D9321.PDF

Rev. sci. tech. Off. int. Epiz., 2000,19 (2), 638-661
Ostrich diseases
D.J. Verwoerd
Onderstepoort Veterinary Institute, Private Bag X5, 0110 Onderstepoort, Republic of South Africa
The terms describing serovars of Salmonella enterica subsp. enterica are presented as follows: Salmonella
Enteritidis, S. Gallinarum, S. Pullorum, S. Typhimurium, etc.
Summary
Scientific knowledge of ostrich diseases is incomplete and very f r a g m e n t e d , w i t h
specific details on t e c h n i c a l aspects of diagnostic and/or screening tests
completely absent in most cases. Salmonella
Typhimurium is c o m m o n in
multispecies collections and causes mortality in chicks younger t h a n three
months on commercial farms, but is rarely found in chicks older than six months,
or slaughter birds of t w e l v e to fourteen months in southern Africa.
Campylobacter
jejuni and Chlamydia psittaci
are occasionally reported, mainly in young
ostriches, but both remain a diagnostic challenge. Crimean-Congo haemorrhagic
fever is transmitted to domestic animals including ostriches, principally by ticks of
the genus Hyalomma. In the ostrich, the disease causes no clinical symptoms
during a viraemia of approximately four days. Spongiform encephalopathy has not
been reliably reported in ostriches, w h i l e anthrax has o c c u r r e d rarely in modern
times but w a s reportedly an important cause of death approximately 100 years
ago in South Africa. Salmonella Gallinarum and S. Pullorum are u n k n o w n in
ostriches. Pasteurella multocida occurs but is easily contained w i t h antibiotics.
Mycoplasma spp. are regularly found in an upper respiratory disease syndrome
complicated by opportunistic bacterial pathogens. Ostriches of all ages are
susceptible to challenge by velogenic N e w c a s t l e disease virus (NDV), but
standard inactivated La Sota poultry v a c c i n e s can stimulate protective immunity
lasting over six months. The viraemic period in vaccinated slaughter ostriches is
b e t w e e n nine and eleven days and there are no indications of a carrier state or
presence of the virus in the meat or any other tissues after this period, w i t h peak
immunoglobulin G response reached on day fourteen post infection.
Haemagglutination inhibition tests are significantly less sensitive and less
specific than enzyme-linked immunosorbent assays. Cloacal and choanal s w a b s
used for direct virological screening in clinically affected cases (field and
experimental) could not detect NDV. All avian influenza isolates reported from
ostriches have been non-pathogenic to poultry, even the H5 and H7 subtypes.
Some of the latter have been associated w i t h mortality of ostrich chicks in
localised outbreaks during periods of inclement w e a t h e r and w i t h significant w i l d
bird (waterfowl) contact. Borna disease causes a nervous syndrome in ostrich
chicks, but to date, has only been reported in Israel. Eastern and W e s t e r n equine
encephalomyelitides cause fatal disease in ostriches and other ratites, w i t h
mortality ranging from less than 20% to over 80% in affected flocks. These
diseases are present in North, Central and South America w h e r e the associated
ornithophilic mosquito vectors occur. Equine and human v a c c i n e s are apparently
safe and efficacious in ratites. Wesselsbron disease, infectious bursal disease
(type 2), adenovirus and Coronavirus infections have been reported from
ostriches but the significance of these diseases is unclear.
Due to the paucity of data regarding ostrich diseases and the unvalidated state of
most poultry tests in this unique group of birds, strict observation of a
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pre-slaughter quarantine of thirty days is strongly advised, w h i l s t live exports and
fertile eggs should be screened through t h e additional use of sentinel chickens
and/or young ostriches.
Keywords
Avian diseases - Avian influenza - Crimean-Congo haemorrhagic fever - Newcastle
disease - Ostriches - Ratites - Salmonella.
Introduction
Public health concerns
Current scientific knowledge of diseases of ratite birds
(ostriches, emus and rheas) is incomplete, fragmented and in
most cases superficial or limited to anecdotal reports. The
domestic ostrich (Struthio camelus domesticus) is the result of
more than 100 years of selective breeding in the arid regions
of South Africa for improved reproductive traits (eggs
produced per breeding season), feather quality and improved
docility, and is the most prominent member of this family in
terms of international trade (live ostriches, fertile eggs and
ostrich meat, leather and feathers). However, since the 1980s,
significant ostrich industries based on indigenous, unselected
birds have developed utilising several subspecies in other
countries of Africa, namely: Botswana, Namibia and
Zimbabwe (different phenotypes of S. c. australis) and Kenya
and Tanzania (S. c. massaicus and S. c. molybdophaenes).
Live
ostriches and/or fertile eggs are exported from these countries
to destinations world-wide, with notable industries
established in Israel, southern Europe, North America, the
People's Republic of China, South-East Asia and Australia,
while small numbers of ostriches are also established in
Arabia, South America and northern Europe.
Salmonellosis (Salmonella Typhimurium and
Salmonella Enteritidis)
The globalisation of trade in live ratites and products has led
to particular difficulties in drawing up sensible, biologically
correct import protocols, as the information necessary is, in
most cases, simply unknown. These birds are also
physiologically so different from galliform poultry species
(chickens, turkeys) or waterfowl (ducks, geese) that mere
extrapolations are extremely inaccurate in most instances.
This paper is designed to present a compilation of available
data on the diseases reported in ostriches which are of
particular concern to the poultry industries. Also included,
where relevant, is information pertinent to public
health (e.g. Crimean-Congo haemorrhagic fever [CCHF])
or other animal industries (e.g. Eastern/Western equine
encephalomyelitides).
To
allow
a more
complete
interpretation, information available on a particular disease is
not limited to ostriches, but also includes emus and rheas.
The relevant papers in this special issue should be studied in
conjunction with these sections, to allow comparisons with
the situations in poultry. Where technical details on tests and
vaccines for ostriches or ratites are not mentioned, this
information is simply not available.
These non-host specific members of the genus Salmonella
cause disease in most warm-blooded animals (including
birds) and are thus of concern in terms of both the economical
production of food animals and the possible transmission to
human consumers, resulting in enteritis and/or septicaemia.
Salmonella
Typhimurium and S. Enteritidis have been
associated with clinical conditions in young, stressed
(immuno-compromised) ostriches, similar to the situation in
other host groups (70, 7 1 , 7 2 , 1 5 2 ; Onderstepoort Veterinary
Institute [OVI], unpublished case reports 1993-1998). In
particular, these agents have been implicated in mortalities of
ostriches and emus from multispecies collections, animal
dealers and similar 'zoo type' situations which are predisposed
to cross-species transmission of pathogens under highly
stressful conditions (147).
Pathology in all peracute and acute cases shows ecchymotic to
suffusive haemorrhages in the serosa of the gastrointestinal
tract (GIT) and parenchymatous organs. The mucosa of the
small intestine (jejunum, ileum) and/or colon is reddened
with patchy ulcerations and adherent fibrinous exudate. The
spleen is constantly enlarged and dark red/purple in colour
(congestion) while the liver is also congested and swollen with
focally disseminated necrosis (white spots) (72, 147).
Outbreaks amongst young ostrich chicks on large ostrich
farms in southern Africa are usually associated with
rodent-contaminated feed or raw materials, exposure to
free-flying feral pigeons, doves, sparrows etc. in the chick
runs, or the use of open water reservoirs or direct piping from
surface water/contaminated bore holes (ground water
contaminated by primitive, long-drop type latrines) (74, 1 4 5 ;
OVI, unpublished case reports 1993-1998). Effective
antibiotics, as determined through antibiograms combined
with complex probiotics in a so-called 'tandem programme'
(morning/evening alternation), followed by constant exposure
to probiotics for a period of one week, have been successful in
most of these outbreaks. Prevention has been achieved
through the use of complex carbohydrates (e.g. mannose
oligosaccarides), at an inclusion rate of 2 kg/tonne, during the
critical first few weeks of life, in conjunction with strict
attention to disinfection and biosecurity issues, especially
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Rev. sci. tech. Off. int. Epiz., 19 (2)
those related to feed and water management ( 7 2 , 1 5 3 ) . Older
animals are typically able to carry and intermittently shed
salmonellae for an extended period (22, 7 5 ) .
Table II
Number of Salmonella isolates from ostriches, 1988-1996
Year
Pre-export testing of more than a thousand live ostriches from
three farms in Namibia destined for Europe, aged seven to
nine months, revealed the following (152):
In total, 2 , 0 0 5 cloacal swabs were cultured for Salmonella
using selective media over a period of seven days. Thirteen
Salmonella isolations were made: four of S. Typhimurium;
three of S. Anatum; two of S. Reading and one each of
S. Tanzania, 5. Lamberhurst, S. Muenchen and S. Enteritidis
(untypable). Of the 2 , 5 7 3 serum samples tested, nineteen
were
positive
for
S. Enteritidis
(0.7%),
ten
for
S. Gallinarum/Pullorum ( 0 . 3 8 % ) , and two for S. Hadar
(0.07%).
The isolates of Salmonella detected by the ostrich diseases
diagnostic programme at the Onderstepoort Veterinary
Institute (OVI), South Africa, during investigations into
clinical cases from 1 9 9 6 to 1997, are shown in Table I (152).
Results of the analysis of all the ostrich Salmonella isolates sent
to the OVI Salmonella laboratory for serotyping between 1 9 8 8
and 1996 are listed in Table II (146). The primary isolations of
these samples were made by the OVI, and by various regional
veterinary and other laboratories in South Africa. The
Table I
Isolations of Salmonella from clinical investigations by the
Onderstepoort Veterinary Institute Ostrich Diagnostic Programme from
1 June 1996 to 25 April 1997
Serotype
Number of isolates
S. Typhimurium
13 + 1 (water)
9
S. Muenchen
S. Tsevie
S. Enteritidis
S. Riggil
S. Georgia
S. Maidiguri
S. Thompson
S. Chester
S. Lamberhurst
S. Papuana
S. Djakarta
S. Isangani
S. Stoneferry
S. type II
Citrobacter
Total
3
3
1
1
1 +1 (feed)
1
2
1
1
1
1
1 (feed)
2
2(a)
45 lb)
a) suspected Salmonella on preliminary bacteriological investigation
b) includes two isolates from feed samples, one water sample and two Citrobacter isolates
Total cases with suspected bacteriological aetiology investigated during this period = 290
thus Salmonella isolates per bacteriological cases seen = 13.8%
Pathogenic Salmonella = 25/45 = 56%: 25/290 = 8.6% of total
1988
Number of isolates
5
1
1989
1990
4
1991
1992
2
12
1993
1994
29
1995
18
13
1996
Total
36
120
Salmonella isolates were sent to the OVI Salmonella laboratory
for serotyping. The majority of the isolates were obtained
from clinical samples. The period mentioned coincided with a
tremendous increase in the number of ostrich farms in South
Africa and thus represents samples that originated from a
wide range of farms, both new and very well established ( 1 0 0
years or more), as well as operations varying from a few
hundred birds to large flocks of 1 0 , 0 0 0 birds or more.
Over this period, 1 2 0 Salmonella isolates were received by the
OVI Salmonella laboratory. For the first four years of the
survey period ( 1 9 8 8 - 1 9 9 1 ) , very few isolates were received (a
total of twelve), but from 1 9 9 2 onwards, twelve to thirty-six
isolates were identified per year. Serovar Typhimurium was
the serovar most frequently isolated ( 2 5 / 1 2 0 ) , followed by
Muenchen (11/120) and Brancaster (8/120). An unexpectedly
high number of Salmonella II isolates was detected (15/120).
However, these were all different isolates, and do not
represent the prevalence of a single serovar. Salmonella II
serovars are not regarded as primary pathogens, and their
presence in these ostriches is not indicative of a disease. In
some of these cases (4/15), other salmonellae were also
isolated which may have been of greater importance.
Typhimurium was the most common Salmonella in all types
of samples, and isolation of this serovar from clinical material
was always of pathological importance. The age of the birds
affected ranged from young chicks to three-month-old
ostriches. The pathological conditions observed were
septicaemia with lesions, especially in the liver, spleen and
lung, as well as enteritis.
From a public health perspective, the Salmonella status of
slaughter ostriches (typically twelve to fourteen months old) is
of much greater importance than that of chicks or clinical
cases. Huchzermeyer mentions the possibility of carcass
contamination during slaughter and notes that unlike
mammals, birds (including ostriches) and reptiles have no
mesenteric lymph nodes, and thus enteric
Salmonella
infections could, in theory, rapidly become septicaemic and
be present in internal organs as a result of severe stress ( 7 1 ,
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Rev. sci. tech. Off. int. Epiz., 19 (2)
72). Ongoing surveillance of the Salmonella status of slaughter
ostriches (partially sponsored by the International Atomic
Energy Agency) is conducted in South Africa. Preliminary
results collected from 3 1 1 ostriches from all regions, over a
nine-month period, are shown in Table III (132).
Table IV
Serotypes of Salmonella isolated from ratites during 1993 in Oklahoma,
United States of America
Serotype
S. Typhimurium
Table III
Salmonella isolations and Salmonella serology agar gel
immunodiffusion (AGID) from the ongoing Meat Hygiene Surveillance
Programme conducted in South Africa on export slaughter ostriches
(preliminary data: 1998/1999)
Salmonella serotype
S. Typhimurium
Bacteriology
Serology
S. Typhimurium (Copenhagen)
S. Muenchen
S. Panama
S. Enteritidis (phagetype 8)
S. Newport
S. Rubislaw
S. livingston
4.2%
0%
4.5%
S. Anatum
S. Enteritidis
2%
S. Hadar
0%
S. Muenchen
Other*
0.3%
0.3%
ND
S. Montevideo
S. Godesberg
Total
1.2%
5.7%
Salmonella (Group B)
ND
Salmonella (Group G)
6.8%
Salmonella (Group C2)
Salmonella (Group E)
* included S. Lamberhurst, S. Salamae tsevie and S. Sandiego, each at approximately 0.4%
prevalence
ND: no data
Testing of exotic birds in the United States of America (USA)
revealed that one out of seventeen ostriches (5.8%) were
positive by the slide agglutination test for S. Typhimurium,
while all seven emus tested were negative ( 5 8 ) . Salmonella
isolation attempts from ratites in 1 9 9 3 in Oklahoma were
positive in forty-six out of 2 4 8 ostriches, thirty-four out of
ninety-nine emus, and sixteen out of sixty rheas. The total
incidence was approximately 2 3 % (96/407). In contrast,
fifteen out of 181 attempts were positive in 1 9 9 2 . Serotypes
isolated from ratites are shown in Table IV.
Other investigators have found disturbingly high positive
serological indications (over 5 0 % ) , using commercial test kits
for S. Enteritidis enzyme-linked immunosorbent assay
(ELISA), in sera from live, mature ostriches imported into
Europe from several countries of southern Africa (I. Capua,
personal communication).
These apparent contradictions indicate an urgent need for the
validation of serological tests for salmonellae in ostriches and
the development of biologically-sound screening procedures
both for live exports and possibly before slaughter. This is
further confounded by the geographical differences in
Salmonella epidemiology between temperate regions in the
northern hemisphere where large concentrations of
commercial poultry are in close proximity to ostriches, and
the extensive nature of ostrich farming in semi-arid areas of
southern Africa, which are largely unsuitable for commercial
poultry. At present, strict attention to hygiene in ostrich
abattoirs and deboning plants, in addition to correct
evisceration procedures, are the best ways to prevent the
contamination of meat during the slaughter process by the
apparently very low incidence of Salmonella' in slaughter
ostriches.
Untypable
Total
Ostrich
Emu
Rhea
20
2
5
13
0
0
2
0
0
1
0
0
2
1
0
0
0
1
0
1
1
0
1
0
1
1
0
0
0
0
0
0
11
3
0
0
0
6
1
7
1
4
2
46
0
34
16
1
3
2
3
Live birds should be screened through culture of cloacal
swabs and possibly the use of sentinel ostriches or chickens.
Where approved, an alternative approach is the irradiation of
meat to ensure freedom from pathogens, including
Salmonella. Samples of meat from bison, ostrich, alligator and
caiman (similar in proximate analysis) which were
experimentally inoculated with several species of Salmonella
and Staphylococcus
aureus, wert effectively sterilised by
gamma irradiation. Based on the average gamma radiation D
values obtained in this study and the minimum dose currently
approved for the irradiation of poultry (1.5 kGy), gamma
irradiation would eliminate 2.8 and 4.1 log units of
Salmonella and S. aureus, respectively (139). The resistance of
Salmonella to gamma radiation on these 'exotic' meats was less
than that reported for beef, lamb and turkey (138). However,
due to the very low prevalence of salmonellae in slaughter
ostriches reported above, such an all-inclusive approach to
treatment is probably unnecessary.
Campylobacteriosis
Campylobacter jejuni has been reported in young ostriches
from several parts of the world. In Israel, two-week- to
four-month-old ostrich chicks showed depression, anorexia,
dehydration and green urine. Mortality reached 4 0 % and the
pathology resembled vibrionic hepatitis in
poultry.
Campylobacter jejuni serotype 8 was isolated from the livers of
affected birds. Treatment with furaltadone (250 mg/1 drinking
water) in the younger birds, and with norfloxacin (30 mg/kg
live weight) in the older birds, reduced mortality (106).
642
Campylobacter was isolated from the intestines of ostriches,
emus and rheas in the USA, with some isolates from emus
displaying uncharacteristic properties ( 1 0 1 , 1 0 2 ) .
In South Africa, C. jejuni was found to be associated with
outbreaks of enteritis and hepatitis in ostrich chicks ranging
from three weeks to two months old. Affected chicks
showed depression, anorexia and diarrhoea, while the
pathological lesions were mainly a pronounced typhlocolitis
and extensive multifocally disseminated micro-abscesses in
the liver. In all cases, the history involved severe stress
(e.g.
long
transport
distances,
cold
temperatures,
overcrowding, mycotoxicoses).
Effective treatment consisted of antibiotics (danofloxacin at
5 mg/kg) coupled with complex probiotics in the food. A
particular contract-chick feeding operation experienced
repeated outbreaks despite changes in management. An
experimental autogenous inactivated Campylobacter bacterin
vaccine in an oil emulsion adjuvant enriched with vitamin E,
given to all chicks on arrival, seemed to assist in preventing
further outbreaks in this specific operation. In most instances,
Campylobacter-associated mortalities or poor growth were
sporadic and were resolved with the treatment described
above and prevented by changing management-related
stressful procedures (OVI, unpublished case reports
1993-1998).
Campylobacter jejuni has also been isolated from rheas in the
USA, where a three-month-old rhea chick was presented with
typical vibrionic hepatitis lesions in one liver lobe. An
in-contact ostrich chick died from yolk sac infection and
C. jejuni was also isolated from the yolk (112). In another
incident, C. jejuni was isolated from a single rhea where a
number of the flock had died from spirochaete-associated
typhlocolitis (60).
Campylobacter is known to be a part of the natural flora of the
intestinal tract of many species of birds (101), as well as many
domestic mammals, with average carrier rates of 6 0 % for
broiler chickens, 2 0 % for cattle and sheep and 8 0 % (C. coli)
for pigs reported from surveys in several countries (127). No
such data are available for slaughter age ostriches, and as mass
mechanised processing is blamed for the high levels' of
cross-contamination associated with poultry meat, individual
slaughter and evisceration procedures during ostrich
slaughter should prevent carcass contamination.
There are no indications for the inclusion of special
Campylobacter
culture testing as part of the screening of
either live ostriches, eggs or ostrich products for international
trade.
Chlamydiosis
The world-wide distribution of strains of Chlamydia psittaci in
a large number of avian species (in 1 9 7 1 , 139 species
Rev. sci. tech. Off. int. Epiz., 19 (2)
representing fourteen orders and approximately thirty
families [28]) and the observation that feral birds could be a
source of infection for domestic poultry, implies that the goal
of total control is unrealistic ( 5 9 ) . An outbreak in young
ostriches, resulting in high mortality and the infection of
human contacts, has been reported from a game park in
France (107). Chlamydiosis has also been reported from an
ostrich chick in North America (74), while the agent was
isolated in Texas from a cloacal swab of an adult ostrich hen
that had a low positive titre and had laid infertile eggs. Isolates
from eleven ratites submitted to diagnostic laboratories in
Texas and California were serotyped using serovar-specific
monoclonal antibodies and characterised by polymerase
chain
reaction
(PCR) restriction
fragment
length
polymorphism of the major outer membrane protein genome.
All were determined to be serovar E. This serovar is known to
have existed in the USA for more than sixty years, while a
number of isolates obtained from ducks in England, during
outbreaks of high mortalities, were also found to be this
serovar, in retrospective studies (11).
In another monoclonal antibody study in Israel, conjunctival,
cloacal and faecal smears from seventy-four ostriches revealed
the presence of C. psittaci antigen in 2 3 % of the birds (88). An
outbreak of chlamydiosis in three- to five-month-old ostriches
in Namibia resulted in 3 7 % mortality in a flock of 160 birds
(84). After translocation from another farm, the birds became
depressed, developed dyspnoea and a 'penguin-like' gait, and
died
acutely.
Macroscopic
pathology
included
fibrinopurulent tracheitis, pneumonia, pericarditis and
perihepatitis. Out of several thousand investigations of
mortality in ostrich chicks from 1993 to 1 9 9 8 , principally
from ostrich farms located in the central (summer-rainfall)
region of South Africa, clinical chlamydiosis was found in a
single case (72; OVI, unpublished case reports 1 9 9 3 - 1 9 9 8 ) .
These chicks displayed a severe necrotising hepatitis and
splenitis, with chlamydial colonies prominent in both organs
on histological examination.
The organism was isolated from a single case of unilateral
conjunctivitis in a juvenile ostrich from Germany (85), while
conjunctivitis or sudden death was also the main disease sign
in rheas in several cases from Texas (57). A further three cases
in rheas ranging in age from two months to three years, with
prominent splenomegaly were reported from Louisiana ( 3 3 ) .
These reports clearly indicate that ostriches and other ratites
typically reared in open-air camps which allow regular direct
and indirect contact with wild birds (including feral pigeons)
are susceptible to Chlamydia infections (comparable to the
situation in turkeys). This is contrary to suggestions of only
'anecdotal evidence of neonatal susceptibility' (145).
Historically, the pandemic of human chlamydial infections of
1 9 2 9 - 1 9 3 0 focused on contact with psittacine species as the
main risk factor. However, shortly afterwards, non-psittacine
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Rev. sci. tech. Off. int. Epiz., 19 (2)
birds, particularly turkeys and ducks, were recognised as
sources of human infection, and inapparent/latent infections
or carrier/intermittent shedding were demonstrated to be
typical of most avian species (121).
Chemoprophylaxis with medicated feed (Chlortetracycline)
during the standard thirty-day quarantine has been regarded
as an effective, practical and economically feasible method to
provide adequate safeguards for quarantine station employees
(e.g. in the USA), against chlamydial transmission from
psittacines. However, as the recommended treatment for
chlamydiosis is constant tetracycline treatment for a period of
forty-five days, even an official thirty-day treatment would fail
to prevent the introduction of chlamydiae into a country via
the exotic bird trade ( 4 9 , 1 1 6 , 121). Recently-developed
antibiotics (quinolones) could possibly offer a solution ( 8 6 ) .
Demonstration or identification of C. psittaci in live birds
during periods of non-shedding remain extremely difficult.
Tests used include culture, serological testing, immunoassays
and molecular (PCR) based tests. These tests are detailed in
the Office International des Epizooties (OIE) Manual of
Standards for Diagnostic Tests and Vaccines ( 9 9 ) , but
comparison studies concluded that any live bird assay may fail
to detect chlamydial infection because of detection limits
(sensitivity thresholds), cross-reactions and non-shedding.
The most recent techniques (i.e. PCR-based technology) have
not been compared with these other tests in a variety of
situations in domestic and exotic birds (51). Although several
reports have described and indicated the advantages in terms
of sensitivity and ease of sampling of the techniques used in
PCR amplification of chlamydial nucleic acid sequences (62,
77), limited comparisons with ELISA showed severe
discrepancies (in both directions), indicating that caution is
still required when interpreting results (47). In particular, the
situation regarding chronically infected birds that harbour
mainly intracellular chlamydiae in target organs, remains a
challenge for diagnosis and screening.
Due to a paucity of information regarding the biology of
C. psittaci in ostriches and in light of the above discussion, the
most that can be concluded in relation to international trade
and human health aspects of ostriches is the following:
a) ostriches are susceptible to C. psittaci infections and
probably display the same outcomes following infection as
most other groups of birds (ranging from inapparent infection
to acute mortality)
b) the sensitivity and specificity of serological tests or
immunoassays for C. psittaci in ostriches is unknown, but
PCR technology would probably be as useful in the testing of
this species as in any other
c) due to the very wide host range and the presence of
C. psittaci in almost all avian groups, the organism can be
regarded as ubiquitous, and before being implemented, the
value of testing or screening live ostrich imports should be
evaluated against the background risk posed by migratory
birds (particularly waterfowl). The testing or treatment of
clinically affected birds or flocks coupled with high levels of
disinfection during quarantine is probably more sensible than
reliance on the screening of healthy birds or the treatment of
sero-negative birds (53).
Crimean-Congo haemorrhagic fever
Crimean-Congo haemorrhagic fever is a zoonotic disease
caused by a tick-borne ribonucleic acid (RNA) virus of the
family Bunyaviridae, genus Nairovirus, which is present in
Africa, Asia and Eastern Europe.
The virus causes only a mild fever and viraemia for up to one
week in cattle, sheep and small mammals (especially hares),
while clinical disease occurs only in humans, resulting in
approximately 2 5 % - 3 0 % mortality (134). Infection can be
caused by contact with body fluids from viraemic hosts but is
mainly associated with tick bites. Although the virus has been
isolated from thirty species of ticks, trans-stadial and
transovarian transmission has only been reported for
Hyalomma
marginatum,
Rhipicephalus
nossicus
and
Dermacentor marginatus, and the distribution of the disease
coincides closely with that of these ticks (66), strongly
suggesting that they are the most important vectors of CCHF
virus.
Limited observations in passerine birds and domestic
chickens have found these birds to be refractory to the virus,
while experimentally infected guinea-fowl developed a
transient viraemia of very low intensity and an antibody
response of only a few weeks duration. Such birds are
therefore unlikely to be able to infect ticks ( 1 2 5 , 134).
However, migratory birds carry immature ticks, and could
thus serve to disseminate CCHF virus which has been
transmitted transovarially in the ticks (67, 6 8 ) . The relatively
high prevalence and titres of antibody found in ostriches,
which commonly carry the xerophilic Hyalomma ticks in the
semi-arid regions where they are farmed on extensive ranches
and riverside alfalfa grazing camps, indicate that ostriches may
be more susceptible to infection than other birds (66, 125).
Approximately fifteen to twenty-five cases of CCHF in
humans are recorded every year in South Africa, mainly in
adult men engaged in the livestock industry (farmers,
labourers, abattoir-workers and veterinarians) in the
semi-arid regions of the country (where
Hyalomma
commonly occurs), with a slight preponderance of cases from
February to March and October to November, when adult
Hyalomma tend to manifest peak questing activity (active
searching by ticks for their vertebrate hosts) ( 1 1 5 , 134).
World attention was again focused on CCHF and ostriches
after seventeen abattoir workers at an ostrich abattoir in
Oudtshoom, South Africa, contracted the disease after contact
with a group of ostriches with a particularly heavy tick
infestation. One patient died, while all the others recovered
fully. Due to concern about the safety of exported ostrich meat
to consumers, the European Union (EU) temporarily
suspended exports from South Africa (41). This prompted the
644
experimental infection of nine ostriches raised under tick-free
conditions with CCHF virus to determine viraemia and the
immune-response curve ( 3 4 , 136). These results can be
summarised as follows:
a) no clinical symptoms are associated with CCHF in
ostriches
b) viraemia lasts approximately four days
c) virus can be isolated from blood and organs
d) virus was not isolated from muscle, but CCHF genetic
material was detected by reverse transcriptase-PCR (RT-PCR)
e) seroconversion begins on day five post-infection and by
day thirteen, antibodies could be detected in all surviving
experimentally infected ostriches.
These results were the foundation for the Decision
97/138/EC, which revoked the ban under certain conditions
(42). This decision included protection measures which were
extended to all countries of Africa and Asia and consisted of
treatment by pyrethroid-based acaricides, with ostriches kept
free of ticks in rodent-controlled areas, for at least fourteen
days prior to slaughter. These requirements apply to both
slaughter birds and ostriches destined for live export.
Although these requirements are practical, economically
feasible and have been strictly applied since 1997 by the
Veterinary Services of South Africa, the potential for the
introduction of CCHF-viraemic ostriches from countries in
Eastern Europe, where the relevant ticks naturally occur and
the virus causes regular clinical infections in humans
(e.g. historically in the Crimean peninsula), was not
considered by the EU authorities ( 3 4 ) . In fact these safety
measures should logically be extended to all domestic
livestock and the movement of both live animals and meat
(pre-slaughter measures) across borders ( 1 3 4 , 1 3 6 ) , as the
risks regarding tick contact or viraemic periods in these
different classes of animals are very similar.
Rev. sci. tech. Off. int. Epiz., 19 (2)
isolations should only be undertaken in a maximum risk
bio-secure laboratory facility.
Spongiform encephalopathy
Bovine spongiform encephalopathy (BSE), also known as
'mad cow disease' is a fatal disease thought to be caused by a
prion (similar to scrapie in sheep) and is associated with
variant Creutzfeldt-Jakob disease in man (36, 113).
Experimental infections were successful in several animal
species, including cattle, pigs, sheep, goats, marmosets and
mice, and disease has been reported in wild captive animals in
the United Kingdom (UK) ( 8 1 ) . The disease causes central
nervous symptoms and is diagnosed by histopathological
examination of brain tissue and the demonstration of
scrapie-associated fibrils by electron microscopy (159).
Spongiform brain lesions were reported in three adult
ostriches from two zoos in Germany which had a history of
central nervous system disease with ataxia, imbalance and
unco-ordinated feeding. The material was not examined for
scrapie-associated fibrils. The birds had been fed a proprietary
poultry feed which included carcass meal. Allegedly, the birds
had also been fed meat, some of which was from injured cattle
slaughtered in cases of emergency. If this was indeed the case,
it was certainly a strange and unnatural husbandry practice
(71, 7 2 ) . Due to the sensitivity over BSE and related
conditions, ostrich rations should not contain carcass meal
(81, 123). From these reports, it is not clear whether
Newcastle disease (ND) was included in the differential
diagnosis, but the authors concluded that a definitive
diagnosis could not be made and that a toxic or nutritional
aetiology could not be discounted.
A review of more than a thousand diagnostic ostrich cases
submitted to the OVI during the period 1 9 9 3 - 1 9 9 8 , as well as
published reports of similar symptomatology in ratites ( 1 5 6 )
is presented below as a differential diagnosis list for 'nervous
conditions' in ratites:
- Newcastle disease
No evidence has been obtained to suggest that CCHF virus
constitutes a public health hazard in meat from any animal or
bird processed and aged according to normal health
regulations (66, 134, 135). The measures outlined above
should be enacted as an additional safeguard, protecting
principally those who would normally come into contact with
fresh blood of potentially viraemic animals (e.g. abattoir
workers).
- hypoglycaemia (e.g. impacted stomach)
-
trauma
- pain (torticollis, head swaying; e.g. penetrating foreign
objects in proventriculus/gizzard)
- Western equine encephalomyelitis
- Eastern equine encephalomyelitis
- Borna disease
Serological screening can be performed using a competitive
ELISA (C-ELISA) (29) or sandwich ELISA using conjugated
antiserum to ostrich immunoglobulins (Ig) (136). The
sandwich ELISA was slightly less sensitive than the former,
but correlated very well over the fourteen day experimental
period. Viral RNA can be detected by RT-PCR in infected
material (30), while the virus can be isolated in Vero cells or
by intracerebral inoculation of day-old mice (124). Due to the
significant zoonotic risk to laboratory personnel, these
- spongiform encephalopathy
- bacterial septicaemia (Clostridium perfringens,
Pseudomonas
aeruginosa, Salmonella spp. and Escherichia coli strains)
- Chandlerella
quiscoli
- Balyascaris
procyonis
- gangliosidosis
- hepatic encephalopathy (fatty degeneration of liver)
645
Rev. sci. tech. Off. int. Epiz., 19 (2)
- lead poisoning (ingested battery plates)
- Clostridium
Poultry diseases
botulinum
- neoplasia (cerebral haemangiosarcoma)
- mycotoxicoses (e.g. from suspected Fusarium
toxins).
moniliforme
In southern Africa, the first four entries above were by far the
most common causes of reported 'nervous signs' in ostriches
over six months of age, while bacterial septicaemia and
hypoglycaemia were the most important in ostrich chicks.
Ostrich products or live ostriches of any age do not appear to
pose any risk to an importing country regarding BSE.
Anthrax
Anthrax is a peracute disease characterised by septicaemia and
sudden death with the exudation of tarry blood from the body
orifices of the cadaver. The disease is caused by Bacillus
anthracis, which forms highly resistant spores upon exposure
to air, protracting the infectivity of a contaminated
environment. The disease occurs world-wide, mainly in
poorly drained alkaline soils and has been reviewed
extensively in standard textbooks ( 2 5 , 4 0 ) .
Ostriches are the only birds known to be susceptible to
anthrax, possibly because of a generally lower body
temperature than other birds (72). Many field cases were
reported in the early 1900s in South Africa (117), while
experimental infections led to the description by Theiler of
two syndromes, namely: sudden death and 'anthrax fever',
both of which could occur simultaneously in a flock (140).
Sudden death was associated with petechial haemorrhages on
the pleura and peritoneum, congestion of the intestines, a
normal or enlarged spleen with very dark pulp and typical
B. anthracis bacilli in the blood, demonstrated by standard
smears.
Anthrax fever caused anorexia and somnolence but ostriches
recovered naturally or after treatment with penicillin. No
bacilli could be found in the blood smears from such birds.
A recent outbreak of anthrax in a dairy herd in the Eastern
Cape, South Africa, was associated with the feeding of infected
bone meal, which was a common method of anthrax
transmission in the UK in the pre-BSE era (25). The outbreak
resulted in several bovine mortalities, but no ostriches on the
same farm became ill or died, despite receiving the same
feedstuff's (OVI, unpublished case reports 1 9 9 3 - 1 9 9 8 ) .
The disease was controlled in cattle in the early part of this
century in South Africa and most parts of the world with the
advent of effective vaccines. These vaccines also successfully
protect ostriches from the disease (140). Clinically healthy
ostriches, fertile eggs and ostrich products therefore' do not
constitute any anthrax risk to an importing country.
Fowl typhoid (Salmonella Gallinarum) and
pullorum disease (Salmonella Pullorum)
No field cases or experimental evidence have reported
infection with either S. Gallinarum or S. Pullorum in ostriches
(145; OVI, unpublished case reports 1 9 9 3 - 1 9 9 8 ) . Salmonella
Pullorum has been reported to have the potential to infect
emus (144), but no cases have been reported from any ratites.
Laboratory diagnosis should be performed according to
requirements stated in the OIE Manual of Standards for
Diagnostic Tests and Vaccines (99). The Manual states that the
serum agglutination test is satisfactory for individual birds for
establishing presence and prevalence within the flock in the
case of poultry. However, due to the significant interference
by non-specific agglutinins present in most ostrich sera in any
agglutination-based test (see discussion of inactivation in
section on Newcastle disease virus), this screening method
has severe limitations when used for ostriches. Positive
reactors should be confirmed as being infected by culture.
The ELISA systems should be established as soon as possible
to allow accurate serological screening or diagnosis of
ostriches.
South Africa, which still dominates world trade in ostriches
and ostrich products and where an estimated 6 0 % or more of
domestic ostriches are found, successfully eradicated both
S. Pullorum and S. Gallinarum from poultry in the 1950s and
has been officially free from these diseases since that time.
They remain 'controlled diseases' under the South African
Animal Diseases Act (Act 35 of 1984) and should any
outbreaks occur, they will be stamped out. Similar
certification from competent Veterinary Services should be all
that is required from countries exporting ostriches and ostrich
products.
Avian mycoplasmosis (Mycoplasma
gallisepticum)
Mycoplasma has been isolated from ostrich chicks as well as
feedlot and breeder birds, and their pathogenicity has been
suspected. This group of organisms was isolated from the
lungs and trachea of 32 out of 3 7 2 ostrich chicks in North
America, unassociated with any pathology (126). Such agents
have been isolated regularly during winter from feedlot
ostriches in South Africa with respiratory symptoms,
concomitant with a range of other opportunistic pathogens,
including E. coli, P. aeruginosa, Pasteurella spp. and even
occasionally Haemophilus
paragallinarum.
The role of
mycoplasmas is unclear in such cases (72; OVI, unpublished
case reports 1993-1998). Mycoplasma synoviae has also been
isolated in several of these cases while mycoplasmas were
demonstrated by electron microscopy in GIT contents from
chicks with enteritis younger than four weeks. Clinical
improvements were noted after treatment with tylosin at 3 0 0
ppm in the starter ration (72; OVI, unpublished case reports
646
1 9 9 3 - 1 9 9 8 ) . Positive serological reactions to the poultry
pathogens M. gallisepticum and M. synoviae in ostriches have
been reported from Italy (104). Experimental inoculation of
six- to eight-week-old ostriches with M. gallisepticum
and
subsequent
recovery through culturing
and PCR,
demonstrated that this agent can colonise the tracheas of
young ostriches. A similar trial with M. synoviae gave
inconclusive results (38).
A chronic severe sinusitis caused by M. gallisepticum was
reported in rheas (109), while M. synoviae was isolated from
another flock of rheas in North America with clinical signs of
mycoplasmosis (162).
Given the apparent susceptibility of ostriches and rheas to
poultry mycoplasmas and the lack of information concerning
the role of these and other species of Mycoplasma
in
pathological conditions of this class of birds, ratite farms are
recommended to be kept free from poultry (72). Ostriches
destined for export should be clinically healthy, especially
regarding upper respiratory infections (i.e. periocular swelling
of sinuses). Due to the limitations of agglutination-based tests
in ratites, quarantine testing of live birds should utilise
sentinels instead. Fertile eggs should originate from clinically
healthy, closed breeding flocks. There are no indications that
ostrich meat is associated with a risk of spreading
Mycoplasma.
Pasteurellosis
Haemorrhagic septicaemia caused by Pasteurella
multocida
has caused ostrich mortality in zoos during outbreaks that
simultaneously affected many species of animals ( 9 5 , 100).
The cases varied from acute deaths to illness lasting several
weeks.
Nine ostriches of ten to twelve months of age died at Frankfurt
Zoo after several weeks of illness and recumbency, during
which time the birds maintained an appetite. The disease
commenced with lacrimation and conjunctivitis, while
splenic abscesses were noted at necropsy and P. multocida was
isolated from heart blood (95).
In Kano Zoo, Nigeria, an ostrich died acutely along with
several game species, kangaroos and a bateleur eagle. The
post-mortem examination revealed generalised congestion
with petechiae and ecchymoses on the epicardium,
endocardium, kidneys and intestines (100).
Pasteurella multocida has also been isolated from several cases
of acute mortality in ostrich chicks from farms in South Africa.
Post-mortem findings were non-specific and resembled the
report from Nigeria. Outbreaks were easily contained with
synthetic penicillins and prevented through improved
biosecurity, especially regarding rodent control and contact
with wild birds and surface water (OVI, unpublished case
reports 1993-1998).
Rev. sci. tech. Off. int. Epiz., 19 (2)
As no clinically ill ostrich should be accepted for export or
slaughter, no specific testing against P. multocida in ostriches
or ostrich products is needed, and certification in that regard
should be the only requirement.
Newcastle disease virus
All avian species are considered susceptible to infection with
Newcastle disease virus (NDV), although members of the
families Anseriformes (waterfowl) and Psittaciformes (parrots)
have been identified as subclinical carriers, intermittently
shedding strains highly virulent for poultry and thus
suggesting a higher innate resistance or threshold level than
domestic poultry (2, 4, 5 6 , 7 0 , 163). This is of particular
importance for the control of the disease in birds allowed free
flight (e.g. racing pigeons and those birds reared in open-air
camps, feedlots or on extensive grazing pastures, such as
turkeys, backyard chickens and ratites). The control of ND in
racing pigeons remains a world-wide challenge due to the
nature of the sport (large numbers of birds from many
different lofts are collected and transported together in
confined spaces, with long flight distances, often across
international borders, and many thousands of pigeons lost'
annually which mix with feral populations) and the
established relationship between NDV outbreaks in poultry
and the pigeon-associated (P-paramyxovirus [PMV]-1) strain
that occurred in the UK in 1 9 8 4 - 1 9 8 5 and again in 1 9 9 7
(2, 5, 6 , 1 6 , 2 4 , 4 4 , 8 7 ) .
This NDV serotype has been isolated from captive wild birds
in South Africa (39), and pigeons and doves regularly visit
ostrich feed containers on farms in this country, but P-PMV-1
has never been isolated from ostriches in South Africa.
Historically, ND in ostriches had been reported as isolated
cases in zoos and circuses only ( 4 3 , 7 9 , 8 2 , 110). In 1 9 8 9 ,
outbreaks occurred in farmed ostriches in Israel ( 1 0 5 , 1 2 0 ) ,
where the birds were reared in close proximity to commercial
poultry. Approximately 3 0 % of five- to nine-month-old birds
died within three weeks. A velogenic NDV isolate (Israel 67')
caused approximately 8 0 % mortality in experimentally
infected three-month-old ostrich chicks within five to ten
days and the virus was isolated from various organs from all
dead birds.
Following a particularly severe outbreak of NDV in poultry
after a twenty year absence, virulent NDV caused mortality in
ostriches during several outbreaks on commercial ostrich
farms in South Africa beginning in 1993 ( 1 4 , 6 9 , 7 0 , 7 3 , 1 4 9 ) .
As the epidemic spread to poultry in other countries in the
region, outbreaks also occurred in ostriches in Namibia,
Botswana and Zimbabwe.
The viruses isolated from these cases were identical to poultry
isolates from this region obtained at the same time (93), and
contact with or trade in backyard chickens and/or commercial
poultry appeared to be the source of NDV in ostriches, rather
than wild birds. Similar conclusions were reported in a recent
647
Rev. sci. tech. Off. int. Epiz., 19 (2)
study conducted in Switzerland (24, 7 2 , 122, 149) (Fig. 1).
Field and experimental data indicate that the route and
mechanism of infection have a major influence on the clinical
severity of the disease in ostriches. Severe respiratory disease
with rapid spread and high mortality is seen only in closed
chick-rearing units, while ostriches kept outdoors usually
contract the disease by the oral route from faeces or water,
resulting in nervous signs and a very slow spread of infection
(70, 7 2 , 1 5 1 , 1 5 4 ) . Similar slow or limited spread of NDV has
been reported in backyard chicken flocks in California (44).
Village chickens,
rural poultry,
free-range,
scavenging
chickens
Waterfowl,
pigeons, wild birds,
carnivores, rodents,
infected faeces,
infected water
Social
Seasonal
Live market
Spent hen market
Vendors
Unvaccinated
Vaccinated
Commercial
ostriches
Infected carcasses,
infected bedding,
feed trucks,
personnel
movements,
wind,
intermittent
shedding by layers
Commercial poultry
Fig. 1
Epidemiology of Newcastle disease in South Africa
These observations may be partly due to the sterilising effect
of the ultraviolet rays of the sun in the semi-arid regions of
southern Africa where ostriches are farmed ( 7 2 ) . Several
experimental challenge studies have been conducted in South
Africa, investigating different aspects of the disease in different
age groups of ostriches, including efficacy testing of
inactivated aluminium hydroxide (AlOH) La Sota-strain
vaccine. In all cases, challenge was with the field isolate of
velogenic NDV, which has been active in southern Africa
since 1 9 9 3 (mean death time [MDT] : 4 2 h to 4 8 h;
intracerebral pathogenicity index [ICPI]: 1.7) (8, 6 9 , 1 5 0 ,
151, 1 5 4 ) .
These results can be summarised as follows:
a) All ages investigated (two weeks to fourteen months old)
were susceptible to velogenic NDV.
b) While clinical signs show a typical progression, no
pathognomonic macro- or microscopical lesions are found in
NDV-affected ostriches. Post-mortem lesions included
subcutaneous head and neck oedema, splenomegaly,
petechiae on serosal surfaces and occasionally paintbrush
haemorrhages in the gizzard below the koilin layer, while
perivascular lymphocytic cuffing was occasionally seen in the
brain. The lesions have also been described from field cases
(8, 7 2 , 145).
c) Currently available La Sota vaccines (live plus inactivated)
can stimulate protective immunity in ostriches which lasts
more than six months. The immune response curves, after
challenge with virulent NDV, from 142 slaughter ostriches
divided into three groups that had been vaccinated
approximately one to two months, two to four months and
four to six months earlier, showed no significant differences
between the groups. The response levelled at maximum titres
on day fourteen post infection. This humoral immunity
correlated very poorly with protection in the case of
haemagglutination inhibition (HI) tests, and very well in the
case of ELISA systems (154).
d) The period of viraemia in vaccinated slaughter ostriches
(twelve to fourteen months old) was determined as nine to
Several field investigations of outbreaks of NDV in ostriches
eleven days.
and poultry in southern Africa have suggested the following
e) No evidence was found of a carrier state for velogenic NDV
important
in slaughter ostriches.
differences between outbreaks in commercial
poultry and in ostriches caused by the same strain of NDV
(151):
a) a significant individual variation exists in susceptibility to
virulent NDV challenge in ostriches
b) susceptible birds are usually younger, are poor performers,
have a poor body condition, concurrent infections (e.g. air
sacculitis), or an unbalanced diet
c) virulent NDV spreads very slowly within a group, and in
practice almost never to adjoining groups, even if groups are
separated only by a fence or poles
d) nervous symptoms predominate, and these follow a
predictable pattern of development in affected birds.
f) The effective vaccination programme enforced by the
Veterinary Services of South Africa, coupled with the
pre-slaughter quarantine period necessary to comply with
CCHF-control regulations, thus covered the determined
viraemic period, and through statistical risk analysis
methodology, it was determined that international trade in
ostrich meat was not likely to spread NDV to non-endemic
areas (e.g. the EU or USA).
g) Virological examination by cloacal or choanal swabs, using
standard virological techniques ( 9 9 ) , was unsuccessful even
in clinical cases and therefore has no practical value as a
screening tool (8, 1 5 1 , 1 5 4 ) . This is possibly due to the
voluminous faeces of ostriches.
Rev. sci. tech. Off. int. Epiz., 19 (2)
648
The serological testing of ostrich sera does not give such
consistent results as in poultry. The HI test is regarded as
unreliable, leading to both false positives and false negative
results (8; OVI, unpublished case reports 1 9 9 3 - 1 9 9 8 ) . Even
heat treatment (56°C for 3 0 min) or absorption with kaolin
does not remove all non-specific agglutinins. However,
pre-treatment adsorption with 2 5 µl packed chicken red
blood cells or ideally, ostrich chick red blood cells, will
improve the accuracy of the HI assay (92; OVI, unpublished
case reports 1 9 9 3 - 1 9 9 8 ) . Positive titres are those equal to or
greater than a 2 dilution using 4 haemagglutination units.
4
Stable conjugated antisera to ostrich Ig for indirect ELISAs
have been developed ( 3 1 , 1 6 1 ) and these are used as standard
practice at the OVI. Recently, a monoclonal blocking ELISA
which shows excellent sensitivity and specificity has become
commercially available ( 4 5 , 8 3 ) , and this ELISA has the added
benefit of not being limited to usage in one host species.
These, or similar ELISAs should be the basis of serological
screening of ostriches destined for export.
Cross-reactions with PMV-6 have also caused difficulties in
the interpretation of NDV HI tests in quarantined, imported
ostriches on two occasions in New Zealand ( 1 5 , 3 7 ) . The
PMV-2 has been reported from ostrich chicks in the USA
(126), while PMV-7 was isolated from two juvenile ostriches,
one of them with impaction (164).
In all cases, the isolation of NDV is the 'gold standard' for
diagnostic purposes (72, 9 9 ) , with new molecular tests,
e.g. RT-PCR, showing promise for the future, once validated
in ostriches, to allow accurate interpretation of results from
field samples or screening. This technology has already been
included in the new OIE definition for NDV.
Avian influenza
Influenza A viruses of all fifteen known haemagglutinin
subtypes have been isolated throughout the world from many
domestic and wild species of bird (129). The highly
pathogenic strains for chickens have all been of the subtypes
H5 and H7, but viruses of these subtypes are not necessarily
highly pathogenic (3). The considerable ability of influenza
viruses to mutate to strains of higher virulence due to gene
mutation or reassortment is well known (e.g. the H5N2
epizootics of 1 9 8 3 - 1 9 8 4 in Pennsylvania [48] and 1 9 9 4 - 1 9 9 5
in Mexico [155]), and this dictates close scrutiny of all H5 and
H7 isolates from any species under any circumstances. The
ability of influenza viruses of avian origin to cause epidemics
of respiratory disease and even death in humans is of
particular concern (1, 7 8 , 1 3 3 ) .
The epidemiology of avian influenza has been closely related
to migrations and movements of wild waterfowl ( 3 , 4 6 , 6 4 ,
65, 130), and indirectly related via the use of untreated
surface water, as the virus can persist in such environments
for up to 2 0 0 days (131).
Domestic poultry that are kept or reared in open-air camps or
utilise riverside grazing camps (e.g. turkeys or ratites), are
particularly vulnerable to cross infection from waterfowl
(3, 1 0 8 , 111). Furthermore, evidence suggests interaction of
influenza viruses of H1N1 subtype between turkeys and pigs
(97).
The first reported outbreaks of avian influenza in ostriches
occurred in 1 9 9 1 and 1992 in the Eastern Cape Province and
Oudtshoom district in South Africa, and were typed as H 7 N 1 ,
with no pathogenicity for chickens (7, 8, 9, 12, 13, 2 7 ) .
Clinically, the affected birds were depressed, had bright green
discoloration of the urine, respiratory signs and ocular
discharge, with mortality reaching 6 0 % in some groups. The
severity of symptoms and lesions depended on age and
concurrent infection with E. coli, P. aeruginosa, S. aureus and
Aspergillus fumigatus (air sacs). On post-mortem examination,
the livers were enlarged, mottled and friable with coagulative
necrosis surrounded by marked heterophil infiltrate and
vasculitis histologically. Areas of necrosis were also present in
the spleen and pancreas, and severe congestion occurred in
the small intestine in addition to necrosis of the tips of the
villi.
Subsequent isolations from these same farms or from
Zimbabwe, were from cases with similar pathology or even
from inapparent infections. The isolates were typed as follows:
South Africa H7N1 ( 1 9 9 1 , 1992), H5N9 ( 1 9 9 4 ) , H9N2
( 1 9 9 5 ) , H6N8 (1998), and Zimbabwe H5N2 ( 1 9 9 5 ) , but
none of these isolates were pathogenic for poultry (93; OVI,
unpublished case reports 1 9 9 3 - 1 9 9 8 ) . However, some ratite
isolates of avian influenza virus were found to have a realistic
potential for interspecies transmission to poultry and for
mutation to more pathogenic variants (137). An apathogenic
virus, subtype H5N2, was isolated from juvenile ostriches in
quarantine in Denmark together with an apathogenic PMV-1,
the mortality associated with this case appeared to have been
stress-related (e.g. impactions and enteritis) ( 7 6 ) .
An inactivated emulsified H7N1 vaccine was successfully
used to curb the outbreaks in South Africa from 1 9 9 1 to
1992; the vaccine prevented morbidity and mortality, but did
not prevent shedding of virus (7, 8). A similar approach has
been used as a temporary measure in poultry, using the
dominant strain associated with a particular outbreak (3, 2 1 ) .
Should the outbreak be caused by a highly pathogenic avian
influenza (HPAI) virus, control should be achieved through
stamping-out and quarantine measures in that vaccination
with such viruses could prevent mortality, but still allow
replication and shedding of the virus (3). Use of live virus
vaccines should not be permitted due to the ability of this
virus to spread, causing mixed infections in the same host
species that will allow gene reassortments and possibly
virulent mutant offspring ( 1 , 3 ) . Several new-generation
vaccines, based on molecular technologies, are being
developed and field tested. These include recombinant
649
Rev. sci. tech. Off. int. Epiz, 19 (2)
vaccines using fowlpox ( 4 1 , 5 2 , 9 6 ) or baculovirus ( 1 6 0 ) as
expression vectors, in addition to deoxyribonucleic acid
(DNA) vaccines (157). The serological testing of ostrich
sera for avian influenza using HI tests is plagued by the sanie
practical difficulties as testing for ND, due to non-specific
agglutinins. Development of ELISA-based avian influenza
serological tests has occurred in different parts of the world
(23), with a C-ELISA in particular showing great promise
after being tested in chickens, turkeys, ostriches and emus
(165).
Very little is known about the pathogenesis of avian influenza
in ratites, so that the outcome of control strategies is more
difficult to predict, compared to the situation in chickens and
turkeys. Recent experimental studies have started to address
some of these aspects: using a highly pathogenic strain
(H5N1) from turkeys as well as a non-pathogenic isolate
(H5N2) from ostriches, Manvell and co-workers infected ten
three-week-old chickens and ten two-week-old ostriches with
each virus ( 9 4 ) . The ostriches infected by the highly
pathogenic isolate failed to show any clinical signs when
inoculated by either the intramuscular or intranasal route,
while the infected chickens all died within 4 2 h.
Seroconversion and isolation of virus from swabs confirmed
that infection with this strain was established. The virus of low
virulence also established infection in ostriches and produced
a higher immune response than in chickens. These findings
suggest a complex relationship between host species and virus
strain, with the possibility of host-adaptations.
Strains of H7N1 and H5N2 subtypes were isolated from emus
and rheas in Texas and North Carolina in the USA, while
positive sera were found in eleven States. These contained
humoral antibodies to all known H-subtypes, except H10,
H13 and H14, and to all nine N-subtypes (103). Experimental
infection of four- to twelve-month-old emus with a highly
pathogenic strain, H7N7 (four birds), and a strain of low
pathogenicity, H5N3, was conducted in Canada (61). The
birds were susceptible, with virus shedding detectable in
tracheal and cloacal swabs between three and ten days post
infection. A brief period of mild clinical signs was noticed only
in the groups infected with the highly pathogenic virus.
Viruses recovered from both groups were similar in
pathogenicity to the respective inoculums. All birds
had seroconverted by ten days post infection, as determined
by HI, agar gel immunodiffusion (AGID) and C-ELISA.
This study indicates a significant threshold difference
between emus and chickens in relation to certain strains of
HPAI.
This discussion reiterates the importance of surveillance for
avian influenza (and ND) in wild birds, particularly
waterfowl, and the crucial role of husbandry practices in the
prevention of outbreaks, particularly ensuring that no contact
occurs between farmed ratites and wild birds, either directly
or indirectly (through surface water). Serology based on
ELISA should be validated as a matter of urgency in ratites,
while vaccines have a limited, probably localised geographical
role in this group of birds. At this stage of limited knowledge
and validation of avian influenza testing in ostriches, the use
of sentinels is recommended during pre-export quarantine to
provide satisfactory screening against avian influenza, with HI
or ELISA serological screening of the in-contact chickens, or
as soon as the technique is validated, ELISA serological
screening of the ostriches themselves.
Borna disease
The causative agent of Borna disease is a single-stranded RNA
virus of the family Rhabdoviridae. The disease is present in
Central Europe, the USA, Japan, Sweden and the Near East,
predominantly
affecting horses and
donkeys,
and
exceptionally a variety of other species, causing a range of
behavioural disturbances with or without neurological signs,
such as paresis and paralysis. The mode of transmission is
unknown, but the presence of the virus in nasal secretions,
saliva and urine suggests that dissemination occurs either by
direct contact or through fomites and feed. The relatively
small amounts of virus found in such secretions, and the low
level of spread suggests that the disease is not highly
contagious. No vertical transmission or free-living reservoirs
have been identified, although rats are suspected to be
involved. Arthropod vectors have also been suggested, but the
situation is unclear ( 1 1 8 , 1 4 2 ) .
Borna disease in ostriches has only been reported from Israel
in 1 9 8 9 - 1 9 9 4 where the disease produced a specific paresis
and mortality in two- to six-week-old ostrich chicks. All
affected birds died within four to eight days. The inoculation
of serum from paretic ostriches to ostrich chicks at risk,
followed by serum from normal adults, was effective in the
prevention of further disease, demonstrating the protective
action of antibodies ( 1 7 , 1 8 , 1 9 , 1 5 8 ) . Laboratory diagnosis is
by virus isolation, the demonstration of viral protein by ELISA
(unvalidated) (91) and histopathology. The latter consists of
lesions of neuronal necrosis, satellitosis, neuronophagia and
multifocal gliosis in the lumbar spinal cord ( 1 8 , 1 9 , 158).
Due to the short incubation period (less than 2 months) and
the high case fatality rate, no special tests should be required
for live ostriches destined for export. The flock of origin
should have no history of Borna disease over the previous six
months and the ostriches should undergo the normal thirty
day pre-embarkation quarantine in addition to a thirty-day
post-arrival quarantine. There are no data to suggest
transmission of the virus via meat, eggs, leather or feathers.
Equine encephalomyelitis (Eastern, Western)
Eastern equine encephalomyelitis (EEE) and Western equine
encephalomyelitis (WEE) are caused by members of the genus
Alphavirus of the family Togaviridae. Both are restricted to
North, Central and South America, where the viruses cycle
Rev. sci. tech. Off. int. Epiz., 19 (2)
650
between birds and specific ornithophilic mosquitoes. The
viruses cause flu-like disease sporadically in horses and
humans from mid-summer to late autumn, when infection
builds up in the bird populations to a level which results in
spillover to other species of mosquito which feed on both
birds and mammals on the margins of swampy areas. Many
infections in horses and humans are inapparent, and result in
a viraemia lasting up to a week, followed by long-lasting
immunity (141). Clinical disease is more common in young
animals, with EEE frequently being fatal in horses and W E E
typically causing a subclinical or mild disease with less than
3 0 % mortality. The viruses have been reported to cause high
mortality in domestic fowl, pheasants, chukars and quail,
most often caused by EEE in the eastern coastal States of the
USA. After introduction by mosquitoes, the horizontal
transmission within flocks is primarily by feather picking and
cannibalism (99) or, in turkeys and pheasants, by the
faecal-oral route (26).
Both EEE and WEE viruses have caused fatal disease in ratites
including ostriches (128), with EEE having a short incubation
period (20 h to 2 5 h), acute haemorrhagic enterocolitis and a
viraemia of up to two days. Birds aged from twenty to
thirty-six months and juveniles are affected principally, with a
morbidity rate of up to 7 0 % and mortality of up to 8 7 % ( 9 9 ,
143). Multifocal areas of coagulative necrosis in the liver have
also been described in emus with EEE (148). Infection with
W E E virus has been reported in emus, which showed
depression, anorexia, leg weakness, ataxia, recumbency and
paralysis. Flock morbidity ranged from. 1 0 % to 5 0 % and
mortality was below 2 0 % . Recumbent birds died within 4 8 h,
but mildly affected birds recovered within two weeks after
supportive therapy (114). In another report describing similar
clinical signs, emus aged from three months to three years old
were diagnosed with WEE. Morbidity ranged from 1 5 % to
5 0 % and mortality was 8.8% (20). Ratites are not regarded as
amplifiers of EEE or W E E viruses in endemic areas and are
considered accidental hosts.
Vaccines for horses and humans are safe and stimulate
effective immunity, and are also used in ratites with good
results in endemic areas (99, 145).
Wesselsbron disease
The causative agent of Wesselsbron disease is an RNA virus of
the family Flaviviridae, and the genus Flavivirus. No strain
variation has been reported.
Wesselsbron disease occurs only in Africa and is an acute
arthropod-borne infection of sheep, cattle and goats. The
virus has been isolated from several species of mosquito,
especially from floodwater-breeding Aedes spp., and from an
Ixodid tick. Mechanical transmission by biting flies during
epidemics seems likely. The virus causes relatively high
mortality in new-born lambs and kids, subclinical infection in
adult animals, occasional abortions in ewes, and congenital
malformations of the central nervous system accompanied by
arthrogryposis of sheep and cattle foetuses. In humans, the
virus causes a non-fatal, influenza-like illness (40).
Wesselsbron disease has been reported in ratites on only one
occasion. The virus was isolated from tissues of ostriches that
died at four months of age. Although field data indicated very
high mortality in the flock, experimental infection of
six-month-old ostriches with the isolate failed to cause illness
or death. Therefore, as none of the ostriches or offspring were
affected, the role played by the virus in the deaths of these
ostriches remains unexplained. A slaughterhouse survey of
apparently healthy ostriches indicated that antibodies to
Wesselsbron disease virus were found in approximately 5 0 %
of adult ostriches. The suspected mode of transmission of the
virus was via arthropod vectors (10).
Laboratory diagnosis is performed by virus isolation
(intracerebral inoculation of new-bom mice, eight-day-old
embryonated chicken eggs and cell culture) and serological
tests (complement fixation, virus neutralisation and ELISA).
The vims does not appear to be vertically transmitted or
disseminated via ostrich or ratite products. Live ratites
exported to non-endemic areas should be seronegative during
pre-export quarantine as the duration of viraemia of
Wesselsbron vims in ostriches is currently unknown. Export
should preferably be during the season of low vector activity
(April to August in southern Africa).
Infectious bursal disease
The OIE Manual of Standards for Diagnostic Tests and Vaccines
recommends the following tests: virus isolation or direct
demonstration of antigen and demonstration of antibody by
complement fixation, HI, ELISA and plaque reduction
neutralisation tests. The detection of seropositive animals
would indicate vaccination or recovery and in neither case
would the birds be viraemic. Therefore, if import regulations
stipulate serological testing, the author recommends that
seronegative as well as serostable birds (tested during the
thirty-day quarantine period) be accepted. No evidence
suggests that eggs or products of ratite origin could serve as
vehicles of transmission of W E E or EEE viruses.
The causative agent of infectious bursal disease is an RNA
virus of the family Birnaviridae, genus Avibirnavirus. Two
serotypes of the virus have been reported, designated serotype
1 and serotype 2.
All highly pathogenic strains belong to serotype 1. Chickens
are the only known avian species to develop clinical disease.
Although infectious bursal disease vims (IBDV) has been
associated with a number of clinical conditions in turkeys, no
isolates of pathogenic infectious bursal disease (IBD) strains
have been obtained. Serotype 2 is widespread in turkeys and
causes no clinical disease. This type has been isolated from
651
Rev. sci. tech. Off. int. Epiz., 1912)
chickens showing no clinical signs, and antibody to serotype 2
has been detected in some flocks of ducks. Antibodies to the
IBDV group antigen have also been detected in sera of wild
birds showing no clinical signs of the disease (89).
Isolation of an avibirnavirus said to be 'identical to IBDV has
been reported from immature ostriches in the USA in flocks
experiencing high mortality (145).
Investigations into ostrich chick mortality in the UK (two
cases of proventricular impaction and one case of enteritis)
resulted in the isolation of IBD type 2 viruses (55). Similar
birnavirus-like agents were detected on two occasions
following direct electron microscopy (EM) examination of
intestinal contents from 192 ostriches in the USA (126). The
circumstances under which the three viruses were isolated
and the prevalence of antibodies in farmed ostriches, poultry
and wild birds world-wide suggest that IBD type 2 viruses are
probably apathogenic for ostriches as well as for most avian
species (55).
Antibodies to the IBDV group antigen have also been detected
in the sera of ducks, turkeys and wild birds from various parts
of the world (89), which suggests that these viruses are widely
distributed in bird populations.
The IBD type 1 virus has not been reported in ostriches or
ostrich products. Eggs should be sterilised by washing with
virucidal disinfectant to prevent faecal contamination with
NDV or other unknown viruses, and this should also
inactivate any possible birnaviruses. Serological screening
with the AGID test will show both type 1 and 2 antibodies and
thus has limited value and should probably only be used in
cases where both types are not present, e.g. in New Zealand
where IBD type 2 is considered exotic (119). Once again it is
stressed that no poultry should be permitted on ostrich or
ratite farms, especially those with export status.
Adenovirus infections
The causative agent is a DNA virus of the family Adenoviridae,
genus Aviadenovirus. Adenoviruses are widespread in poultry
all over the world. In general, avian adenoviruses are divided
into three groups. The first contains conventional group 1
fowl adenoviruses (FAV-1 to FAV-12) with FAV 1 as the type
species. The second group includes adenoviruses associated
with egg drop syndrome 1 9 7 6 (EDS 7 6 ) , with the virus '127'
as the type species. The third group comprises so-called
type II fowl adenoviruses and includes turkey haemorrhagic
enteritis (THE) virus, marble spleen disease virus of
pheasants, and the avian adenosplenomegaly virus of
chickens, with THE virus as the type species (75).
Adenoviruses have been implicated as the cause of wasting
disease in ostriches at approximately two months of age in the
USA. The clinical signs associated with these outbreaks
included non-specific wasting, anorexia and
(145).
depression
An adenovirus was isolated from a four-month-old ostrich
which died without showing any obvious disease signs.
However, the precise role of the virus has not been
established. Subsequent studies of this isolate showed the
similarity to FAV-1 ( 3 5 , 5 4 ) .
The FAV-1 principally affects quail, causing a specific clinical
syndrome known as quail bronchitis. The disease is highly
contagious and morbidity and mortality may reach 8 0 % to
100% (90).
Another study found six adenoviruses in young and adult
ostriches, all belonging to group I. One isolate (FAV-2) was
from a six-week-old ostrich with gross lesions of pancreatitis.
The other five isolates (FAV-8) were either from young
ostriches showing signs of diarrhoea or from apparently
healthy breeding female ostriches producing eggs with shell
aberrations (119). Other FAV-8 isolates have been detected in
poultry in association with inclusion body hepatitis and
respiratory disease in broiler chickens (75).
The FAV serotype 8 is, among other adenovirus group I
serotypes, said to be implicated in natural outbreaks of
inclusion body hepatitis in chickens. The disease is
characterised by a sudden onset. Affected chickens die within
48 h. Morbidity is low, while mortality may reach 1 0 % to
3 0 % (32).
An adenovirus was isolated from ostrich chicks with liver
lesions in outbreaks on ten farms in the USA ( 1 2 8 ) and was
also demonstrated by EM in the liver of one ostrich chick
(126). Raines and co-workers in Oklahoma reported further
cases in ostrich chicks younger than two months with liver
pathology (72). Clinical signs of 'chick fading syndrome' were
produced when the isolates were inoculated orally into five
test ostrich chicks (three negative controls). However, two
adenovirus isolates from ostriches examined at the University
of Georgia were found to be apathogenic for experimentally
infected ostrich chicks (98).
Adenovirus and rotavirus particles have been found in the
intestines of an emu chick with enteritis and E. coli
septicaemia (63). Adenoviruses associated with EDS 7 6 or
adenoviruses belonging to group II have not been isolated
from ratites.
Laboratory diagnosis is based on virus isolation (host specific
cell lines), immunofluorescence, haematoxylin and eosin
staining and virus neutralisation tests to identify the serotype.
Adenoviruses are ubiquitous and the role of these viruses as
pathogens in ostriches and other ratites has not been defined.
652
None of the available data suggest that live ostriches, ostrich
meat or other products pose a risk of transmitting diseases
caused by adenoviruses. Special control measures are
therefore not indicated.
Coronavirus infections of ostriches
The causative agent is an RNA virus of the family
Coronaviridae and the genus Coronavirus. A Coronavirus has
been isolated, along with a wide range of bacteria and other
viruses, from young ostriches affected with an enteritis.
However, the Coronavirus may not have been the primary
cause of the syndrome. A coronavirus-like agent has also been
detected in a six-week-old rhea chick experiencing weakness,
ataxia and death. The ostrich Coronavirus has been suggested
as a new species ( 5 0 , 8 0 , 1 4 5 ) .
Coronaviral enteritis has also been diagnosed in ostriches in
South Africa, associated with a chronic 'fading' syndrome or
explosive outbreaks. The virus could not be isolated with
conventional techniques, but was identified using EM
(8; OVI, unpublished case reports 1993-1998).
Coronaviruses can also occur in domestic chickens (infectious
bronchitis), turkeys, pheasants and pigeons, and are generally
considered to be species-specific.
Only clinically healthy ostriches should qualify for export. No
evidence has been found of transmission of coronaviruses via
products.
General comments
The preceding discussions clearly indicate that in most
instances, substantial knowledge concerning diseases of
ostriches with international trade or public health significance
is not currently available to allow national health screening for
these diseases. Furthermore, most standard tests employed in
the poultry industry are not validated in ostriches, and as
illustrated in the case of HI tests, significant confounding
effects occur in this species. Validated serological tests
(e.g. ELISAs) are available as species-specific assays
(e.g. indirect ELISAs against ND) or even non-species specific
assays in exceptional cases (e.g. monoclonal blocking ELISA
against ND). Even PCR-based investigations are limited, due
to unknown pathogenesis and shedding patterns of most
pathogens in ostriches. Lastly, the relative novelty of ostriches
as a production species means that regulatory authorities are
faced with an 'unknown factor' in terms of possible disease
associations. The following suggestions should allow
reasonable safety guarantees for consumers and importing
countries:
a) Regulations regarding control of vegetation, rodents and
ticks, designed as additional safety measures against CCHF for
abattoir workers, as well as a thirty-day pre-slaughter
Rev. sci. tech. Off. int. Epiz., 19 (2)
residency ('quarantine'), should be enforced at all ostrich
abattoirs in the areas were CCHF is endemic (Africa, Middle
East, Asia, southern and eastern Europe).
b) Abattoirs approved for ostrich meat exports should have a
functional hazard analysis critical control point (HACCP)
action plan that is regularly evaluated by the Veterinary
Services of the country concerned, with particular reference to
control of Salmonella.
c) If importation of live ostriches is to be undertaken,
pre-embarkation quarantine should allow the use of sentinel
chickens held in cages with drinking water artificially
contaminated with faeces from the ostriches in question. This
is preferable to reliance on a battery of unvalidated poultry
serological tests or virus isolation attempts. These tests should
instead be used on the sentinel chickens, a species in which
the tests are validated.
d) Fertile eggs should be disinfected with a recognised
virucidal agent before packing for export.
e) Day-old chicks should originate from closed flocks
registered for this purpose. As breeder ostriches do not
tolerate regular disturbance or handling during the breeding
season, sampling during the typical nine-month laying period
would be impractical. Unvaccinated ostriches older than six
months can be used as sentinels in breeder camps and the sera
of these sentinels tested against viruses such as avian influenza
or NDV on a three-monthly basis. Alternatively, or in
addition, faecal material or drinking water from the breeder
camps could be used to contaminate the drinking water of a
flock of caged sentinel chickens on the same premises, these
chickens could then be subjected to the required test
protocol.
Finally, it is of utmost importance to stress that perceived risks
related to trade in ostriches and ostrich products, other ratites
or any other animals, should always be evaluated against the
background risk situation already existing in the importing
country.
In this particular case, those disease risks already present in
domesticated or wild birds, racing pigeons and those
associated with migrating birds should be considered. No
country or region can claim zero risk against any pathogen
over an extended period, and as one risk can only be
compared to another, it is suggested that 'conflicting
interpretations of data between trading partners be resolved
with the aid of sophisticated computer programs developed
for risk analysis in situations such as these.
653
Rev. sci. tech. Off. int. Epiz., 19 (2)
Les maladies des autruches
D.J. Verwoerd
Résumé
Les connaissances scientifiques sur les maladies des autruches sont
incomplètes et très fragmentaires, et dans la plupart des cas on ignore t o u t des
aspects techniques des épreuves utilisables pour le diagnostic et/ou le dépistage
de ces maladies. Salmonella Typhimurium est commune à plusieurs espèces
d'autruches ; elle est à l'origine d'une mortalité chez les jeunes de moins de trois
mois dans les élevages, mais elle est rarement décelée chez ceux âgés de plus de
six mois ou chez les autruches de douze à quatorze mois destinées à l'abattage en
Afrique
australe.
Campylobacter
jejuni
et Chlamydia
psittaci
sont
occasionnellement observés, surtout chez les jeunes autruches, mais le
diagnostic reste dans les deux cas difficile. La fièvre hémorragique de
Crimée-Congo peut être transmise aux animaux domestiques, y compris aux
autruches, principalement par des tiques appartenant au genre Hyalomma. Chez
les autruches, l'infection est asymptomatique et la virémie persiste environ quatre
jours. A u c u n cas d'encéphalopathie spongiforme n'a été rapporté de f a ç o n
certaine chez les autruches et les cas de fièvre charbonneuse ont été rares au
cours des dernières décennies, alors que cette infection était, semble-t-il, une
importante cause de mortalité il y a environ cent ans en Afrique du Sud.
Salmonella Gallinarum et S. Pullorum n'ont pas été décelés chez les autruches, et
l'infection due à Pasteurella multocida cède aisément à l'antibiothérapie. Quant
aux Mycoplasma
spp., ils sont régulièrement associés à une infection de
l'appareil respiratoire supérieur avec complications dues à des agents bactériens
opportunistes. Les autruches de tous âges sont sensibles au virus vélogène de la
maladie de N e w c a s t l e , mais des v a c c i n s à virus inactivé standard (souche La
Sota) peuvent leur conférer une protection pendant six mois. La période de
virémie chez les autruches v a c c i n é e s destinées à l'abattoir est de neuf à onze
jours et aucun signe n'indique l'existence d'un portage ou la présence du virus
dans les muscles ou dans d'autres tissus au-delà de cette période, la réponse
maximale des immunoglobulines G étant atteinte le quatorzième jour après
l'infection. La réaction d'inhibition de l'hémagglutination est nettement moins
sensible et moins spécifique que les épreuves immuno-enzymatiques. Les
écouvillonnages cloacaux et choanaux utilisés pour le dépistage sérologique
direct chez des autruches cliniquement atteintes (infection naturelle et
expérimentale) n'ont pas permis de déceler le virus de la maladie de N e w c a s t l e .
Tous les isolats de virus influenza aviaire retrouvés chez des autruches se sont
avérés non pathogènes pour les volailles, même les sous-types H5 et H7.
Certaines souches de ces derniers sous-types ont été associées à la mortalité de
jeunes autruches dans des foyers localisés, survenus dans des conditions
climatiques difficiles et au contact d'oiseaux d'eau sauvages. La maladie de
Borna provoque un syndrome nerveux chez les jeunes autruches, mais à ce jour,
elle n'a été signalée qu'en Israël. L'encéphalomyélite équine de l'Est et de l'Ouest
est mortelle chez les autruches et les autres ratites, le taux de mortalité variant de
moins de 20 % à plus de 80 % dans les élevages atteints. Ces maladies sont
présentes en A m é r i q u e du Nord, du Centre et du Sud, où elles sont transmises par
des moustiques ornithophiles. Les v a c c i n s destinés aux chevaux et à l'homme
sont apparemment efficaces et sans danger pour les ratites. La maladie de
W e s s e l s b r o n , la bursite infectieuse (type 2) et les infections dues à des
adénovirus et à des Coronavirus ont été signalées chez les autruches, mais on
ignore encore l'importance exacte de ces maladies.
En raison de l'insuffisance des données sur les maladies des autruches et du fait
que la plupart des épreuves destinées aux volailles n'ont pas été validées pour ce
groupe très particulier d'oiseaux, la stricte observation d'une quarantaine de
trente jours avant l'abattage est fortement r e c o m m a n d é e , tandis que les
654
Rev. sci. tech. Off. int. Epiz., 19 (2)
autruches vivantes et les œufs f é c o n d é s destinés à l'exportation doivent être
soumis à une surveillance basée sur la mise en place de poulets et/ou de jeunes
autruches sentinelles.
Mots-clés
Autruches - Fièvre hémorragique de Crimée-Congo - Influenza aviaire - Maladie de
Newcastle - Maladies aviaires - Ratites - Salmonella.
Enfermedades del avestruz
D.J. Verwoerd
Resumen
El conocimiento científico que se tiene de las enfermedades del avestruz es
incompleto y muy fragmentario, con grandes y frecuentes lagunas sobre
determinados aspectos t é c n i c o s de las pruebas para el diagnóstico y/o la
detección masiva de estas enfermedades. En el África meridional, Salmonella
Typhimurium, microorganismo asiduo de las instalaciones que reúnen a distintas
especies, es causa de mortalidad sobre todo entre polluelos de menos de tres
meses de explotaciones industriales, pero está mucho menos extendido en
polluelos mayores de seis meses o ejemplares asaderos de entre doce y catorce
meses de edad. Aunque ocasionalmente se detecta la presencia de
Campylobacter jejuniy Chlamydia psittaci, principalmente en avestruces jóvenes,
el diagnóstico de ambos microorganismos sigue planteando problemas. La fiebre
hemorrágica de Crimea-Congo se transmite a los animales domésticos - entre
ellos el avestruz - sobre todo a través de garrapatas del género Hyalomma. En el
avestruz, esta enfermedad no induce ningún síntoma clínico durante la fase de
viremia, que dura aproximadamente cuatro días. Por otra parte, no hay informes
fidedignos que demuestren la presencia de encefalopatía espongiforme en el
avestruz. En cuanto al carbunco bacteridiano, y aunque en la era moderna se
haya c o m u n i c a d o muy rara vez su presencia en el avestruz, esta e n f e r m e d a d
constituía, según los informes, una causa importante de muerte en Sudáfrica
hace cerca de 100 años. Salmonella Gallinarum y S. Pullorum no se han detectado
nunca en avestruces, y Pasteurella
multocida
es fácil de controlar con
antibióticos. Regularmente se detectan especies de Mycoplasma asociadas a un
síndrome de las vías respiratorias superiores complicado por infecciones
oportunistas de patógenos bacterianos. Aunque el avestruz es susceptible a la
cepa velogénica del virus de la enfermedad de N e w c a s t l e a cualquier edad, las
vacunas inactivadas La Sota, de uso estandarizado en aves de corral, pueden
inducir inmunidad protectora durante más de seis meses. En avestruces de
engorde v a c u n a d a s , la fase virémica dura entre nueve y once días, y una vez
transcurrido este periodo (con un pico de inmunoglobulina G a los catorce días de
la infección) no queda en la carne ni en ningún otro tejido el menor indicio de la
presencia del virus o de la condición de ejemplar portador. Las pruebas de
inhibición de la hemoaglutinación presentan una sensibilidad y una especificidad
significativamente menores que los ensayos inmunoenzimáticos. El estudio
virológico directo de muestras cloacales y coanales de ejemplares afectados
clínicamente (de forma tanto natural como experimental) no permitió detectar la
presencia del virus de la enfermedad de N e w c a s t l e . Todas las cepas de influenza
aviar aisladas en avestruces han resultado no patogénicas para las aves de
corral, comprendidos los subtipos H5 y H7. Algunas cepas de este último subtipo
parecen relacionadas con brotes de mortalidad de pollitos de avestruz, de
carácter bastante localizado, sobrevenidos en épocas de mal tiempo y después
655
Rev. sci. tech. Off. int. Epiz., 19 (2)
de un estrecho c o n t a c t o c o n aves salvajes (anseriformes). La enfermedad de
Borna provoca un síndrome nervioso en los pollitos de avestruz, aunque hasta la
f e c h a sólo se ha c o m u n i c a d o su presencia en Israel. La encefalomielitis equina
(del Este o d e l Oeste) p r o v o c a u n a e n f e r m e d a d fatal e n a v e s t r u c e s y otras aves
c o r r e d o r a s , c o n t a s a s de mortalidad que oscilan entre menos de un 20% y más de
un 8 0 % en las bandadas afectadas. Estas e n f e r m e d a d e s están presentes en
A m é r i c a del N o r t e , Central y del Sur, donde se e n c u e n t r a el mosquito ornitofílico
que ejerce de v e c t o r asociado a la e n f e r m e d a d . La a p l i c a c i ó n de las v a c u n a s
equinas y h u m a n a s a las aves c o r r e d o r a s p a r e c e s e g u r a y eficaz. Por último,
t a m b i é n se han descrito en avestruces la e n f e r m e d a d de W e s s e l s b r o n , la bursitis
infecciosa (de tipo 2) y las i n f e c c i o n e s por adenovirus y Coronavirus, aunque no
está claro hasta qué punto tienen una incidencia significativa.
Teniendo en cuenta la escasez de datos sobre las e n f e r m e d a d e s del avestruz y el
h e c h o d e q u e m u c h a s d e las p r u e b a s a p l i c a d a s a las aves d e c o r r a l n o se h a n
validado para este singular grupo de aves, resulta muy aconsejable observar una
estricta cuarentena de treinta días antes del sacrificio, y utilizar además polluelos
y/o avestruces jóvenes a modo de centinelas para controlar las exportaciones de
ejemplares vivos y huevos fértiles.
Palabras clave
Aves corredoras - Avestruces - Enfermedad de Newcastle - Enfermedades aviares Fiebre hemorrágica de Crimea-Congo - Influenza aviar - Salmonella.
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