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Effects of gastrointestinal nematode infection on the ruminant immune system.

Gastrointestinal (GI) nematodes of ruminants evoke a wide variety of immune responses in their hosts. In terms of specific immune responses directed against parasite antigens, the resulting immune responses may vary from those that give strong protection from reinfection after a relatively light exposure (e.g. Oesophagostomum radiatum) to responses that are very weak and delayed in their onset (e.g. Ostertagia ostertagi). The nature of these protective immune responses has been covered in another section of the workshop and the purpose of this section will be to explore the nature of changes that occur in the immune system of infected animals and to discuss the effect of GI nematode infections upon the overall immunoresponsiveness of the host. The discussion will focus primarily on Ostertagia ostertagi because this parasite has received the most attention in published studies. The interaction of Ostertagia and the host immune system presents what appears to be an interesting contradiction. Protective immunity directed against the parasite is slow to arise and when compared to some of the other GI nematodes, is relatively weak. Although responses that reduce egg output in the feces or increase the number of larvae undergoing inhibition may occur after a relatively brief exposure (3-4 months), immune responses which reduce the number of parasites that can establish in the host are not evident until the animal's second year. Additionally, even older animals that have spent several seasons on infected pastures will have low numbers of Ostertagia in their abomasa, indicating that sterilizing immune responses against the parasite are uncommon. In spite of this apparent lack of specific protective immune responses, infections with Ostertagia induce profound changes in the host immune system. These changes include a tremendous expansion of both the number of lymphocytes in the local lymph nodes and the number of lymphoid cells in the mucosa of the abomasum. This expansion in cell numbers involves a shift away from a predominant classic T cell population (CD2 and CD3 positive), to a population where T cell percentages are decreased and B cells (immunoglobulin-bearing) and gamma-delta cells are increased. At the same time the expression of messenger RNAs for T cell cytokines (IL2, IL4, IL10 and gamma-interferon) is changed to that of increased expression of IL4 and IL10 and decreased expression of IL2 and perhaps of gamma-interferon. The reasons for these changes remain to be elucidated, but it is evident that the lack of protective immune responses is not the result of a poor exposure of the host to parasite products, or to the stomach being an immunoprivileged site. In fact, a superficial look at the responses elicited indicates that Ostertagia induces responses (the so-called TH2 mediated responses) that are widely considered to be the type of responses necessary for protection against GI nematodes. There are many factors that could lead to this apparent lack of immunity in the face of a strong stimulation of immune responses including: (1) the elicitation of suboptimal responses; (2) the failure of the abomasum to function as an efficient effector organ; (3) active evasion of the functional immune response by the parasite; and (4) that these classic responses are not protective in this particular ruminant-parasite system and that novel protective mechanisms may be required. The strong stimulation of the host gut immune system by Ostertagia and perhaps by other GI nematode infections, raises questions about the potential effects of such infections on the overall well-being of the host. A number of authors have indicated that Ostertagia infections may diminish the host's ability to mount subsequent immune responses to antigenic challenges such as vaccination against other infectious organisms. In addition, recent studies have indicated that infections with GI nematodes may result in increased circulatory levels of stress-related hormo

Animals↗

Nematode infections in dog breeding kennels in The Netherlands, with special reference to Toxocara.

Faecal samples from 286 adult dogs and 159 pups and dust and soil samples from 32 dog breeding kennels in the Netherlands were examined for nematode eggs. Dogs that shed nematode eggs were found in 41% of the kennels. The kennel prevalence of nematode infection of adult dogs was 33%. The kennel prevalence for infection of adult dogs and pups with nematode species was 21% and 48% for Toxocara canis, respectively, 29% and 0% for Trichuris vulpis, and 20% and 0% for Toxascaris leonina. Kennels with more than two litters per year and with regular import of new animals had a significantly higher prevalence of T. canis (p < 0.01 and p < 0.05 respectively). T. vulpis infections in adult dogs occurred significantly more often in kennels that used deworming products other than benzimidazoles (p < 0.05). Embryonated T. canis ova were recovered from 20% of the house and kennel dust samples and from 50% of the soil samples. This survey shows that the nematode infection rate in dog breeding kennels is high. Better deworming strategies should be used to improve the health status of the dogs and to reduce the risk of zoonotic infection in humans.

Animal Husbandry↗

Nematode infection in Mugil incilis (Lisa) from Cartagena Bay and Totumo Marsh, north of Colombia.

Nematode infection indices were recorded in Lisa, Mugil incilis, from Cartagena Bay and Totumo Marsh, north of Colombia, during an 8-mo period (February to September 2002). Parasite prevalence (74.67% vs. 53.48%), intensity (9.73 +/- 2.98 vs. 2.73 +/- 1.07), and abundance (7.49 +/- 2.21 vs. 2.04 +/- 1.17) were significantly greater in Cartagena Bay, an estuary polluted by domestic sewage and industrial discharge, compared with those of Totumo Marsh, a body of water with low levels of contamination. Parasites were found below the spine, within the liver and the intestinal mesenteries, and a small percentage in muscle. Morphological analysis of nematodes indicated the presence of the third larval stage of several species belonging to the Anisakidae. Size correlated moderately and significantly with parasite intensity in fish collected from Totumo Marsh (R = 0.336; P < 0.001); in Cartagena Bay the correlation was also significant, but low and negative (R = -0.212; P = 0.003), clearly showing differences in host-parasite ecology. Fish health status, as represented by condition factor and hepatosomatic index, did not show any correlation with the parasite prevalence in fishes collected in either sampling areas. These results suggest, for the first time, that the consumption of Lisa from the Atlantic coast of Colombia could represent a risk for human infection.

Analysis of Variance↗

Neuroparasitic infections: nematodes.

Globalization has produced an increase in the number of people at risk for contracting parasitic infection. Central nervous system infection by nematodal parasites can be devastating. Early recognition and treatment of infection can significantly decrease morbidity of the parasitic infection, as well as the risk of secondary superinfection. The clinical presentation, diagnosis, and treatment for five of the more common nematodal infections of the nervous system--Angiostrongylus spp., Baylisacaris procyonis, Gnathostoma spinigerum, Strongyloides stercoralis, and Toxocara spp.--is reviewed.

Angiostrongylus↗

Soil-transmitted nematode infections and mebendazole treatment in Mafia Island schoolchildren.

In August 2000, a cross-sectional study was performed to assess the prevalence and intensity of soil-transmitted nematode infections in schoolchildren on Mafia Island. Hookworm infection was widespread (72.5% prevalence) whereas Trichuris trichiura was less prevalent (39.7%) and Ascaris lumbricoides was present at a low prevalence (4.2%), mainly in urban areas. In a subsample of the study population, both Necator americanus and Ancylostoma duodenale were found, although N. americanus was more prevalent. This survey was followed by a parasitological evaluation of mebendazole treatment using a single, 500-mg dose. The data on outcome were used for comparison with those from recent studies of similar treatment regimens in the neighbouring island of Pemba, Zanzibar, where periodic chemotherapy with mebendazole to schoolchildren has been implemented as part of a helminth-control programme since 1994. A higher efficacy of mebendazole against hookworm infection was found in Mafia Island (where a cure 'rate' of 31.3% and an egg-reduction 'rate' of 78.1% were recorded) when compared with that observed in Pemba Island, possibly indicating that hookworms may be developing mebendazole resistance on Pemba Island as a result of intense exposure to the drug there.

Adolescent↗

Epidemiology and effects of nematode infections on beef cow-calf systems of Argentina's western pampas.

The epidemiology and the effects of nematode infections on cow-calf systems were followed from 3 weeks before calving to 7 months afterwards. Two groups, each of 15 cow-calf pairs grazed on separate lucerne pastures. Group I (GI) were treated monthly with oxfendazole (4.5 mg kg-1), cows being dosed from calving and calves starting 45 days later. Animals in Group II (GII) were not treated. The egg output of the cows was very low. An increase was recorded 2 months after parturition, consisting mainly of Ostertagia spp. The egg output and worm burdens of calves remained low until late summer and reached a peak in autumn. Ostertagia, Cooperia and Haemonchus were the main genera recovered from slaughtered calves. The pasture contamination and tracer calf worm counts remained consistently low until autumn when they began to increase. Inhibited early fourth stage larvae of Ostertagia were recovered during spring. After calving, the live-weight gains (LWG) of treated GI cows were significantly higher (P less than 0.004) than those of GII cows, whereas the LWG of GI calves were significantly higher during December (P less than 0.037) and March (P less than 0.029) than those of GII calves. There were significant (P less than 0.04) cumulative LWG responses between GI and GII calves with no differences in cow cumulative LWG at the end of the trial. For spring-born calves, these results suggest that strategic deworming programs in cow-calf systems may produce benefits.

Animals↗

Farm history and breeding management influences on the intensity and specific diversity of nematode infection of dairy goats.

Sixteen dairy-goat farms were investigated in the centre-west of France for nematode infection. The intensity of infection was assessed by means of faecal egg counts and nematode counts at necropsy for digestive-tract nematodes and faecal larval counts for Muellerius capillaris. The specific diversity and prevalence were estimated by worm counts of 28 necropsied culled goats. The history and breeding management were recorded by means of a questionnaire. Specific diversity was estimated on two culled goats. Specific diversity and prevalence were related to the area of permanent pasture, age of farm, and to the number of goats introduced at the establishment of the farm. The most common species were Teladorsagia circumcincta and Trichostrongylus colubriformis. Teladorsagia trifurcata was absent from zero-grazing farms. Trichostrongylus vitrinus and Oesophagostomum venulosum were present in significant numbers on only one farm out of 16. The importance of Haemonchus contortus varied from farm to farm. The historical and breeding management factors that influenced the proportions of the most common species were the age of farm, size of flock, percentage of Alpine breed, duration of kidding period, age of goats and number of farms of origin. Age of farm and size of flock exerted opposing effects on the proportions of Teladorsagia circumcincta and Trichostrongylus colubriformis, respectively. The historical and breeding management factors were confounded and their respective effects on infection and the proportions of species was difficult to assess.

Animal Husbandry↗

Seasonal occurence of infective nematode larvae on irrigated pasture grazed by cattle in California.

During the period extending from Dec 1, 1975, to Dec 22, 1976, 3 distinct peaks in the concentration of infective nematode larvae on pasture forage were detected by use of helminth-free tracer calves. Two of these peaks, 1 occurring in the spring and 1 in the fall, consisted mainly of Ostertagia ostertagi and Cooperia sp. It is concluded that these 2 peaks can be anticipated annually and constitute unsafe periods of grazing. The 3rd peak was comprised largely of Haemonchus placei and Cooperia sp. It is concluded that this peak occurred as the result of unusual rainfall and reduced evaporation in August. Arrested developed (24% to 30%) of O ostertagi larvae occurred only during the spring peak. This finding indicates that on irrigated pastures in California, type I ostertagiasis can be expected to occur as the result of infection during the spring and/or fall peaks, whereas type II ostertagiasis can be expected to occur in the fall as a result of infection obtained during the spring peak. Arrestment in development of Cooperia sp occurred during spring (14%) and fall (23%) peaks. Haemonchus placei larvae increased their propensity for arrestment in development from zero to 82% during the months following the peak level of infection in summer. Other nematodes encountered were Trichostrongylus axei and Nematodirus helvetianus.

Animals↗

Discovery of quantitative trait loci for resistance to parasitic nematode infection in sheep: I. Analysis of outcross pedigrees.

BACKGROUND: Currently most pastoral farmers rely on anthelmintic drenches to control gastrointestinal parasitic nematodes in sheep. Resistance to anthelmintics is rapidly increasing in nematode populations such that on some farms none of the drench families are now completely effective. It is well established that host resistance to nematode infection is a moderately heritable trait. This study was undertaken to identify regions of the genome, quantitative trait loci (QTL) that contain genes affecting resistance to parasitic nematodes. RESULTS: Rams obtained from crossing nematode parasite resistant and susceptible selection lines were used to derive five large half-sib families comprising between 348 and 101 offspring per sire. Total offspring comprised 940 lambs. Extensive measurements for a range of parasite burden and immune function traits in all offspring allowed each lamb in each pedigree to be ranked for relative resistance to nematode parasites. Initially the 22 most resistant and 22 most susceptible progeny from each pedigree were used in a genome scan that used 203 microsatellite markers spread across all sheep autosomes. This study identified 9 chromosomes with regions showing sufficient linkage to warrant the genotyping of all offspring. After genotyping all offspring with markers covering Chromosomes 1, 3, 4, 5, 8, 12, 13, 22 and 23, the telomeric end of chromosome 8 was identified as having a significant QTL for parasite resistance as measured by the number of Trichostrongylus spp. adults in the abomasum and small intestine at the end of the second parasite challenge. Two further QTL for associated immune function traits of total serum IgE and T. colubiformis specific serum IgG, at the end of the second parasite challenge, were identified on chromosome 23. CONCLUSION: Despite parasite resistance being a moderately heritable trait, this large study was able to identify only a single significant QTL associated with it. The QTL concerned adult parasite burdens at the end of the second parasite challenge when the lambs were approximately 6 months old. Our failure to discover more QTL suggests that most of the genes controlling this trait are of relatively small effect. The large number of suggestive QTL discovered (more than one per family per trait than would be expected by chance) also supports this conclusion.

Animals↗

Prevalence of gastro-intestinal nematode infection in the dromedary camel (Camelus dromedarius) in the Butana plains, Sudan.

The prevalence and intensity of gastro-intestinal nematode infection in their relation to season and rainfall were investigated from 429 female dromedary camels at Tambul market in the Butana plains (Sudan), during 1985-1986. The investigation revealed a similar seasonal pattern in the prevalence as well as the intensity of egg output. The seasonality is mainly brought about by Haemonchus spp. and Impalaia spp. while Trichostrongylus spp. seem to be present as adults throughout the year. There is a good correlation between high egg counts and rainfall ensuring optimal development of preparasitic stages.

Animals↗

Nematode infections of the eye: toxocariasis, onchocerciasis, diffuse unilateral subacute neuroretinitis, and cysticercosis.

Nematode infections of the eye are common in different parts of the world, but some are usually encountered only in developing nations, such as onchocerciasis and cysticercosis. Ocular toxocariasis is a well-known cause of unilateral ocular disease affecting mainly children and young adults, and is usually caused by T canis. Prevention of ocular toxocariasis is based on such measures as appropriate health care for dogs and cats, including regular anthelmintic treatments, preventing contamination of the environment with feces, and promoting responsible pet ownership [1,49-51]. Onchocerciasis is caused by infection with the filarial parasite O volvulus, and occurs in endemic areas along rivers and streams. In hyperendemic areas almost every person is infected and about half of the population is eventually blinded by onchocerciasis. Because of this, elimination of host-vector contact is very important. DUSN is caused by a motile nematode and is found in the Southeastern and Midwestern United States and in many parts of the world. In Brazil, DUSN is becoming an important cause of posterior uveitis in children and young healthy adults. The destruction of the worm during the early stages of the disease can prevent progression of the visual loss. It is important to remain aware of this entity, not only in areas where it has been described, but also in regions not yet identified as being endemic [52]. Cysticercosis is caused by the encystment of the larvae of the tapeworm T solium, and usually results from ingesting eggs from food, water, or other material contaminated with human feces. Surgical removal of the cyst is usually indicated when possible.

Cysticercosis↗

Epidemiology and seasonal dynamics of gastrointestinal nematode infections of sheep in a semi-arid region of eastern Ethiopia.

A study on the epidemiology and seasonal dynamics of gastrointestinal nematode infections of sheep was carried out in a semi-arid region of eastern Ethiopia for 2.5 years (May 2003 to September 2005). The experimental flock comprised a total of 60 Black Head Ogaden sheep, consisting of four equal groups of young male and female and old male and female sheep. These grazed on communal pastures together with a larger university flock, as well as with animals owned by neighbouring small-holder farmers. A new experimental flock was established each year of the study. Parasitological data (EPG, faecal culture L3, PCV and FAMACHA estimates) and animal performance (weight change) were recorded each month on all experimental animals. In addition, four tracer lambs were assigned each month to the flock to determine the seasonal patterns of infective larvae acquired from pasture. Results showed distinct seasonal patterns associated with the bi-modal annual rainfall. High levels of infection occurred during the short and long rain seasons with peaks occurring in May and September of each year. Haemonchus contortus was the most prevalent parasite, followed by Trichostrongylus spp., with a number of other nematode species being occasionally recorded. H. contortus showed and increased propensity to undergo arrested development during the dry seasons. Correlations between EPG and PCV, EPG and FAMACHA eye scores, and PCV and FAMACHA eye scores were all highly significant (P<0.001). However, there was no significant association between the EPG and LW of the study animals during each study year. This information will provide a basis for developing epidemiologically based control strategies for gastrointestinal nematode parasites that are appropriate for flocks owned by small-holder farmers of semi-arid areas of eastern Ethiopia.

Age Factors↗

Impact of eprinomectin on grazing behaviour and performance in dairy cattle with sub-clinical gastrointestinal nematode infections under continuous stocking management.

Forty spring-calving cows and heifers (20 of each) were allowed to acquire infection with gastrointestinal (GI) nematodes naturally during grazing. The control group (10 cows and 10 heifers) were compared with 20 similar animals treated with eprinomectin in order to evaluate the effect of GI nematodes on grazing behaviour, milk production, body condition score and live weight. The animals were paired according to parity and milk yield during the week prior to treatment, then within replicate pair randomly allocated to a different treatment group. The grazing area was sub-divided into 20 replicated paddocks of equivalent size and topography. Grazing pairs of either control or treated animals were randomly assigned to each paddock over the duration of the study (one pair per paddock). Grazing behaviour was recorded for both groups over a 10-day period commencing 4 days after treatment with eprinomectin. Milk yield was recorded daily and milk quality was recorded weekly. Live weight and body condition score were recorded on the day of allocation, the day of initial treatment and thereafter at weekly intervals until the end of the 4-week trial. Faecal samples were collected from each animal prior to, and after, allocation and submitted for counts of nematode eggs. Additional faecal samples were taken at the end of the study for culture and nematode identification. Individual faecal samples were also analysed for residual digestibility. Pasture samples for nematode larval counts were taken at the same time as faecal sampling. The parasitological results showed low levels of faecal nematode egg output throughout the study, with the heifers having higher counts than the cows. Faecal culture yielded species of Ostertagia, Cooperia, and Trichostrongylus. Pasture larval levels were very low throughout with no value exceeding 68 larvae/kg dry matter (DM) of herbage. There were significant (P < 0.05) effects of treatment on grazing time, eating time, total bites, total grazing jaw movements (TGJM), idling time and mean meal duration. Treated cows and heifers grazed for 47 and 50 min longer per day, respectively, than controls (P = 0.016). Mean meal duration was extended as a result of anthelmintic treatment by 11 and 38 min, in cows and heifers, respectively (P = 0.012). There were no significant (P > 0.05) treatment effects on ruminating time or residual faecal digestibility, but idling time was significantly reduced in both treated cows and heifers, by 50 and 110 min, respectively (P = 0.010). In the treated cattle, there was an increase in solids-corrected milk yield compared with the control cattle, which was significant (P < 0.05) in weeks 2 and 3 after treatment. The response was particularly marked in heifers, where the difference in yield between treated and controls was up to 2.35 kg/day. The differences in live weight gain and condition score over 28 days post-treatment were significant (P < 0.05) in both cows and heifers, in favour of the treated animals.

Animal Husbandry↗

Potential for diagnosis of intestinal nematode infections through antibody detection in saliva.

The present study was the first to investigate the potential of saliva in community diagnosis of the major human intestinal nematode infections, Trichuris trichiura, Ascaris lumbricoides, and the hookworms. Immunoglobulin G (IgG) antibodies specific to parasite antigens were quantified in saliva samples of 187 individuals (all ages) from a St Lucian community, and 120 school-aged children from Tanga region, Tanzania, and relationships with current infection status (determined by numbers of parasite eggs in stool) were examined. For T. trichiura infection, the age relationships of parasite-specific salivary IgG antibodies mirrored those of infection intensity at the community level. Within both areas, children with current T. trichiura infection exhibited significantly higher anti-T. trichiura salivary IgG responses than uninfected children. Similar trends were apparent for A. lumbricoides and hookworm infections, though not to a level of statistical significance. Comparison of mean T. trichiura infection levels and antibody responses in age-matched children from St Lucia and Tanzania suggested that measurement of parasite-specific salivary IgG may have potential as a marker of transmission intensity at the community level.

Adolescent↗

The population dynamics of nematode infections of ruminants: the effect of seasonality in the free-living stages.

A previously published differential equation model for the dynamics of nematode infections of ruminants is modified to allow for time-dependent development and loss rates in the free-living stages. This converts the nonlinear autonomous system to one with periodic coefficients. Fourier transform methods are used to analyse the response of the modified system to these forced oscillations. For biologically reasonable parameter values, the annual pattern of parasitism is determined for the nonautonomous system, and compared with that for the autonomous system with periodic perturbations, and a system incorporating both effects. It is found that, whereas periodic perturbations due to management intervention determine the qualitative annual patterns of larval abundance and host infection, the seasonal dynamics of the larval stages change the magnitude of the adult worm burden.

Animals↗

The population dynamics of nematode infections of ruminants: periodic perturbations as a model for management.

We propose and analyse a model for the dynamics of directly transmitted nematode infections of ruminants which allows for the long-term effects of the annual removal of hosts. The model is a simple continuous-time formulation which captures the principal features of parasite transmission and the acquisition of immunity to infection by the host. Analysis of the simplest version of the model, which assumes a constant host population through time, indicates that its equilibrium is locally stable for feasible biological parameters. The regular removal of hosts involved in most management strategies is modelled in terms of periodic perturbations. The analysis indicates that the periodic removal of parasitized hosts corresponds effectively to a reduction in the basic reproductive rate of infection. We also demonstrate that the system exhibits a dramatic peak in parasite numbers during each grazing season at its dynamic equilibrium. This phenomenon (which is characteristically observed in real systems) is discussed in terms of the balance between acquired immunity and periodic perturbations of the parasite population.

Animals↗

Activation of caspases in intestinal villus epithelial cells of normal and nematode infected rats.

BACKGROUND: Small intestinal epithelial cells (IEC) show apoptosis in physiological turnover of cells and in certain inflammatory diseases. AIMS: To investigate the role of caspases in the progression of IEC apoptosis in vivo. METHODS: IEC were separated along the villus-crypt axis from the jejunum of normal and Nippostrongylus brasiliensis infected rats at 4 degrees C. Caspases were examined by a fluorometric assay method, histochemistry, and immunoblotting. RESULTS: Villus cell rich IEC from normal rats exhibited a high level of caspase-3-like activity whereas activities of caspase-1, -8, and -9 were negligible. Immunoblotting analysis of villus cell rich IEC revealed partial cleavage of procaspase-3 into a 17 kDa molecule as well as cleavage of a caspase-3 substrate, poly(ADP-ribose) polymerase (PARP), whereas in crypt cell rich IEC, caspase-3 cleavage was less significant. Caspase-3 activity was also observed histochemically in villus epithelium on frozen sections of the normal small intestine. IEC prepared at 4 degrees C did not reveal nuclear degradation whereas subsequent incubation in a suspension at 37 degrees C induced intense nuclear degradation within one hour in accordance with increases in active caspase-3. This apoptosis was partially suppressed by the caspase inhibitor Z-VAD-fmk. Nematode infected animals showed villus atrophy together with significant increases in levels of caspase-3 in IEC but not of caspase-1, -8, or -9. CONCLUSION: Caspase-3 may have an important role in the physiological replacement of IEC as well as in progression of IEC apoptosis induced by nematode infection.

Animals↗