Prevalence and distribution of pig helminths in the Dongting Lake Region (Hunan Province) of the People's Republic of China

The prevalence of helminths in pigs was investigated in five rural communities situated on the embankment of Dongting Lake in Zhiyang County, Hunan Province, People's Republic of China, in an area known to be endemic for Schistosoma japonicum. The helminth prevalences identified on the basis of faecal egg count analysis were: Oesophagostomum spp. (86.7%), Ascaris suum (36.7%), Metastrongylus spp. (25.8%), Strongyloides spp. (25.8%), Trichuris suis (15.8%), Globocephalus spp. (6.7%), Gnathostoma spp. (4.2%), Schistosoma japonicum (5.0%) and Fasciola spp. (1.3%). Post mortem examinations of a small number of pigs depositing eggs of different helminth species revealed the presence of Oesophagostomum dentatum, O. quadrispinulatum, A. suum, Metastrongylus apri, M. pudendotectus, T. suis, G. hispidum and Ascarops dentata. Prevalences of all helminths, with the exception of Oesophagostomum spp., were higher in young pigs (< 8 months old) compared with adult pigs. Prevalences of trematodes were very low, especially for S. japonicum which had decreased dramatically compared with previous reports from this area of P.R. China, whereas prevalences of nematodes were generally in agreement with those reported from other Yangtze River Provinces. Results from helminth prevalence studies in pigs, conducted in other provinces of P.R. China between 1987 and 1997, are presented and discussed. It was concluded that a government helminth control programme, implemented in 1995 to control S. japonicum infection in pigs in Hunan Province, may have resulted in a greatly reduced prevalence of S. japonicum in pigs in this region.     

Sequence variability in three mitochondrial genes between the two pig nodule worms Oesophagostomum dentatum and O. quadrispinulatum

In this study, sequence variation in three mitochondrial DNA regions, namely cytochrome c oxidase subunit (cox1) and NADH dehydrogenase subunits 1 and 4 (nad1 and nad4), between Oesophagostomum dentatum and O. quadrispinulatum isolated from pigs in different geographical origins in Mainland China was examined, and their phylogenetic relationships were reconstructed. A partial of the cox1 (pcox1), nad1, and nad4 genes (pnad1 and pnad4) were amplified separately from individual nodule worms by PCR and were subjected to direct sequencing in order to define sequence variations. While the intraspecific sequence variations within each of the two species were 0.3-5.2% for pcox1, 0-4.9% for pnad1, and 0-7.1% for pnad4, the interspecific sequence differences were significantly higher, being 10.7-13.4% for pcox1, 11-14.6% for pnad1, and 14.9-18% for pnad4, respectively. There were a number of nucleotide positions in the pcox1, pnad1, and pnad4 sequences with no apparent intraspecific variation but distinct interspecific differences among those samples of Oesophagostomum spp. examined, which may be used as genetic makers for the identification and differentiation of the Oesophagostomum spp. Phylogenetic analyses using three inference methods, namely Bayesian inference, maximum likelihood, and maximum parsimony based on the combined sequences of pcox1, pnad1, and pnad4 revealed that the O. dentatum and O. quadrispinulatum form monophyletic groups, respectively. These findings demonstrated clearly the usefulness of the three mitochondrial sequences for studying systematics, population genetic structures, and the molecular ecology of Oesophagostomum spp.     

Anthelmintic resistance: the state of play revisited

Helminthosis is one of the major constraints in the successful wool and mutton industry throughout the world. Anthelmintic Resistance (AR) is said to have been established when previously effective drug ceases to kill exposed parasitic population at the therapeutically recommended dosages. Anthelmintic resistance is almost cosmopolitan in distribution and it has been reported in almost all species of domestic animals and even in some parasites of human beings. Some of the most important species of parasites of small ruminants in which AR has been reported include: Haemonchus spp., Trichostrongylus spp. Teladorsagia spp., Cooperia spp. Nematodirus spp., and Oesophagostomum spp. All the major groups of anthelmintics have been reported for development of variable degrees of resistance in different species of gastrointestinal nematodes. This paper describes the global scenario of prevalence and methods used for detection of AR in small ruminants. Different mechanisms and contributory factors for the development of AR are discussed. Various options and alternate strategies for the control and/or delay in the onset of AR are suggested in the light of available information.     

Faecal egg output and herbage contamination with infective larvae of species of Ostertagia and Oesophagostomum from naturally infected farmed sika deer Cervus nippon in Lithuania

Faecal egg outputs and subsequent herbage larval contamination with third stage larvae (L3) of Ostertagia spp. and Oesophagostomum spp. from a herd of naturally infected sika deer Cervus nippon were examined in the same pasture in 2001/2002 in Lithuania. Sika deer were infected with Ostertagia circumcincta, O. kolchida, O. spiculoptera, Oesophagostomum radiatum, O. columbianum and O. venulosum. Faecal egg output in adult deer peaked in the spring during the periparturient period and also in late August, compared with a peak in egg output in calves during September to November. Herbage contamination with L3 of Ostertagia spp. peaked in June but larvae were not present on pastures from the end of September. Hence the highest risk of infection was in early born calves grazed on pastures in July. Infective larvae of Oesophagostomum spp. did not survive during the winter, but the nematodes were reintroduced onto the pastures by adult deer in the spring.     

Oesophagostomum infections in humans

Oesophagostomum spp are normally found as nematode parasites of ruminants, pig and monkeys. Occasionally humans are involved. In the past decade it became clear that, in some parts of Africa, humans are adequate final hosts. In those areas, prevalences of infection are high and morbidity is significant. The presence of lumen-dwelling adult worms, which do not seem to cause a great deal of pathology, can be demonstrated through coproculture. The presence of immature worms, encapsulated in nodules and responsible for pathology, on the other hand, is more difficult to confirm. It is not known what factors limit the distribution of endemic human oesophagostomiasis to a small focus in West Africa. The relationship between the 'helminthomas' described a long time ago in Uganda and the human Oesophagostomum infections in West Africa is unclear and it remains a mystery how humans get infected so effectively by ingesting L3 larvae. In this overview, Ton Polderman and Coby Blotkamp give an account of what is known and what is still to be elucidated in human Oesophagostomum infections.     

Morphological variability within Oesophagostomum bifurcum among different primate species from Ghana

Adult Oesophagostomum bifurcum (Nematoda: Strongylida) from human and non-human primates from Ghana were compared in order to investigate the extent of morphological variability within the species. Using analysis of variance and principal component analysis, significant differences in morphological characters (such as parasite length, width, length of the oesophagus and length of spicules) were demonstrated between O. bifurcum worms from humans, the Mona, Patas or Green monkey and/or Olive baboons. These findings suggest that O. bifurcum from different species of primate host represent distinct population variants, also supported by recent epidemiological and genetic studies of O. bifurcum from such hosts.     

Biology of mammalian Isospora

Isospora species are coccidial parasites that can cause serious disease in humans and pigs. Disease is observed less frequently in non-human primates, dogs or cats. Isospora species do not produce disease in horses, domestic ruminants or domestic poultry, and reports of isosporan oocysts in the feces of these hosts probably represents pseudoparasites that originated in feed or water contaminated with wild bird feces. David Lindsay and Byron Blagburn here summarize what is known about the biology of the Isospora species of domestic animals and non-human primates.     

Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self‐medication in wild apes influence disease progression?

Nodular worms (Oesophagostomum spp.) are common intestinal parasites found in cattle, pig, and primates including humans. In human, they are responsible for serious clinical disease called oesophagostomosis resulting from the formation of granulomas, caseous lesions or abscesses in intestinal walls. In wild great apes, the fecal prevalence of this parasite is high, but little information is available concerning the clinical signs and lesions associated. In the present study, we describe six cases of multinodular oesophagostomosis in free-ranging and ex-captive chimpanzees and captive gorillas caused by Oesophagostomum stephanostomum. While severe clinical signs associated with this infection were observed in great apes raised in sanctuaries, nodules found in wild chimpanzees do not seem to affect their health status. One hypothesis to explain this difference would be that in wild chimpanzees, access to natural environment and behavior such as rough leaves swallowing combined with ingestion of plants having pharmacological properties would prevent severe infection and decrease potential symptoms.     

Changes in antigen and glycoprotein patterns during the development of Oesophagostomum dentatum

During its development from free-living infectious third-stage larvae to the adult worms in the large intestines of pigs, Oesophagostomum dentatum experiences several environmental changes. Differences in protein patterns can reflect such changes. Somatic and ES antigens and glycoproteins of pre-parasitic, histotropic and intestinal stages were compared by single-dimension SDS–PAGE and stage-specific proteins were defined. Furthermore, fourth-stage larvae derived from different sources—in-vitro cultivation and intestinal contents—were compared and also found to be different. It is hypothesised that O. dentatum reacts to environmental stimuli by differential expression of specific proteins as a possible mode of adaptation to the host.     

Escherichia coli O157:H7 colonization in small domestic ruminants

Enterohaemorrhagic Escherichia coli O157:H7 was first implicated in human disease in the early 1980s, with ruminants cited as the primary reservoirs. Preliminary studies indicated cattle to be the sole source of E. coli O157:H7 outbreaks in humans; however, further epidemiological studies soon demonstrated that E. coli O157:H7 was widespread in other food sources and that a number of transmission routes existed. More recently, small domestic ruminants (sheep and goats) have emerged as important sources of E. coli O157:H7 human infection, particularly with the widespread popularity of petting farms and the increased use of sheep and goat food products, including unpasteurized cheeses. Although the colonization and persistence characteristics of E. coli O157:H7 in the bovine host have been studied intensively, this is not the case for small ruminants. Despite many similarities to the bovine host, the pathobiology of E. coli O157:H7 in small domestic ruminants does appear to differ significantly from that described in cattle. This review aims to critically review the current knowledge regarding colonization and persistence of E. coli O157:H7 in small domestic ruminants, including comparisons with the bovine host where appropriate.     

Cryptosporidial infections in captive wild animals

Neonatal diarrhea was an important cause of morbidity and mortality in a hand-rearing facility for exotic ruminants at the San Diego Wild Animal Park. Studies undertaken to determine the causes of the problem revealed that oocysts of Cryptosporidium sp. were demonstrable in auramine O stained fecal smears from 52 of 183 (28.4%) animals examined. Cryptosporidial infection was identified in 21 of 40 species of exotic ruminants with diarrhea. In addition, cryptosporidia were associated with gastroenteric disease in two primates and two reptiles. It was observed also that auramine O stained coccidial oocysts of the genus Eimeria, which were present in five of 183 (2.7%) of the specimens examined.     

The prevalence and diversity of intestinal parasitic infections in humans and domestic animals in a rural Cambodian village

In Cambodia, intestinal parasitic infections are prevalent in humans and particularly in children. Yet, information on potentially zoonotic parasites in animal reservoir hosts is lacking. In May 2012, faecal samples from 218 humans, 94 dogs and 76 pigs were collected from 67 households in Dong village, Preah Vihear province, Cambodia. Faecal samples were examined microscopically using sodium nitrate and zinc sulphate flotation methods, the Baermann method, Koga Agar plate culture, formalin-ether concentration technique and Kato Katz technique. PCR was used to confirm hookworm, Ascaris spp., Giardia spp. and Blastocystis spp. Major gastrointestinal parasitic infections found in humans included hookworms (63.3%), Entamoeba spp. (27.1%) and Strongyloides stercoralis (24.3%). In dogs, hookworm (80.8%), Spirometra spp. (21.3%) and Strongyloides spp. (14.9%) were most commonly detected and in pigs Isospora suis (75.0%), Oesophagostomum spp. (73.7%) and Entamoeba spp. (31.6%) were found. Eleven parasite species were detected in dogs (eight helminths and three protozoa), seven of which have zoonotic potential, including hookworm, Strongyloides spp., Trichuris spp., Toxocara canis, Echinostoma spp., Giardia duodenalis and Entamoeba spp. Five of the parasite species detected in pigs also have zoonotic potential, including Ascaris spp., Trichuris spp., Capillaria spp., Balantidium coli and Entamoeba spp. Further molecular epidemiological studies will aid characterisation of parasite species and genotypes and allow further insight into the potential for zoonotic cross transmission of parasites in this community.     

The incidence, pathogenesis and treatment of helminth infections in rhesus monkeys (Macaca mulatta).

In a survey of 259 newly-imported rhesus monkeys, 5 species of nematode parasites were commonly found. Of these 5 species, Oesophagostomum spp. and Strongyloides fulleborni were implicated in the deaths of 3 monkeys. 5 other nematode species, 2 cestode species and 1 trematode species were also found; their pathogenicity is discussed. The results of treatment of parasitic infections with 6 different drugs is reported. Thiabendazole at an initial dose of 100 or 133 mg/kg and repeated at 50 mg/kg was found to be the most effective treatment against Oesophagostomum spp.     

Molecular Investigation and Phylogeny of Anaplasma spp. in Mediterranean Ruminants Reveal the Presence of Neutrophil-Tropic Strains Closely Related to A. platys

Few data are available on the prevalence and molecular typing of species belonging to the genus Anaplasma in Mediterranean ruminants. In this study, PCR analysis and sequencing of both 16S rRNA and groEL genes were combined to investigate the presence, prevalence, and molecular traits of Anaplasma spp. in ruminants sampled on the Island of Sardinia, chosen as a subtropical representative area. The results demonstrate a high prevalence of Anaplasma spp. in ruminants, with animals infected by at least four of six Anaplasma species (Anaplasma marginale, A. bovis, A. ovis, and A. phagocytophilum). Moreover, ruminants host a number of neutrophil-tropic strains genetically closely related to the canine pathogen A. platys. The high Anaplasma spp. prevalence and the identification of as-yet-unclassified neutrophil-tropic strains raise concerns about the specificity of serological tests routinely used in ruminants and provide additional background for reconstructing the evolutionary history of species genetically related to A. phagocytophilum.     

Self-induced Increase of Gut Motility and the Control of Parasitic Infections in Wild Chimpanzees

When physiological adaptation is insufficient, hosts have developed behavioral responses to avoid or limit contact with parasites. One such behavior, leaf-swallowing, occurs widely among the African great apes. This behavior involves the slow and deliberate swallowing without chewing of whole bristly leaves. Folded one at a time between tongue and palate, the leaves pass through the gastro-intestinal (GI) tract visibly unchanged. Independent studies in two populations of chimpanzees (Pan troglodytes schweinfurthii) showed significant correlations between the swallowing of whole leaves and the expulsion of the nodule worm Oesophagostomum stephanostomum and a species of tapeworm (Bertiella studeri). We integrate behavioral, parasitological and physiological observations pertaining to leaf-swallowing to elucidate the behavioral mechanism responsible for the expulsion and control of nodule worm infections by the ape host. Physical irritation produced by bristly leaves swallowed on an empty stomach, increases motility and secretion resulting in diarrhea which rapidly moves leaves through the GI tract. In the proximal hindgut, the site of third-stage larvae (L3) cyst formation and adult worm attachment, motility, secretion and the scouring effect of rough leaves is enhanced by haustral contractions and peristalsis-antiperistalsis. Frequently, at the peak of reinfection, a proportion of nonencysted L3 is also predictably vulnerable. These factors should result in the disruption of the life cycle of Oesophagostomum spp. Repeated flushing during peak periods of reinfection is probably responsible for long-run reduction of worm burdens at certain times of the year. Accordingly, leaf-swallowing can be viewed as a deliberate adaptive behavioral strategy with physiological consequences for the host. The expulsion of worms based on the activation of basic physiological responses in the host is a novel hitherto undescribed form of parasitic control.     

Babesia spp. identified by PCR in ticks collected from domestic and wild ruminants in southern Switzerland

Concurrent infections with vector-borne pathogens affected a cattle herd in Switzerland, and one of the pathogens was identified as Babesia bigemina, which had never been observed in this country before. Therefore, a survey of the occurrence of ruminant Babesia spp. and their tick vectors in Switzerland was conducted. A total of 2,017 ticks were collected from sheep, goats, cattle, and wild ruminants (deer, roe deer, and chamois) in southern parts of Switzerland and identified morphologically. The vast majority of the ticks (99.2%) were Ixodes ricinus, but 14 ticks from sheep and goats were identified as Dermacentor marginatus and two ticks from wild ruminants were identified as Hemaphysalis punctata. PCR analyses of 700 ticks revealed the presence of Babesia divergens (n = 6), Babesia sp. genotype EU1 (n = 14), and B. major (n = 2), whose suggested occurrence was confirmed in this study by molecular analysis, and the presence of novel Babesia sp. genotype CH1 (n = 4), which is closely related to B. odocoilei and to Babesia sp. genotype RD61 reported from North America. The identification of B. divergens and B. major in ticks collected from wild ruminants cast doubt on the postulated strict host specificity of these bovine Babesia species. Furthermore, the zoonotic Babesia sp. genotype EU1 was detected in ticks collected from domestic animals but was obtained predominantly from ticks collected from wild ruminants. More than one tick containing DNA of different Babesia spp. were collected from two red deer. Hence, the role of these game animals as reservoir hosts of Babesia spp. seems to be important but requires further investigation.     

Rapid evolution of a primate sperm protein: relaxation of functional constraint or positive Darwinian selection?

Protamines are arginine-rich proteins that replace histones and bind sperm DNA during spermatogenesis in vertebrates. Previous studies have shown that protamine exons evolve faster than does the protamine intron. It has been suggested that this is a result of a relaxation of functional constraint. However, a more likely explanation is that the evolutionary rate of exons has been accelerated by positive Darwinian selection, because introns are generally believed to evolve in a neutral fashion. Therefore, we examined the possibility that positive selection has been acting on the protamine genes of three groups of placental mammals: primates (hominoids and Old World monkeys), rodents (mice, rats, and guinea pigs), and pecoran ruminants (deer and bovids). We found that the nucleotide substitution rate at nonsynonymous sites is significantly higher than the rate at synonymous and intron sites for protamine P1 of hominoids and Old World monkeys. This result suggests that positive selection has been operating on protamine P1 of these species. In contrast, no clear-cut evidence of positive selection was found for protamine P1 of ruminants and rodents or protamine P2 of primates. The agent of positive selection on primate protamine P1 remains unknown, though sperm competition is a possibility. Further investigations on the function and intraspecific polymorphism of this protein are needed in order to identify the selection agent.     

Molecular characterization of nodule worm in a community of Bornean primates

Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates’ home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross‐species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum, the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.     

Materno-foetal exchanges and utilisation of nutrients by the foetus: comparison between species

Several general features of nutrient uptake and utilisation by foetuses are similar among mammalian species. Nevertheless, there are also differences linked mainly to differences in placental permeability. Glucose and lactate are the main energetic substrates of the foetus. In normal conditions, the oxidation of carbohydrates accounts for about 75, 60 and 50% of oxygen uptake in the foetal pig, foal and lamb, respectively, and acetate accounts for about 10% in ruminants. Acidic amino acids are synthesised by the foetus, whereas neutral and basic amino acids are transported from the placenta. As shown by the high urea level in foetal blood, amino acids are partly involved in the oxidative metabolism of foetuses; their contribution is higher in ruminants than in humans, horses and pigs. Fatty acids cross the haemochorial placenta of rodents, rabbits and primates, and are incorporated into the foetal lipids, whereas their uptake by ruminant, pig and horse foetuses is very low.     

A Study on the Transmission of Oesophagostomum dentatum and Hyostrongylus rubidus among Outdoor Reared Pigs in Denmark

This study was carried out to obtain basic information on the transmission of Oesophagostomum dentatum and Hyostrongylus rubidus in outdoor reared pigs in Denmark. Eighteen 10 weeks old worm-free pigs were allocated into 3 groups of 6 pigs each. In May, all pigs were turned out on the same parasitologi-cally naive pasture, and after 2 weeks the pigs in groups 2 and 3 were experimentally infected with 10,800 O. dentatum and 8,700 H. rubidus infective larvae, respectively. Pigs in group 1 served as non-infected controls. All pigs were reared together on the experimental pasture for further 134 days until slaughter in October. Strongyle egg counts, differentiation of infective larvae at species level, serum pepsinogen, and herbage larval infectivity were monitored at regular intervals throughout. Both strongyle species established in the originally parasite-free pigs (group 1) and cross infections were established in group 2 and 3. The pigs were exposed to steadily increasing herbage infectivity of both species of strongyles. At the end of the experiment, geometric mean worm burdens of O. dentatum in groups 1,2 and 3 were 1202, 6136 and 1431 respectively, the burden in group 2 being significantly higher (p<0.05) than that of the 2 other groups. The geometric mean worm burdens of H. rubidus in groups 1, 2 and 3 were 4907, 3679 and 5246 respectively, showing no significant differences between groups.