Helminth parasites of the wood mouse Apodemus sylvaticus in Southern England: levels of infection, species richness and interactions between species.

Helminth parasites of the wood mouse, Apodemus sylvaticus (n = 440), were surveyed in five localities, comprising woodland and grassland sites, in Southern England. Seven species of helminths were identified, among which Heligmosomoides polygyrus and Syphacia stroma were dominant (prevalence = 79.1% and 54.1%, respectively). Less common species were the trematode Corrigia vitta (14.8%), cestodes Catenotaenia pusilla (8.4%), Hydatigera taeniaeformis (4.1%) and Microsomacanthus crenata (3.4%) and the nematode Aonchotheca murissylvatici (0.2%). Differences in prevalences between localities were found for H. polygyrus, H. taeniaeformis and M. crenata and in abundances of H. polygyrus, S. stroma and C. vitta. Age-dependent increases in both parameters were identified among species and for helminth species richness. The only species to show significant host sex bias was S. stroma with prevalence values being higher in male mice. A number of different methods for exploiting raw data, and data corrected for significant confounding factors, were used to determine whether there were significant associations (prevalence) between species or quantitative interactions (abundance). The strongest evidence for a positive association was shown in concurrent infections with the trematode C. vitta and the cestode C. pusilla (significant in the whole dataset and evident in each locality, both sexes and both age classes). The abundance of C. pusilla was also higher in mice with C. vitta and vice versa. Overall, however, there was little support for associations or quantitative interactions between species, especially after data had been corrected for significant extrinsic/intrinsic factors, and we conclude that the helminths of wood mice in these communities are largely non-interactive and hence, perhaps better referred to as assemblages.

A century of the Journal of Helminthology.

The Journal of Helminthology (JHL) was first published in 1923 and was originally created as a house journal of the London School of Hygiene and Tropical Medicine. The JHL was devised by its first Editor, Robert Leiper, to allow for rapid publication of results from the Department of Helminthology and its offshoot the Institute of Agricultural Parasitology. From this initial narrow focus the JHL has subsequently become not only internationally recognized but also retained its original emphasis on morphological, taxonomic and life cycle studies while embracing the emergence of new fields and technological advancements. The present review covers the historical development of the JHL over the last century from 1923 to 2023.

Spatial interactions between two nematode species along the intestine of the wood mouse Apodemus sylvaticus from woodland and grassland sites in southern England.

The distributions of the nematode parasites Heligmosomoides polygyrus and Syphacia stroma were quantified in three equal-length sections along the intestine of wood mice (Apodemus sylvaticus) trapped in three different locations in the south of England. The distribution of H. polygyrus did not change in the presence of S. stroma, this species being largely confined to the anterior third of the intestine, whether S. stroma was or was not present. However, while in single infections with S. stroma, worms were equally distributed in the anterior and middle sections of the intestine, in the presence of H. polygyrus, a higher percentage of worms was located in the middle section. This was a dose-dependent response by S. stroma to increasing worm burdens with H. polygyrus, and even relatively low intensities of infection with H. polygyrus (e.g. ≤10 worms) were sufficient to cause a posterior redistribution of S. stroma into the middle section. A similar posterior shift in the percentage distribution of S. stroma in the intestine was evident in juvenile and mature mice of both sexes, and in mice from all three study sites. The ecological significance of these results is discussed.

Reinhard Hoeppli (1893-1973): The life and curious afterlife of a distinguished parasitologist.

Reinhard Hoeepli was a Swiss-German physician with a distinguished career as a researcher and historian of medical parasitology. He spent the majority of his career at the Peking Union Medical College in Beijing, China, where he undertook research on host responses to parasitic infections, in particular describing the 'Splendore-Hoeppli phenomenon', between 1929 and 1952. During the Second World War, he acted as the Swiss honorary Consul in Japanese-occupied Beijing. After leaving China following the militarization of the College in the wake of the Korean War, he subsequently worked in Singapore and Liberia before retiring to Switzerland. Hoeppli is most widely known for his association with Sir Edmund Backhouse, a controversial and enigmatic Chinese scholar, who was his war-time patient towards the end of his life. With Hoeppli's encouragement, Backhouse wrote two scandalous and unpublishable memoirs which remained in Hoeppli's safe-keeping until his own death in 1973. However, the revelations by the historian Hugh Trevor-Roper in 1976 that Backhouse was a fraudster and fantasist has had a detrimental effect on Hoeppli's posthumous reputation that has overshadowed his many lifetime achievements. Alongside a biography of his life, an examination of the controversies of the Backhouse revelations on Hoeppli's repute is presented.

Influence of an extreme climatic event on bilateral asymmetry and occurrence of eye flukes in perch (Perca fluviatilis) and roach (Rutilus rutilus) from a lake in southeast England.

Eye flukes are common infections of freshwater fish and their occurrence as metacercarial stages may occur non-randomly resulting in an asymmetrical distribution within the host eyes. However, from previous studies the presentation of bias by these trematodes lacks consistency suggesting that congenital asymmetrical effects are unlikely to be the cause and exogenous factors, such as environmental stress, may be more influential. The present study, undertaken over a 4-year period, investigates the impact of an extreme heatwave and drought on the annual bilateral asymmetry and occurrence of two eye fluke species (Diplostomum sp. in the lens and Tylodelphys sp. in the vitreous humour) from perch (Perca fluviatilis) and roach (Rutilus rutilus). The onset of the extreme climatic event resulted in a significant negative effect on the occurrence of the eye flukes. Bilateral asymmetry, which was present within both trematode species and hosts, appeared to be highly variable between eye fluke and fish species and also year of study. However, during the pre-drought period both host species demonstrated significant asymmetry for Tylodelphys sp. but not for Diplostomum sp. while during the drought this bias was reversed. The potential role of fluctuating asymmetry of fish hosts in structuring the bilateral asymmetry of eye flukes is discussed.

Influence of Ligula intestinalis plerocercoids (Cestoda: Diphyllobothriidea) on the occurrence of eyeflukes in roach (Rutilus rutilus) from a lake in south-east England.

Vertebrate hosts commonly harbour concurrent infections of different helminth species which may interact with each other in a synergistic, antagonistic or negligible manner. Direct interactions between helminths that share a common site in the host have been regularly reported, but indirect interactions between species that occur in different sites are rarely described, especially in fish hosts. Plerocercoids of Ligula intestinalis are common infections of the peritoneal (body) cavity of roach (Rutilus rutilus) in freshwater habitats. These larval cestodes can cause extensive systemic pathologies to the fish host, which in turn may alter its susceptibility as a target host for other helminth species. The present study, using an existing dataset, investigates the influence of L. intestinalis (ligulosis) on frequently occurring eyefluke infections in roach sampled from a lake in south-east England. The occurrence of two species of eyefluke (Diplostomum sp. and Tylodelphys sp.) in the roach population demonstrated no significant levels of interaction with each other. The prevalence but not mean intensity or abundance of Diplostomum sp. was significantly increased in ligulosed roach, while the incidence of Tylodelphys sp. remained unchanged. Analyses of bilateral asymmetry in the occurrence of eyeflukes in left and right eyes of infected fish demonstrate that Tylodelphys sp. shows significant asymmetry in non-ligulosed roach, which is not replicated in ligulosed individuals. In contrast, Diplostomum sp. shows no evidence of asymmetry in either ligulosed or non-ligulosed fish.

Influence of Triaenophorus nodulosus plerocercoids (Cestoda: Pseudophyllidea) on the occurrence of intestinal helminths in the perch (Perca fluviatilis).

Concurrent infections of helminths in vertebrates are widespread and may demonstrate synergistic, antagonistic or negligible levels of interactions between species that share a common site. However, indirect interactions between species that occur in different organs of a host are poorly documented, particularly in fish. Plerocercoids of Triaenophorus nodulosus are common liver infections of European perch (Perca fluviatilis). These larval cestodes cause extensive liver damage, resulting in systemic pathologies that include alteration of the physiochemical environment of the intestine. Perch harbour a wide range of intestinal helminths whose occurrence may be potentially influenced by the concurrent presence of T. nodulosus plerocercoids. The present study, using an existing dataset, investigated the effects of T. nodulosus on the infection levels of four common perch helminths - Acanthocephalus lucii, Camallanus lacustris, Proteocephalus percae and Bunodera luciopercae. The prevalences of A. lucii and C. lacustris were significantly reduced in fish infected by T. nodulosus, although the mean intensity of infections remained unaffected for any helminth species, while the mean abundance of C. lacustris was significantly reduced in plerocercoid-affected perch. Differences in site selection and individual interactions between the four helminth species in the intestine of T. nodulosus-infected and non-infected perch were rarely observed.

Thermodynamics of egg production, development and hatching in trematodes.

Temperature is a key factor influencing the rate of biological processes of ectothermic animals and is intrinsically linked to climate change. Trematode parasites may be potentially susceptible to temperature changes and, in order to develop a predictive framework of their response to climate change, large-scale analyses are needed. In particular, the biology of the egg of all species is at some time influenced by environmental conditions. The present study uses Arrhenius activation energy (E*), a common measure of temperature-mediated reaction rates, to analyse experimental data from the scientific literature on the effects of temperature on the production, development and hatching of trematode eggs. Egg production declines at high temperatures, with habitat-specific climatic factors determining the optimal thermal range. Egg development, as is typical of invertebrates, shows a simple response to temperature, with minimal differences between mid- (35-60°) and low-latitude (<35°) species. Egg hatching demonstrates variable thermodynamics with high E* values at low temperature ranges and thermostability at mid-temperatures, before declining at high temperature ranges, with wide thermostable zones being a common feature. Comparisons between development and hatching indicate that these two parameters demonstrate different thermodynamical responses. The significance of these results in furthering our understanding of trematode egg biology under natural conditions is discussed.

Symbiotic bacteria of helminths: what role may they play in ecosystems under anthropogenic stress?

Symbiotic bacteria are a common feature of many animals, particularly invertebrates, from both aquatic and terrestrial habitats. These bacteria have increasingly been recognized as performing an important role in maintaining invertebrate health. Both ecto- and endoparasitic helminths have also been found to harbour a range of bacterial species which provide a similar function. The part symbiotic bacteria play in sustaining homeostasis of free-living invertebrates exposed to anthropogenic pressure (climate change, pollution), and the consequences to invertebrate populations when their symbionts succumb to poor environmental conditions, are increasingly important areas of research. Helminths are also susceptible to environmental stress and their symbiotic bacteria may be a key aspect of their responses to deteriorating conditions. This article summarizes the ecophysiological relationship helminths have with symbiotic bacteria and the role they play in maintaining a healthy parasite and the relevance of specific changes that occur in free-living invertebrate-bacteria interactions under anthropogenic pressure to helminths and their bacterial communities. It also discusses the importance of understanding the mechanistic sensitivity of helminth-bacteria relationships to environmental stress for comprehending the responses of parasites to challenging conditions.

Inotuzumab ozogamicin in the management of acute lymphoblastic leukaemia.

Whilst most adult patients with acute lymphoblastic leukaemia will go into remission with standard induction chemotherapy, many will relapse. Response rates to standard salvage chemotherapy regimens are low and the outlook on relapse is very poor and associated with significant morbidity and mortality hence the need for newer targeted approaches. Inotuzumab ozogamicin (previously known as CMC-544) is an antibody-drug conjugate and consists of a monoclonal anti-CD22 antibody bound to calicheamicin. The target, CD22, is widely expressed on acute lymphoblastic leukaemia cells making it a potential therapeutic target. The calicheamicin is delivered intracellularly and causes leukaemia cell apoptosis. Overall response rates of 57% were observed in a Phase II study and the final results of a Phase III randomised controlled trial comparing this drug to the investigator choice 'standard of care' chemotherapy are eagerly awaited. Whilst initial results are promising, there have been concerns regarding liver toxicity and the incidence of veno-occlusive disease of the liver especially in patients who have previously received or go on to allogeneic stem cell transplant.

Thermodynamics of trematode infectivity.

Temperature is an important factor influencing the biology of organisms and is intrinsically linked to climate change. The establishment of trematodes in target hosts is potentially susceptible to temperature changes effecting parasite infectivity or host susceptibility, and therefore in order to develop predictive frameworks of host-parasite dynamics under climate change large-scale analyses are required. The present study analyses the thermodynamics of the infectivity of larval trematodes including miracidia, cercariae and metacercariae from experimental data contained in the scientific literature using the Arrhenius critical incremental energy of activation (E*), an accurate measure of temperature-driven reaction rates. For miracidia and cercariae, infectivity increases as the temperature rises reaching a plateau over optimal thermal ranges before declining at higher temperatures. In contrast, metacercarial infectivity is at its greatest at low temperatures, declining with increasing temperature.

Thermodynamics of cercarial development and emergence in trematodes.

SUMMARY Temperature is an important factor influencing the biology of ectothermic organisms and is intrinsically linked to climate change. Trematodes are potentially susceptible to temperature changes and in order to develop predictive frameworks of their responses to climate change large-scale analyses are needed. The present study, using the Q 10 value, analyses experimental data from the scientific literature on the effects of temperature on cercarial development and emergence across a wide range of temperature in low (⩽35°) and mid-latitude (36-60°) species. Temperature appears to have no significant effect on the rate of development of cercariae within molluscan hosts. Data on cercarial emergence, corrected to incorporate the minimum emergence temperature threshold (METT) and acclimation status, was found to be largely unaffected by temperature over optimum ranges of ≈20 °C (15-25 °C) for mid-latitude species and ≈25 °C (20-30 °C) for low-latitude species. In addition, a decline in emergence rates was shown at higher temperatures. These results are contrary to a previous study on the meta-analysis of cercarial emergence. Some evidence of strain-specific differences and thermostability over a wide temperature range for both cercarial development and emergence was apparent. The significance of these results in furthering our understanding of cercarial biology under natural conditions is discussed.

Thermodynamics of miracidial survival and metabolism.

Miracidia are short-lived, non-feeding (lecithotrophic) free-living stages of trematodes, whose survival is potentially influenced by temperature. Climate change may result in elevated temperatures affecting trematode transmission. Therefore understanding their thermobiology forms an important step in determining the future dynamics of parasite populations. An empirical relationship exists between the mean expected life span of lecithotrophic larvae and the half life of their population (t(0·5)) and therefore t(0·5) is a good indicator of glycogen utilization. In this study experimental data on the effects of temperature on miracidial survival were compiled from the scientific literature and evaluated in terms of metabolism using Q 10 and Arrhenius activation energy (E* or µ). Temperature poorly influenced survival/metabolism with all miracidia having distinct zone(s) of thermostability. Overall there were few differences in Q(10) and E* values between most species temperature ranges whilst there were only limited strain-specific variations in thermal responses of laboratory-maintained Schistosoma mansoni. Miracidia demonstrated a trend of greater thermal resistance than cercariae. In particular, comparative studies on 4 strains of the same species of miracidia and cercariae showed little correlation in thermal biology between the 2 life-history stages. The importance of these results for trematode transmission under global climate change is discussed.

Structural changes in freshwater fish and chironomids exposed to bacterial exotoxins.

Mass fish mortalities have been reported in the past decade from British waters, often coinciding with blooms of filamentous actinobacteria, particularly strains of Streptomyces griseus. The present study has shown that some fractions of the exudate of S. griseus, prepared after a series of high pressure liquid chromatography (HPLC) separations, and analysed with liquid chromatography mass spectrometry (LC-MS), induced pathological changes to the gills of carp and/or tench fry following exposure under laboratory conditions up to 96 h Similar changes were induced by streptomycin, a secondary metabolite of S. griseus, and these included loss of microridging and fusion of secondary lamellae, with carp fry in the case of the exudate of S. griseus being more sensitive than tench fry, especially with exposure to fraction 9 and selected sub-fractions of 9. Some deformities using a severity index were also observed in the head capsule of larvae of the non-biting midge Chironomus riparius, including loss and splitting of teeth on the mentum. The results are discussed in relation to further identification of metabolites derived from samples of the organic filtrate of S. griseus and implications for the functioning of freshwater ecosystems.

The effects of radioactive pollution on the dynamics of infectious diseases in wildlife.

The interactions between infectious diseases and chemical pollution are well known and recognised as important factors in regulating the way wild animals respond to contaminant exposure. However, the impact of ionising radiation and radionuclides has often been overlooked when assessing host-pathogen interactions in polluted habitats, despite often occurring together with chemical contamination. Nevertheless, a comprehensive body of literature exists from laboratory and field studies on host-pathogen relationships under radiation exposure, and with a renewed interest in radioecology developing; an evaluation of infectious disease dynamics under these conditions would be timely. The present study assesses the impact of external ionising radiation and radionuclides on animal hosts and pathogens (viruses, bacteria, protozoans, helminths, arthropods) in laboratory studies and collates the data from field studies, including the large number of investigations undertaken after the Chernobyl accident. It is apparent that radiation exposure has substantial effects on host-pathogen relationships. Although damage to the host immune system is a major factor other variables, such as damage to host tissue barriers and inhibition of pathogen viability are also important in affecting the prevalence and intensity of parasitic diseases. Field studies indicate that the occurrence of host-pathogen associations in radioactively contaminated sites is complex with a variety of biotic and abiotic factors influencing both pathogen and host(s), resulting in changes to the dynamics of infectious diseases.

Thermodynamics of cercarial survival and metabolism in a changing climate.

Cercariae are non-feeding free-living stages in the life cycles of trematodes, highly influenced by temperature. Their life span is brief, limited by the depletion of a non-renewable glycogen store. Warmer temperatures under the influence of climate change may promote the transmission of parasites and therefore understanding their thermobiology forms an important step in discerning the future dynamics of parasite populations. An empirical relationship exists between cercarial mean expected life span and the half-life of the population (t0·5) and therefore t0·5 is a good indicator of glycogen utilization. In this study experimental data on the effects of temperature on cercarial survival is compiled from the scientific literature and evaluated in terms of metabolism using Q10 and Arrhenius activation energy (E* or µ), common measures of temperature-mediated reaction rates. Cercariae have a variable response to temperature, which does not appear to be influenced by their life-history attributes or size. There were little differences in Q10 and E* values between most temperature ranges. In almost half the studies examined (7 of 16) cercariae demonstrated a discrete zone of thermostability over a range equivalent to typical individual mean summer temperatures. Distinct intraspecific differences in temperature responses between 3 laboratory strains of Schistosoma mansoni and 2 natural strains of Echinoparyphium recurvatum sensu stricto were apparent. The importance of these results for cercarial biology under global climate change is discussed.

Aquatic molluscs as auxiliary hosts for terrestrial nematode parasites: implications for pathogen transmission in a changing climate.

Nematodes are common parasites of molluscs but are often overlooked. Both metastrongyloid and rhabditoid species dominate the fauna within land snail and slug populations. Nevertheless, a key characteristic of many laboratory studies is the ability of these terrestrial nematodes to utilize aquatic molluscs as auxiliary hosts. The significance of this to the ecology of the parasite has never been evaluated. There is increasing concern as to the impact of climate change on the epidemiology of many parasitic diseases. In particular, it has been suggested that host switching may increase under the pressure of extreme climatic conditions. It is therefore timely to assess the role that aquatic molluscs may play in transmitting terrestrial nematodes, which include species of medical and veterinary importance such as Angiostrongylus cantonensis, A. vasorum, and Muellerius capillaris. The present review assesses the mechanisms of terrestrial nematode transmission through aquatic molluscs focusing on metastrongyloid and rhabditoid species, the importance of variable susceptibility of molluscan hosts, field studies on natural occurrence within aquatic habitats, and the impact of extreme climatic events (floods and droughts) that may increase in frequency under climate change.

The effects of host size and temperature on the emergence of Echinoparyphium recurvatum cercariae from Lymnaea peregra under natural light conditions.

The production of cercariae from their snail host is a fundamental component of transmission success in trematodes. The emergence of Echinoparyphium recurvatum (Trematoda: Echinostomatidae) cercariae from Lymnaea peregra was studied under natural sunlight conditions, using naturally infected snails of different sizes (10-17 mm) within a temperature range of 10-29 degrees C. There was a single photoperiodic circadian cycle of emergence with one peak, which correlated with the maximum diffuse sunlight irradiation. At 21 degrees C the daily number of emerging cercariae increased with increasing host snail size, but variations in cercarial emergence did occur between both individual snails and different days. There was only limited evidence of cyclic emergence patterns over a 3-week period, probably due to extensive snail mortality, particularly those in the larger size classes. Very few cercariae emerged in all snail size classes at the lowest temperature studied (10 degrees C), but at increasingly higher temperatures elevated numbers of cercariae emerged, reaching an optimum between 17 and 25 degrees C. Above this range emergence was reduced. At all temperatures more cercariae emerged from larger snails. Analysis of emergence using the Q10 value, a measure of physiological processes over temperature ranges, showed that between 10 and 21 degrees C (approximately 15 degrees C) Q10 values exceeded 100 for all snail size classes, indicating a substantially greater emergence than would be expected for normal physiological rates. From 14 to 25 degrees C (approximately 20 degrees C) cercarial emergence in most snail size classes showed little change in Q10, although in the smallest size class emergence was still substantially greater than the typical Q10 increase expected over this temperature range. At the highest range of 21-29 degrees C (approximately 25 degrees C), Q10 was much reduced. The importance of these results for cercarial emergence under global climate change is discussed.

Interactive effects of infectious diseases and pollution in aquatic molluscs.

Aquatic molluscs are ideal invertebrate model systems for environmental monitoring and toxicology. However, like all animals, they are subjected to a wide range of infectious diseases that can have significant effects on host ecology and physiology and are therefore a source of natural stress to populations. Anthropogenic activities, especially involving chemical contaminants that pollute the environment, can also affect molluscan ecological and physiological parameters. In combination, pollution and pathogens represent a serious threat to the health of aquatic communities that has been increasingly recognised. The present article reviews the interactive effects of viral, bacterial, protozoan, and trematode infections with toxic pollutants on aquatic molluscs. The interactions between pollution and other less well studied infectious diseases as well as the differing responses to pathogens and pollution between wild and cultured molluscan populations are also considered.

Effects of a chemically polluted discharge on the relationship between fecundity and parasitic infections in the chub (Leuciscus cephalus) from a river in southern England.

In fish there is a close association between endocrine and immune function that during seasonal changes in reproductive status can affect the fishes susceptibility to parasitic infection. The effects of endocrine-disrupting pollution on this association are not known. The present study investigates the effects of a chemically polluted (ammoniacal nitrogen, zinc, bromide) discharge in Cranleigh Waters, a river in southern England, on the fecundity and parasitism of chub, Leuciscus cephalus, over an 18-month period. In the polluted site, the gonado-somatic index (GSI) of fish was lower in females and higher in males compared to an unpolluted upstream site, indicating an androgenic effect on reproduction. Parasite species richness, especially the intestinal helminths Proteocephalus torulosus and Pomphorynchus laevis, was increased in fish in the polluted site. However, the occurrence of the two most common parasite species in the river-Myxobulus sp. 1, a gill myxozoan, and Diplostomum sp., a trematode found in the eye-was unchanged between polluted and unpolluted river sites. Nevertheless, there was a significant relationship between GSI and the prevalence of these two parasite species in the unpolluted site but not the polluted site suggesting that endocrine disruption of reproduction did not lead to an increase in host susceptibility. The reasons for this are discussed.