Newcastle Disease

British Poultry Science
ISSN: 0007-1668 (Print) 1466-1799 (Online) Journal homepage: http://www.tandfonline.com/loi/cbps20
Newcastle disease
Dennis J. Alexander
To cite this article: Dennis J. Alexander (2001) Newcastle disease, British Poultry Science, 42:1,
5-22, DOI: 10.1080/713655022
To link to this article: http://dx.doi.org/10.1080/713655022
Published online: 28 Jun 2010.
Submit your article to this journal
Article views: 895
View related articles
Citing articles: 78 View citing articles
Full Terms & Conditions of access and use can be found at

http://www.tandfonline.com/action/journalInformation?journalCode=cbps20
Download by: [Gadjah Mada University]
Date: 17 February 2016, At: 12:21
British Poultry Science (2001) 42: 522
GORDON MEMORIAL LECTURE
Newcastle disease
DENNIS J. ALEXANDER
Downloaded by [Gadjah Mada University] at 12:21 17 February 2016
Avian Virology, VLA Weybridge, Addlestone, England

Abstract 1. In this paper several historical and contemporary aspects of Newcastle disease (ND) are
reviewed, with particular reference to the greater understanding which modern techniques have
allowed.
2. Virulent ND viruses were generally thought to have emerged in 1926 as a result of transfer from a
wild bird host reservoir but there is evidence that the virulent virus may have existed in poultry before
1926. Recent findings suggest that the virulent virus may emerge in poultry as a result of mutations
in viruses of low virulence.
3. The history of ND in Great Britain reflects the four known panzootics that have occurred and
serves as a model for the impact this disease may have on poultry populations.
4. Attempts to control and eradicate ND are not as straightforward as it may appear; in particular
vaccination, while preventing deaths and disease, on challenge may not prevent virus replication and
could therefore lead to the virulent virus becoming endemic.
5. Village chickens are extremely important assets in most developing countries, representing a
significant source of protein in the form of eggs and meat but endemic ND can cause mortality of up
to 60% in village chickens.
I run eight hundred hens to the acre.

They die by dozens mysteriously . . .
I am more than doubtful concerning my Maker.
Why has the Lord afflicted me?
From Natural Theology
by Rudyard Kipling, August 1914
INTRODUCTION
The virulent forms of Newcastle disease virus
(NDV) cause a devastating disease of poultry. As
stated previously (Alexander, 1988a), hardly a
single commercial flock of poultry is reared that,
if not infected, is not influenced in some way by
measures aimed at controlling ND and spread of
the virus. In many areas where poultry are reared
commercially reliance is placed on vaccination to
keep ND in check, but ND nevertheless represents a major limiting factor for increasing
poultry production in many countries.
The greatest impact of ND may well be on
village or backyard chicken production (Spradbrow, 1993). In developing countries throughout
Asia, Africa, Central America and some parts of
South America the village chicken is an extremely
important asset representing a significant source
of protein in the form of eggs and meat. However,
ND is frequently responsible for devastating
losses in village poultry. For example, Spradbrow
(1992) estimated that each year 90% of the village
Dennis J. Alexander 18th Gordon Memorial Lecturer
chickens in Nepal die as a result of ND. Social and

financial restraints mean the control of ND in
village chickens in developing countries is
extremely difficult, if not impossible, and this situation impinges on the further development of
Correspondence to: Dennis J. Alexander, Avian Virology, VLA Weybridge, Addlestone, Surrey KT15 3NB, England. E-mail:
dalexander.vla@gtnet.gov.uk
This lecture, the 18th given in memory of the late Dr R. F. Gordon, was delivered at the Spring meeting of the UK Branch of
the Worlds Poultry Science Association in Scarborough March 2000
ISSN 00071668(print)/ISSN 14661799(online)/01/01000518 2001 Crown Copyright
DOI: 10.1080/0007166002003503 7
DENNIS J. ALEXANDER
commercial poultry production and the establishment of trade links.

It is rare to have the unrestricted choice of
writing on a subject in which one is so intimately
involved. I have taken this opportunity to review
three disparate areas of ND that I believe put our
present understanding of this most important
disease of animals into context and to indicate
areas where future developments are essential.
Firstly, the emergence of ND because I believe it
is not as straightforward as accounts written to
date would have us believe and that the retrospective application of modern techniques has
given a greater insight into possible mechanisms
involved in the emergence of virulent NDV
strains. Secondly, the history of ND in Great
Britain because there are careful records of the
disease in Great Britain since 1926, but these
have not been put together in a single account
for many years. In Great Britain the effect ND
has had on the poultry industry may be considered an example of the situation in a developed
Western country. Thirdly, control of ND
because this represents the biggest challenge for
the future and, to date, attempts at control have
been often inept and unsuccessful.
Emergence of a new disease
The beginning
The text books insist that the history of Newcastle
disease (ND) began in 1926 with the description
of a highly pathogenic disease at two geographical
sites on different sides of the world, Newcastle-onTyne, England and the island of Java, now part of
Indonesia (Doyle, 1927; Kraneveld, 1926).
However, in the literature there is some evidence
that there may have been outbreaks of disease very
similar to ND before 1926. It seems unlikely that
the disease Kipling had in mind in his poem
written in 1914 was ND but it does give some idea
of the knowledge of diseases affecting poultry at
the beginning of the 20th century. It appears quite
possible that at a time when travel, communication and the international nature of commercial
poultry production were so very different from
today, ND outbreaks may have occurred, but
because of misdiagnosis or lack of reporting were
not drawn to the attention of the international
veterinary profession.
Widespread outbreaks of highly pathogenic
disease had been reported in poultry in Europe
and Asia throughout the mid-19th century and
there have been retrospective suggestions that
some of these outbreaks may have been ND.
One of the problems in assessing the accuracy of
potential outbreaks of ND prior to 1926, and
possibly some of those in subsequent years, is the
lack of pathognomonic clinical signs produced
by virulent ND virus infections. The greatest
difficulty is differentiating between ND and

highly pathogenic avian influenza (HPAI,
formerly known as fowl plague), as the latter also
causes respiratory signs and rapid high
mortality. It is known that HPAI was widespread
in many parts of the world during the last
quarter of the 19th and first quarter of the 20th
centuries and, as concluded by Lancaster
(1977), it seems much more likely that the 19th
century outbreaks were HPAI. At the time, many
eminent veterinarians working with poultry
diseases were quite sceptical of Doyles claim of
discovering a new disease (Doyle, 1927),
suggesting his virus was merely a form of HPAI
(Manninger, 1932). Doyle, clearly stung by this
questioning of his scientific ability, settled this
argument once and for all in his scathing paper
in 1935 (Doyle, 1935).
There is more compelling evidence that ND
might have occurred before 1926. Levine
(1964), citing Ochi and Hashimoto considered
that ND may have been present in Korea at least
2 years before its appearance in England and
Indonesia. But there are even earlier reports.
Descriptions of diseases in poultry that appear to
be very similar to ND, and distinguishable from
HPAI, were published at the beginning of the
20th century. For example, Halasz (1912)
reported a very pathogenic disease of both
pigeons and poultry in which nervous signs were
a prominent feature.
However, possibly the most persuasive argument for an outbreak of ND predating 1926 was
that put forward by MacPherson (1956). He was
convinced that a mysterious disease resulting in
the death of all domestic fowl in the Western Isles
of Scotland in 1898 was ND. This epizootic was
recorded in a contemporary Gaelic poem, Call
nan, Caero (The loss of the hens) by John Campbell. In this poem the important observation is
made that while the disease killed domestic fowl,
ducks were unaffected, this would apply equally to
ND and HPAI. However, in his PhD thesis
MacPherson quotes Alexander Campbell from
the Isle of Skye, who had witnessed the disease
episode, as describing respiratory and nervous
signs in affected birds. The observation of nervous
signs suggests this was unlikely to have been HPAI
as, unlike ND, such signs are rarely seen.
MacPherson (1956) also makes the point of
the amazing similarity between the epizootic in
1898 and that occurring in 19491951 in the
Western Isles. The more recent epizootic was
thought to have been the result of introduction
of NDV by cormorants and shags, although the
evidence that these birds transmitted the disease
to poultry and not the other way round is somewhat circumstantial (Blaxland, 1951).
The possibility that cormorants represent a
source of virus has been raised again in recent
years as a result of a series of isolations from

double-crested
cormorants
(Phalacrocorax
auritus) in North America during the 1990s.
NDV had been isolated from cormorants in 1975
in Quebec (Cleary, 1977) but the more recent
outbreaks were first reported in 1990 in Alberta,
Saskatchewan and Manitoba in Canada
(Wobeser et al., 1993). In 1992 the disease reappeared in cormorants in western Canada,
around the Great Lakes and North Mid-West
USA, in the latter case spreading to domestic
turkeys (Mixson and Pearson, 1992; Heckert
1993, Meteyer et al., 1997). Disease in doublecrested cormorants was observed again in
Saskatchewan, in 1995 (Kuiken et al., 1998) and
in California in 1997 (Docherty and Friend,
1999). Antigenic and genetic analysis suggested
that all the 1990 and 1992 viruses were very
closely related despite the geographical separation of the hosts (Heckert et al., 1996). Because
these outbreaks involved birds that would follow
different migratory routes it seemed most probable that initial infection occurred at a mutual
wintering area in Central America. In addition
to this historical association of cormorants and
ND, it has also been demonstrated that in
cormorants infected experimentally, excretion
of pathogenic NDV occurs in the absence of clinical signs (Kuiken et al., 1998). It is tempting,
therefore, to speculate that these birds could
represent a natural reservoir of virulent NDV
that predates the emergence of the disease in
1926.
In his paper published in 1944 Beach
demonstrated that a virus (Stover, 1942) responsible for a disease first described some 9 years
earlier in poultry in California (Beach 1942) was
NDV. That this had not been recognised before
was due to the entirely different disease signs of
pneumonecephalitis and the low death rate in
infected poultry, which while variable was only
rarely above 15%. By 1946 NDV infections had
been identified in 17 states across the USA
(Lancaster, 1966) sometimes with evidence of
the presence of the virus as early as the 1930s.
Although inactivated vaccines were used initially
to combat ND in the USA, the continued isolation of mild strains led to the concept and
development of live vaccine strains. Beaudette et
al. (1949) selected the Roakin strain after
screening 105 NDV isolates of low virulence.
However, this strain proved too virulent for
young susceptible birds and strains B1
(Hitchner and Johnson, 1948; Hitchner, 1975)
and La Sota (Goldhaft, 1980) were selected and
were to become the most used animal vaccines.
In discussing the origins of ND in North
America most early reviewers such as Shope
(1964) considered that the USA virus was the
panzootic virus described by Doyle that had
undergone some modification. No writers have

given any credibility to the possible separate,
second emergence of a virulent virus.
Whether or not ND existed earlier, the
apparent emergence of ND as a highly pathogenic disease of poultry in 1926 initially
predominantly in SE Asia, but spreading rapidly,
suggested some sudden major change had
occurred either in the virus or its hosts. Hanson
(1972,1978) considered that the various hypotheses put forward could be grouped into three
categories { not quoted exactly} :
1. The virus had always been present as an
unrecognised disease of chickens. Changes in
the host population resulted in the selection
and emergence of the virulent virus.
2. The virus, essentially in its virulent form, was
enzootic in some other species in which it
produced no disease or an unrecognised
disease.
3. The virus originated at some point in time
and place as the result of a major mutation.
The first explanation remains a possibility. It
seems quite conceivable that the virulent virus
had always existed in poultry in SE Asia but it was
not until the beginning of the commercialisation of the industry in that part of the world that
the disease with its enormous economic impact
was noticed as a significant problem. Some
consider it unlikely that the disease would have
gone unreported if it was enzootic in village
chickens but even today village chickens
throughout Africa, Asia and the Americas often
show high levels of mortality either regularly or
as large die-offs every few years which go largely
undiagnosed.
The second explanation was favoured by
Hanson (1978) and was accepted generally as
the most likely until recent years. This was reinforced by the finding during the 1970 to 1973
panzootic, that movement of captive caged birds
particularly psittacines, which may be resistant
excreters, was to some extent responsible for the
introduction and spread in some regions, most
noticeably California (Francis, 1973; Walker et
al. 1973). As a result the theory that natural
reservoirs of virulent NDV existed in bird
species, particularly psittacines in tropical rain
forests was proposed and that spread to
domestic poultry occurred as a result of the
incursion of man into their habitat. It is always a
problem, as highlighted above with cormorants,
to know whether feral birds have introduced
virulent NDV to poultry or vice versa. Numerous
routine surveillance studies of feral birds
resulted in the isolation of ND viruses, especially
from waterfowl and other water-associated birds.
These viruses have invariably been of low virulence for chickens. Apart from the cormorants
DENNIS J. ALEXANDER
in North America described above, there have

been no reports identifying reservoirs of virulent
NDV in feral birds. There is no doubt that caged
birds infected with virulent ND have been
detected regularly in quarantine (Senne et al.,
1983; Panigrahy et al., 1993), but Kaleta and
Baldauf (1988) have suggested that caged birds
are most probably infected after they have been
trapped. Maintenance of virus in any feral bird
species affected by the virus seems unlikely
because of the effect infection is likely to have on
the survival of the bird.
The third explanation was considered
unlikely by Hanson (1972,1978) for two reasons.
Firstly, because ND appeared in several locations
at the same time, which he felt was not compatible with the emergence at a single origin with
subsequent dissemination. Lancaster (1976)
took issue with this point, drawing attention to
Doyles (1927) opinion that the early spread to
areas remote from the probable origins in Indonesia were due to transport by shipping, in
advance of a more natural spread. Secondly,
because at the time of writing Hanson (1978)
knew . . . of no other instance of a new virus
arising from another one by mutation . . ..
However, the advances in biotechnology over
the intervening years have been so great that
such possibilities can be investigated. It is now
widely accepted that in the case of avian influenza virus, not only have viruses of low virulence
mutated to high, but that this is the usual mechanism for the emergence of strains causing
highly pathogenic avian influenza (Garcia et al.,
1996; Perdue et al., 1998). Other drawbacks to
the emergence of virulent ND virus by mutation
are that the degree of change is too big to be
within the bounds of probability of occurring in
one step. Equally there is no apparent evolutionary advantage that would result in selection
of the intermediates if changes were brought
about by the accumulation of point mutations.
However, results obtained with viruses isolated
from ND outbreaks in Ireland and Australia
during the 1990s have suggested this may be how
some virulent ND viruses emerge. The evidence
for this is presented below.
It is tempting, taking the analogy with influenza even further, to hypothesise that in view of
the normal absence of virulent NDV in feral
birds, such mutations probably take place after
the virus has been introduced to poultry. The
mutation theory also has a further attraction in
that while it could be a relatively rare event it
may have occurred more than once in the 20th
century from different gene pools of viruses of
low virulence. This could explain marked differences seen between virulent ND viruses,
especially the greater antigenic and genetic similarity of viruses of high virulence in the USA with
some viruses of low virulence from the same

geographical area than with highly virulent
Eurasian viruses. In addition, virulent viruses
arising from an avirulent pool in feral birds may
well have occurred before 1926 and accounted
for the earlier reports of ND-like diseases.
Molecular basis of pathogenicity and the emergence of
virulent viruses
On the surface of NDV particles are two important functional proteins, haemagglutinin/
neuraminidase { HN} and fusion { F} , that can be
visualised in the electron microscope as spikes.
The HN protein is responsible for the attachment of virus particles to cell receptors and the
F protein brings about fusion between the virus
membrane and the cell membrane so that the
virus genome enters the cell and replication can
begin. The F protein is therefore essential for
replication but during replication NDV particles
are produced with a precursor glycoprotein, F0,
which has to be cleaved to F1 and F2 polypeptides that remain bound by disulphide bonds for
the virus particles to be infectious (Rott and
Klenk 1988). This post-translation cleavage is
mediated by host cell proteases (Nagai et al.,
1976a). Trypsin is capable of cleaving F0 for all
NDV strains and in vitro treatment of noninfectious virus with trypsin will restore infectivity
(Nagai et al., 1976b).
The cleavability of the F0 molecule was
shown to be related directly to the virulence of
viruses in vivo. This was done by demonstrating
that viruses pathogenic for chickens could replicate in a wide range of cell types in vitro with or
without added trypsin, whereas strains of low
virulence could replicate only when trypsin was
added (Rott, 1979, 1985). It would appear that
the F0 molecules of viruses virulent for chickens
can be cleaved by a host protease or proteases
found in a wide range of cells and tissues. This
results in virus spreading throughout the host
damaging vital organs. In contrast, F0 molecules
in viruses of low virulence are restricted in their
sensitivity to host proteases to trypsin-like
enzymes resulting in limiting growth of these
viruses to certain host cell types only.
Collins et al., (1993) compared the deduced
amino acid sequences of the F0 precursor of 26
PMV-1 (NDV) isolates at the cleavage site. Fourteen viruses that were pathogenic for chickens
had the sequence 112R/K-R-Q-K/R-R 116 at the
C-terminus of the F2 protein and F (phenylalanine) at residue 117, the N-terminus of the F1
protein. In contrast the 11 viruses of low virulence had sequences in the same region of 112G/
E-K/R-Q-G/E-R 116 and L (leucine) at residue
117. Thus, there appeared to be the requirement of a double pair of basic amino acids at
residues 112 and 113 and 115 and 116 plus a

phenylalanine at residue 117 if the virus was to
show virulence for chickens. The exception was
the single pigeon variant virus { PPMV-1} examined which had the sequence 112G-R-Q-K-R-F 117
was tested When this virus was tested in vivo
pathogenicity indices typical of PPMV-1 isolates
were obtained, indicating that it was virulent for
chickens. Jestin and Cherbonnel (1992) have
shown a similar motif at the F2/F1 cleavage site
for two viruses isolated from chickens which they
group antigenically with PPMV-1 viruses (Jestin
et al., 1989). Further studies have indicated that
this variation was usual for PPMV-1 viruses but
had no significance in the variability of pathogenicity for chickens recorded with these viruses
(Collins et al., 1994).
The major influence on the pathogenicity
of NDV is therefore the amino acid motif at the
F0 cleavage site. The presence of basic amino
acids at positions 113, 115 and 116 and phenylalanine at 117 in virulent strains means that
cleavage can be effected by protease or proteases
present in a wide range of host tissues and
organs. However, for lentogenic viruses,
cleavage can occur only with proteases recognizing a single arginine, such as trypsin-like
enzymes. Lentogenic viruses are therefore
restricted in the sites where they are able to
replicate to areas with trypsin-like enzymes, such
as the respiratory and intestinal tracts, whereas
virulent viruses can replicate in a range of tissues
and organs resulting in a fatal systemic infection
(Rott, 1979).
That the virulence of NDV strains is
governed by the F0 cleavage site is sufficiently
accepted that it has been incorporated into the
most recent definition of ND. The definition of
ND adopted at the 67th General Session of the
Office Internationale des Epizooties { OIE} held
in Paris in May 1999 was:
Newcastle disease is defined is an infection of
birds caused by a virus of avian paramyxovirus
serotype 1 (APMV-1) that meets one of the
following criteria for virulence: a) The virus
has an intracerebral pathogenicity index
(ICPI) in day-old chicks (Gallus gallus) of 07
or greater. or b) Multiple basic amino acids
have been demonstrated in the virus (either
directly or by deduction) at the C-terminus of
the F2 protein and phenylalanine at residue
117, which is the N-terminus of the F1 protein.
The term multiple basic amino acids refers
to at least three arginine or lysine residues
between residues 113 to 116. Failure to
demonstrate the characteristic pattern of
amino acid residues as described above would
require characterisation of the isolated virus
by an ICPI test.
In this definition, amino acid residues are
numbered from the N-terminus of the amino

acid sequence deduced from the nucleotide
sequence of the F0 gene, 113116 corresponds to residues 4 to 1 from the cleavage
site.
At present in the European Union (EU) the
definition in Directive 92/66/EEC (CEC, 1992)
is comparable only to part a) of the OIE definition but presumably it will soon be redefined.
Recently our understanding of the molecular basis of pathogenicity has led to suggestions
of how virulent viruses may emerge. In 1990 in
Ireland two outbreaks of ND occurred in egglaying birds. The viruses isolated were highly
virulent and apparently identical (Alexander et
al., 1992). Interestingly, these viruses were very
closely related antigenically and genetically
(Collins et al., 1998) to viruses of low virulence
normally isolated from feral waterfowl, but
known to have infected chickens on the island of
Ireland in 1987 (McNulty et al., 1988). The
group formed by these viruses was both antigenically and genetically distant from all other ND
viruses. Collins et al., (1993) had shown that the
virulent 34/90 virus had four nucleotide differences at the site coding for the F0 cleavage site
compared to the related viruses of low virulence
(Table 1), which would explain the higher virulence for chickens. However, while the
distinctiveness of this group of viruses from
other ND viruses make the theory that the virulent viruses arose from those of low virulence by
mutation, the mechanisms by which this may
have occurred are not at all clear.
Phylogenetic studies have shown the virulent viruses responsible for outbreaks in
Australia in 1998 and 1999 to be extremely
closely related to each other and to a virus of low
virulence isolated from chickens in the same
geographical area. This suggests that the virulent virus emerged by mutation, which in this
instance required only two point mutations
(Table 2).
If mutations to virulence do occur it is not
clear whether these take place in feral birds and
are then passed to poultry or occur once the
virus has been introduced in poultry, the lack of
virulent isolations from feral birds suggests the
latter is the more likely.
Table 1. Nucleotide/amino acid sequences at the F0 cleavage site of
virus of high virulence {34/90} isolated from poultry in Ireland
compared to antigenically and genetically closely related virus of low
virulence isolated from ducks
Virus
Virulence
MC110
Low
34/90
High
Nucleotide/amino acid sequence at

F0 cleavage site
GAA CGG CAG GAG CGT CTG
112
ERQER*L117
AAA CGG CAG AAG CGT TTT
112
KRQKR*F117
10
DENNIS J. ALEXANDER
Table 2. Nucleotide/amino acid sequence at the F0 cleavage sites of

viruses of high and low virulence isolated in Australia in 1998
Virus
Virulence
1154/98
Low
1238/98
High
1249/98
High
Nucleotide/amino acid sequence at

F0 cleavage site
GGA AGG AGA CAG GGG CGT CTT
111
GRRQGR*L117
GGA AGG AGA CAG AGG CGT TTT
111
GRRQRR*F117
GGA AGG AGA CAG AGG CGT TTT
111
GRRQRR*F117
If virulent ND strains do emerge from those

of low virulence by mutation then this may have
important repercussions for the current philosophy on control of ND, not least in view of the
enormous amount of live vaccines used
throughout the world.
Panzootics
Regardless of whether ND emerged as a truly new
disease in 1926 or had existed prior to that date,
there is no doubt that several panzootics have
occurred in poultry since that time. The first
appeared to spread very slowly throughout the
world. Hanson (1972) estimated that it took 16
years to become a true panzootic. Possibly it took
even longer and may never have reached poultry
in the USA. The spread of this virus was probably
confused by the unusual circumstances resulting
from the Second World War and the ensuing
disruption to trade. The beginning of the second
ND panzootic was first recognised at the end of
the 1960s and within 4 years had reached all areas
of the world (Hanson, 1972). The reason for the
difference in the rate of spread of the two
panzootics is complex. During the 40 years or
more separating the start of the two panzootics
the poultry industry had been revolutionised in
the West and in many of the more developed
countries in Asia. Commercial poultry production had moved from relatively small privately
owned flocks to much larger flocks owned by
international companies. Poultry food production had become commercialised. While this
greatly reduced the risks of poultry being fed
contaminated offal, it meant that there was
greater contact between separate farms as food
delivery vehicles moved from one to another.
Transport had also developed beyond recognition and birds could be moved relatively easily
and quickly by air to all parts of the world. This
last factor was largely responsible for the huge
and growing trade in captive caged birds. In
Great Britain exact records of imported caged
birds were not kept before 1975, but in that year
370 679 birds were imported (Inskipp and
Thomas, 1976). There is no doubt that imported
caged birds were responsible for introducing the
panzootic virus into poultry in California
(Hanson, 1972; Francis, 1973) and Walker et al.

(1973) were able to link most of the outbreaks
occurring in the USA between 1970 and 1972 to
importations of exotic birds. This association in
the USA of the panzootic virus with caged birds,
especially psittacines that appear to be able to
excrete virulent NDV for long periods in the
absence of clinical signs (Erickson et al., 1977),
gave rise to the theory of a natural reservoir of
ND in psittacine species (discussed above).
Antigenic and genetic evidence (Alexander
et al., 1997b; Lomniczi et al., 1998) indicates that
there was probably a spread of a third virulent
virus world wise during the late 1970s. The start
and spread of this third panzootic is unclear,
presumably as a result of the almost universal use
of vaccines, especially live vaccines, since the mid
1970s. Monitoring of viruses responsible for
panzootics is further complicated as it appears
that viruses with specific genetic or antigenic
characteristics do not necessarily disappear when
other variants arise and may continue to be
isolated many years after their first appearance
(Alexander et al., 1997b; Lomniczi et al., 1998).
It is indisputable that another ND panzootic
occurred in the 1980s. This time the affected
birds were not poultry but racing and show
pigeons (Columba livia), although some spread of
the virus to poultry did occur. The world population of pigeons kept for racing or show purposes
is enormous and at the end of the 1970s these
birds were largely unvaccinated and fully susceptible to infection by NDV. The first reports of ND
infections in pigeons were probably in the
Middle East in the late 1970s (Kaleta et al., 1985).
The NDV strain responsible for the pigeon
panzootic showed some antigenic variation from
other ND viruses, especially using monoclonal
antibodies, and as a result its spread around the
world could be followed without confusion with
live vaccines or other virulent viruses (Alexander
et al., 1985a). By 1981 this virus, termed pigeon
paramyxovirus type 1 (PPMV-1), had reached
Europe (Biancifiori and Fiorini, 1983) and by
1985 was a true panzootic. In many countries
where outbreaks occurred there was also a spread
to feral pigeons and doves, presumably as a result
of contact with infected racing pigeons that failed
to return home. Control measures, usually in the
form of compulsory vaccination of birds taking
part in races or shows were enforced in many
countries. However, in general, this panzootic
has proven difficult to bring under control and in
several countries it remains probably endemic in
racing and possibly feral pigeons.
ND in Great Britain
ND takes its name from an outbreak of the
disease that occurred on a poultry farm near
11
Figure 1. Outbreaks of Newcastle disease in poultry in Great Britain. The confirmed outbreaks of ND each year are shown. Note the differences in
scale for each graph.
Newcastle-on-Tyne in the spring of 1926 (Doyle,

1927). Doyle did not seem to be particularly at
ease with the name and in a footnote to a later
paper (Doyle, 1935) stated: The term
Newcastle disease was given provisionally when
it was first recognised to be a separate entity; it is
obviously unsuitable, yet it would appear advisable to retain it until such time as a more
appropriate one is coined. Apart from calling
the virus avian paramyxovirus serotype 1 (PMV1 now APMV-1) which was initiated by Tumova et
al. (1979) and has been reasonably well
adopted, there is no sign of an acceptable alternative for the disease 74 years later. The location
of the first outbreak in Britain suggests a
possible method of introduction. In 1926
Newcastle-upon-Tyne was an exceptionally busy
port. Doyle (1927) made the point that food for
poultry was supplemented with offal from
Newcastle and, even more categorically, Brown
(1965) states that the offal came from foreign
ships. During 1926 the disease was reported on
180 farms in 11 counties before it died out
(Report of the Committee on Fowl Pest Policy,
1962).
As shown in Figure 1a the disappearance
was complete and for the next 20 years only one
outbreak was reported, in 1933. This single
outbreak, in which 6,000 of 10,000 birds died,
occurred on a farm in Kings Langley, Hertfordshire (MAFF, 1934) and although the origin was
never traced, it was not without significance.
Firstly, because it resulted in the isolation of

strain Herts 33 which is widely used in many
countries as the standard virulent challenge
strain. Secondly, because it did not spread. This
was due largely to the farmers decision to
slaughter all the remaining birds and only
restock after disinfection (Report of the
Committee on Fowl Pest Policy, 1962). This
control strategy was spoilt only by the disease reoccurring in the replacement birds, which was
attributed to inadequate disinfection of the
whole premises. Thirdly, the 1933 outbreak was
the stimulus for the Fowl Pest Order, 1936 which
made ND and fowl plague notifiable diseases
and imposed a slaughter policy on affected
flocks (Report of the Committee on Fowl Pest
Policy, 1962).
The Second World War caused great
disruptions to trade and consequently influenced the progression of diseases such as ND. It
seems likely that the inexorable East-to-West
spread of the panzootic virus was accelerated in
some areas and prevented in others. During the
war years ND spread throughout Eastern Europe
(Reid, 1961). Although this seemed to be known
in Great Britain, shortages of animal protein
were so great it was decided to import poultry
meat in the form of frozen carcases from
Europe. On 22th February 1947, 13 days after
the first large-scale release of imported frozen
carcases from Europe, most notably Poland and
Hungary, the first of 2222 ND outbreaks to
12
DENNIS J. ALEXANDER
occur that year was confirmed (Dobson and

Simmins, 1951).
It is interesting that over 50 years later, with
pressures resulting from the formation of international organisations to allow freer trade in
agricultural products, one of the most debated
key issues in trade in poultry meat is the risk of
introducing ND. In Great Britain in 1947 there
was no doubt. The absence of protein for human
food was mirrored by an absence for animal
food and any available source was used. Retail
poultry were sold as whole carcases with just the
feathers removed and this is how the imported
birds had been frozen. Most of the outbreaks
occurred in small, backyard flocks, many in
urban areas. Although there was secondary
spread, often owing to trade in live birds, over a
third of the outbreaks were associated with
feeding of untreated swill containing poultry
offal (Dobson and Simmins, 1951; Gordon et al.,
1948; Reid, 1961). The outbreaks resulted in
legislation requiring the boiling of all swill to be
used as animal food and the demand that
poultry carcases imported into Britain should be
eviscerated and the head and feet removed
(MAFF, 1949). These latter measures were
primarily aimed at reducing the poultry offal
available but must also have greatly reduced the
viral burden. Nevertheless, frozen carcases still
represented a threat as sampling studies on
carcases immediately after import revealed the
continued presence of NDV. Dobson and
Simmins (1951), using samples of skin from
around the evisceration lesion, showed 25/42
lots of chicken from Country A and 5/13 from
Country B were positive for NDV.
The restrictions imposed seemed to have
had some success and in 1948 the number of
outbreaks of ND declined to 267. However, in
that year a further complication had arisen.
This was the observations of antibodies to NDV
in healthy hens (MAFF, 1950). The immediate
assumption was that there was a sub-acute form
of NDV present in Britain. Over the next few
years this proved to be correct and, although no
legal distinction was made between infections
of the different viruses, in 1951 all but 28 of the
844 outbreaks confirmed were considered to be
attributable to sub-acute ND (MAFF, 1953).
The vast majority of the outbreaks recorded
during 1950 to 1969 (Figure 1b) were considerably milder than the viruses introduced in 1947
and the two earlier occasions. Nevertheless
some were sufficiently serious to be termed
acute rather than sub-acute. This led to the
recognition of three types of ND in Great
Britain: per-acute, acute and sub-acute (Report
of the Committee on Fowl Pest Policy, 1962)
although all types remained ND for statutory
purposes.
The origins of the milder form of ND were

never definitely established but Reid (1961)
pointed out that the first cases were associated
with waste food from a United States Air Force
base. Because poultry carcases were imported
from the USA to feed personnel, Reid makes the
obvious speculation that the milder forms were
the result of spread of the virus from the USA
where the form of ND prevalent was known to be
less severe than the Asian or European forms
(see above). None of the viruses isolated during
that time are available now for detailed analysis.
The exception is strain F a particularly mild
strain isolated in 1949 by Asplin (1952) who
suggested it could be used as a live vaccine.
Recent studies have shown this virus to be antigenically (Alexander et al., 1997b) and
genetically (Ballagi-Pordany et al., 1996) close to
the USA strains of the same period.
The presence of the milder virus caused
something of a problem for diagnosis, as heavy
reliance was put on acute disease signs for
suspecting disease and of course these were
often absent. Whether all the viruses responsible
for outbreaks during the 1950s and 1960s, especially the so-called sub-acute, would fall within
current definitions of those that cause statutory
ND is arguable. Clearly some of them were as
mild as viruses that are now widely used as live
vaccines (Asplin, 1952). Nevertheless evidence
of infection with any NDV strain was recorded as
an outbreak of ND.
Throughout the 1950s the number of
confirmed outbreaks each year hovered around
1000 (Figure 1b) and then showed a sudden
increase in 1959 reaching a peak of 3384 in
1962. Clearly, in terms of both the number of
birds slaughtered and the cost of compensation,
the situation was untenable. A Committee on
Fowl Pest Policy was set up in July 1960 and
reported in March 1962 (Report of the
Committee on Fowl Pest Policy, 1962). As a
result of the recommendations of this
committee a new policy was adopted that abandoned slaughter with compensation except for
per-acute ND, but allowed the use of inactivated
vaccines (MAFF, 1964). This policy came into
force in April 1963. Initially there were problems
with the uptake and use of vaccine and it was not
until 1965 that a dramatic decrease in ND
outbreaks was seen.
By 1969 the number of outbreaks, still
essentially of the acute and sub-acute type of
disease, had declined to 69. Kelly (1973) indicated that this resulted in some complacency
among poultry farmers and a considerable
decline in vaccine uptake was seen during 1969
and 1970 so that only half the national flock was
being vaccinated. In 1970, 27 outbreaks were
confirmed in Great Britain up to 23rd August. In
the next few days the whole situation changed

and, starting in the east of England, the spread
of peracute ND resulted in a total of 3329
outbreaks for the year (MAFF, 1971). The
second ND panzootic had reached Great
Britain. The number of outbreaks in 1970 wasnt
quite the largest number ever recorded in Great
Britain in one year, but the 4217 outbreaks in
1971 easily claimed that record (MAFF, 1972).
The impact and alarm these outbreaks
caused cannot be over-emphasised. The live
vaccines Hitchner B1 and La Sota were licensed
for use, in December 1970 and August 1971
respectively and use of vaccine was encouraged
but never made compulsory (MAFF, 1972). A
Fowl Pest Review Panel (which included Dr
Robert F. Gordon) was set up in May 1971 and
reported in October of that year (Report of the
Review Panel, 1971). Essentially they endorsed
the control policy of voluntary vaccination and
recommended removal of restriction on
infected premises and the slaughter policy for
peracute ND, although notification of infection
was to remain a legal requirement. These recommendations were adopted.
In the face of universal vaccination with the
live vaccines (1321 million doses were used in
1971) often given by aerosol, which tended to
produce severe reactions, the number of
outbreaks declined precipitously (Figure 1c).
Between 1977 and 1983 Great Britain was
essentially free of ND in poultry. A single
outbreak had occurred in a small backyard flock
in 1978 (MAFF, 1980). There was good evidence
that this was due to contact with infected
imported psittacines.
International poultry trade is extremely
competitive and every trading advantage is
usually seized. In 1981 the British poultry
industry considered that there was little threat
from ND and that it would be of commercial
benefit if birds were not vaccinated. On 1st
September 1981 the control policy became one
of slaughter and vaccination against ND was
made illegal. The poultry industry invested in an
insurance scheme to cover compensation
payments for slaughtered birds in the event of
an outbreak.
At about the time the ND legislation was
being changed in Great Britain reports were
being received of the racing pigeon panzootic
reaching Europe. By early 1983 it had spread
throughout the pigeon populations of most
mainland European countries. Racing and
other movements of pigeons from the continent
were banned from March 1983 in an effort to
prevent introduction to Great Britain, but in July
the first outbreak was confirmed in a pigeon loft
in Cornwall. Between this outbreak and the end
of the year, 192 outbreaks in racing pigeons
13
were recorded, but 869 lofts were confirmed as

infected in 1984 (Alexander et al., 1994). The
virus spread to feral pigeons (Lister et al., 1986),
presumably as a result of infected racing pigeons
failing to return home. One particular concentration of infected feral pigeons appeared to be
the colony of 50,000+ birds at Liverpool and
Birkenhead docks.
In February 1984 NDV was isolated from a
flock of approximately 200,000 egg-layers and
ND confirmed (Alexander et al., 1985b). At that
time a panel of 9 monoclonal antibodies (mAbs)
was being used to characterise ND viruses with
which the pigeon panzootic virus gave a unique
binding pattern (Russell and Alexander, 1983).
Characterisation of the fowl isolate suggested
this was indistinguishable from the pigeon
panzootic virus and allowed the assumption that
the virus had spread from pigeons to the egglayers. It was considered unlikely that pigeons
had directly invaded the infected premises or
the site food stores, but investigations revealed
that constituents of the food had been stored at
Liverpool. These constituents were mixed with
other ingredients at food mills to give balanced
rations to be fed untreated to laying hens. Investigations of the food stores at Liverpool docks
showed them to be infested with infected
pigeons (Figure 2) and virus was isolated from
pigeon carcases found in the food and even in
small samples of the food (Alexander et al.,
1985b). Restrictions were placed on the food
stores to prevent further spread of the virus by
this route. In all, 23 outbreaks were confirmed in
1984. The majority had links to the infested food
at Liverpool docks, although some were the
result of secondary spread. Results with the mAb
panel on the viruses isolated showed all to be the
pigeon panzootic virus, apart from one which
appeared to be more closely related to vaccine
viruses (Alexander et al., 1985b).
The disease in pigeons has not proven easy
to control and eradicate. Slaughter policies were
considered inappropriate in Great Britain as in
most countries. Initial control consisted of
voluntary vaccination and restriction of movement of birds. Although the number of
confirmed cases in pigeons fell from the high in
1984, for several years these were maintained at
several hundred outbreaks each year. Compulsory vaccination for birds taking part in races was
introduced in April 1994 (The Racing Pigeon
(Vaccination) Order, 1994) and further
reduced the number confirmed each year, but
still outbreaks occur and in 1999 there were 16
confirmed (Figure 3).
The single outbreak of ND that occurred in
pheasants in 1996 was also identified as being
caused by the pigeon panzootic virus (Alexander et al., 1997a). In this case the virus showed
14
DENNIS J. ALEXANDER
Figure 2. Pigeons infecting food stores at Liverpool docks in 1984 (photograph K. Taylor).
Figure 3. Confirmed outbreaks of APMV-1 in racing pigeons in Great Britain.
a slight variation from other pigeon viruses and

identical viruses were shown to be infecting freeflying doves and pigeons in the vicinity.
In 1997 there were 11 outbreaks confirmed
in chickens and turkeys in Great Britain
between early January and late April (Alexander et al., 1998). Control followed the
movement restriction and slaughter imposed by
EU Directive 92/66/EEC (CEC, 1992) and
spread was localised. Epidemiological investiga-
tions suggested that most of the outbreaks were

the result of secondary spread by human agency
from one or two primary introductions. Nucleotide sequencing and phylogenetic analysis
showed very close similarity between the British
isolates and the viruses responsible for ND
outbreaks in Scandinavian countries in 1996,
including an isolate from a feral goosander
(Alexander et al., 1999). The unusual patterns
of movement of migratory birds at the end of
1996 and beginning of 1997 suggest they may

have been the vehicle for the primary introduction of the causative virus into Great Britain.
It appears that ND has been introduced
into Great Britain on at least eight separate occasions: 1926, 1933, 1947, around 1948 (possibly
multiple introductions over a number of years),
1970, 1978, 1983 (into the racing pigeon population, infecting poultry in 1984 and 1996) and
1997. In this respect Great Britain is probably
typical of Western European countries despite
its island status. Equally typical is the response of
introducing new legislation and methods of
control to combat the disease in response to
each new introduction. In Great Britain, as in
other countries, legislative processes are
perceived to be cumbersome and slow. The
frequency and rapidity with which parliamentary acts and orders have been introduced and
revoked to reflect the changes in the ND situation over the last 75 years is therefore
remarkable.
Control
As can be deduced from the accounts above of
the emergence of ND and its history in Great
Britain, it is difficult to describe any aspect of the
disease without also considering how to prevent
or control it. The message in Kiplings poem
Natural Theology was that it is wrong for us to
blame God in adversity and do nothing. His
thesis was that most problems are brought on
oneself and it is up to us to avoid them or solve
them. This is certainly the case for ND.
Biosecurity
The term biosecurity encompasses any measure
that is employed to prevent the transmission of
an infectious organism from one host to
another. For ND it is usually taken to mean
measures that may be used to prevent the introduction of NDV on to a farm or into a flock. It
should be noted that vaccination is not included
as a biosecurity measure as it does nothing to
prevent introduction of NDV to a flock. To
impose the restrictions implicit in good biosecurity it is, of course, necessary to understand how
the virus is spread. It is not intended to give a
lengthy account of all the methods by which
NDV may be spread (see Alexander, 1988b) and
the relative risks each of these presents. Essentially the virus may be spread by any animal that
can be infected and any medium that can be
contaminated (usually with infective faeces) that
results in contact directly or indirectly with
susceptible poultry. There is one area of spread
where some discussion is necessary, and that is
airborne spread.
15
For both farmers and those involved in the

control of disease, airborne spread can sometimes seem an attractive proposition. If the
infection arrives by such a natural method then
no person can be blamed or suffer guilt for
introducing the virus, as in Kiplings poem only
God can be held responsible. In recent years the
significance of airborne transfer of virus has
been the subject of some debate. During the
1960s and 1970s this was thought to be a major
method of spread, and Smith (1964) considered
it the most logical explanation of spread in
outbreaks occurring in 1960 and 1962 in Great
Britain. In the same country Dawson (1973)
considered windborne spread to be of major
significance during the 1970 to 1972 outbreaks
that were noted for the severe respiratory signs
and unusual patterns of spread. In this epizootic, respiratory signs were sometimes so
severe, contemporary descriptions are reminiscent of anaphylactic shock. It would have been
of interest to know the vaccination history or
immune status of flocks showing these signs. By
contrast, in the 1971 to 1973 epizootic in California with ostensibly the same virus, respiratory
signs were not especially prominent and Utterback and Schwartz (1973) considered airborne
spread to be of little significance.
There have been few attempts to assess the
survival of airborne virus but Hugh-Jones et al.
(1973) were able to detect virus 64 metres but
not 165 metres downwind of an infected
premises. These authors stressed the importance of environmental conditions particularly
relative humidity on the likelihood of airborne
spread.
It is difficult not to conclude that when
climatic conditions have been right and poultry
farms sufficiently concentrated, as in Northern
Ireland in 1973, airborne spread may have
played a significant role in epidemics of ND
(McFerran, 1989). But in recent years airborne
spread has not been an issue in reported
outbreaks and there has nearly always been an
alternative, more likely cause, particularly the
movement of poultry and the agency of man. If
windborne spread over any distance was
normally a significant factor in ND epizootics
then little could be done in terms of biosecurity
short of maintaining poultry in HEPA-filtered
environments. That this is not normally the case
means that other measures can be employed to
reduce the risk of introduction to a farm or
flock.
The measures needed to ensure ND prevention by biosecurity are dealt with generically but
in detail by Zander et al. (1997), but I would like
to discuss some of the issues that arise. One of
the problems with implementing good biosecurity is that ideally one would start with a new
16
DENNIS J. ALEXANDER
industry and a plentiful supply of land on which

to site it. In that way commercial poultry farms
and flocks could be well separated, hatcheries
kept remote from poultry farms and fresh water
supplies (not surface water) ensured. In practice
in many countries, the poultry industry has been
developed with little attention to such planning.
So that in countries such as The Netherlands
and Hong Kong (Higgins and Shortridge, 1988)
with high populations and little land, poultry
farms and flocks are closely packed together and
it seems inevitable that disease will spread
rapidly once introduced. However, this may not
necessarily be the case. If measures (such as:
bird-proofing houses, food stores and water
tanks; minimising movements on and off the
farm; ensuring all equipment, especially vehicles, is disinfected before access to the site is
permitted; ensuring movements between
different farms for egg collection, carcase collection, food delivery etc. are to and from a
specified collection and delivery point away
from the poultry flocks) are enforced in these
and less densely populated areas the result may
be a dramatic reduction in the spread of NDV.
Possibly the most important consideration
is who has actual contact with the flock. Access to
the birds should be kept to a minimum. If it is
unavoidable then visits by personnel who may
have visited other poultry farms such as
bleeding, thinning or vaccination crews, inseminators and veterinarians must be considered the
most likely method of introduction of ND and
regimens of clothing change, equipment disinfection and other basic hygiene controls
enforced before access to the birds is allowed.
Such measures should not only reduce the
risk of introduction of ND but will also reduce
the spread of other endemic diseases that may
affect the birds and reduce their yield. Although
many biosecurity measures may often be
regarded as costly, laborious and time
consuming by those involved, in fact they represent a good investment in future profitability of
poultry production.
To vaccinate or not?
The objective of vaccination of any animal is to
produce an immune response that will prevent
disease. For some viruses, in some animals, vaccination may lead to immunity at a sufficient level
for a sufficient time so that, not only is the
animal protected for a considerable period
(even for the life of the animal) but also should
virus challenge occur replication of the challenge virus is effectively prevented. For some
viruses in some hosts such solid immunity may
be achieved following only a single dose of
vaccine. For NDV with currently available
vaccines such desirable immunity cannot be

achieved in poultry even using multiple
vaccinations.
Following ND vaccination of poultry the
protective immune response appears to be transient. In addition experimental evidence
published as early as 1952 (Asplin, 1952) has
shown that, although vaccination may protect
birds from the more serious consequences of
NDV infection, virulent epizootic virus may
infect, replicate, be excreted and be present in
the tissues and organs of apparently healthy
birds. During the outbreaks in California during
1971 and to 1973 it was recorded that vaccination did not prevent birds becoming infected
with the epizootic virus and that such birds shed
the virus for long periods (Utterback and
Schwartz, 1973). More recent experimental
work supports this observation. Guittet et al.
(1993) challenged 40-d-old birds that had been
vaccinated at 14 d old with velogenic NDV. From
2 to 3 ds after challenge up to 6 ds after challenge, when the experiment was stopped, virus
could be isolated from organs, muscle and
faeces of sampled birds, although none showed
any signs of disease. Similarly, Parede and Young
(1990) report only mild clinical signs in some
immune birds challenged with virulent virus but
were able to isolate virus for up to 19 ds after
challenge in sampled birds. Capua et al. (1993)
reported the isolation of virulent NDV from clinically normal breeder hens with high levels of
antibodies to NDV, and showed the presence of
virus in embryonated eggs from the flock and
from hatched progeny that had experienced
episodes of mortality. Clinically normal, vaccinated birds which are excreting virulent virus
represent a threat in terms of overt disease to
unvaccinated birds which may come in contact
with them either directly, such as by trade in
birds, especially for backyard flocks, or indirectly
through transfer of infective faeces. Even wellvaccinated birds, including progeny and other
birds on the same farm site, may be at risk if
other factors, such as infectious bursal disease,
reduce the effectiveness of the immune
response. It is therefore extremely important to
focus carefully on what is hoped to be achieved
by pursuing a policy of prophylactic vaccination
against ND.
The marked contrast in attitude to vaccination even by different countries in the EU is an
indication of both the complexity of the situation and the perceived risk, either of the
probability of outbreaks occurring or of the
economic damage that may be done as a result.
In debating any vaccination policy the following
points need to be addressed: countries
importing live birds may demand vaccination;
correctly administered efficacious ND vaccines
17
may prevent death, clinical signs and even egg

production problems if high enough antibody
titres are achieved; virulent ND viruses may
infect and replicate in vaccinated birds even
though clinical signs may be absent; as a corollary to the point above, vaccination does not
prevent confirmation of ND as defined by OIE;
vaccination reactions may occur. The immune
response achieved by live vaccines appears to be
directly related to the virulence of the vaccine
strain. Even mild strains such as Hitchner B1
may cause slight clinical signs that might be
more severe if exacerbated by other organisms
or environmental problems. Vaccine reactions
may also vary with the method of presentation,
as might the immune response and these two
variables appear to be related inversely; vaccination of breeder birds will result in maternal
antibodies in their progeny that may result in
difficulties in achieving a good response to vaccination early in the life of progeny; vaccination
involves expense. Multiple doses of live vaccines
must be given to ensure an immune response in
the face of maternal antibodies and to maintain
sufficient immunity during the birds life. For
laying birds inactivated oil emulsion vaccines are
usually considered essential. In addition to the
direct cost of vaccination Leslie (2000) estimated that vaccination resulted in a loss of about
2% of egg production in laying birds and 114 g
per broiler; where live vaccines are used, regimens and programmes must be devised to
complement vaccines to other organisms;
because vaccination may prevent clinical signs
but not infection and virus replication, it is
possible that introduction and spread of virulent
ND virus may go unnoticed. This could result in
an endemic situation that only becomes
apparent when immunity is not achieved owing
to a failure of vaccination or immune suppression due to other agents.
Possibly the most important consideration
in assessing the need to vaccinate is the risk of
disease occurring. In many African and Asian
countries, ND appears to be endemic either in
commercial poultry or in village or backyard
poultry. There is little possibility of enforcing
efficient biosecurity measures to prevent spread
to commercial poultry and as a consequence
there is little alternative to vaccination. In other
countries where ND is absent or occurs only
sporadically it is difficult to see why control by
good biosecurity at the farm level with national
and international controls on poultry, poultry
products and other birds aimed at preventing
introduction of ND would not be effective. In
such countries in the EU it is implicit in Directive 92/66 (CEC, 1992) that the rapid careful
application of the eradication policies outlined
in the Directive with emergency vaccination
Table 3. Outbreaks of Newcastle disease in European Union countries

during 1990 and 1997 compared to vaccination policies
Country
ND
outbreaks
19901997
Germany
255
Vaccination Policy
compulsory, was for
flocks >200, from 1994
all flocks
compulsory
compulsory from 1991
voluntary, compulsory
from 1992
Netherlands
Portugal
Belgium
77
56
88
Luxembourg
France
Greece
Italy
Spain
UK
Austria
10
13
58
2
46
6
as Belgium?
voluntary
voluntary
voluntary
voluntary
voluntary
voluntary
Ireland
Denmark
Sweden
Finland
Norway
6
18
2
2
1
banned to 1997
banned
banned
banned
banned
Total
Total
486
76%
125
195%
29
45%
640
when needed should result in control of occasional introductions.

In Western European countries decisions to
impose, allow or ban prophylactic vaccination
may be as much a political decision, based on
perceived trading advantages, as one of disease
control. Assessment of the success of the
different strategies is difficult and, as shown in
Table 3, straightforward comparison of the
number of outbreaks in recent years appears to
indicate that a non-vaccination policy is the most
successful. Of course an analysis like this does not
take into account factors such as the relative size
of the poultry industries and different risks of
introduction for different countries, but equally
vaccination may lead to complacency and
increased risk of introduction. The rarity of introductions may also be an important consideration
in assessing the value of any vaccination policy.
For example in Great Britain the voluntary vaccination and non-slaughter policy adopted after
the 1984 outbreaks could be considered a great
success because there were no outbreaks during
1985 to 1992 when it was in place (Figure 1 d).
But if no introductions of ND virus to poultry
occurred during that time then any policy or no
policy at all would have been successful.
Future
Pathogenicity and definition
Almost since the first isolations of ND viruses,
certainly since the recognition of viruses showing
variations in virulence and the capacity to
produce disease, attempts have been made to
18
DENNIS J. ALEXANDER
differentiate between different types of NDV. A

variety of in vitro methods were employed in early
studies (Hanson, 1978). But none was truly satisfactory either from an epidemiological point of
view or as an in vitro assessment of virulence.
Use of monoclonal antibodies, especially in
panels has proved a powerful tool in grouping
isolates on an antigenic basis (Alexander et al.,
1997b) but while such techniques gave a strong
indication of the likely virulence of the virus for
poultry, findings could not be regarded as diagnostic. The need to assess the virulence of any
NDV isolate and distinguish the highly virulent
viruses from those of low virulence was seen to
be extremely important for the control of ND,
especially after the use of live vaccines became
widespread. Essentially, the in vivo tests first
described over 45 years ago by Hanson and
Brandly (1955), especially the ICPI test, are still
necessary to make an acceptable assessment of
the virulence of NDV isolates for chickens. As
discussed above, our understanding of the
molecular basis of pathogenicity is sufficient to
allow an in vitro test in the form of assessment of
the basic amino acids at the cleavage site of
viruses to be included in the OIE definition.
Allowing an in vitro test for the confirmation of
virulent virus, is a major step forward. However,
it is still necessary to retain the ICPI test in the
definition, primarily because in the case of
mixtures of virulent and avirulent viruses (a
fairly common occurrence) primers may preferentially select the virus of low virulence giving a
false result. At present it is also necessary to
isolate viruses before sequencing. Although
some workers have examined the possibility of
sequencing PCR products obtained directly
from tissues or faeces of infected birds, at
present this is unreliable.
The present constraints on using
sequencing directly appear to represent a fairly
minor technical problem. It seems likely that
one immediate future development will be to
produce a reliable test that will enable rapid
detection of the presence of NDV and simultaneously the deduced F0 cleavage site sequence
by testing infected organs or faeces.
Linked to this development, and probably
facilitating it, is a fuller understanding of the
significance of the amino acids in the F0
cleavage site motif. Currently the exact
minimum requirements for virulence based on
the amino acid residues between 112 and 117 on
the F0 precursor are unclear. Factors that need
to be resolved are: the influence of a basic amino
acid at residue 112, the exact effect of interchanging lysine and arginine at various positions
and the significance of phenylalanine at 117, the
3 end of the F1 polypeptide. Recently the entire
nucleotide sequence of the genome of NDV has
been published (de Leeuw and Peeters, 1999)

and an infectious clone established (Peeters et
al., 1999). This is an important advance as it
allows genetic manipulation of the virus using
reverse genetics techniques (Conzelmann,
1996) which could be used to produce any
required combination of amino acids at the F0
cleavage site. Findings such as the minimum
essential amino acid motif required for virulence will lead to tighter definitions of ND and
simplify rapid diagnostic techniques based on
PCR and sequencing.
Pigeons
Although pigeons appear to be fully susceptible
to all strains of NDV, the virus responsible for
the panzootic in racing and show pigeons
during the 1980s showed sufficient antigen
divergence that it could be compartmentalised,
more or less as a different virus. This, added to
the reluctance of authorities to impose the same
strict control measures on pigeons as they do for
poultry (see Directive 92/66/EEC), has greatly
facilitated the continued perpetuation of the
virus in these birds. Over 20 years have passed
since the first observations of the disease in
racing pigeons but, although the number of
outbreaks in most countries has diminished,
infections of racing, show and feral pigeons are
still regularly reported.
The continued presence of this ND virus in
pigeons has produced several anomalous situations in the control of ND. For example, in some
countries infection of one or two backyard hens
would be reported internationally as an
outbreak of ND, with all the repercussions to
trade and the poultry industry that involves.
While infection, with the same virus in a loft of
several hundred racing pigeons would not be
reported as ND and only minimum control
measures applied. In at least one country the
variant virus infecting pigeons was considered to
be of low pathogenicity.
Although the new OIE definition of ND
should cover the latter point, an important
future development in the control of ND must
be to properly address the disease in birds other
than commercial poultry. It would appear that
in many countries the measures applied to date
have been unsuccessful at eradicating the
disease from racing pigeons. This represents a
pool of virus that is not only a continued threat
to commercial poultry but also to indigenous
feral birds.
ND control in developing countries
The economic impact of ND and its effect on
trade in commercial poultry is important. Never-
theless the biggest challenge of this disease is its

endemic presence in developing countries and
the effect on village chicken production (Spradbrow, 1993; Awan et al., 1994). Populations of
village chickens in many countries of Asia, Africa
and Central and South America are enormous
and in most of the countries in these areas ND is
endemic in such birds. In papers published in
1987 Tint (1987) estimated that about 85% of
some 40 million chickens reared in Burma each
year were village chickens, while Atienza (1987)
reported 65% to 75% of the 59 million birds in
the Philippines were reared as village chickens.
In Africa similar numbers may be recorded, for
example Mukiibi-Muka (1992) estimated rural
chickens to represent 80% of the 20 million
poultry population in Uganda; while in Nigeria
a similar portion of the 150 million chickens are
rural scavengers (Olabode et al., 1992). Whether
in S.E. Asia (Copland, 1987) or Africa (Rweyemamu et al., 1992) ND is seen as a major factor
in the high mortality of village chickens which
may be routinely as high as 60%.
In many developing countries village
chickens are part of a useful tradition, usually
tended by woman and children (Kitalyi, 1996)
and their true economic and nutritional value
are never properly measured (Tint, 1987). In
areas of exceptional hardship and nutritional
deprivation village chickens and their eggs may
be the difference between life and death.
Despite the ravages ND may have on rural, scavenging chickens in many countries, farmers and
villagers may have little concept of the nature of
the disease and assume ND is a natural consequence of keeping chickens (Moerad, 1987).
ND may represent a disaster to those relying
on village chickens as a food or trading
commodity but this reservoir of virulent NDV
must also be considered a continuing threat to
poultry populations throughout the world. It
would appear in everyones interest that in the
near future concerted efforts are made to bring
much greater control to ND in this area of
poultry production. Led by Spradbrow efforts
have been made in many developing countries
to introduce vaccination to village chickens in
the form of heat-resistant live vaccines (Spradbrow, 1996). Such projects are an important
contribution and should be applauded and
supported. However, it appears unlikely that
vaccination alone will be sufficient to completely
resolve the problem unless run in parallel with
education programmes about disease spread
and poultry husbandry.
REFERENCES
ALEXANDER , D.J. (1988a) Preface, in: ALEXANDER , D.J. (Ed)
Newcastle Disease p. XI (Boston MA, Kluwer Academic
Publishers).
19
A LEXANDER , D.J. (1988b). Newcastle disease: Methods of

spread, in: A LEXANDER , D.J. (Ed) Newcastle Disease, pp.
256272 (Boston, MA, Kluwer Academic Publishers).
A LEXANDER , D.J., B ANKS, J., COLLINS, M.S., M ANVELL , R.J.,
FROST, K.M., SPEIDEL , E.C. & ALDOUS, E.W. (1999) Antigenic and genetic characterisation of Newcastle disease
viruses isolated from outbreaks in domestic fowl and
turkeys in Great Britain during 1997. Veterinary Record,
145: 417421.
A LEXANDER , D.J., CAMPBELL, G., M ANVELL , R.J., COLLINS , M.S.,
P ARSONS, G. & M CN ULTY, M.S. (1992) Characterisation of
an antigenically unusual virus responsible for 2 outbreaks
of Newcastle disease in the Republic of Ireland in 1990.
Veterinary Record, 130: 6568.
A LEXANDER , D.J., M ANVELL, R.J., FROST, K.M., POLLITT , W.J.,
W ELCHMAN , D. & P ERRY , K. (1997a) An outbreak of
Newcastle disease in pheasants in Great Britain in May
1996. Veterinary Record, 140: 2022.
A LEXANDER , D.J., M ANVELL, R.J., LOWINGS, J.P., FROST, K.M.,
COLLINS , M.S., RUSSELL, P.H. & S MITH , J.E. (1997b) Antigenic diversity and similarities detected in avian
paramyxovirus type 1 (Newcastle disease virus) isolates
using monoclonal antibodies. Avian Pathology, 26: 399
418.
A LEXANDER , D.J., M ORRIS, H.T., POLLITT , W.J., S HARPE, C.E.,
ECKFORD R.L., SAINSBURY , R.M.Q., M ANSLEY , L.M., G OUGH
R.E. & PARSONS , G. (1998) Newcastle disease outbreaks in
domestic fowl and turkeys in Great Britain during 1997.
Veterinary Record, 143: 209212.
A LEXANDER , D.J., PARSONS , G., M ANVELL , R.J. & SAYERS, A.R.
(1994) Characterisation of avian paramyxovirus type 1
infections of racing pigeons in Great Britain during 1983
to 1990, in: M CN ULTY , M.S. & M CFERRAN , J.B. (Eds)
Proceedings of the European Commission, Virus Diseases of
Poultry, New and Evolving Pathogens, Brussels, 1992, pp. 65
75.
A LEXANDER , D.J., R USSELL , P.H., P ARSONS, G., ABU ELZEIN ,
E.M.E., BALLOUGH, A., CERNIK , K., E NGSTROM, B.,
FEVEREIRO , M. et al. (1985a) Antigenic and biological
characterisation of avian paramyxovirus type 1 isolates
from pigeonsan international collaborative study. Avian
Pathology, 14: 365376.
A LEXANDER , D.J., W ILSON , G.W.C., R USSELL, P.H., LISTER , S.A.
& PARSONS , G. (1985b) Newcastle disease outbreaks in
fowl in Great Britain during 1984. Veterinary Record, 117:
42934.
A SPLIN , F.D. (1952) Immunisation against Newcastle disease
with a virus of low virulence (strain F) and observations on
sub-clinical infection in partially resistant fowls. Veterinary
Record, 64: 245249.
A TIENZA, V.C. (1987) Phillipines, in: COPLAND , J.W. (Ed)
Newcastle disease in poultry: a new food pellet vaccine pp. 93
95. The Australian Centre for International Agricultural
Research, Canberra.
A WAN, M.A., O TTE, M.J. & JAMES , A.D. (1994) The epidemiology of Newcastle disease in rural poultry: a review. Avian
Pathology, 23: 405423.
B ALLAGI -P ORDANY , A., W EHMANN , E., H ERCZEG, J., B ELAK , S. &
LOMNICZI, B. (1996) Identification and grouping of
Newcastle disease virus strains by restriction site analysis of
a region from the F gene. Archives of Virology, 141: 243261.
B EACH, J.R. (1942) Avian pneumoencephalitis. Proceedings of the
Annual Meeting of the US Livestock Sanitary Association, 46:
203223.
B EACH, J.R. (1944) The neutralization in vitro of avian pneumoencephalitis virus by Newcastle disease immune serum.
Science, 100: 361362.
B EAUDETTE , F.R., B IVINS , J.A. & M ILLER , B.R. (1949) Newcastle
disease immunization with live virus. Cornell Veterinaria n,
39: 302334.
B IANCIFIORI , F. & FIORONI, A. (1983) An occurrence of
Newcastle disease in pigeons: virological and serological
20
DENNIS J. ALEXANDER
studies on the isolates. Comparative Immunology, Microbiology and Infectious Diseases, 6: 247252.
BLAXLAND , J.D. (1951) Newcastle disease in shags and cormorants and its significance as a factor in the spread of this
disease among domestic poultry. Veterinary Record, 63:
731733.
BROWN, A.C.L. (1965) The epidemiology of Newcastle disease
in Great Britain. Proceedings of the Royal Society of Medicine,
58: 801802.
CAPUA , I., SCACCHIA, M., T OSCANI, T. & CAPORALE , V. (1993)
Unexpected isolation of virulent Newcastle disease virus
from commercial embryonated fowls eggs. Journal of Veterinary Medicine B, 40: 609612.
CEC (1992) Council directive 92/66/EEC of 14 July 1992
introducing Community measures for the control of
Newcastle disease. Official Journal of the European Communities, L260: 120.
CEC (1993) Commission decision of 8 February 1993 laying
down the criteria to be used against Newcastle disease in
the context of routine vaccination programmes. Official
Journal of the European Communities, L59: 35.
CLEARY , L. (1977) Succs de reproduction du cormoran
aigrettes, Phalacrocorax auritus auritus, sur trois les du St
Laurent, en 1975 et 1976. M Sc Thesis, LUniversit Laval,
Ste-Foy, Quebec pp. 168.
COLLINS, M.S., B ASHIRUDDIN , J.B. & ALEXANDER , D.J. (1993)
Deduced amino acid sequences at the fusion protein
cleavage site of Newcastle disease viruses showing variation in antigenicity and pathogenicity. Archives of Virology,
128: 363370.
COLLINS, M.S., S TRONG , I. & ALEXANDER , D.J. (1994) Evaluation of the molecular basis of pathogenicity of the variant
Newcastle disease viruses termed pigeon PMV-1 viruses.
Archives of Virology, 134: 403411.
COLLINS, M.S., F RANKLIN , S., STRONG, I, M EULEMANS , G. &
A LEXANDER , D.J. (1998) Antigenic and phylogenetic
studies on a variant Newcastle disease virus using antifusion protein monoclonal antibodies and partial
sequencing of the fusion protein gene. Avian Pathology,
27: 9096.
CONZELMANN , K.-K. (1996) Genetic manipulation of nonsegmented negative-strand RNA viruses. Journal of General
Virology, 77: 381389.
COPLAND , J.W. (1987) (Ed) Newcastle Disease in Poultry: a new
food pellet vaccine. The Australian Centre for International
Agricultural Research, Canberra.
DAWSON, P.S. (1973) Epidemiological aspects of Newcastle
disease. Bulletin of the Office International des Epizooties, 79:
2734.
DOBSON, N. & S IMMINS , G.B. (1951) The introduction of
Newcastle disease by means of frozen poultry carcases.
Report of the 9th Worlds Poultry Congress, Paris, 3: 1821.
DOCHERTY, D.E. & FRIEND , M. (1999) Newcastle disease, in:
F RIEND , M. & F RANSON , J.C. (Eds) Field Manual of Wildlife
Diseases pp. 175180. (Madison, WI, U.S. Geological
Survey).
DOYLE , T.M. (1927) A hitherto unrecorded disease of fowls
due to a filter-passing virus. Journal of Comparative Pathology
and Therapeutics, 40: 144169.
DOYLE , T.M. (1935) Newcastle disease of fowls. Journal of
Comparative Pathology and Therapeutics, 48: 120.
ERICKSON , G.A., M ARE , C.J., GUSTAFSON, G.A., M ILLER , L.D.,
P ROTOR, S.J. & CARBREY , E.A. (1977) Interactions between
viscerotropic velogenic Newcastle disease virus and pet
birds of six species. 1. Clinical and serologic responses and
viral excretion. Avian Diseases, 21: 642654.
FRANCIS , D.W. (1973) Newcastle and psittacines, 197071.
Poultry Digest, 32: 1619.
GARCIA, M., CRAWFORD , J.M., LATIMER , J.W., R IVERACRUZ, E. &
P ERDUE , M.L. (1996) Heterogeneity in the haemagglutinin gene and emergence of the highly pathogenic
phenotype among recent H5N2 avian influenza viruses

from Mexico. Journal of General Virology, 77: 14931504.
GOLDHAFT , T.M. (1980) Historical note on the origin of the La
Sota strain of Newcastle disease virus. Avian Diseases, 24:
297301.
GORDON , R.F., R EID , J. & ASPLIN , F.D. (1948) Newcastle disease
in England and Wales. Official Report of the 8th Worlds
Poultry Congress, Copenhagen, 1: 642650.
GUITTET , M., LE COQ , H., M ORIN, M., JESTIN, V. & B ENNEJEAN ,
G. (1993) Proceedings of the 10th World Veterinary Poultry
Association Congress, Sydney, p. 179.
H ALASZ , F. (1912) Contributions to the knowledge of fowlpest.
Veterinary Doctoral Dissertatio n, Communications of the
Hungarian Royal Veterinary School, Patria, Budapest, pp.
136.
H ANSON , R.P. (1972) World wide spread of viscerotropic
Newcastle disease. Proceedings of the 76th Meeting of the US
Animal Health Association, Florida. pp. 276279.
H ANSON , R.P. (1978) Newcastle disease, in: H OFSTAD , M.S.,
CALNEK , B.W., H ELMBOLDT , C.F., REID , W.M. & YODER,
H.W. (Eds) pp. 513535. Diseases of Poultry, (Iowa State
University Press).
H ANSON , R.P. & BRANDLY, C.A. (1955) Identification of vaccine
strains of Newcastle disease virus. Science, 122: 156157.
H ECKERT, R.A. (1993) Newcastle disease in cormorants. Canadian Veterinary Journal, 34: 184.
H ECKERT, R.A., COLLINS, M.S., M ANVELL, R.J., STRONG , I.,
PEARSON , J.E. & A LEXANDER , D.J. (1996) Comparison of
Newcastle disease viruses isolated from cormorants in
Canada and the USA in 1975, 1990 and 1992. Canadian
Journal of Veterinary Research, 60: 5054.
H IGGINS, D.A. & SHORTRIDGE , K.F. (1988) Newcastle disease in
tropical and developing countries, in: ALEXANDER , D.J.
(Ed) pp. 273302. Newcastle Disease, (Boston, MA, Kluwer
Academic Publishers).
H ITCHNER , S.B. (1975) Serendipity in sciencediscovery of
the B-1 strain of Newcastle disease virus. Avian Diseases, 19:
215223.
H ITCHNER , S.B. & JOHNSON , E.P. (1948) A virus of low virulence for immunizing fowls against Newcastle disease
(avian pneumoencephalitis). Veterinary Medicine, 43: 525
530.
H UGH-JONES , M., ALLAN , W.H., DARK , F.A. & H ARPER , G.J.
(1973) The evidence for the airborne spread of Newcastle
disease. Journal of Hygiene, Cambridge, 71: 325339.
INSKIPP , T.P. & T HOMAS, G.J. (1976) Airborne Birds, Royal
Society for the Protection of Birds, Sandy.
JESTIN , V. & CHERBONNEL, M. (1992) Use of monoclonal antibodies and gene amplification (PCR) for characterisation
of a-PMV-1 strains. Proceedings of the CEC Workshop on Avian
Paramyxoviruses ,
Rauischholhausen,
1992.
Institut
Geflugelkrankheiten, Giessen pp. 157166.
JESTIN , V., CHERBONNEL, M., M ORIN, M., G UITTET , M. & B ENNE JEAN, G. (1989) Characterisation of French avian
paramyxovirus type 1 (PMV 1) isolates with a panel of
monoclonal antibodies to the Ploufragan strain of
Newcastle disease virus. Archives of Virology, 105: 189198.
KALETA, E.F. & B ALDAUF, C. (1988) Newcastle disease in freeliving and pet birds, in: ALEXANDER , D.J. (Ed) Newcastle
Disease, pp. 197246 (Boston, MA, Kluwer Academic
Publishers).
KALETA, E.F., A LEXANDER , D.J. & RUSSELL , P.H. (1985) The
first isolation of the avian PMV-1 virus responsible for the
current panzootic in pigeons? Avian Pathology, 14: 553
557.
KELLY , A. (1973) Newcastle disease in Great Britain, The 1970
71 epidemic and the current disease situation. Bulletin
Office Internationale des Epizooties, 79: 127136.
KITALYI, A.J. (1996) Socio-economic aspects of village chicken
production in Africa: Role of women, children and nongovernmental organizations. Proceedings of the 20th World
Poultry Congress, New Delhi, India, 1: 3545.

KRANEVELD , F.C. (1926) A poultry disease in the Dutch East
Indies. Nederlands Indisch Bladen voor Diergeneeskunde, 38:
448450.
KUIKEN , T., H ECKERT, R.A., R IVA , J., LEIGHTON, F.A. &
W OBESER, G. (1998) Excretion of pathogenic Newcastle
disease virus by double-crested cormorants (Phalacrocorax
auritus) in the absence of mortality or clinical signs of
disease. Avian Pathology, 27: 541546.
LANCASTER , J.E. (1966) Newcastle diseasea review 1926
1964. Monograph No 3, Canada Department of Agriculture ,
Ottawa.
LANCASTER , J.E. (1977) Newcastle diseasea review of the
geographical incidence and epizootiology. Worlds Poultry
Science Journal, 33: 155165.
DE L EEUW , O. & PEETERS, B. (1999) Complete nucleotide
sequence of Newcastle disease virus: evidence for the
existence of a new genus within the subfamily Paramyxovirinae. Journal of General Virology, 80: 131136.
LESLIE , J. (2000) Newcastle disease: outbreak losses and
control policy costs. Veterinary Record, 146: 603606.
LEVINE , P.P. (1964) World dissemination of Newcastle disease,
in: H ANSON, R.P. (Ed) Newcastle disease, an evolving pathogen, pp. 6569. (Madison, WI, University of Wisconsin
Press).
LISTER , S.A., ALEXANDER , D.J. & H OGG, R.A. (1986) Evidence
for the presence of avian paramyxovirus type 1 in feral
pigeons in England and Wales. Veterinary Record, 118: 476
479.
LOMNICZI, B., W EHMANN , E., H ERCZEG, J., B ALLAGI-P ORDANY ,
A., K ALETA , E.F., W ERNER , O., M EULEMANS , G.,
JORGENSEN , P.H. et al. (1998) Newcastle disease outbreaks
in recent years in Western Europe were caused by an old
(VI) and a novel genotype (VII). Archives of Virology, 143:
4964.
M ACP HERSON , L.W. (1956) Some observations on the epizootiology of Newcastle disease. Canadian Journal of Comparative
Medicine, 20: 155168.
MAFF (1934) Report of the Proceedings under the Diseases of Animals
Act 1933. HMSO, London.
MAFF (1949) Report of the Proceedings under the Diseases of Animals
Act for the years 19381947. HMSO, London.
M AFF (1950) Report on Animal Health Services for the year 1948.
HMSO, London.
M AFF (1953) Report on Animal Health Services for the years 1949,
1950 & 1951. HMSO, London.
M AFF (1964) Report on Animal Health Services for the years 1961 &
1962. HMSO, London.
M AFF (1971) Report on Animal Health Services for the year 1970.
HMSO, London.
M AFF (1972) Animal Health 1971 HMSO, London.
M AFF (1980) Animal Health 1978 HMSO, London.
M ANNINGER , R. (1932) The relations between Newcastle
disease and fowl plague: Do the causal agents represent
different virus types? Archiv Fr Wissenschaflich und praktische Tierheil kunde, 65: 256265.
M CF ERRAN , J.B. (1989) Control of Newcastle disease in
Northern Ireland. ProceedingsAvian Exotic Disease Control
Seminar. pp. 1621. Animal Health Report 2, NSW Agriculture & Fisheries, Glenfield, NSW, Australia.
M CN ULTY, M.S., A DAIR, B.M., OLOAN , C.J. & A LLAN , G.M.
(1988) Isolation of an antigenically unusual paramyxovirus type 1 from chickens. Avian Pathology, 17: 509513.
M ETEYER , C.U., DOCHERTY, D.E., GLASER, L.C., FRANSON, J.C.,
SENNE , D.A. & D UNCAN , R. (1997) Diagnostic findings in
the 1992 epornitic of neurotropic velogenic Newcastle
disease in double-crested cormorants from the upper
midwestern United States. Avian Diseases, 41: 171180.
M IXSON , M.A. & P EARSON, J.E. (1992) Velogenic neurotropic
Newcastle disease (VNND) in cormorants and commercial turkeys, FY 1992. Proceedings of the 96th Annual Meeting
of the US Animal Health Association, Louisville, KY pp. 357
360.
21
M OERAD , B. (1987) Indonesia: Disease control, in: COPLAND ,

J.W. (Ed) Newcastle disease in poultry: a new food pellet vaccine.
pp. 7376. The Australian Centre for International Agricultural Research, Canberra.
M UKIIBA -MUKA , G. (1992) Epidemiology of Newcastle disease
in rural Uganda, in: R WEYEMAMU , M.M., P ALYA, V., W IN , T.
& SYLLA , D. (Eds) Newcastle disease vaccines for rural Africa.
pp. 7576. FAO Panvac, Debre Zeit.
N AGAI, Y., K LENK , H-D. & ROTT , R. (1976a) Proteolytic
cleavage of the viral glycoproteins and its significance for
the virulence of Newcastle disease virus. Virology, 72: 494
508.
N AGAI, Y., O GURA, H. & K LENK , H-D. (1976b) Studies on the
assembly of the envelope of Newcastle disease virus.
Virology, 69: 523538.
O LABODE, A.O., SHIDALI, N.N. & LAMORDE , A.G. (1992) Epidemiology of Newcastle disease in Nigeria, in: RWEYEMAMU ,
M.M., P ALYA, V., WIN, T. & SYLLA , D. (Eds) Newcastle Disease
Vaccines for Rural Africa. pp. 5359. FAO Panvac, Debre
Zeit.
P ANIGRAHY , B., SENNE , D.A., P EARSON , J.E., M IXSON , M.A. &
CASSIDY, D.R. (1993) Occurrence of velogenic viscerotropic Newcastle disease in pet and exotic birds in 1991.
Avian Diseases, 37: 254258.
P AREDE, L. & YOUNG , P.L. (1990) The pathogenesis of velogenic Newcastle disease virus infection of chickens of
different ages and different levels of immunity. Avian
Diseases, 34: 803808.
P EETERS , B.P.H., DE LEEUW, O., K OCH, G. & GILKENS , A.L.J.
(1999) Rescue of Newcastle disease virus from cloned
cDNA: Evidence that cleavability of the fusion protein is a
major determinant for virulence. Proceedings of the Joint 5th
Annual Meetings of the National Newcastle Disease and Avian
Influenza Laboratories of Countries of the EU. Vienna 1998, pp.
5460.
P ERDUE , M., CRAWFORD , J., GARCIA, M., LATIMER , J. & S WAYNE ,
D. (1998) Occurence and possible mechanisms of
cleavage-site insertions in the avian influenza hemagglutinin gene. Proceedings of the 4th International Symposium on
Avian Influenza. pp. 182189. US Animal Health
Association.
R EID , J. (1961) The control of Newcastle disease in Great
Britain. British Veterinary Journal, 117: 275288.
R EPORT OF THE COMMITTEE ON F OWL P EST POLICY (1962)
HMSO, London.
R EPORT OF THE REVIEW PANEL (1971) Newcastle disease epidemic
19701971. HMSO, London.
R OTT, R. (1979) Molecular basis of infectivity and pathogenicity of myxoviruses. Archives of Virology, 59: 285298.
R OTT, R. (1985) In vitro Differenzierung von pathogenen und
apathogenen aviaren Influenzaviren. Berliner und
Munchener Tieraerztliche Wochenschrift, 98: 3739.
R OTT, R. & KLENK , H-D. (1988) Molecular basis of infectivity
and pathogenicity of Newcastle disease virus, in: A LEX ANDER , D.J. (Ed) Newcastle Disease, pp. 98112. (Boston,
MA, Kluwer Academic Publishers).
R USSELL , P.H. & A LEXANDER , D.J. (1983) Antigenic variation of
Newcastle disease virus strains detected by monoclonal
antibodies. Archives of Virology, 75: 243253.
R WEYEMAMU , M.M., PALYA , V., WIN, T. & S YLLA , D. (1992)
Newcastle Disease Vaccines for Rural Africa. FAO Panvac,
Debre Zeit.
SENNE , D.A., PEARSON , J.E., M ILLER , L.D. & GUSTAFSON, G.A.
(1983) Virus isolations from pet birds submitted for importation into the United States. Avian Diseases, 27: 73144.
S HOPE, R.E. (1964) The birth of a new disease, in: H ANSON ,
R.P. (Ed) Newcastle DiseaseAn Evolving Pathogen. pp. 3
22. (Madison, WI, University of Wisconsin Press).
S MITH , C.V. (1964) Some evidence for the windborne spread
of fowl pest. Meteorological Magazine, 93: 257263.
S PRADBROW, P.B. (1992) Newcastle disease respite for poultry.
Shell Agriculture, 12: 2931.
22
DENNIS J. ALEXANDER
SPRADBROW, P.B. (1993) Newcastle disease in village chickens.

Poultry Science Reviews, 5: 5796.
SPRADBROW, P.B. (1996) Protection against important diseases
including Newcastle disease. Proceedings of the 20th World
Poultry Congress, New Delhi, India, 1: 3134.
STOVER, D.E. (1942) A filterable virus, the cause of a respiratory-nervous disorder of chickens. American Journal of
Veterinary Research, 3: 207213.
THE RACING P IGEON (V ACCINATION ) O RDER (1994) Statutory
Instrument No. 944, HMSO, London.
TINT, U.T. (1987) Burma, in: COPLAND , J.W. (Ed) Newcastle
Disease in Poultry: a new food pellet vaccine. pp. 6668. The
Australian Centre for International Agricultural
Research, Canberra.
TUMOVA, B., ROBINSON, J.H. & EASTERDAY, B.C. (1979) A hitherto unreported paramyxovirus of turkeys. Research in
Veterinary Science, 27: 135140.
UTTERBACK , W.W. & S CHWARTZ, J.H. (1973) Epizootiology of

velogenic viscerotropic Newcastle disease in southern
California, 19711973. Journal of the American Veterinary
Medical Association, 163: 10801088.
W ALKER , J.W., H ERON , B.R. & M IXSON, M.A. (1973) Exotic
Newcastle disease eradication program in the United
States of America. Avian Diseases, 17: 486503.
W OBESER, G., LEIGHTON , F.A., N ORMAN , R., M YERS , D.J.,
O NDERKA , D., P YBUS, M.J., NEUFELD , J.L., FOX, G.A. &
ALEXANDER , D.J. (1993) Newcastle disease in wild water
birds in western Canada. Canadian Veterinary Journal, 34:
353359.
ZANDER , D.V., B ERNUDEZ , A.J. & M ALLINSON , E.T. (1997)
Principles of disease prevention: diagnosis and control,
in: CALNEK , B.W., B ARNES , H.J., B EARD , C.W., M CD OU GALD , L.R. & S AIF, Y.M. Diseases of Poultry 10th Edn, pp. 3
46.

Newcastle Disease

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Newcastle Disease

Uploaded by

Copyright:

Available Formats

British Poultry Science

ISSN: 0007-1668 (Print) 1466-1799 (Online) Journal homepage: http://www.tandfonline.com/loi/cbps20

Published online: 28 Jun 2010.

Submit your article to this journal

Article views: 895

View related articles

Citing articles: 78 View citing articles

Full Terms & Conditions of access and use can be found at

Date: 17 February 2016, At: 12:21

British Poultry Science (2001) 42: 522

GORDON MEMORIAL LECTURE

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

Avian Virology, VLA Weybridge, Addlestone, England

I run eight hundred hens to the acre.

Dennis J. Alexander 18th Gordon Memorial Lecturer

chickens in Nepal die as a result of ND. Social and

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

commercial poultry production and the establishment of trade links.

difficulty is differentiating between ND and

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

GORDON MEMORIAL LECTURE

years as a result of a series of isolations from

undergone some modification. No writers have

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

in North America described above, there have

some viruses of low virulence from the same

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

GORDON MEMORIAL LECTURE

residues 112 and 113 and 115 and 116 plus a

numbered from the N-terminus of the amino

Nucleotide/amino acid sequence at

Table 2. Nucleotide/amino acid sequence at the F0 cleavage sites of

Nucleotide/amino acid sequence at

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

If virulent ND strains do emerge from those

(Hanson, 1972; Francis, 1973) and Walker et al.

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

GORDON MEMORIAL LECTURE

Newcastle-on-Tyne in the spring of 1926 (Doyle,

Firstly, because it resulted in the isolation of

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

occur that year was confirmed (Dobson and

The origins of the milder form of ND were

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

GORDON MEMORIAL LECTURE

the next few days the whole situation changed

were recorded, but 869 lofts were confirmed as

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

Figure 3. Confirmed outbreaks of APMV-1 in racing pigeons in Great Britain.

a slight variation from other pigeon viruses and

tions suggested that most of the outbreaks were

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

GORDON MEMORIAL LECTURE

1996 and beginning of 1997 suggest they may

For both farmers and those involved in the

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

industry and a plentiful supply of land on which

vaccines such desirable immunity cannot be

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016

GORDON MEMORIAL LECTURE

may prevent death, clinical signs and even egg

Table 3. Outbreaks of Newcastle disease in European Union countries

when needed should result in control of occasional introductions.

Downloaded by [Gadjah Mada University] at 12:21 17 February 2016