Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures.

Gastrointestinal nematodes threaten the productivity of grazing livestock and anthelmintic resistance has emerged globally. It is broadly understood that wild ruminants living in sympatry with livestock act as a positive source of refugia for anthelmintic-susceptible nematodes. However, they might also act as reservoirs of anthelmintic-resistant nematodes, contributing to the spread of anthelmintic resistance at a regional scale. Here, we sampled managed sheep and cattle together with feral goats within the same property in New South Wales, Australia. Internal transcribed spacer 2 (ITS-2) nemabiome metabarcoding identified 12 gastrointestinal nematodes (Cooperia oncophora, Cooperia punctata, Haemonchus contortus, Haemonchus placei, Nematodirus spathiger, Ostertagia ostertagi, Teladorsagia circumcincta, Oesophagostomum radiatum, Oesophagostomum venulosum, Trichostrongylus axei, Trichostrongylus colubriformis and Trichostrongylus rugatus). Isotype-1 ß-tubulin metabarcoding targeting benzimidazole resistance polymorphisms identified 6 of these nematode species (C. oncophora, C. punctata, H. contortus, H. placei, O. ostertagi and T. circumcincta), with the remaining 3 genera unable to be identified to the species level (Nematodirus, Oesophagostomum, Trichostrongylus). Both ITS-2 and ß-tubulin metabarcoding showed the presence of a cryptic species of T. circumcincta, known from domestic goats in France. Of the gastrointestinal nematodes detected via ß-tubulin metabarcoding, H. contortus, T. circumcincta, Nematodirus and Trichostrongylus exhibited the presence of at least one resistance genotype. We found that generalist gastrointestinal nematodes in untreated feral goats had a similarly high frequency of the benzimidazole-resistant F200Y polymorphism as those nematodes in sheep and cattle. This suggests cross-transmission and maintenance of the resistant genotype within the wild ruminant population, affirming that wild ruminants should be considered potential reservoirs of anthelmintic resistance.

Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon.

BACKGROUND: Zoonotic diseases are a serious threat to both public health and animal conservation. Most non-human primates (NHP) are facing the threat of forest loss and fragmentation and are increasingly living in closer spatial proximity to humans. Humans are infected with soil-transmitted helminths (STH) at a high prevalence, and bidirectional infection with NHP has been observed. The aim of this study was to determine the prevalence, genetic diversity, distribution and presence of co-infections of STH in free-ranging gorillas, chimpanzees and other NHP species, and to determine the potential role of these NHP as reservoir hosts contributing to the environmental sustenance of zoonotic nematode infections in forested areas of Cameroon and Gabon. METHODS: A total of 315 faecal samples from six species of NHPs were analysed. We performed PCR amplification, sequencing and maximum likelihood analysis of DNA fragments of the internal transcribed spacer 2 (ITS2) nuclear ribosomal DNA to detect the presence and determine the genetic diversity of Oesophagostomum spp., Necator spp. and Trichuris spp., and of targeted DNA fragments of the internal transcribed spacer 1 (ITS1) to detect the presence of Ascaris spp. RESULTS: Necator spp. infections were most common in gorillas (35 of 65 individuals), but also present in chimpanzees (100 of 222 individuals) and in one of four samples from greater spot-nosed monkeys. These clustered with previously described type II and III Necator spp. Gorillas were also the most infected NHP with Oesophagostomum (51/65 individuals), followed by chimpanzees (157/222 individuals), mandrills (8/12 samples) and mangabeys (7/12 samples), with O. stephanostomum being the most prevalent species. Oesophagostomum bifurcum was detected in chimpanzees and a red-capped mangabey, and a non-classified Oesophagostomum species was detected in a mandrill and a red-capped mangabey. In addition, Ternidens deminutus was detected in samples from one chimpanzee and three greater spot-nosed monkeys. A significant relative overabundance of co-infections with Necator and Oesophagostomum was observed in chimpanzees and gorillas. Trichuris sp. was detected at low prevalence in a gorilla, a chimpanzee and a greater spot-nosed monkey. No Ascaris was observed in any of the samples analysed. CONCLUSIONS: Our results on STH prevalence and genetic diversity in NHP from Cameroon and Gabon corroborate those obtained from other wild NHP populations in other African countries. Future research should focus on better identifying, at a molecular level, the species of Necator and Oesophagostomum infecting NHP and determining how human populations may be affected by increased proximity resulting from encroachment into sylvatic STH reservoir habitats.

Trophic relationship between the Patinga hybrid (Piaractus mesopotamicus x Piaractus brachypomus) and Echinorhynchus gomesi Machado Filho, 1948 in fish farms.

A total of 122 Patinga specimens were collected from fish farms (P1, P2 and P3), and only those from fish farm P1 were shown to be infected with Echinorhynchus gomesi. In addition, fish in this study were shown to have diets that consisted of 21 different food items, and Notodiaptomus sp. (Copepoda: Calanoida) was identified as a potential intermediate host for E. gomesi.

Protozoan and Helminth Infections of Aviary-Reared Alectoris rufa (Galliformes: Phasianidae) before Releasing for Hunting in the Czech Republic: Infection Dynamics and Potential Risks.

Age-related dynamics of protozoan and helminth infections in the red-legged partridge, Alectoris rufa, were studied in an intensive breeding aviary in the Czech Republic before releasing birds for hunting purposes. Pooled fecal samples (n = 900) were examined over 3 rearing seasons (2012-2014). A total of 4 protozoan species, Cryptosporidium baileyi, Cryptosporidium meleagridis, Eimeria kofoidi, and Eimeria legionensis, and 4 helminths, Capillaria phasianina, Eucoleus perforans, Heterakis gallinarum, and Syngamus trachea, was found. The most common parasite was S. trachea (prevalence 20-26%) in dead birds (n = 99), which represents a high risk for breeders. Co-occurrence of protozoans and helminths indicated similarities in infection dynamics throughout the 3 breeding seasons. Mixed infections of Cryptosporidium baileyi and C. meleagridis with other parasitic species are reported for the first time. Our findings provide new insights into breeding of A. rufa and may help to improve the efficacy of disease control strategies and prevention, especially with the potential for spreading of parasitic infections to wildlife through released birds into open areas.

Alien parasitic infections in the endangered Ryukyu long-furred rat (Diplothrix legata) on Amami-Oshima Island, Japan.

There is limited knowledge about parasites of the endangered Ryukyu long-furred rat, Diplothrix legata (Murinae, Rodentia) endemic to Okinawa, Tokunoshima, and Amami-Oshima Islands in Japan. In the present study, postmortem histopathological examination of an individual found on Amami-Oshima Island revealed a mixed helminth infection of Calodium hepaticum, Hydatigera taeniaeformis, and Angiostrongylus cantonensis. These helminths are considered non-native to Amami-Oshima Island and are maintained by invasive mammals, such as non-native rats and outdoor cats. This observation presents a new host record for C. hepaticum and H. taeniaeformis and the first record of A. cantonensis in Ryukyu long-furred rat on Amami-Oshima Island.

Ungulate Helminth Transmission and Two Evolutionary Puzzles.

Grazing mammals, ungulates, pose two evolutionary puzzles as helminth hosts. First, why do some helminths infect intermediate hosts prior to infecting ungulates, given that grazers could directly consume propagules on vegetation? Second, ungulates are large and long-lived, so why are they occasionally intermediate instead of definitive hosts, as in taeniid cestodes? We comprehensively surveyed helminth life cycles and transmission involving ungulates. We identified six transmission routes and found that ungulate helminth parasitism has evolved some 25 times. Direct egg transmission to ungulates is rare, and we suggest this is due to a transmission barrier caused by ungulate faecal avoidance. Our survey confirmed that ungulates are almost always definitive hosts, and we discuss the exceptional cases when they are not.

Egg fibrils and transmission in the acanthocephalan Acanthocephalus dirus.

Acanthocephalans have multi-host life cycles that include arthropods as intermediate hosts and vertebrates as definitive hosts. Eggs are dispersed into the habitat from definitive hosts and in some species eggs possess fibrils, which have been proposed to facilitate transmission to intermediate hosts. We examined the potential role of fibrils in transmission of the acanthocephalan Acanthocephalus dirus to its intermediate host Caecidotea intermedius, a stream-dwelling isopod. We identify three properties of fibrils that could favor transmission. First, there was a slow rate of fibril release, which was dependent on the actions of stream microorganisms. Second, eggs with fibrils were more likely to adhere to the substrate than those without fibrils. Third, in feeding trials, isopods exposed to eggs with fibrils had a higher infection prevalence than isopods exposed to eggs without fibrils. These properties could favor transmission by increasing the likelihood that eggs sink to the sediment occupied by their target hosts before adhering to items on the substrate (e.g., leaves) and by increasing recruitment after the eggs have been consumed.

Long-Tailed Macaques (Macaca fascicularis) in Urban Landscapes: Gastrointestinal Parasitism and Barriers for Healthy Coexistence in Northeast Thailand.

Gastrointestinal parasites have diverse life cycles that can involve people, animals, and the environment (e.g., water and soil), demonstrating the utility of One Health frameworks in characterizing infection risk. Kosumpee Forest Park (Thailand) is home to a dense population of long-tailed macaques (Macaca fascicularis) that frequently interact with tourists and local residents. Our study investigated the presence of zoonotic parasites, and barriers to healthy coexistence by conducting stool analysis on macaques (N = 102) and people (N = 115), and by examining risk factors for infection with a household questionnaire (N = 95). Overall, 44% of macaques and 12% of people were infected with one or more gastrointestinal helminths, including Strongyloides spp., Ascaris spp., and Trichuris sp. An adults-only generalized linear mixed model identified three factors significantly associated with human infection: household size, occupational exposure, and contact with macaque feces at home. Participants identified both advantages and disadvantages to living in close contact with macaques, suggesting that interventions to improve human and animal health in Kosumpee Forest Park would be welcome.

Transmission of Corynosoma australe (Acanthocephala: Polymorphidae) from fishes to South American sea lions Otaria flavescens in Patagonia, Argentina.

Acanthocephalans display a two-host life cycle that involves arthropods as intermediate hosts and vertebrates as definitive hosts. Some species also use paratenic hosts to bridge the trophic gap between both obligatory hosts. However, the relative role of these paratenic hosts in the transmission to definitive hosts has seldom been assessed quantitatively. We report on infection patterns of cystacanths of Corynosoma australe Johnston, 1937 in 20 common teleost species and the Argentine shortfin squid Illex argentinus (Castellanos) from the Patagonian shelf of Argentina. We also explore the role of different fish species in the transmission of C. australe to the most important definitive host in the area, i.e. the South American sea lion Otaria flavescens Shaw. Cystacanths of C. australe were found in all host species except Heliconus lahillei Norman, Merluccius hubbsi Marini and I. argentinus. In eight fish species, the prevalence of C. australe was > 50% and mean intensity > 4, i.e. Acanthistius patachonicus (Jenyns), Nemadactylus bergi (Norman), Paralichthys isosceles Jordan, Percophis brasiliensis Quoy & Gaimard, Prionotus nudigula Ginsburg, Scomber colias Gmelin, Raneya brasiliensis (Kaup) and Xystreurys rasile (Jordan). Two surveys on the trophic ecology of South American sea lions in the study area consistently found a generalist diet dominated by M. hubbsi, and data on the frequency of occurrence and number of other fish and cephalopod species in stomach contents strongly suggest that only R. brasiliensis may play a prominent role in the transmission of C. australe. This result raises interesting questions on the costs of paratenicity.

Goats worm burden variability also results from non-homogeneous larval intake.

For small ruminants, Gastrointestinal Nematodes (GINs) are responsible for severe economic losses and they are also an animal welfare problem. GIN use their host to reproduce and disperse eggs on the pasture, from where they can re-infect another animal. The high density of hosts on the pasture and the extreme tolerance of GIN to environmental constraints make GIN eradication almost impossible. In addition, significant resistance to anthelmintic treatment requires sustainable and integrated management to maintain the health and financial well-being of livestock farming. In this context, models of the complex interactions between host, GIN and environment can help us to design long term optimal management strategies. To build such models, quantitative information is needed but are generally very challenging to collect. In this article, we focus on the number of ingested larvae per animal, which we propose to characterise by using a simulation framework based on the estimation of the spatial distribution of the host over time. Our framework allows us to show that worm burden individual variation is not only explained by the host's genetics, as is often the case, but is also a result of the grazing spatial process.

First survey on zoonotic helminthosis in urban brown rats (Rattus norvegicus) in Spain and associated public health considerations.

The brown rat, Rattus norvegicus, with a worldwide distribution, is the most commensal species among synanthropic rodents, since its main habitat, in urban as well as in rural areas, is always linked to humans. Therefore, people living in close proximity to rodent populations can be exposed to infection. Whereas bacteria and viruses are the best known rat-associated zoonoses in urban environments, the role of brown rats as reservoirs for helminth parasites and the associated risk for humans are less well known. Specifically, this role has not been analyzed in Spain to date. A total of 100 R. norvegicus trapped in the sewage system (n = 85), and parks (n = 15) of Barcelona was examined. The overall prevalence of helminth infection was 85%. The helminths found were Hymenolepis nana (17%), H. diminuta (33%) (Cestoda), Calodium hepaticum (17%), Eucoleus gastricus (28%), Aonchotheca annulosa (12%), Trichosomoides crassicauda (7%), Nippostrongylus brasiliensis (46%), Heterakis spumosa (62%), Gongylonema neoplasticum (20%) (Nematoda) and Moniliformis moniliformis (6%) (Acanthocephala). Five of the ten helminth species are considered zoonotic parasites, with rats acting as reservoirs for human infection, i.e. H. nana, H. diminuta, C. hepaticum, G. neoplasticum and M. moniliformis. G. neoplasticum and M. moniliformis are reported for the first time in urban rats in Europe. H. nana, H. diminuta and C. hepaticum are the most widespread species in European cities. For H. nana and C. hepaticum, rats act as effective spreaders of the human infective stage (eggs). For H. diminuta, G. neoplasticum and M. moniliformis, rats act as indirect reservoirs of the zoonoses since the eggs shed by the rats are infective for their insect intermediate hosts only. Medical practitioners need to be made aware of the range of parasites carried by rats, as there is a realistic likelihood that ill health currently caused by rat infestations may be misdiagnosed.

Control of helminth ruminant infections by 2030.

Helminth infections have large negative impacts on production efficiency in ruminant farming systems worldwide, and their effective management is essential if livestock production is to increase to meet future human needs for dietary protein. The control of helminths relies heavily on routine use of chemotherapeutics, but this approach is unsustainable as resistance to anthelmintic drugs is widespread and increasing. At the same time, infection patterns are being altered by changes in climate, land-use and farming practices. Future farms will need to adopt more efficient, robust and sustainable control methods, integrating ongoing scientific advances. Here, we present a vision of helminth control in farmed ruminants by 2030, bringing to bear progress in: (1) diagnostic tools, (2) innovative control approaches based on vaccines and selective breeding, (3) anthelmintics, by sustainable use of existing products and potentially new compounds, and (4) rational integration of future control practices. In this review, we identify the technical advances that we believe will place new tools in the hands of animal health decision makers in 2030, to enhance their options for control and allow them to achieve a more integrated and sustainable approach to helminth control in support of animal welfare and production.

The helminth community of a population of Rattus norvegicus from an urban Brazilian slum and the threat of zoonotic diseases.

Urban slums provide suitable conditions for infestation by rats, which harbour and shed a wide diversity of zoonotic pathogens including helminths. We aimed to identify risk factors associated with the probability and intensity of infection of helminths of the digestive tract in an urban slum population of Rattus norvegicus. Among 299 rats, eleven species/groups of helminths were identified, of which Strongyloides sp., Nippostrongylus brasiliensis and, the human pathogen, Angiostrongylus cantonensis were the most frequent (97, 41 and 39%, respectively). Sex interactions highlighted behavioural differences between males and females, as eg males were more likely to be infected with N. brasiliensis where rat signs were present, and males presented more intense infections of Strongyloides sp. Moreover, rats in poor body condition had higher intensities of N. brasiliensis. We describe a high global richness of parasites in R. norvegicus, including five species known to cause disease in humans. Among these, A. cantonensis was found in high prevalence and it was ubiquitous in the study area - knowledge which is of public health importance. A variety of environmental, demographic and body condition variables were associated with helminth species infection of rats, suggesting a comparable variety of risk factors for humans.

Mass Mortality Attributed to Acanthocephaliasis at a Gull-billed Tern (Gelochelidon nilotica) Colony in Coastal California, USA.

From 12 May 2013 to 29 May 2013, the Gull-billed Tern (Gelochelidon nilotica) colony at the San Diego Bay National Wildlife Refuge, California, US, experienced a mass die-off of at least 92 adults, representing 71-92% of the breeding population on the US west coast. Cause of death was determined to be peritonitis due to perforations of the intestine by a large quantity of acanthocephala (Profilicollis [=Polymorphus] altmani). This is a unique report of P. altmani infecting G. nilotica, and a report of a great impact to a tern population in southern California. Mole crabs (Emerita analoga), the intermediate host for P. altmani and a major component of the Gull-billed Tern diet in San Diego, were found in the stomachs of necropsied terns along with cystacanths, and are the presumed source of the parasite infection. The tern's dietary reliance upon mole crabs likely amplified parasite transmission and infection. We suggest additional research to determine factors that influence parasite infection of intermediate and definitive hosts, particularly mole crabs, given that they are a vital resource for migrating birds within the coastal zone.

Vector-Borne Pathogens in Stray Dogs in Northeastern Turkey.

This experiment was carried out to attain prevalence and molecular characterization of pathogens causing canine vector-borne diseases (CVBDs) including babesiosis, hepatozoonosis, leishmaniasis, filariosis (Dirofilaria immitis, Dirofilaria repens, and Acanthocheilonema reconditum), ehrlichiosis (Ehrlichia canis), and anaplasmosis (Anaplasma platys) in stray dogs. The study material consisted of 133 asymptomatic female (n = 96) and male (n = 37) stray dogs (≤1 year old, n = 16 and 1-6 years old, n = 117) housed in the Animal Care and Rehabilitation Center, Erzurum, Northeastern Turkey. Conventional and nested PCR were performed on blood samples to detect Babesia spp., Leishmania spp., Hepatozoon spp., D. immitis, D. repens, A. reconditum, E. canis, and A. platys. Sex and age association with the pathogen prevalence was determined using X2 statistics. The positivity rate for at least one CVBD pathogen was 48.9% (65/133). DNA of B. canis, Hepatozoon spp., H. canis, D. immitis, and E. canis were detected in 5.3% (7/133), 27.1% (36/133), 5.3% (7/133), 1.5% (2/133), and 9.8% (13/133) of the dogs, respectively. Leishmania spp., D. repens, A. reconditum, and A. platys DNA were not detected. Mixed pathogens were determined in seven (10.8%) of the infected dogs, with predominant involvement of Hepatozoon spp. or H. canis. The pathogen prevalence did not vary by sex or age. Nucleotide blast analysis of Erzurum isolates showed 99.8-100% identities with the corresponding reference isolates. This study indicates presence of five CVB pathogens, including the first report of E. canis, in stray dogs in Erzurum, Turkey.

The role of domestic dogs in the transmission of zoonotic helminthes in a rural area of Mekong river basin.

Dogs have been bred since ancient times for companionship, hunting, protection, shepherding and other human activities. Some canine helminth parasites can cause significant clinical diseases in humans as Opisthorchis viverrini causing cholangiocarcinoma in Southeast Asian Countries. In this study, socio-cultural questionnaire, canine parasitological analysis, necropsy, parasite molecular confirmation and dog roaming data were evaluated in Savannakhet, Lao-PDR, a typical Mekong Basin area. Dog owners comprised 48.8% of the studied population, with 61.2% owning one dog, 25.1% 2 dogs, 8.5% 3 dogs and 1.8% owning more than 4 dogs. Data from GPS logger attached to dogs showed they walked from 1.4 to 13.3 km per day, covering an area of 3356.38m2 average, with a routine of accessing water sources. Thirteen zoonotic helminth species were observed. Causative agents of visceral and cutaneous larva migrans occurred in 44.1% and 70% of the samples respectively. Spirometra erinaceieuropaei was detected in 44.1% of samples. Importantly, O. viverrini was found in 8.8% of samples. Besides the known importance of dogs in the transmission of Ancylostoma spp., Toxocara spp. and S. erinaceieuropaei, the observed roaming pattern of dogs confirmed it as an important host perpetuating O. viverrini in endemic areas; their routine access to waterbodies may spread O. viverrini eggs in a favorable environment for the fluke development, facilitating the infection of fishes, and consequently infecting humans living in the same ecosystem. Therefore, parasitic NTDs control programs in humans should be done in parallel with parasite control in animals, especially dogs, in the Mekong River basin area.

[Infection of the pacific saury Cololabis saira by acanthocephalans in the Kuril Islands area].

The Pacific saury Cololabis saira (Brevoort, 1856) is one of the important target species of commercial fisheries. Food manufacturers and consumers encounter problems due to the infection of the saury by acanthocephalans, which are quite difficult to clean out completely during on-board catch processing. Infection of C. saira was not studied on a regular basis, therefore, our knowledge about the parasites of saury is fragmentary. This paper contains infection indices (only acanthocephalans) of the Pacific saury caught in the Kuril Islands area (Russian Exclusive Economic Zone) in 2015.

Epidemiological survey of zoonotic helminths in feral cats in Gran Canaria island (Macaronesian archipelago-Spain).

The presence of zoonotic parasites in feral cats have been widely considered all over the world. In Gran Canaria (Macaronesian archipelago, Canary Islands, Spain) the number of feral cats has grown out of control in urban and rural areas. 48 of Felis catus captured in different Gran Canaria areas were studied. Animals were necropsied and several organs were systematically examined in order to collect and identify macroscopic parasites. In addition, coprological tests were done in 28 cats. There were no statistically significant differences in the prevalence rate among sex, age or capture area, showing an overall prevalence of helminths of 77.1%. The most common tapeworms were Dipylidium caninum (64.6%) and Taenia taeniaeformis (31.3%), followed by the nematodes Toxocara cati (20.8%), Ancylostoma tubaeforme (18.8%), Aelurostrongylusabstrusus (10.4%) and Trichuris vulpis (2.08%). We also find several eggs of Alaria alata in the small intestine of one cat (2.08%), being the first description of this trematode in cats in the Canary Islands. Aproximatelly, 40% of the studied cats harboured more than one parasite. High rates of zoonotic species found in these animals suggest the need of controling parasitic infections and preventive measures against them.

Host immunity shapes the impact of climate changes on the dynamics of parasite infections.

Global climate change is predicted to alter the distribution and dynamics of soil-transmitted helminth infections, and yet host immunity can also influence the impact of warming on host-parasite interactions and mitigate the long-term effects. We used time-series data from two helminth species of a natural herbivore and investigated the contribution of climate change and immunity on the long-term and seasonal dynamics of infection. We provide evidence that climate warming increases the availability of infective stages of both helminth species and the proportional increase in the intensity of infection for the helminth not regulated by immunity. In contrast, there is no significant long-term positive trend in the intensity for the immune-controlled helminth, as immunity reduces the net outcome of climate on parasite dynamics. Even so, hosts experienced higher infections of this helminth at an earlier age during critical months in the warmer years. Immunity can alleviate the expected long-term effect of climate on parasite infections but can also shift the seasonal peak of infection toward the younger individuals.