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Studies in parasitology: application for the award of the degree of Doctor of Science

Arme, Christopher


Christopher Arme


Analysis of the interactions that occur between parasites and their hosts is complicated by the fact that the environment of an endoparasite is another living organism. A frequent starting point for such analyses is the study of isolated hosts and parasites in vitro and, although such studies may provide useful basic data, it is usually difficult to predict to what extent results so obtained may be applicable in vivo. This is due to the complexity of interactions that often occur between host and parasite, with the result that the properties of the intact symbiosis :!lay differ substantially from a mere sum of those of parasite and host, determined independently. For example, physiological characteristics of the intestine of rats parasitised by the cestode, Hymenolepis diminuta, differ in many important respects from those of the uninfected animal. Similarly, aspects of parasite physiology, previously determined by experimentation in vitro, undoubtedly differ in the complex environment provided by the host.
The publications submitted in support of this application are concerned with the physiology and biochemistry of parasites and their hosts. Their broad orientation is towards an understanding of
host-parasite interactions in the intact symbiosis. Several species have been studied, the choice of organism being partly determined by the availability of suitable experimental material in the institutions in which I have studied. A continuing theme is the biology of adult tapeworms and metacestodes. The work of the Parasitology Research Laboratory at Keele is exclusively in this latter area and a short paper listing personnel, research interests and current grant support is attached.
Unrefereed papers, broadcasts and abstracts of communications, although contained in the attached sheets (A1-A53), are not offered for examination. For the purpose of this commentary, books and parts of books (B1-B8) and original refereed papers (1-59), submitted for examination, have been divided into groups, and these are introduced below:
A. Papers on the host-parasite relationships of certain pseudophyllidean tapeworm parasites of fish.
(Publications 2,3,4,S,11,20,28,32,33,36,37,44,45,59,B1,B2,B4,B8)
Ligula intestinalis and Schistocephalus solidus are pseudophyllidean tapeworms, the plerocercoid of which occupies an extra-intestinal site, the body cavity of fish. In terms of longevity and degree of host-involvement, the plerocercoid is the dominant phase of the life cycle of the parasite.
A unique feature of parasitism involving these species is the high intensity of infection that may be encountered, in some instances the weight of parasite tissue exceeding that of the host. Under such circumstances it is hardly surprising that the presence of these parasites may be associated with pronounced pathological effects in the host. These include reductions in organ-weights and in blood packed-cell volume and haemoglobin levels. (3,4,5,32,33). In addition, Ligula exhibits an unusual intimacy with the pituitary-gonadal axis of its host. With the exception of gudgeon (Gobio gobio), in all cyprinids examined,
Ligula-infection is associated with a lack of host gonadal development, which prevents the fish from reproducing. Associated changes in the cytology of the pituitary gland are not restricted to the normal host, but also occur in the toad, Xenopus laevis, and these are similar to those found in non-infected animals following testosterone implantation.
Ligula-infections of gudgeon, however, are unusual in several respectsi in particular the inhibition of gonadal development is less marked than in other cyprinid hosts. Observations using electrophoretic techniques have offered a possible explanation of this enigma viz. that the ligulid infecting gudgeon may be a species different froiitthat infecting other Cyprinidae.(4,5,37,B1,B2,B8). Experimental and ultrastructural studies
(11,36,44,45,59) have been employed to study the cells of the host-tissue response and the mechanism whereby the plerocercoid can survive in the potentially hostile environment of the body cavity of the fish host. Eubothrium crassum is a pseudophyllid that is found as an adult in the intestine of trout. The scolex is located in a pyloric caecum, with the strobila extending back into the gut lumen. This unusual site-preference, shown by the worm, prompted studies on aspects of its biology and that of its fish host (20,28). Ultrastructural studies showed that the scolex of the worm contained gland cells of a type not previously described in cestodes (B4).
B. Studies on Hymenolepis diminuta (Publication numbers 6,7,8,9,10,12,14,18,19,22,41,46,48,49,51,52,53,55,56,58,B2,B3,B5,B6,B7,B8)
These papers describe studies in vivo and in vitro on aspects of the biology of the rat tapeworm. For the purpose of this commentary the work is presented under three main headings, although it is emphasized that there exist within the publications, numerous overlapping themes.
(i) Studies on nutrition in adult Hymenolepis diminuta include the first accounts of the kinetics of fatty acid uptake by cestodes (6,9). Publication (8), describes the fluxes of amino acids between the rat and parasite in vivo and demonstrates that patterns of nutrient-flow in vivo are predictable from data collected in vitro. This paper also attempted to address important questions relating to host physiology, in particular the extent to which endogenous amino acids contribute to the lumenal free amino acid pool. Paper (12) describes the characteristics of a phosphohydrolase active at the surface of the parasite. In addition to demonstrating a digestive capacity of the cestode tegument, and permitting the development of the concept of the cestode surface as a digestive-absorptive epithelium, this publication provided a direct stimulus for many further studies (for example by s.c. Dike and P.W. Pappas). Publications (47,B3,B5) contain detailed comments on the significance of these findings. Prior to 1971, all reported studies on the nutrition of Hymenolepis dealt with the 10-day-old adult worm. However, the cysticercoid is a stage in the life cycle of the parasite that inhibits the haemocoel of certain Coleoptera, an environment that contrasts sharply, in many of its
physico-chemical characteristics, with the lumen of the rat intestine. Publications (14,18,19,49,55,58) represent attempts to analyse the properties of the membrane transport systems in rnetacestodes. It is clear from these studies that membrane uptake systems, in both cysticercoid and adult worm, share many features in common. However a major difference has been found in the
apparent Kt of proline, with higher values in metacestodes being possibly related to high concentrations of proline in host haemolymoph (see publication 51).
(ii) Studies on metacestode biology have recently been extended to include observations on the pathophysiology in Tenebrio molitor (Coleoptera), associated with H. diminuta infections (51,52). Striking physiological and biochemical evidence has been obtained indicating that the parasite interferes with parts of the host endocrine system (possibly the corpora allata), affecting various aspects of beetle fecundity.
(iii) Collaborative studies with Professor L.T. Threadgold and Dr. K.S. Richards have attempted to provide a bridge between ultrastructure and function, with special reference to nutrition and physiology (7,10,33,56) and metacestode development (41,46,48,53).
c. Parasite form and function : ultrastructural studies
(Publications 21,34,35,3.8,39; see also papers listed in A and Biii above)
All too often, specialists in different research disciplines disregard benefits that may accrue from an interdisciplinary approach to problems of mutual interest. The papers listed above are offered as evidence of the value of such collaborative investigations in Fasciola hepatica and Caryophyllaeus laticeps.
D. Studies on Monogenea
(Publications 13,15,23,24,26,27)
For reasons outlined in publication (23), prior to the papers listed above, virtually no data on the physiology and biochemistry of Monogenea were available. In Northern Ireland, the ready availability of the marine gill-fluke, Diclidophora merlangi, permitted the development of in vitro techniques for its maintenance and study. Observations on occurrence, chemical composition and oxygen and amino acid metabolism were undertaken.
E. Studies on metacestodes of Echinococcus granulosus
(Publications 42,43,50,57)
The hydatid organism is the third species of metacestode currently under investigation at Keele, (the other two being Rymenolepis diminuta and Ligula intestinalis, see above) Despite the medical and veterinary importance of this species, surprisingly little is known concerning much of its basic biology when compared, for example, with a common laboratory model like Hymenolepis diminuta. Use of even the most promising chemotherapeutic agents, the benzimidazoles, has achieved only very variable degrees of success in hydatidosis and it is therefore believed that studies on the basic membrane physiology and biochemistry of the parasite may be a necessary pre-requisite for the rational design of chemicals for use in hydatid therapy. Echinococcus will undoubtedly feature large in the work of the applicant in the future; however, it is a relatively new area of study and, to date, only papers relating to in vivo and in vitro culture and the lysosomal system have been published.
F. Miscellaneous publications
(Publications 1,16,17,25,29,30,31,40,47,54)
G. Books, parts of books and reviews
(Publications B1-BB)
A number of opportunities have been taken to review aspects of parasite physiology and biochemistry. Publications B6 - B7 represent an attempt to bring together, in two volumes, articles by experts on the broad sp'ectrum of tapeworm biology.
H. Material submitted for another degree
Parts of the data incorporated into publications (1,2,3,4 and 5) were submitted in a thesis for which I was awarded the degree of Doctor of Philosophy by the University of Leeds in 1964. The publications are included here because, in all cases but (1), additional material from post-doctoral studies was incorporated into them.
I. Comments on contributions to co-authored papers
In all con-joint studies I have played the principal role in terms of their initiation and direction and, before 1979, I was also largely responsible for all laboratory work. Post-1979, although I have always made contributions to bench work, these have inevitably been variable and constrained by other University commitments. In ultrastructural studies my principal role has been the experimental manipulation of parasites (often equalling

Publication Date Jan 1, 1986

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