The parasites, predators, places and people I have known: a great adventure
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Transcript of The parasites, predators, places and people I have known: a great adventure
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The parasites, predators, places and people I have
known: a great adventure$
Max Murray*
The University of Glasgow Veterinary School, Bearsden Road, Bearsdon, Glasgow G61 1QH, UK
Abstract
I am extremely proud to receive the WAAVP/Pfizer Animal Health award, and particularly so in
Africa, the continent where I have spent a large part of my professional life. In the nearly 40 years
in research I have had the privilege and excitement of being involved with many great parasites,
predators, places and people. In my early days in Kenya I saw all the great wild animal predators,
but soon came to appreciate that the greatest predator of all was disease, particularly parasitic
disease, with the devastating effects of tsetse and ticks and the infections they transmitted, and of
the all-prevailing roundworms. I learned several key lessons while working with research teams to
develop better diagnostics, to improve epidemiological understanding as a basis for rational
treatment and control, and to extend the understanding of disease processes with the view to
developing novel methods of treatment or prevention. The Power of Pathology in diagnosing
diseases, identifying new diseases and as a major tool for pathogenic diseases. The Power of
Pathogenesis in identifying key mechanisms that led to new diagnostic techniques, improved
methods of treatment, and possibly to future vaccines. The Power of Application of what we already
know; while recognising that molecular biology will make a massive contribution to improving
animal and human health, it is important to appreciate that we already have a very powerful
armamentaria to diagnose, treat, control or prevent disease, and when used properly they have been
successful and cost-effective. The Power of Genetic Resistance: the recognition that certain species,
certain breeds, and certain individuals within breeds possess remarkable resistance to certain
parasitic diseases such as trypanosomosis and helminthosis, and that this trait is genetically
correlated with production, opens up a very powerful additional approach to improving animal
health. The Importance of Measurement: I completely endorse the sentiments of Lord Kelvin,
Professor of Natural Philosophy at Glasgow University who stated in 1846: `̀ When you can
measure what you are speaking about, and express it in numbers, you know something about it: but
when you cannot measure it, your knowledge is of a meagre and unsatisfactory kind.'' This applies
Veterinary Parasitology 81 (1999) 149±158
* Tel.: +44-141-339-8855; fax: +44-141-942-7215; e-mail: [email protected]$WAAVP Pfizer Award for Excellence in Research in Veterinary Parasitology , Presented at the 16th WAAVP
conference, held in Sun City, South Africa in August 1997. Plenary papers from this conference have beenpublished in Veterinary Parasitology (vol 71, pp. 67±222).
0304-4017/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 4 0 1 7 ( 9 8 ) 0 0 2 4 2 - 8
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very much to Parasitology. The future is bright. The combination and integration of the new
technologies of Biotechnology, Mathematical Methods and Bioinformatics coupled with advances
in Computer Power will produce new standards in animal and human health in the 21st century.
New methods of predicting, diagnosis, treating, controlling, prognosing and preventing disease will
become available. WAAVP has a major role to play by ensuring that veterinary parasitologists are
provided with the proper training, infrastructure and forum to advance new technologies and that
the veterinary profession plays a leading role in the future direction they take. # 1999 Elsevier
Science B.V. All rights reserved.
1. Introduction
I am greatly honoured to receive the WAAVP/Pfizer award in veterinary parasitology
and to be given the opportunity to wander down memory lane with the parasites,
predators, places and people I have known. In the early 1960s when I was employed at the
Veterinary School at Kabete, Nairobi, Kenya I had the privilege to work with the Kenya
Game Department and others involved with wildlife. At that time, I saw both the beauty
and the savagery of the great wild animal predators of Africa: the lion, leopard, cheetah,
hyena etc., as well as the destruction that the magnificent elephant could invoke on local
agriculture. However, I soon came to appreciate that the greatest predator of all was
disease; for example, the effects of tsetse and ticks and the infections they transmitted,
and the all-prevailing roundworms, were devastating. As a consequence, much of my
professional life has been devoted to the challenge of disease, particularly parasitic
disease. I would now like to share with you some of the experiences I have had and some
of the lessons I have learned since my early days in East Africa. The lessons that taught
me the power of pathology, the power of pathogenesis, the power of application of what
we already know, the power of genetic resistance and the power of measurement.
* The power of pathology
Bill Jarrett stimulated me from the day I first met him in 1960 and still continues to do
so. Bill has been the most exciting and brilliant researcher with whom I worked. He is an
intellectual colossus. Bill showed me the Power of Pathology in Diagnosing Disease,
Identifying New Disease and in Understanding of Pathogenesis.
My first necropsy in Africa in September 1963 was carried out on rare Hunters
Antelope which had been dying in large numbers. It was done on a muram road in the
Tsavo National Park with David and Daphne Sheldrick and Tony Harthoorn. Bill helped
me to confirm that the problem was widespread Muscular Dystrophy in these and other
antelope species (Jarrett et al., 1964). The response to Vitamin E/selenium treatment was
dramatic: no more deaths ± The Power of Pathology.
* The power of pathogenesis
I was again privileged to study the pathogenesis of parasitic disease with
multidisciplinary groups comprising giants in the subject, Bill Jarrett, Ian McIntyre,
George Urquhart, Bill Mulligan, Frank Jennings and of course, Jimmy Armour.
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One of the most productive and enjoyable periods was our investigations into
ostertagiosis in cattle and sheep. This parasite produces a remarkable hyperplastic
gastritis in which the key event is the replacement of the functional differentiated gastric
gland cells, including the acid-secreting parietal cells, by rapidly dividing undiffer-
entiated cells (Murray et al., 1970) with the consequence that,
1. abomasal pH becomes elevated with the result that pepsinogen is not activated to the
proteolytic enzyme pepsin with the consequent failure to initiate digestion. At the
same time, there is a logarithmic increase in bacteria in the abomasum;
2. the tight junctions between the rapidly dividing undifferentiated cells are not properly
formed, allowing protein to leak between cells and resulting in a protein-losing
gastropathy.
An exciting finding was that the new benzimidazole drugs by effectively removing all
parasite stages, rapidly reversed these pathogenic processes (Armour et al., 1967).
Subsequently, with Bill Jarrett and Hugh Miller we studied the pathogenesis of worm
expulsion from the gastrointestinal tract using the model system of Nippostrongylus
brasiliensis in the rat, as well as ostertagiosis in cattle and sheep. It was established that
immediate hypersensitivity reactions with subepithelial mast cell proliferation, discharge
of their vasoactive compounds, and consequently related mucosal hyperpermeability
appeared to play a key role in the exponential expulsion of worms from the
gastrointestinal tract (Murray et al., 1971; Murray, 1972). It was also shown by
histochemistry and electron microscopy that the intra-epithelial globule leukocyte (a cell
frequently found in association with mucosal parasitism) was in fact a sub-epithelial mast
cell that had discharged its vasoactive compounds, and was not, as had previously been
proposed, a Russell body-containing plasma cell (Murray et al., 1968).
Other important lessons learnt were that objective quantified clinical observations
often hold the key to identifying and understanding what the important pathogenic
processes are, and that disease is a kinetic process that can change with time. An
outstanding example of this was the appreciation that anaemia was the key indicator of
disease status and process in bovine African trypanosomosis. Many workers throughout
the ages recognised that anaemia was an important disease factor in bovine African
trypanosomosis, but it was Ian McIntyre who appreciated that it was the key driving force
in the disease process and the key marker in evaluating the status and severity of the
disease in any one particular animal (Morrison et al., 1981). We soon realised that several
factors contributed to the onset and progress of the anaemia and that the relative
importance of these factors changed with time (Murray and Dexter, 1988). Thus while
there was a highly significant correlation between the intensity of parasitaemia and the
severity of anaemia over time, in a one-off examination, an animal could be parasitaemic
but not anaemic; equally, it could be anaemic but not detectably parasitaemic.
More recently with advances in technology we are in a position as never before to
investigate and understand disease processes at the molecular level with the real hope that
such an understanding will lead to improved methods of diagnosing, treating or even
presenting disease. An example of this approach involved Peter Kennedy, the brilliant
Burton Professor of Neurology at Glasgow and Frank Jennings; in these studies we used a
mouse model system developed by Frank to study the neuropathogenesis of African
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trypanosomiasis. This model simulates all phases of human African trypanosomosis
(HAT). We found in both in vivo and in vitro studies that astrocytes stimulated directly by
trypanosomes appear to play a pivotal role in producing the cytokines that initiate and
maintain the severe meningoencephalitis that is the main feature of the disease (Hunter
et al., 1992). Subsequently, it was shown that the polyamine inhibitor eflornithine
appeared to selectively block cytokine production by astrocytes and this drug could be
used to prevent or ameliorate the CNS inflammatory process (Jennings et al., 1997).
Further, it was demonstrated that antagonists of substance P (a neuropeptide) had a
significant effect in alleviating the CNS pathology (Kennedy et al., 1997). Both these
findings could lead to novel treatments of HAT and other cytokine-mediated
inflammatory conditions in man (including HIV encephalitis) and animals.
For the first time, it was found using this mouse model that the highly toxic arsenical
drugs which are given intravenously to treat HAT can be administered topically thereby
avoiding the serious side effects of intravenous usage (Jennings et al., 1996). At the same
time, it was shown that the dose of a topical arsenical drug could be reduced by topical
combination chemotherapy with other trypanocidal drugs. While this work was carried
out in the mouse model system, we believe that it will have major significance for the
treatment of HAT. It is another example of the amazing innovative creativity of Frank
Jennings who has contributed so much to improve chemotherapy in African
trypanosomiasis.
* The power of application of what we already know
Molecular biology is making and will make a massive contribution to future
approaches to improving animal and human health. However, we should not forget that
we already have very powerful tools available and that these tools have been and can be
highly successful if used properly. Of the tools available, possibly the most powerful and
least recognised is the clinician/epidemiologist. This is a lesson I learned from Ian
McIntyre and subsequently John Trail in a number of Animal Health Control programmes
in which we were involved in tsetse-infested Africa. Ian, with his understanding of the
disease in both the individual animal and in the herd, played a key role in the successful
implementation of chemoprophylactic and or therapeutic trypanocidal drug control
programmes in beef ranches (Mkwaja Ranch in Tanzania: (Trail et al., 1985), in dairy
ranches (Kilifi Plantations in Kenya: Murray and Trail, 1986), in advising in village/small
holder situations (Muhaka Villages, Coast Province of Kenya; Maloo et al., 1988) etc.
With accurate diagnosis of animal health problems, strategic use of drugs, effective
analysis of databases, demonstration of cost-effectiveness and involvement of the owners,
highly successful sustainable livestock programmes have been maintained in several
tsetse-infested areas of Africa. For one such programme (Muhaka in Kenya), we were
awarded a British Government DTI Technology Transfer Industry Year Award in 1986 for
the successful implementation of Animal Health Control Programmes in Developing
Countries. This award to Glasgow University Veterinary School was in partnership with
May and Baker Pharmaceuticals (James McAinsh and David Niven), International
Livestock Centre for Africa (ILCA, John Trail), International Laboratory for Research on
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Animal Diseases (ILRAD) and Ministry of Agriculture and Livestock Development of
Kenya (Seif Maloo and Sam Chema).
* The power of genetic resistance
During my African Adventure, it became obvious to me, as it had to many others, that
certain breeds of cattle and small ruminants were able to survive in tsetse-infested areas
where other breeds such as Bos indicus-types and imported exotics rapidly succumbed, if
left untreated. This trait was termed trypanotolerance and has been attributed mainly to
the indigenous taurine breeds of cattle in West and Central Africa, namely, the N'Dama
and the West African Shorthorn. However, while this trait has been recognised for many
years and these animals are the core breeds for livestock and mixed agricultural
development in many areas of West and Central Africa, they still make up only a small
proportion of the cattle breeds of Africa, even in tsetse-infested areas. The main reasons
for this are that because of their smaller stature they were believed to have poor
productive potential, and that their resistance was thought to be acquired only to local
populations of trypanosomes with the result that if moved to a distant location they would
be fully susceptible.
However, standing with Ian McIntyre in a small holding in a tsetse-infested area
of The Gambia looking at N'Dama, as fat as butter, grazing with emaciated Zebu
immediately convinced us that this trait and these animals offered a powerful weapon
in our fight against the tsetse fly. Again driven on by Ian McIntyre and later by the
amazing quantitative talents of John Trail ably assisted by Guy d'Ieteren a
complementary series of field and laboratory studies showed that the trypanotolerant
breeds of cattle had unique characteristics that could be exploited in the development of
livestock production and agriculture in tsetse-infested Africa (Murray et al., 1982, 1991;
Trail et al., 1991).
It was confirmed that trypanotolerance was an innate trait characterised by the capacity
to control parasitaemia and the ability to resist the development of anaemia. Such animals
possessed a superior immune response to variable and non-variable trypanosome
antigens, had a better immunological memory and had a greater capacity to acquire
resistance to the effects of infection. This was confirmed in N'Dama taken from The
Gambia to ILRAD as embryos (Jordt et al., 1986). It was also found that these animals
had significant resistance to ticks, tick-borne infections and helminths.
In a magnum opus involving 18 countries in West and Central Africa, John Trail and
his colleagues at ILCA (ILCA, 1979) computed that trypanotolerant breeds were at least
as productive as Bos indicus breeds in areas of no or low tsetse risk, in areas where the
tsetse risk was higher comparison was not possible because only trypanotolerant breeds
were present in significant numbers. In The Gambia first at MRC Fajara and later at the
International Trypanotolerance Centre, it was demonstrated that the N'Dama if properly
managed and fed, possessed remarkably dual purpose potential in terms of milk and meat,
as well as making excellent oxen.
The main clinical manifestation of the disease, namely, anaemia and the ability to resist
it, and the main parasitological manifestation, namely, parasitaemia and the ability to
control it, were found to be variable within the breed but were repeatable, heritable and
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positively genetically correlated with production. This showed for the first time that,
using these phenotypic criteria, programmes for identification, selection and improve-
ment of the resistance and productive traits, both in trypanotolerant and other breeds are
possible.
More recently workers in Glasgow, in particular Mike Stear, working in collaboration
with Kenya Agricultural Research Institute (KARI) and Roslin Institute (Edinburgh) have
been investigating the question of genetic resistance of small ruminants to helminthosis.
Firstly, the earlier observations of John Preston and Ed Allonby (Preston and Allonby,
1979) of the remarkable resistance of the Red Maasai sheep in Kenya to Haemonchus
contortus were confirmed (Mugambi et al., 1997). This work was extended to British
sheep, particularly Scottish Blackface, and the major helminth parasite of temperate
climates Ostertagia (Telodorsagia) circumcincta. In an outstanding multidisciplinary
series of studies (Stear et al., 1997a, b) involving molecular genetics, quantitative
genetics, immunology, pathology, parasitology, clinical evaluation, animal production
and nutrition and epidemiology, Mike Stear and his group demonstrated: remarkable
within-breed variation in faecal egg output in both field and laboratory studies; using
faecal egg output as a marker for resistance, it was shown that resistance to O.
circumcincta was a heritable trait that was genetically correlated with growth rate. A gene
was identified that strongly affects faecal egg production; it is one of the most powerful
parasitic disease-resistant genes demonstrated to date. The basic mechanism of the
resistance trait would appear to be related to the host's ability to regulate egg production
within the worm; this is significantly correlated to worm length which is strongly
correlated to the quantity and specificity of local IgA production. The immediate
hypersensitivity reaction, discussed earlier, that is associated with worm burden kinetics
in the gastrointestinal tract does not appear to have a role in regulating worm length and
fecundity, but is associated with expulsion of adult worms from the gastrointestinal tract.
At the same time, a strong and significant interaction has also been found between
genetic resistance and nutrition, for example, resistant breeds thrive on diets which are
inadequate for genetically susceptible animals while susceptible breeds show a marked
increase in resistance and productivity following dietary supplementation.
Although much still requires to be done, the knowledge already available makes
selective breeding feasible and this has now been initiated in commercial flocks.
* Importance of measurement
Lord Kelvin who was 22 years old when he was appointed to the Chair of Natural
Philosophy (Physics) at Glasgow University stated in 1846: I often say that when you can
measure what you are speaking about, and express it in numbers, you know something
about it: but when you cannot measure it, your knowledge is of a meagre and
unsatisfactory kind.
This statement, which is possibly even more relevant now than it was then, bearing in
mind the mass of data and information that we have to deal with in all aspects of our
lives, was inculcated in my psyche by Bill Jarrett, John Trail and George Gettinby.
Biological studies, whether in the field or in the laboratory, must be properly measured
and quantified.
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The equation I have evolved during my working life is something like
M1 �M2 � E1
E2� TT � SS
where
M1 medicine and disease research
M2 measurement, quantification
E1 cost-effectiveness (socially acceptable)
E2 environment (socially acceptable)
TT dissemination of knowledge
SS sustainable solutions
* The places where the lessons were learned
Glasgow has played a major influence in my work. I graduated from Glasgow and I am
now proud to be a member of the staff. The university will be 550 years old in 2001; it is
the fourth oldest university in the UK and the 17th oldest in the world. The university is
the heart beat of a city with an incredible academic and industrial heritage. Just 100 years
ago, 80% of all ships afloat were Clyde-built with the launching of 1000 ships per year,
an astonishing three per day. Times have changed but Glasgow still flourishes and as you
know is now a major centre of excellence in Parasitology, an achievement that was
unquestionably stimulated by Jimmy Armour and what Jimmy and I call the big 5, Jarrett,
McIntyre, Urquhart, Mulligan and Jennings, who, by developing the first and as far as I
know still the only commercially produced parasitic vaccine against the bovine lung
worm Dictyocaulus viviparus over 40 years ago, laid the foundation for modern
Parasitology (Jarrett et al., 1960).
My path led to Africa. Africa covers 30 million km2, one-fifth of the world's land
mass. It is a continent dominated and constrained by disease, for example, tsetse flies
infest some 50% of the land available for agricultural development. In 1963 we went to
East Africa, to Kenya, to the Veterinary Faculty at Kabete which Ian McIntyre
transformed virtually overnight to produce the first-ever veterinary graduates of the
University of East Africa, a programme that was supported by the incredible foresight of
the Rockefeller Foundation and John McKelvey Jr. It was at this time the concept of
developing a world class research laboratory located in Africa was created. This
laboratory would bring to bear on tropical disease the best brains in the world. What a
magnificent dream! After many international meetings and politicising held mainly at the
Villa Serbaloni, the magnificent facility owned by the Rockefeller Foundation at
Bellagio, Lake Como, ILRAD was established in Nairobi under the auspices of the
Consultative Group on International Agricultural Research (CGIAR). It is important to
recognise that it was Ian McIntyre, and John McKelvey and John Pino of the Rockefeller
Foundation who were the driving force to create what was arguably the finest Animal
Disease Research Institute in the world. I was the first scientist appointed in 1975 by the
then Director General, Jim Henson. Consequently the same team, Ian McIntyre and John
McKelvey, with the encouragement of Sir Dawda Jawara, the then President of The
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Gambia and a Glasgow Veterinary Graduate, established the International Trypanotoler-
ance Centre (ITC), a laboratory created to develop and exploit the disease resistance trait
by carrying out more applied research in the laboratory, and adaptive research in the
villages and small holdings of the Sene±Gambia which in themselves represented a
unique field laboratory. I was very privileged to be an active member of the group and to
work with many great men, including, Bakary Sanyang, Bakary Touray, Tony Davies and
the irrepressible Jos Mortelmans. This African experience was strengthened by my long
relationship with the World Health Organisation (WHO) and the Special Programme for
Research and Training in Tropical Diseases. There I learnt much about Africa from the
dedicated Peter De Raadt of the WHO who directed a highly successful programme,
Adriel Njogu, the first Director General of the Kenya Trypanosomiasis Research Institute
and one of the world's great gentlemen, and the energetic David Molyneux, currently
Director of the Liverpool School of Tropical Medicine.
* The future
The future is bright. While major achievements have been made in our ability to
diagnose, treat, control and prevent disease, much still needs to be done. There is no
doubt that modern science has the technology to make massive inroads into reducing the
still enormous economic losses caused by disease.
Biotechnology is developing new diagnostics, new vaccines, new therapies and even
designer animals; Biomathematics is now recognised as a very powerful tool that ensures
proper quantification, measurement, analysis and modelling of biological processes;
Bioinformatics, by exploiting medical and other data through the use of the massive
analytical power of computers and the Information Technologies, is providing a totally
new approach to interpretation and decision support by improving our capabilities in
diagnosing, prognosing, predicting and preventing disease, thereby, allowing much more
effective application of treatment and control measures. At the same time, the
miniaturisation of the engineering technologies backed by computerisation means that
a whole new generation of Smart Machines is becoming available; these will provide, not
only results rapidly and reliably in a user-friendly way, but also decision support back up
for understanding what the results mean. The VS2000 being developed at The University
of Glasgow Veterinary School is an example of a forerunner of the Smart Machine. This
instrument is a haematology analyser that is high-tech, low cost and easy to use; it not
only delivers results but helps the clinician to interpret what they mean.
The combination and integration of the developments in Biotechnology, Mathematical
Methods and Bioinformatics coupled with advances in Computer Technology and Smart
Machines will establish new standards in Animal and Human Health in the 21st century.
These are lessons I have learnt from George Gettinby, Colin Johnstone, Roger Clampitt
(of VetTest 8008 fame) and Stuart Reid, the recently appointed Professor of Veterinary
Informatics and Epidemiology. Stuart is a veterinary graduate who has been trained in
molecular biology, statistics and epidemiology. He is one of the first joint professorial
appointments between the Universities of Glasgow and Strathclyde. Our initiative in
veterinary informatics would not have been possible without the remarkable foresight and
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support of Dr. Elisabeth Svendsen of The Donkey Sanctuary, and of Professor Derek
Tavernor, James McAinsh, the late Brigadier John Spurry and Paul Irby of The Home of
Rest for Horses.
It is essential that the veterinary profession embraces these technologies to ensure that
we play a leading role in the future direction that they take.
It is reassuring to see at this conference that the WAAVP is pro-active in all of these
areas.
Acknowledgements
In conclusion, I would like to thank WAAVP/Pfizer Animal Health for this award. I am
extremely proud to be recognised in this way and particularly pleased to receive the
award in Africa, the continent I love and where I have learned so many of my lessons. I
cannot let this occasion go by without recognising the presence and the achievements of
Lord and Lady Soulsby, Lawson and Annette ± we know that beside every great man is an
even greater woman. Lawson has been the Le Patron of WAAVP in particular and of the
Veterinary Profession in general. Lawson encouraged, stimulated and supported me from
the moment we met over 30 years ago, as he has done for so many in the audience. I know
everyone would agree that he is a true Social and Academic Aristocrat.
Finally, and most of all, I would like to recognise the support of my family, particularly
over the last few years, my beautiful wife Christine, my daughters, Katie and Kirsty, and
my son, Max. As James Cagney once said in the wonderful movie `Yankee Doodle
Dandy,' `̀ My mother thanks you, my father thanks you, my family thanks you and I
thank you.'' It has been a `Great Adventure.'
References
Armour, J., Jennings, F.W., Kirkpatrick, K.S., Malczewski, A., Murray, M., Urquhart, G.M., 1967. The use of
thiabenzadole in bovine ostertagiasis: Treatment of experimental type I disease. Vet. Rec. 80, 510±514.
Hunter, C.A., Jennings, F.W., Kennedy, P.G.E., Murray, M., 1992. Astrocyte activation correlates with cytokine
production in the central nervous system of Trypanosoma brucei brucei-infected mice. Lab. Invest. 67,
635±642.
ILCA, 1979. Tyrpanotolerant Livestock in West and Central Africa, Monograph 2, ILCA, Addis Ababa,
Ethiopia.
Jarrett, W.F.H., Jennings, F.W., McIntyre, W.I.M., Mulligan, W., Urquhart, G.M., 1960. Immunological studies
on Dictyocaulus viviparus infection. Immunity produced by the administration of irradiated larvae.
Immunology 3, 145±151.
Jarrett, W.F.H., Jennings, F.W., Murray, M., Harthoorn, A.M., 1964. Muscular dystrophy in wild Hunter's
antelope. East African Wildlife J. 2, 158±159.
Jennings, F.W., Atouguia, J.M., Murray, M., 1996. Topical chemotherapy for experimental murine African CNS-
trypanosomiasis: the successful use of the arsenical, melarsoprol, combined with the 5-nitroimidazoles,
feximidazole or MK-436. Tropical Medicine and International Health. 1, 590±598.
Jennings, F.W., Gichuki, C.W., Hunter, C.A., Rodgers, J., Kennedy, P.G.E., Murray, M., Burke, J.M., 1997. The
role of the polyamine inhibitor eflornithine in the neuropathogenesis of experimental murine African
trypanosomiasis. Neuropathology and Applied Neurobiology. 23, 225±234.
Jordt, T., Mahon, G.D., Touray, B.N., Ngulo, W.K., Morrison, W.I., Rawle, J., Murray, M., 1986. Successful
transfer of frozen N'Dama embryos from The Gambia to Kenya. Trop. Anim. Health Prod. 18, 65±75.
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Kennedy, P.G.E., Rodgers, J., Jennings, F.W., Murray, M., Leeman, S.E., Burke, J.M., 1997. A substance P
antagonist, RP-67,580, ameliorates a mouse meningoencephalitic response to Trypanosoma brucei brucei.
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