelmintics play an important role. (Also see Anthelmintics.) They may be used to reduce pasture contamination, particularly at times when seeding of the pasture with parasite eggs is a prerequisite for development of an infective challenge necessary to cause clinical parasitism. Coordination with other methods of control, such as alternate or mixed grazing with different host species, integrated rotational grazing of different age groups within a single host species (including creep grazing), inclusion of tannin-rich forages in pasture, and alternation of grazing and cropping, are other management techniques that can help to provide safe pasture and give economic advantage when combined with anthelmintic treatment.

The “ideal” anthelmintic should be safe, highly effective against adult and immature stages (including inhibited larvae) of the important worms, available in convenient formulations, economical, and compatible with other commonly used compounds.

Broad-spectrum anthelmintics currently available belong to five different chemical groups: 1) benzimidazoles (white drenches), 2) imidazothiazoles (yellow drenches), 3) macrocyclic lactones (clear drenches) and two new groups, 4) amino-acetonitrile derivatives, and 5) spiroindoles. The benzimidazoles include thiabendazole, the forerunner of modern broad-spectrum anthelmintics, which set a new standard in efficacy and is still widely used today.

Thiabendazole's ineffectiveness against inhibited Ostertagia larvae in cattle and one or two specific worm species led to the development of other benzimidazoles (such as fenbendazole, oxfendazole, and albendazole) and the probenzimidazoles (thiophanate, febantel, and netobimin). These compounds are effective against most of the major GI parasites of ruminants and have varying levels of activity against inhibited larvae. The imidazothiazoles include levamisole, morantel, and pyrantel, which also are highly effective, safe, broad-spectrum anthelmintics but have little activity against inhibited larvae in cattle. The macrocyclic lactones, which include the avermectins and milbemycins, often administered as pour-on products or by injection, are highly effective against adult and larval stages, including inhibited larvae of all the common GI nematodes of ruminants and some of the important ectoparasites. The latter group may persist in some ruminant species for several weeks after a single subcutaneous or topical administration and confer protection against reinfection during this period. Moxidectin is also persistent after oral administration. Unlike many other anthelmintics, eprinomectin may also be used in lactating cows without the need for a milk withdrawal period. The amino-acetonitrile derivatives (monepantel) and the spiroindoles (derquantel) are given as oral drenches in sheep, the latter in combination with abamectin in New Zealand. Both of these drugs have been used in the control of multiresistant GI nematode populations, although they require careful administration if their useful life is to be preserved.

Some narrow-spectrum anthelmintics, such as the salicylanilides, closantel, and rafoxanide, bind strongly to plasma proteins and have excellent activity against Haemonchus contortus in sheep and remain in the host for a long time, conferring prolonged prophylactic activity after administration.

Routes of administration other than drenching or injection (eg, incorporating into feed, drinking water, and mineral or energy blocks) are used to reduce labor costs and may be useful under drylot conditions or when grazing animals are being given supplemental feed. Another advantage of these “in-feed” routes is that continual low-level administration of a drug can be achieved and pasture contamination reduced during periods that are optimal for free-living development of the parasites. Disadvantages include erratic consumption of anthelmintic, tissue residues (requiring observance of recommended withdrawal periods), and possible encouragement of drug resistance by continual exposure. Another labor-saving route of administration is the “pour-on” topical treatment, used for some of the organophosphates (eg, trichlorfon), levamisole, and avermectins. A number of bolus preparations (eg, morantel, levamisole, ivermectin, or benzimidazoles) release drug in a sustained fashion or in pulses at intervals approximately equal to the prepatent period of the most important GI parasites. The boluses used in cattle have been designed to give entire grazing season protection in temperate areas if administered at turn-out to set-stocked herds. Boluses are also available that provide treatment and subsequent prophylaxis of animals already exposed to contaminated pasture and harboring parasites. Boluses in sheep may be used to reduce the periparturient rise in fecal egg output and thus the pasture contamination responsible for disease in their offspring later in the grazing season. Despite their efficacy, some boluses used in either cattle or sheep have been withdrawn from the market because they are not commercially viable.

Niclosamide, morantel, praziquantel, and the newer benzimidazoles (albendazole, fenbendazole, and oxfendazole) are effective against tapeworms (Moniezia spp) in cattle and sheep. Successful treatment of the fringed tapeworm, Thysanosoma actinioides, has been reported using either fenbendazole or praziquantel.

When treating clinically affected animals, the following should be considered: 1) provide adequate nutrition; (2) treat all animals in the group, as a preventive measure and to reduce further pasture contamination; and 3) either house or move stock to “clean” pastures to minimize reinfection. The definition of safe pastures varies in different climates and depends on local knowledge of the seasonal mortality of infective larvae. Some authorities have suggested treating only the most severely affected animals in a flock or herd, ie, targeted selective treatment (TST). Where Haemonchus is a problem in sheep or goats, animals most likely to benefit from such treatment can be identified using the FAMACHA score card. This links the color of the ocular mucous membranes, measured using a color chart, with the degree of anemia associated with the blood-sucking parasite. Animals with the palest mucous membranes are those likely to have the heaviest worm burdens and be chosen for treatment. The severity of diarrhea and/or the quantitative fecal egg count for parasitic gastroenteritis in sheep or cattle can also be used to determine the need for individual treatment. The rationale behind TST is that a very large proportion of worm egg output (and thus pasture contamination) is produced by a relatively small proportion of the host animal population. Treatment of only these animals significantly reduces pasture contamination and reduces the overall selection pressure, exerted by the use of an anthelmintic, for resistant parasite genes. Untreated animals will continue to pass low numbers of worm eggs onto the pasture and so maintain a "susceptible" parasite gene pool "in refugia" (ie, unexposed to anthelmintic treatment). In contrast, the established practice of blanket treatment and movement of stock onto a clean pasture may encourage emergence of anthelmintic resistance. Any worms carrying resistance genes surviving the treatment will then seed the previously clean pasture with a largely resistant parasite population.

Finally, the development of multiple drug resistance in populations of Haemonchus contortus, Trichostrongylus spp, and Ostertagia spp in sheep and goats to benzimidazoles, levamisole, and avermectins/milbemycins has been demonstrated. Although such resistance is currently a problem only in certain areas, it should be considered when other factors have been excluded, such as improper dosage, rapid reinfection, poor nutrition, or some disease state other than parasitism. Drug resistance in parasites of cattle has been demonstrated, although much less frequently than in small ruminants; overuse and otherwise indiscriminate treatment should be avoided.

If anthelmintic resistance is suspected on a farm, a fecal egg count reduction test may be conducted onsite that will indicate the likelihood of resistance. Fifteen to twenty animals should be randomly selected and assigned to either control or treatment groups, one for each anthelmintic group selected. Fecal samples are collected before treatment from all groups and then again either 7 days (after levamisole treatment) or 14 days (after benzimidazole or macocyclic lactone treatment) later. Pre- and post-treatment fecal worm egg counts are then compared and anthelmintic resistance suspected if the reduction in output after dosing is <95%.

The high cost of developing new anthelmintic drugs has encouraged researchers to look for alternative approaches to GI parasite control, such as development of a “hidden antigen” vaccine against Haemonchus, the use of tannin-rich forages (such as clover and lucerne or alfalfa), which have some anthelmintic action, and nematophagous fungi.

General Control Measures

“Control” generally implies the suppression of parasite burdens in the host below that level at which economic losses occur. To do this effectively requires a comprehensive knowledge of the epidemiologic and ecologic factors that govern pasture larval populations and the role of host immunity in combating infection.

The goals of control are as follows: 1) prevent heavy exposure in susceptible hosts (recovery from heavy infection is always slow), 2) reduce overall levels of pasture contamination, 3) minimize the effects of parasite burdens, and 4) encourage the development of immunity in the animals (less important in fattening animals than in those to be kept for breeding purposes).

The strategic use of anthelmintics is designed to reduce the build up of worm burdens and, as a result, pasture contamination. The timing of anthelmintic treatment is based on knowledge of the seasonal changes in infection and the regional epidemiology of the various helminthoses. Prompt recognition of circumstances likely to favor development of parasitic disease, eg, weather, grazing behavior, and loss of weight and condition, is essential.

For example, in the UK, where the pattern of disease caused by Nematodirus battus infection in sheep is clearly defined, strategic treatments with two or three doses of an anthelmintic at 2- to 3-wk intervals, beginning just before the disease characteristically appears, are recommended. The timing of these treatments is designed to coincide with peak numbers of Nematodirus larvae on pasture in the spring; timing of the latter can be predicted accurately using a simple formula that incorporates soil temperatures 1 ft below the surface during March. Similarly, in the northern USA, Canada, and western Europe, pasture levels of Ostertagia and other parasites increase substantially after mid-July, ie, the general pattern of infectivity is minimal in spring but increases rapidly to peak levels in late summer and early fall. Current practices in these areas indicate the effectiveness of two or more carefully timed anthelmintic treatments given during the first grazing season after turnout in the spring. Calculating the interval between treatments requires knowledge of the parasite's prepatent period (3 wk in the case of Ostertagia in cattle) and the duration of residual (or prolonged) activity of the anthelmintic being used, ie, the period of protection provided after a single treatment; the treatment interval is calculated as the sum of the two. For example, treatment with a macrocyclic lactone with a 5-wk period of residual activity at turnout and again 8 wk later should result in highly effective control of worm egg output and minimal numbers of larvae appearing on pasture during the fall. No further treatment is likely to be required, because any larvae surviving on pasture from the previous year would have died by the time the prophylactic effect of the second treatment had worn off.

In other countries, with either a cool or warm temperate climate, similar controls may be used if the seasonal pattern of the disease is known, but in most regions a tactical use of anthelmintics is used, eg, during warm, moist conditions.

Cattle—Special Considerations

Worm problems are seen most frequently in young beef cattle from time of weaning and several months thereafter, and in segregated groups of dairy calves during the first season at grass. Immunity to GI nematodes is acquired slowly; two grazing seasons may be required before a significant level is attained. In endemic areas, cows may continue to harbor low burdens, which may contribute to suboptimal production on some farms. GI parasitism in young stock may be controlled by use of broad-spectrum anthelmintics in conjunction with pasture management to limit reinfection; the latter includes a move to “clean” pastures (eg, grass conservation areas or silage or hay aftermath, although anthelmintic resistance concerns should be noted [above]), alternate grazing with other host species, or integrated rotational grazing in which susceptible calves are followed by immune adults. Alternate grazing with other host species may be ineffective in areas where parasite species (eg, Nematodirus) infect both hosts; simple pasture rotation is not effective, because the bovine fecal mass can protect larvae from adverse environmental conditions for several months, infecting rotating calves at a later date.

In beef herds, anthelmintic treatment at weaning is of value, particularly if the young cattle are to be retained, eg, as replacement heifer stock or as steers to be fed. Cattle finished on grass should receive treatment at weaning and at intervals throughout the next 12 mo and, if possible, should be moved to safe pastures to maximize liveweight gain.

When cattle cannot be moved readily to other pastures, strategic treatments (described earlier) may be given to limit contamination of pastures and rapid reinfection. Alternatively, intraruminal boluses may be used in countries where approved. In warm temperate regions of the world, such as Australia and New Zealand, the southern USA, and the large cattle-raising regions of southern Brazil, Uruguay, and Argentina, young cattle may be given two or more treatments from late summer and into fall for prevention of large increases in pasture contamination and infection during winter and spring. Two or three strategic treatments, administered with a short interval, from the time of weaning in such regions could be just as effective as spring treatments in cool temperate regions. However, survival of infective larvae on pasture from the time of fall weaning in warm temperate regions is most often persistent, and longer intervals between treatments (eg, at weaning, during winter, and in late spring) may be more applicable. In many areas, anthelmintics are simply given at regular intervals after weaning. Intervals between treatments must necessarily vary according to local parasite epidemiology and the duration of prolonged activity exhibited by the anthelmintic. When Type II ostertagiosis is a problem, treatment with an anthelmintic effective against inhibited larvae is recommended before the expected time of outbreak.

Sheep—Special Considerations

A special strategic treatment is required in most regions to counter the postparturient relaxation of immunity (resulting in the periparturient rise in worm egg output) seen in breeding ewes. The precise timing of such treatment varies between regions and for different species of parasites and will, in temperate regions, depend on whether ewes and lambs are turned out onto clean or contaminated pasture. On clean grazing, only the ewes (with an existing parasite burden) act as a source of worm eggs and, therefore, require treatment to prevent pasture contamination and subsequent infection of their lambs. Ewes treated during the month before lambing should not only exhibit a drop in worm egg output but may also show improved productivity. On contaminated pasture, both ewes and lambs pass worm eggs in their feces (ewes from their existing worm burden and lambs from larvae overwintering on pasture). The aim of treating ewes should be to prevent fecal worm egg output; this can be achieved by treating with an albendazole or ivermectin anthelmintic bolus (available in some countries), injectable long-acting moxidectin, or medicated feed blocks. In temperate areas, lambs should be dosed at weaning before a move to clean grazing.

A treatment 2 wk before breeding, as part of a “flushing” program, is another strategic application of anthelmintics. Supportive management after treatment includes movement of sheep from contaminated pastures to cattle pastures, grass conservation areas, root crops, or pasture not grazed by sheep for several months. The latter period varies according to the seasonal pattern of larval mortality in different countries and may be as long as 1 yr in some temperate countries.

Sheep are more consistently susceptible to the adverse effects of worms than other livestock, and clinical disease is more common. Immunity to the parasites is acquired slowly and is generally incomplete. Frequent treatments may be required, particularly during the first year of life, although a good understanding of local parasite epidemiology will ensure that such treatments are appropriately timed.

Last full review/revision September 2014 by Mark T. Fox, BVetMed, PhD, DEVPC, FHEA, MRCVS

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