Nematodirus Spathiger Research Articles

Parasites of the blackbuck antelope (Antilope cervicapra) in Texas.

Three blackbuck antelope were examined for external and internal parasites. The latter were listed by location and number present. External parasite species found were as follows: Amblyomma americanum, larval Ixodidae and Tricholipeurus parallelus. Internal parasite species found were as follows: Taenia hydatigena (cysticercus), Camelostrongylus mentulatus, Haemonchus cortortus, Trichostrongylus axei, Trichostrongylus colubriformis, Trichostrongylus probolurus, Nematodirus spathiger, Oesophagostomum sp. and Trichuris sp. C. mentulatus and T. probolurus are two helminth species not indigenous to the United States which have survived translocation from India to parts of Texas.

Anthelmintic Activity of Levamisole against Nematodims spathiger and Trichostrongylus axei in Sheep

Controlled anthelmintic trials were carried out with levamisole administered orally or subcutaneously at 7·5 mg./kg. against all life-cycle stages of Nematodirus spathiger and Trichostrongylus axei in sheep. Efficiencies greater than 97% were recorded for all stages of both parasites except in the case of third-stage T. axei larvae. In general, results compare with those of other workers using tetramisole at 15 mg./kg.

Comparative Activity of Pyrantel Tartrate, Parbendazole, and Levamisole at Two Dose Levels against Naturally Acquired Helminth Infections in Sheep

Forty-nine ram lambs similarly exposed on pasture to common gastrointestinal helminth infections were assigned to 7 groups of 7 lambs each in a controlled anthelmintic trial involving 2 dose levels of each of 3 anthelmintics. All lambs were necropsied 5 to 7 days posttreatment for residual worm counts. Both mature and immature stages of some nematode parasites were recovered from the lambs. The most numerous species in the unmedicated controls were Ostertagia spp. (mainly 0. circumcincta), Haemonchus contortus, and Trichostrongylus spp. (mainly T. vitrinus). The drugs and dosages were: pyrantel tartrate 25 and 50 mg/kg; parbendazole 15 and 20 mg/kg; levamisole 8 and 12 mg/kg; unmedicated controls. The calculated efficacies at the 2 dose levels were, respectively, H. contortus: pyrantel tartrate 99 and 100%, parbendazole 54 and 78%, levamisole 99 and 99%8; Ostertagia spp.: pyrantel tartrate 86 and 96%, parbendazole 88 and 87%, levamisole 82 and 88%; Trichostrongylus spp.: pyrantel tartrate 98 and 99%, parbendazole 99 and 100%, levamisole 99 and 98%; Nematodirus spathiger: pyrantel tartrate 100 and 100%, parbendazole 85 and 91%, levamisole 91 and 96%; Oesophagostomum venulosum: pyrantel tartrate 96 and 100%, parbendazole 100 and 100%, levamisole 100 and 100%. In most instances, the higher dosages of the 3 anthelmintics appeared to be more efficacious than the lower dosages, but in most cases these differences were not statistically significant. Both 4thand 5th-stage H. contortus were somewhat resistant to parbendazole at the 2 dose levels used, but they were highly susceptible to pyrantel tartrate and levamisole. Three of the newer broad-spectrum anthelmintics for use in sheep are pyrantel tartrate (Austin et al., 1966), parbendazole (Actor et al., 1967), and levamisole, the active isomer of dl-tetramisole (Thienpont et al., 1966; Bullock et al., 1968). Although the accumulated data indicate that all three drugs have a similar spectrum of activity in sheep, each has been somewhat ineffective occasionally against certain species, stages, or strains when administered as a drench at the recommended therapeutic dose. The purpose of this trial was to compare the efficacy of two dose levels of the three drugs against naturally acquired multiple species infections in sheep. Most of the reports on the activity of parbendazole and levamisole against gastrointestinal nematodes of sheep were summarized recently by Kates et al. (1971). Parbendazole at 15 mg/kg of body weight does not compare favorably with other available anthelmintics against certain strains of H. contortus and Received for publication 6 April 1971. * National Animal Parasite Laboratory, Veterinary Sciences Research Division, ARS, Beltsville, Maryland 20705. tAnimal Science Research Division, ARS, Beltsville, Maryland 20705. against Nematodirus spp., whereas levamisole at 8 mg/kg of body weight is not reliably effective against Ostertagia spp. Austin et al. (1966) first published on the anthelmintic activity of pyrantel tartrate against sheep nematodes. Several investigators have confirmed the initial findings that a dosage of 25 mg/kg of body weight was highly effective against many nematode species (Corwell, 1966; Corwell et al., 1966a, b, 1967a, b; Cornwell and Jones, 1969b; Gibson and Parfitt, 1968; Colglazier et al., 1971; Reinecke and Anderson, 1967). Also, low-level continuous administration was effective prophylactically (Cornwell and Jones, 1969a, b), and in certain limited studies dosages of 45 or 50 mg/kg tended to enhance efficacy slightly against some species (Comwell, 1966). MATERIALS AND METHODS Origin and infection of experimental lambs These aspects were similar to those reported previously (Kates et al., 1971). Fifty-three lambs (black-faced, crossbred) were purchased from a dealer in the western United States and shipped by truck to Beltsville, Maryland, in mid-May 1969. Upon arrival the lambs averaged 31 kg in weight, and initial fecal examinations indicated that they had minimal infections of a few nematode species,

Comparative Activity of Thiabendazole, Levamisole, and Parbendazole against Natural Infections of Helminths in Sheep

Forty-five ram lambs uniformly exposed to natural infections of various helminths were assigned to 5 groups of 9 lambs each and used to conduct controlled anthelmintic trials. One group of lambs served as unmedicated controls, and 4 groups were treated as follows: (1) thiabendazole 50 mg/ kg; (2) thiabendazole 100 mg/kg; (3) levamisole 8 mg/kg; (4) parbendazole 15 mg/kg. All lambs were necropsied 4 to 6 days posttreatment for residualworm counts. Both mature and immature stages of several parasite species were recovered from the unmedicated control lambs; Haemonchus contortus was the most numerous. For the medicated groups 1, 2, 3, and 4 above, the calculated efficacies of the treatments against all stages of parasites were, respectively, H. contortus 48, 88, 99, and 79%; Ostertagia spp. (mainly 0. circumcincta) 94, 99, 76, and 99%; Trichostrongylus spp. (T. axei, T. vitrinus, and T. colubriformis) 99, 100, 99, and 100%; Nematodirus spathiger 90, 100, 96, and 83%; Oesophagostomum venulosum 98, 100, 100, and 99%. The data indicate the H. contortus strain in these lambs was somewhat resistant to thiabendazole and parbendazole. Fourth-stage larvae were recovered only of H. contortus, Ostertagia spp., and N. spathiger, and generally were not removed as effectively as 5th-stage parasites. However, levamisole was highly effective against 4th-stage H. contortus and N. spathiger, and 100 mg/kg of thiabendazole removed all 4th-stage N. spathiger. The 3 anthelmintics significantly reduced strobilar volume of Moniezia expansa, but had no activity against the scoleces. During the last decade, three new broadspectrum anthelmintics, viz., thiabendazole, tetramisole, and parbendazole, have shown considerable promise against helminths, particularly gastrointestinal nematodes of sheep and other domestic animals. The effective action of thiabendazole [2-(4'thiazolyl)-benzimidazole] against a wide variety of nematode parasites of various animals was first reported by Brown et al. (1961). Since that time a substantial literature (see Gibson, 1965, 1969; Levine, 1968) has accumulated supporting the original findings. Recently, however, Theodorides et al. (1970) and Colglazier et al. (1970a) summarized a number of published reports pertaining to strains of Haemonchus contortus that were resistant to the drug. Thienpont et al. (1966) first reported on the anthelmintic activity of dl-tetramisole [2,3,5,6tetrahydro-6-phenyl-imidazo (2,1-b) thiazole hydrochloride] in man and animals. Subsequently, Bullock et al. (1968) separated the dextro and levo isomers of the drug, and showed that the anthelmintic action was attribReceived for publication 3 September 1970. * National Animal Parasite Laboratory, Veterinary Science Research Division. t Animal Science Research Division, ARS, USDA, Beltsville, Maryland 20705. utable primarily to the levo form. Considerable published data have now accumulated which attest to the broad-spectrum activity of this chemical, and to the fact that the levo isomer (levamisole) is about twice as active as the dl compound (Walley, 1966; Fitzsimmons, 1966; Forsyth, 1966, 1968; Gibson, 1966; Gibson et al., 1968a, b; Hart and Curr, 1968; Hart et al., 1969; Lyons et al., 1968; Pankhurst and Sutton, 1966; Pretorius, 1967; Ross, 1966; Shone and Philip, 1967; Colglazier et al., 1969, 1970b). In 1967, Actor et al. published the first report on another promising livestock anthelmintic, parbendazole [5(6)-butyl-2-benzimidazole carbamate], a benzimidazole compound related chemically to thiabendazole. Parbendazole had an anthelmintic spectrum similar to that of thiabendazole, but it was active at lower dose level. Several studies on the activity of parbendazole against gastrointestinal nematodes of sheep and goats have been reported which essentially confirm and extend the earlier findings, viz., Bennett (1968), Danek et al. (1969), Johns and Mendel (1969), Lammler et al. (1969), Luque Forero et al. (1969), Ross (1968), Theodorides et al. (1968, 1969). Theodorides et al. (1970) also reported that a number of thiabendazole-resistant strains of H. contortus were also cross-resistant to parbendazole.

Gastrointestinal Nematode Parasites from Domestic Sheep, Ovis aries, in Nebraska

Necropsies of 80 domestic lambs from Nebraska established the presence of the following 14 nematode parasites in that state: Haemonchus contortus, Ostertagia circumcincta, Trichostrongylus axei, Pseudostertagia bullosa, T. colubriformis, Strongyloides papillosus, Nematodirus spathiger, N. abnormalis, N. helvetianus, N. oiratianus, Cooperia curticei, C. oncophora, C. surnabada, and Trichuris spp. In general, small numbers of worms were recovered. This study confirms the presence in Nebraska of the common species of sheep nematodes and establishes new distribution records for P. bullosa, N. helvetianus, N. oiratianus, and C. surnabada. Little information is found in the literature concerning nematode parasites of sheep from Nebraska. Kelley (1955) made an oral report at the Conference on Parasites and Parasitic Diseases of Domestic Ruminants, which was later reproduced for limited distribution. In his report he listed nematodes recovered from cattle, and spoke of Haemonchus contortus, and Nematodirus spp. in sheep. The revised checklist of internal and external parasites of domestic animals in the United States and possessions and Canada (Becklund, 1964) states only that the geographical distribution of the common nematode species from sheep is generally in North America. Geographical distributions of the more uncommon species are recorded as specific areas where they have been recovered. Only one of these records includes Nebraska. Becklund and Walker (1967) reported Nematodirus spathiger and N. abnormalis in one lot of specimens collected from Nebraska sheep. With the opening of the U. S. Meat Animal Research Center, Clay Center, Nebraska, a comprehensive research program on sheep began. This program afforded the authors an opportunity to examine the viscera of some Nebraska lambs for gastrointestinal nematode parasites to establish further the presence of specific parasites in this state. The results of these examinations and information on the species recovered, including several new distribution records, are reported herein. MATERIALS AND METHODS Eighty lambs from the Meat Animal Research Center, Clay Center, Nebraska, were necropsied, 37 in January and 43 in July 1967. Suffolks, TarReceived for publication 24 February 1970. ghees, Corriedales, and various crossbred lambs were represented. All lambs were born at Clay Center, though their dams, except for the Corriedales, had been brought to Clay Center from Fort Wingate, New Mexico, in April 1966. The Corriedale ewes originated in Nebraska. The lambs which were killed and examined in January 1967 were born in May-June 1966; lambs killed in July 1967 were born in February-March 1967. Each group grazed the same permanent pastures but in different seasons in successive years. The lambs were killed at an abattoir, and the viscera were collected, frozen with dry ice, and taken to the Parasitological Laboratory at Beltsville, Maryland. There they were thawed and the procedures of Porter (1942) and Herlich (1956) were used to recover and enumerate the various nematode parasites. Representative specimens of most of the helminths recovered were deposited in the National Parasite Collection (Table I).

Two new host records for Nematodirus species

Nematodirus spathiger (Railliet, 1896) Railliet and Henry, 1909 from a horse, and Nematodirus odocoilei Becklund and Walker, 1967 from the white-tailed deer Odocoileus virginianus, constitute new host–parasite records.

Nematodirus of Domestic Sheep, Ovis aries, in the United States with a Key to the Species

One hundred and thirty lots of specimens deposited in the U. S. National Museum Helminthological Collection and labeled as containing Nematodirus from domestic sheep, Ovis aries, in the United States were examined. Specific determinations were made on the 90 of these lots which contained males. They were collected in 21 states and the District of Columbia. Nematodirus spathiger was found in 80% of the 90 lots, N. abnormalis in 53%, N. filicollis in 22%, N. lanceolatus in 9%, N. helvetianus in 4%, and N. davtiani in 2%. Nematodirus spathiger is the most common species and was found among specimens collected in 19 states. Nematodirus abnormalis, previously reported from only eight states, was found from 18 states. Contrary to general belief, it appears to be, on the basis of this material, considerably more prevalent than N. filicollis, which was found in small numbers in lots collected in 10 states. Nematodirus helvetianus and N. lanceolatus were both found among specimens collected in four states and N. davtiani in one state. The distribution of the six species is given by state along with a discussion of each species, and a key with illustrations as an aid in their identification. Accurate information on the geographic distribution of parasites of domestic animals in the United States is still incomplete. The sources of such information and the problems involved in its compilation have been discussed in a checklist (Becklund, 1964). Several sources were consulted in compiling this checklist, including the records of the U. S. National Museum Helminthological Collection. At that time, some of the determinations in the Collection records of the genus Nematodirus were checked with their corresponding specimens on deposit and inaccuracies were found, e.g., specimens determined as being N. filicollis (Rudolphi, 1802) Ransom, 1907, were actually N. spathiger (Railliet, 1896) Railliet and Henry, 1909, or were a composite of several species. Subsequently, incorrect determinations were again noted when specimens of Nematodirus from domestic sheep were being examined for possible representatives of a new species. These observations suggested that a complete study of the specimens deposited as Nematodirus from domestic sheep in the United States would be of considerable value to correct the Collection records, ascertain the species present, and contribute accurate information on their distribution. The information reported herein is a result of that study. MATERIALS AND METHODS This study encompassed the examination of almost every lot of Nematodirus collected from Received for publication 6 February 1967. domestic sheep in the United States that has been deposited in the U. S. National Museum Helminthological Collection since its inception in 1893. The lots on deposit contain from one to several thousand specimens. The condition of the specimens varies from excellent to partially decomposed and fragmented. Relatively few Nematodirus from domestic sheep were deposited after 1950. Males only were selected for use in making specific determinations. The chief characters used in making these determinations were the morphologic structure of the spicule tip, the size of the lobules on the dorsal lobe of the bursa, and the relationship of the externodorsal ray to the dorsal margin of the lateral bursal lobes. The males were removed from the preserving fluid (92% of 70% alcohol, 3% formalin, and 5% glycerin) and cleared in lacto-phenol or pheno-alcohol for study. When male specimens were present in large numbers they were initially cleared, studied under the dissecting microscope (up to 54 X magnification), and a representative sample selected for close study and specific determination. The number of specimens in the sample varied, depending primarily on total number of males and on apparent number of kinds as revealed by the initial examination; in many instances more than a hundred males were examined. In the lots containing a smaller number of males, usually all specimens in the bottle were subjected to careful study.

THE DYNAMICS OF THE HOST-PARASITE RELATIONSHIP. I. NEMATODIRUS SPATHIGER INFECTION IN SHEEP.

The studies presented in this paper describe the effects of control exerted by the immunological response of the host (sheep) on the developmental stages and fecundity of the parasite Nematodirus spathiger. Thirty Merino lambs, maintained worm-free, were randomly divided among three treatment groups each containing ten animals. The group 1 lambs were each given a single dose of 50,000 infective larvae, the group 2 animals were given a single dose of 130,000 infective larvae, and the group 3 animals were given twenty-five consecutive daily doses of 2000 infective larvae. Group fecundity was estimated by performing worm egg counts on daily faecal samples and development of the parasite burden was followed by carrying out differential worm counts on animals slaughtered at crucial stages during the infections. Total fecundity was greatest in group 1 and least in group 3 with group 2 intermediate. An inverse relationship between total fecundity and percentage retardation of development (percentage of 4th-stage larvae in the total worm burden) was demonstrated between the three treatment groups.The results of the studies also show that control of the parasitic infection is mediated about threshold levels of immunological responsiveness and is expressed by (1) elimination at the infective (L3) stage, (2) retardation of development at the L4 stage, (3) reduction in egg production of the adult female, (4) elimination of adult worms, and (5) discrimination against the female in both the degree of retardation in the L4 stage and the extent of elimination in the adult stage.Great variation in response was observed between individuals within treatment groups. The source of variation is attributed to differences in degree of antigenic disparity of the parasite with individual members of the heterozygous host population in which antigenic characters are not uniformly segregated.The concept of ‘fitness’ of the parasitic species was introduced into the discussion to provide a rational interpretation of the results.We are indebted to Dr S. S. Y. Young, Division of Animal Genetics, C.S.I.R.O., for advice and assistance with the statistical analyses, which were performed by Mrs M. Tonkin, and to Dr D. F. Stewart for his constructive criticism of the manuscript. Careful technical assistance was given by Mr E. Teleki and Misses Helen Giller and Berenice Merchant.

Gastrointestinal Nematode Infection of Lambs Raised in Drylot

Twenty lambs from ewes heavily parasitized with gastrointestinal nematodes (mostly Haemonchus) were weaned at approximately 85 days of age and left in drylot apart from their dams. They were slaughtered approximately 70 days after weaning. Fecal nematode egg counts were made on the ewes at the time of weaning and on the lambs at the time of slaughter. The lambs' gastrointestinal tracts were subjected to critical examination for nematodes at the time of slaughter. At the time of weaning, the ewes were passing an average of 5,300 nematode eggs per gram (e.p.g.) of feces, while the lambs were passing none. At the time of slaughter, the lambs were passing an average of 80 e.p.g. Extremely few adult nematodes were found in the lambs at slaughter. None at all were found in six, and averages of 9.6 Trichuris ovis, 1.0 Nematodirus spathiger, 0.5 Trichostrongylus axei, and 0.2 Haemonchus contortus were found in the whole group. These data, obtained by critical examination of parasite load, support the view that lambs grown in drylot are relatively free of nematodes even when their dams are carrying relatively heavy infections of several species. This information further undergirds the theory that quality lamb production is possible under intensified drylot conditions without recourse to use of vermifuges on the lambs so produced.

The Activity of Bephenium Embonate against the Free-Living and Adult Stages of Nematodirus spathiger

The Activity of Bephenium Embonate against the Free-Living and Adult Stages of Nematodirus spathiger

Nitrogen Catabolism in Nematode Parasites

Nematodirus /ilicollis, Nematodirus spathiger, and Ascaridia galli were maintained for periods of 24 hours in' a non-nutrient medium containing streptomycin and penicillin to prevent bacterial growth. UnEler aerobic 'conditions the total soluble nitrogenous material excreted by Nematodirus spp. in three experiments was 1.23-1.59 mg. nitrogen per g. dry wt. of tissue. Peptide nitrogen accounted for 33-37 per cent. of the total soluble nitrogen excreted, ammonia nitrogen 40-42 per cent., and urea nitrogen 11-17 per cent. Small amounts of uric acid werc found. Under similar conditions the total soluble nitrogen excreted by Ascaridia gaUi was 0.29-0.41 mg. per g. dry wt.; of this, 14-15 per cent. was due to peptide nitrogen, and 8 per cent. to urea nitrogen. No uric' acid was found.

The Tricarboxylic Acid Cycle in Nematode Parasites

IN nematode parasites the anaerobic breakdown of glycogen to pyruvate and lactate with a consequent formation of adenosine triphosphate follows a course similar to that in vertebrate muscle1. Since it appears that aerobic mechanisms may play an important part in the metabolism of certain nematode parasites2, studies on the carbohydrate metabolism of the parasites have been extended to include some aspects of the oxidative utilization of pyruvate. The organisms used were Ascaridia galli from the chicken small intestine and Nematodirus spathiger and N. filicollis from the sheep small intestine. Some experiments were also carried out with Neoaplectana glaseri, a parasite of the Japanese beetle, which, however, was grown in vitro for the present experiments. Owing to its relatively large size and its position in the host, A. galli may not have an active aerobic metabolism in vivo. However, it has been shown that Nematodirus spp. probably respire actively in vivo, and oxygen is essential for the survival in vitro of Neoaplectana glaseri.

On the Relative Importance of Aerobic Metabolism in Small Nematode Parasites of the Alimentary Tract I. Oxygen Tensions in the Normal Environment of the Parasites

As a preliminary to the study of the relative importance . of aerobic mechanisms in the metabolism of Nippostrongylus muris, Nematodirus spathiger, Nematodirus filicollis, and Haemonchus contortus at oxygen pressures of the normal environmental fluids of these parasites, the determination of oxygen in the contents of the small intestine of the rat and sheep, and the abomasum of the sheep, has been carried out. The method which was used allowed measurements to be made close to the mucosa of the alimentary canal of anaesthetized animals in which the circulation was left intact, and the procedure ensured that conditions in the normal gut were very little disturbed.

On The Relative Importance of Aerobic Metabolism in Small Nematode Parasites of the Alimentary Tract II. the Utilization of Oxygen at Low Partial Pressures by Small Nematode Parasites of the Alimentary Tract

Nippostrongylus muris, Haemonchus contortus, Nematodirus spathiger, and N. filicollis are all capable of utilizing oxygen for respiratory purposes even when it is present at very low oxygen tensions. Thus with a partial pressure as low as 5 mm. of mercury the respiration of Nippostrongylus muris may reach 40 per cent. of its maximum rate, whereas Nematodirus spp. and H. contortus may respire at 25 and 12 per cent. of their maximum rates respectively. Further, the results indicate that in vivo the oxygen consumption rates may sometimes reach 80 per cent. of the maximum in vitro rate in the case of Nippostrongylus muris in the small intestine of the rat and 40 per cent. in the case of Nematodirus spp. in the small intestine of the sheep. Haemonchus contortus in the sheep abomasums probably respires at a relatively lower rate than either of the intestinal parasites in vivo.

On some Nematode Parasites of the Camel in India

Whilst working through the collections of Nematodes at the Punjab Veterinary College in Lahore I had the opportunity of examining a number of Strongylid worms from the Indian camel (Camelus dromedarius) belonging to two species, labelled Haemonchus longistipes and Nematodirus spathiger, respectively.