Increased virulence due to multiple infection in Daphnia leads to limited growth in 1 of 2 co-infecting microsporidian parasites.

Recent outbreaks of various infectious diseases have highlighted the ever-present need to understand the drivers of the outbreak and spread of disease. Although much of the research investigating diseases focuses on single infections, natural systems are dominated by multiple infections. These infections may occur simultaneously, but are often acquired sequentially, which may alter the outcome of infection. Using waterfleas (Daphnia magna) as a model organism, we examined the outcome of sequential and simultaneous multiple infections with 2 microsporidian parasites (Ordospora colligata and Hamiltosporidium tvaerminnensis) in a fully factorial design with 9 treatments and 30 replicates. We found no differences between simultaneous and sequential infections. However, H. tvaerminnensis fitness was impeded by multiple infection due to increased host mortality, which gave H. tvaerminnensis less time to grow. Host fecundity was also reduced across all treatments, but animals infected with O. colligata at a younger age produced the fewest offspring. As H. tvaerminnensis is both horizontally and vertically transmitted, this reduction in offspring may have further reduced H. tvaerminnensis fitness in co-infected treatments. Our findings suggest that in natural populations where both species co-occur, H. tvaerminnensis may evolve to higher levels of virulence following frequent co-infection by O. colligata.

A walk on the wild side: A review of the epidemiology of Toxocara canis and Toxocara cati in wild hosts.

Toxocara species are cosmopolitan nematode parasites of companion, domestic and wild hosts. Of the 26 known species of Toxocara, only Toxocara canis and Toxocara cati are definitively zoonotic. The significance of wild carnivores as definitive hosts of T. canis and T. cati respectively, has received far less attention compared to domestic dogs and cats. Complex environmental changes have promoted increasing contact between wildlife, domestic animals and humans that can enhance the risk of pathogen spillover. This review lists a total of 19 species of wild canid host that have been shown to act as definitive hosts for T. canis and a total of 21 species of wild felid host. In general, the number of publications focusing on felid host species is fewer in number, reflecting the general paucity of data on T. cati. The wild canids that have received the most attention in the published literature include the red fox (Vulpes vulpes), the wolf (Canis lupus), and the golden jackal (Canis aureus). The wild felid species that has received the most attention in the published literature is the Eurasian lynx (Lynx lynx). Some non-canid and non-felid hosts also act as definitive hosts of Toxocara species. Certainly, red foxes would appear to be the most significant wild species in terms of their potential to transmit Toxocara to domestic dogs and humans via environmental contamination. This can be explained by their increasing population densities, encroachment into urban areas and their dietary preferences for a wide range of potential paratenic hosts. However, a major challenge remains to assess the relative importance of wild hosts as contributors to environmental contamination with Toxocara ova. Furthermore, one major constraint to our understanding of the significance of wildlife parasitism is a lack of access to samples, particularly from rare host species.

The timid invasion: behavioural adjustments and range expansion in a non-native rodent.

Animal behaviour can moderate biological invasion processes, and the native fauna's ability to adapt. The importance and nature of behavioural traits favouring colonization success remain debated. We investigated behavioural responses associated with risk-taking and exploration, both in non-native bank voles (Myodes glareolus, N = 225) accidentally introduced to Ireland a century ago, and in native wood mice (Apodemus sylvaticus, N = 189), that decline in numbers with vole expansion. We repeatedly sampled behavioural responses in three colonization zones: established bank vole populations for greater than 80 years (2 sites), expansion edge vole populations present for 1-4 years (4) and pre-arrival (2). All zones were occupied by wood mice. Individuals of both species varied consistently in risk-taking and exploration. Mice had not adjusted their behaviour to the presence of non-native voles, as it did not differ between the zones. Male voles at the expansion edge were initially more risk-averse but habituated faster to repeated testing, compared to voles in the established population. Results thus indicate spatial sorting for risk-taking propensity along the expansion edge in the dispersing sex. In non-native prey species the ability to develop risk-averse phenotypes may thus represent a fundamental component for range expansions.

Strongyloides coinfection in COVID-19 patients treated with corticosteroids: A systematic review.

The COVID-19 pandemic linked to the virus SARS-CoV-2, which began in China, affected ∼765 million people as of 30 April 2023. The widespread use of corticosteroids for the symptomatic treatment of COVID-19 could lead to the reactivation of infections of opportunistic pathogens, including Strongyloides. We sought to determine the clinical symptoms and demographic characteristics of SARS-CoV-2-Strongyloides co-infection, particularly in patients with severe disease and being treated with immunosuppressive drugs. To do this, we undertook a systematic review of the literature, and searched public accessible scientific databases-the Web of Science, Scopus, PubMed/Medline and Embase -for eligible studies (1 December 2019 to 30 August 2022). The review protocol is registered in PROSPERO (CRD42022377062). Descriptive statistical analyses were used to present the clinical and laboratory parameters of the co-infection; for this, we calculated prevalence using the following formula: positive cases/total number of cases × 100. Of a total of 593 studies identified, 17 studies reporting 26 co-infected patients met the criteria for inclusion in this review. The median age of these patients was 55.14 years. Most of cases (53.8%) were treated with dexamethasone, followed by methylprednisolone (26.9%). Eighteen of 26 patients were immigrants living in European countries or the USA; most of these immigrants originated from Latin America (58%) and South-East Asia (11%). The commonest symptoms of co-infection were abdominal pain (50%), fever (46.1%), dyspnoea (30.7%) and cough (30.7%), and frequently reported laboratory findings were high absolute eosinophil count (38.4%), high white blood cell count (30.7%), high C-reactive protein (23.0%) and high neutrophil count (19.2%). Two of the 26 patients (7.7%) had fatal outcomes. Most of the SARS-CoV-2-Strongyloides coinfected cases were immigrants living in developed countries, emphasising the need for clinicians in these countries to be aware of clinical and laboratory parameters associated with such co-infections, as well as the key importance of rapid and accurate diagnostic tests for timely and effective diagnosis and patient management.

Caring for Canines: A Survey of Dog Ownership and Parasite Control Practices in Ireland.

Dogs are an important part of life for many people. Dog ownership can confer various health benefits to their owners, but it also presents some risks. In order to establish if dog owners were aware of these risks, an online survey of dog ownership practices was carried out. The survey was open during the month of January 2022 and received 662 responses regarding 850 individual dogs. Overall, 52% of people reported deworming their dog between zero and twice a year, which is unlikely to reduce the risk of infection to humans. The majority of dog owners (71%) reported disposing of faeces correctly; however, when comparing urban and rural environments, 33% of those in rural environments did not dispose of their dogs' faeces at all, compared with 3% of people in urban locations. People who obtained their dog during the pandemic brought their dog to the vet and dewormed them more frequently than those who obtained their dog before the pandemic. There were no differences in how faeces was disposed of between these groups. These results indicate that we, as researchers and veterinarians, have much work to do in terms of educating dog owners about the ways in which we can reduce the risk of infection to ourselves and our communities.

An investigation of Mycobacterium bovis and helminth coinfection in the European badger Meles meles.

We investigated the relationship between the presence of helminth parasites in European badgers, and their tuberculosis (TB) status, culled as part of the bovine TB eradication programme in Ireland. Data on the worm burden or faecal egg or larval count was available for all helminth taxa recorded. Lymph node tissue samples were taken from the badgers and tested for TB. We then explored the correlation, in full-grown badgers, between the likelihood of M. bovis infection and both the prevalence and burden of certain helminth species. Specifically, our analyses focused upon the gastrointestinal species, Uncinaria criniformis and Strongyloides spp. We found that male badgers were more likely to have TB than female badgers, and that badgers infected with U. criniformis or Strongyloides spp. were more likely to have TB than badgers without such helminth infections. There was a suggestion that badgers with higher U. criniformis worm burdens were more likely to have TB than those with lesser burdens. Although our sampling protocols did not allow us to determine which infection came first, it strongly suggests that once badgers are infected with either gastrointestinal helminths or TB, they are likely to become coinfected. As Ireland works towards a national TB-free status, it will be important to appreciate the implications of such coinfection.

Global prevalence of Ascaris infection in humans (2010-2021): a systematic review and meta-analysis.

BACKGROUND: Ascariasis is one of the most important neglected tropical diseases of humans worldwide. The epidemiology of Ascaris infection appears to have changed with improvements in sanitation and mass drug administration, but there is no recent information on prevalence worldwide. Here, we performed a systematic review and meta-analysis to assess the global prevalence of human Ascaris infection from 2010 to 2021. METHODS: We searched MEDLINE/PubMed, and Scopus databases for studies measuring prevalence of Ascaris infection, published between 1 January 2010 and 1 January 2022. We included studies of the general human population in endemic regions, which used accepted coprodiagnostic methods, and excluded studies of people with occupations with an increased risk or probability of ascariasis and/or specific diseases other than ascariasis. We applied random-effects models to obtain pooled prevalence estimates for six sustainable development goal regions of the world. We extrapolated the prevalence estimates to the global population in 2020, to estimate the number of individuals with Ascaris infection. We conducted multiple subgroup and meta-regression analyses to explore possible sources of heterogeneity, and to assess relationships between prevalence estimates and demographic, socio-economic, geo-climatic factors. RESULTS: Of 11,245 studies screened, we analysed 758 prevalence estimates for a total number of 4,923,876 participants in 616 studies from 81 countries. The global prevalence estimated was 11.01% (95% confidence interval: 10.27-11.78%), with regional prevalences ranging from 28.77% (7.07-57.66%) in Melanesia (Oceania) to 1.39% (1.07-1.74%) in Eastern Asia. We estimated that ~ 732 (682-782) million people harboured Ascaris worldwide in 2021. The infected people in Latin America and the Caribbean region had a higher prevalence of high intensity infection (8.4%, 3.9-14.1%). Prevalence estimates were higher in children, and people in rural communities or in countries or regions with lower income and human development indices. There was a trend for a higher prevalence in regions with increasing mean annual relative humidity, precipitation and environmental temperature. CONCLUSIONS: Our findings indicate that, despite a renewed commitment by some communities or authorities to control ascariasis, a substantial portion of the world's human population (> 0.7 billion) is infected with Ascaris. Despite the clinical and socioeconomic importance of ascariasis, many past routine surveys did not assess the intensity of Ascaris infection in people. We propose that the present findings might stimulate the development of customised strategies for the improved control and prevention of Ascaris infection worldwide.

Toxocara: time to let cati 'out of the bag'.

Zoonotic toxocariasis is increasingly prominent as knowledge of its insidious impact on human health accumulates. Toxocara canis dominates research attention, with Toxocara cati relegated to the periphery. We argue that there are few grounds to support this bias, and that differences in life history and epidemiology between T. canis and T. cati could have implications for disease impacts and control. Research on T. cati should be cognisant of its unique characteristics and not extrapolate uncritically from knowledge about T. canis. Key research gaps identified long ago remain largely unfilled. We set challenges for future research to better understand the biology of T. cati and its role in zoonotic disease - essential for guiding urgently needed actions in support of public health.

The Invasive Bank Vole (Myodes glareolus): A Model System for Studying Parasites and Ecoimmunology during a Biological Invasion.

The primary driver of the observed increase in emerging infectious diseases (EIDs) has been identified as human interaction with wildlife and this increase has emphasized knowledge gaps in wildlife pathogens dynamics. Wild rodent models have proven excellent for studying changes in parasite communities and have been a particular focus of eco-immunological research. Helminth species have been shown to be one of the factors regulating rodent abundance and indirectly affect disease burden through trade-offs between immune pathways. The Myodes glareolus invasion in Ireland is a unique model system to explore the invasion dynamics of helminth species. Studies of the invasive population of M. glareolus in Ireland have revealed a verifiable introduction point and its steady spread. Helminths studies of this invasion have identified enemy release, spillover, spillback and dilution taking place. Longitudinal studies have the potential to demonstrate the interplay between helminth parasite dynamics and both immune adaptation and coinfecting microparasites as M. glareolus become established across Ireland. Using the M. glareolus invasion as a model system and other similar wildlife systems, we can begin to fill the large gap in our knowledge surrounding the area of wildlife pathogen dynamics.

Distinct hepatic myeloid and lymphoid cell repertoires are associated with susceptibility and resistance to Ascaris infection.

The soil-transmitted helminth Ascaris lumbricoides infects ~800 million people worldwide. Some people are heavily infected, harbouring many worms, whereas others are only lightly infected. The mechanisms behind this difference are unknown. We used a mouse model of hepatic resistance to Ascaris, with C57BL/6J mice as a model for heavy infection and CBA/Ca mice as a model for light infection. The mice were infected with the porcine ascarid, Ascaris suum or the human ascarid, A. lumbricoides and immune cells in their livers and spleens were enumerated using flow cytometry. Compared to uninfected C57BL/6J mice, uninfected CBA/Ca mice had higher splenic CD4+ and γδ T cell counts and lower hepatic eosinophil, Kupffer cell and B cell counts. Infection with A. suum led to expansions of eosinophils, Kupffer cells, monocytes and dendritic cells in the livers of both mouse strains and depletions of hepatic natural killer (NK) cells in CBA/Ca mice only. Infection with A. lumbricoides led to expansions of hepatic eosinophils, monocytes and dendritic cells and depletions of CD8+, αß, NK and NK T cells in CBA/Ca mice, but not in C57BL/6J mice where only monocytes expanded. Thus, susceptibility and resistance to Ascaris infection are governed, in part, by the hepatic immune system.

Warming can alter host behavior in a similar manner to infection with behavior-manipulating parasites.

Parasites are ecologically ubiquitous and, by modifying the physiology and behavior of their host organisms, act as key regulators of the dynamics and stability of ecosystems. It is, however, as yet unclear how parasitic relationships will act to moderate or accelerate the ecological impacts of global climate change. Here, we explore experimentally how the effects of parasites on both the physiology and behavior of their hosts can be moderated by warming, utilising a well-established aquatic host-parasite model system-the ecologically important amphipod Gammarus duebeni and its acanthocephalan parasite Polymorphus minutus. We show that, while only warming affected measured components of host physiology, parasite infection and warming both supressed predator-avoidance behavior of the host independently, yet in a similar manner. Six degrees of warming altered geotactic behaviors to the same extent as infection with behavior-manipulating parasites. These results indicate a novel mechanism by which parasites impact their ecosystems that could be critical to predicting the ecological impacts of warming. Our findings highlight the need for holistic knowledge of interaction networks, incorporating multiple interaction types and behaviors, to predict the effects of both warming and parasitism on the dynamics and stability of ecosystems.

Whipworm and roundworm infections.

Trichuriasis and ascariasis are neglected tropical diseases caused by the gastrointestinal dwelling nematodes Trichuris trichiura (a whipworm) and Ascaris lumbricoides (a roundworm), respectively. Both parasites are staggeringly prevalent, particularly in tropical and subtropical areas, and are associated with substantial morbidity. Infection is initiated by ingestion of infective eggs, which hatch in the intestine. Thereafter, T. trichiura larvae moult within intestinal epithelial cells, with adult worms embedded in a partially intracellular niche in the large intestine, whereas A. lumbricoides larvae penetrate the gut mucosa and migrate through the liver and lungs before returning to the lumen of the small intestine, where adult worms dwell. Both species elicit type 2 anti-parasite immunity. Diagnosis is typically based on clinical presentation (gastrointestinal symptoms and inflammation) and the detection of eggs or parasite DNA in the faeces. Prevention and treatment strategies rely on periodic mass drug administration (generally with albendazole or mebendazole) to at-risk populations and improvements in water, sanitation and hygiene. The effectiveness of drug treatment is very high for A. lumbricoides infections, whereas cure rates for T. trichiura infections are low. Novel anthelminthic drugs are needed, together with vaccine development and tools for diagnosis and assessment of parasite control in the field.

The hidden faces of a biological invasion: parasite dynamics of invaders and natives.

One of the primary drivers of emerging infectious diseases (EIDs) is human intervention via host or parasite translocations. A unique opportunity to study host and parasite dispersal during a bio-invasion currently exists in Ireland due to the introduction of the bank vole (Myodes glareolus) in the 1920s. The continuing range expansion of M. glareolus within Ireland presents a natural large-scale perturbation experiment. This study used the Irish M. glareolus model to conduct a spatiotemporal study analysing the parasite dynamics of native and invasive species throughout their range. Myodes glareolus and native Apodemus sylvaticus were trapped in woodlands across Ireland and surveyed for their helminth parasites. Myodes glareolus in Ireland were found to have lower parasite diversity in comparison to records of M. glareolus from across Europe and A. sylvaticus in Ireland. Increased density of M. glareolus resulted in a dilution effect, with significantly lower levels of parasitism overall in native hosts, where M. glareolus has been established longest. However, three helminth parasite species of A. sylvaticus increased in abundance in the presence of M. glareolus. Furthermore, M. glareolus at the expansion front were less parasitised (lower abundance and prevalence of certain parasites and lower parasite diversity) than M. glareolus from the core population. This "enemy release" is believed to be mediating the continued successful spread of the invader across Ireland. Our results identify two important variables, seasonality and the stage of the invasion, which should not be overlooked when investigating or managing the changing distribution of hosts and their parasites. Studies of bio-invasions and parasite transmission have primarily focused on the invasive host species or the native host species in cases where virulent pathogen spillover is observed. Our results demonstrate how the concurrent study of invasive and native hosts, and the careful identification of their parasite communities, allows the dynamic processes influencing the parasite component and intracommunity to be identified.

Seroprevalence estimates for toxocariasis in people worldwide: A systematic review and meta-analysis.

BACKGROUND: Human toxocariasis is an important neglected disease. We performed a systematic review and meta-analysis study to estimate the global and regional prevalence of anti-Toxocara serum antibodies (referred to as 'T-seroprevalence') in human populations around the world. METHODS: We searched five international databases (PubMed, EMBASE, Web of Science, SciELO and Scopus) for seroprevalence studies published from 1 January 1980 to 15 March 2019. We used random effect models to calculate the overall T-seroprevalence (with 95% CIs) in all six WHO regions and worldwide. We also conducted subgroup and linear meta-regression analyses to evaluate the impact of socio-demographic, geographical and climatic parameters on seroprevalence. RESULTS: We identified 250 eligible studies (253 datasets) comprising 265,327 participants in 71 countries for inclusion in the present meta-analysis. The estimated global T-seroprevalence rate was 19.0% (95%CI, 16.6-21.4%; 62,927/265,327); seroprevalence was highest in the African region (37.7%; 25.7-50.6%) and lowest in the Eastern Mediterranean region (8.2%; 5.1-12.0%). The pooled seroprevalence for other WHO regions was 34.1% (20.2-49.4%) in the South-East Asia; 24.2% (16.0-33.5%) in the Western Pacific; 22.8% (19.7-26.0%) in the American; and 10.5% (8.5-12.8%) in the European regions. A significantly higher T-seroprevalence was associated with a lower income level; lower human development index (HDI); lower latitude; higher humidity; higher temperature; and higher precipitation (P-value < 0.001). Potential risk factors associated with seropositivity to Toxocara included male gender; living in a rural area; young age; close contact with dogs, cats or soil; consumption of raw meat; and the drinking of untreated water. CONCLUSIONS: The present findings indicate high levels of infection with, or exposure to Toxocara spp. in many countries, which calls for increased attention to human toxocariasis and improved measures to prevent adverse health risks of this disease.

The role of the liver in the migration of parasites of global significance.

Many parasites migrate through different tissues during their life-cycle, possibly with the aim to enhance their fitness. This is true for species of three parasite genera of global importance, Ascaris, Schistosoma and Plasmodium, which cause significant global morbidity and mortality. Interestingly, these parasites all incorporate the liver in their life-cycle. The liver has a special immune status being able to preferentially induce tolerance over immunity. This function may be exploited by parasites to evade host immunity, with Plasmodium spp. in particular using this organ for its multiplication. However, hepatic larval attrition occurs in both ascariasis and schistosomiasis. A better understanding of the molecular mechanisms involved in hepatic infection could be useful in developing novel vaccines and therapies for these parasites.

The liver proteome in a mouse model for Ascaris suum resistance and susceptibility: evidence for an altered innate immune response.

BACKGROUND: Ascariasis is a neglected tropical disease that affects 800 million people worldwide. Whereas most people only experience light worm burden, some people experience heavy worm burdens even after several rounds of chemotherapy, a phenomenon known as predisposition. Such heavy infections are associated with more severe symptoms and increased chronic morbidity. METHODS: In order to investigate potential mechanisms that may explain the observed predisposition, we infected mice with the porcine ascarid Ascaris suum using an established mouse model with two different mouse strains, where the C57BL/6J strain is more susceptible to infection and therefore a model for heavy infection and the CBA/Ca strain is more resistant and thus a model for light infection. At day 7 post-infection we investigated the liver proteome, using shotgun mass spectrometry, of both infected and control mice of each strain. RESULTS: We identified intrinsic differences, between the two mouse strains, in both oxidative phosphorylation proteins and proteins involved in retinol metabolism. Additionally, we found differences between the two mouse strains in activation of the complement system, where the CBA/Ca strain has higher protein abundances for lectin pathway proteins and the C57BL/6J strain has higher protein abundances for complement inhibiting proteins. The CBA/Ca strain had a higher abundance of proteins involved in the activation of the complement cascade via the lectin pathway. In contrast, the C57BL/6J strain demonstrated a higher abundance of proteins involved in arresting the complement pathway. CONCLUSIONS: We observed clear differences between the two mouse strains both intrinsically and under infection.

Infection with behaviour-manipulating parasites enhances bioturbation by key aquatic detritivores.

The ecological ubiquity of parasites and their potential impacts on host behaviour have led to the suggestion that parasites can act as ecosystem engineers, structuring their environment and physical habitats. Potential modification of the relationship between parasites and their hosts by climate change has important implications for how hosts interact with both their biotic and abiotic environment. Here, we show that warming and parasitic infection independently increase rates of bioturbation by a key detritivore in aquatic ecosystems (Gammarus). These findings have important implications for ecosystem structure and functioning in a warming world, as alterations to rates of bioturbation could significantly modify oxygenation penetration and nutrient cycling in benthic sediments of rivers and lakes. Our results demonstrate a need for future ecosystem management strategies to account for parasitic infection when predicting the impacts of a warming climate.

A comparison of helminth infections as assessed through coprological analysis and adult worm burdens in a wild host.

Coprological analysis is the most widely used diagnostic tool for helminth infection in both domestic and wild mammals. Evaluation of the efficacy of this technique is rare, due to the lack of availability of adult worm burden. Where information is available the majority of studies are in small ruminants and seldom in a wild host. This study of 289 wild badgers is the first to report the relationship between faecal egg/larval counts and adult worm burden in badgers whilst also evaluating the reliability of coprological analysis as a diagnostic tool for hookworm (Uncinaria criniformis) and lungworm (Aelurostrongylus falciformis) infection. The prevalence of hookworm and lungworm infection, as assessed through adult worm burden was 59.2% and 20.8% respectively. For both species of helminth, infection was consistently under-reported by coprological analysis compared to adult worm burden with a reported 41% sensitivity for hookworm and 10% for lungworm. A significant positive relationship was found between faecal counts and adult worm burden for both species of helminths. Additionally the density -dependent relationship often reported in helminth infection appears to be weak or non-existent in this study, up to the observed worm intensity of 500.

Human toxocariasis.

Parasitic nematodes of the genus Toxocara are socioeconomically important zoonotic pathogens. These parasites are usually directly transmitted to the human host via the faecal-oral route and can cause toxocariasis and associated complications, including allergic and neurological disorders. Although tens of millions of people are estimated to be exposed to or infected with Toxocara spp, global epidemiological information on the relationship between seropositivity and toxocariasis is limited. Recent findings suggest that the effect of toxocariasis on human health is increasing in some countries. Here we review the salient background on Toxocara and biology, summarise key aspects of the pathogenesis, diagnosis, and treatment of toxocariasis, describe what is known about its geographic distribution and prevalence, and make some recommendations for future research towards the prevention and control of this important disease.

Parasite dynamics in an invaded ecosystem: helminth communities of native wood mice are impacted by the invasive bank vole.

It is becoming increasingly evident that biological invasions result in altered disease dynamics in invaded ecosystems, with knock-on effects for native host communities. We investigated disease dynamics in an invaded ecosystem, using the helminth communities of the native wood mouse (Apodemus sylvaticus) in the presence and absence of the invasive bank vole (Myodes glareolus) in Ireland. Native wood mice were collected over 2 years from four sites to assess the impact of the presence of the bank vole on wood mouse helminth community dynamics both at the component and infracommunity level. We found evidence for dilution (Syphacia stroma), spill-back (Aonchotheca murissylvatici) and spill-over (Taenia martis) in native wood mice due to the presence of the bank vole. Site of capture was the most important factor affecting helminth community structure of wood mice, along with year of capture and host-age and the interactions between them.