D6921.PDF

Rev. sci. tech. Off. int. Epiz., 1983, 2 (2), 311-334.
Respiratory diseases
induced in small ruminants
by viruses and mycoplasma*
W.B. MARTIN**
Summary : In this paper the primary virus and mycoplasma invaders of
the respiratory tract of sheep and goats are considered, including those
which do not produce clinically apparent disease.
Among acute viral infections, the widespread occurrence of parain-
fluenza 3 virus and the established findings that it allows other more
sinister organisms to invade the lower respiratory tract would indicate
that it is a virus of considerable economic importance. Little is known
about the significance of infections caused by adenoviruses and reovi-
ruses. Peste des petits ruminants (PPR), caused by a rinderpest-like
virus, is of considerable economic importance in West Africa. The her-
pesvirus of infectious bovine rhinotracheitis (IBR) is capable of infect-
ing goats and sheep. Infections caused by pox viruses and the border
disease virus are not primarily respiratory diseases.
Sheep pulmonary adenomatosis, maedi-visna and retrovirus infec-
tion in goats are the main virus infections associated with progressive
pneumonias of small ruminants.
At present six identified species of mycoplasma have been recovered
from the respiratory tract of sheep and goats, not all of which have
been associated with disease. M. ovipneumoniae is considered to be res-
ponsible for chronic respiratory infection which progresses slowly; Pas-
teurella haemolytica is a frequently associated pathogen. Contagious
caprine pleuropneumonia (CCPP) is a serious and economically impor-
tant disease, affecting exclusively goats. Three mycoplasmas have been
considered as its aetiological agent : M. mycoides subsp. capri, M.
mycoides subsp. mycoides, and the unclassified strain F 38.
INTRODUCTION
Respiratory problems are common in all species and many agents have
now been recovered from the respiratory tracts of animals. Though one agent
* Report presented at the 50th General Session of the O.I.E., Paris, 24-29 May 1982
(Technical Item III).
** Moredun Research Institute, 408 Gilmerton Road, Edinburgh, EH17 7JH, U.K.

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may be the primary invader, most respiratory infections are complicated by
the presence of secondary or opportunist organisms. Indeed these secondary
organisms may be those which cause the most severe lesions or result in a
fatal outcome.
In this paper the primary virus and mycoplasma invaders of the respira-
tory tract of sheep and goats are considered. Some may be capable of infect-
ing without producing clinically apparent disease. The term « disease » has
been loosely interpreted therefore and information on agents has been includ-
ed even if their pathogenicity for the respiratory tract is limited.
I. — ACUTE VIRAL INFECTIONS
A. PARAINFLUENZA 3
There is no doubt that infection with the virus of parainfluenza type 3
(PI 3) is one of the most prevalent in the world.
The first isolation of this Paramyxovirus from sheep was made by Hore
(1966). Since then evidence of infection in sheep, by the isolation of virus or
the presence of antibodies, has been recorded in many countries and it is pro-
bable that the virus is present in most, if not all countries.
The percentage of sheep showing antibodies varies according to each sur-
vey and the country in which the survey has been carried out. In general a
high percentage of sheep show antibodies to this virus, for example over 70%
of sheep sera contain antibody in the U.S.A. (Fischman, 1967), France (Faye,
Charton and Le Layec, 1967), Turkey (Erhan and Martin, 1969), Australia
(St. George, 1971) and South Africa (Erasmus, Boshoff and Pieterse, 1967).
Clearly infection with PI 3 is both frequent and widespread in sheep.
1. Clinical disease.
The clinical signs of infection with PI 3 probably go undetected in the
field in most cases though signs of a mild infection, mainly of the upper res-
piratory tract, may occasionally be seen (Hore et al., 1968; Belak and Palfi,
1974a). Clinical signs following experimental infection are variable but com-
bined intratracheal and intranasal inoculation can produce transient pyrexia,
nasal discharge, coughing and other respiratory signs (Hore and Stevenson,
1969).
The relatively mild respiratory disease produced by experimental infection
of specific pathogen free (SPF) lambs with PI 3 is markedly altered when
Pasteurella haemolytica of biotype A is given by aerosol, about seven days
after the initial viral infection (Sharp et al., 1978; Davies et al., 1977). Com-
bined infections of this type will result in a high percentage of lambs develop-
ing moderate to severe pneumonic lesions in which high counts of pasteu-

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relia can be found. Pasteurella haemolytica without a previous PI 3 infection
does not generally produce a high percentage of severe disease when given in
an aerosol.
It seems probable that infection in the field situation with PI 3 is one way
in which biotype A Pasteurella haemolytica can infect the lungs of sheep to
produce outbreaks of respiratory disease (Gilmour, 1978).
Immunity to PI 3 virus is not absolute so that nasal shedding of virus may
follow infection even in sheep with moderate levels of circulating antibodies.
2. Pathology.
The apical lobes are most frequently affected. Usually small red, linear
areas of consolidation are present. On cross-section the consolidated lesions
are distributed extensively and follow smaller bronchi and bronchioles.
Pseudo-epithelialization of alveoli, hyperplasia of bronchiolar epithelium,
infiltration of alveolar septa and acidophilic cytoplasmic inclusions in bron-
chiole and alveolar epithelial cells are evident microscopically (Hore and Ste-
venson, 1969).
3. Diagnosis.
Serum neutralization (SN), haemagglutination-inhibition (HI) and ELISA
tests are used to determine evidence of previous infection. Generally a four-
fold rise in HI titre is taken as indicating recent infection but such a rise does
not always occur despite evidence of infection confirmed by recovery of virus
in nasal secretions. Virus can only be isolated from lungs for up to 7-10 days
following infection.
4. Immunity and control.
PI 3 infection is usually considered to be relatively mild and unnecessary
to control. However the complications which may follow invasion by other
organisms has led to an increasing interest in PI 3 vaccines. Live attenuated
vaccines and subunit vaccines are likely to become available for sheep.
Experimentally live PI 3 virus administered intranasally will stimulate the
production of specific IgA antibody into nasal secretions (Smith et al., 1975).
5. Economic significance.
The widespread occurrence of this virus and the established findings that
it allows other more sinister organisms to invade the lower respiratory tract
would indicate that it is a virus of considerable economic importance.
B. OTHER PARAMYXOVIRUSES AND ORTHOMYXOVIRUSES
There is no confirmed evidence that either of the Paramyxoviruses,
parainfluenza 1 and 2, is an important pathogen of sheep. Because of the

heterologous reactions which may occur between members of this group
some doubt exists as to the value which can be placed on surveys which sug-
gest that antibody to these viruses is present in sheep.
Sheep do not appear to be important reservoirs of influenza virus, though
evidence of infection has been reported from Hungary (Romvary et al.,
1962). Experimental infection of sheep with influenza A did not result in cli-
nical illness (McQueen and Davenport, 1963).
C. ADENOVIRUS
All serotypes of mammalian adenovirus share a common group-specific
antigen which can be detected by complement-fixation (CF) and gel-diffusion
(GD) tests. These tests have been used to show that adenovirus infection
occurs in sheep. The first isolation of adenovirus from sheep was reported in
1969 by McFerran et al.
Surveys carried out in a number of countries have shown a variable per-
centage of sheep with antibodies : Iran : 14% (Ashfar, 1969), Greece : 31%
(Pashaleri-Papadopoulou, 1968), but less than 1% in Britain (Darbyshire and
Pereira, 1964) and the Republic of Ireland (Timoney, 1971).
Five serotypes of sheep adenovirus which can be distinguished by SN
tests, have been isolated, though several isolates are as yet untyped. A survey
in Scotland has shown the following percentage of sheep with antibodies to
4 types : type 1 : 20.8%, type 2 : 40.4%, type 3 : 67.8% and type 4 : 71.1%
(Sharp, 1977). The high percentage of infection found in this survey contrasts
with the low prevalence in the earlier British surveys. The use of different test
methods (viz. GD and SN) is probably the major reason for the differing
results.
1. Clinical disease.
Little is known about adenovirus infections in sheep. Adenoviruses have
been isolated from apparently healthy sheep (Bauer et al, 1975) and from
lambs with respiratory signs (Sharp, 1977). It is not clear what natural infec-
tion with adenovirus may produce and experimental infection has generally
not resulted in notable clinical disease, though the virus may replicate and
produce lesions. In experiments described by Sharp et al. (1976) virus was
recovered following infection (p.i.) from nasal swabs (days 1-8 p.i.) and rec-
tal swabs (days 3-9 p.i.). Even when experimental adenovirus infection is fol-
lowed by an aerosol of Pasteurella haemolytica biotype A, no serious disease
results (Sharp, 1977; Davies et al., 1981).
2. Pathology.
Ovine adenovirus type 4 has been shown to be capable of causing pulmo-
nary oedema and mild hepatic lesions (Sharp et al., 1976; Rushton and
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Sharp, 1977). Histology of the lungs showed accumulation of fluid in peri-
vascular and peribronchiole areas. In the liver focal necrosis was evident and
basophilic inclusion bodies were present in hepatocytes and lymphatic endo-
thelial cells (Rushton and Sharp, 1977).
Virus has been recovered up to 14 days p.i. from tissues in the respiratory
and enteric tracts of lambs infected experimentally, which developed areas of
atelectasis and in some consolidation of the lungs. Microscopically there was
proliferative bronchiolitis and bronchopneumonia with cytomegaly and
karyomegaly of epithelial cells. In some nuclei basophilic inclusions were
seen containing crystalline arrays of virus particles (Davies et al., 1981).
3. Diagnosis.
Serum antibody can be determined by SN tests and some strains of virus
will agglutinate red blood cells of certain species. Rising titres are indicative
of recent infection but the isolation of virus is confirmatory of infection.
4. Immunity and control.
Colostral antibody levels decline progressively and lambs are free from
such antibody after 3-5 months. New infections can then result in active
immunity and at the same time a concomitant increase in pneumonia has
been noted in the lambs in such flocks suggesting rapid spread of infection
through a susceptible population (Davies et al., 1980).
Vaccination of pregnant ewes has been suggested to provide passive
immunity for lambs during the first few weeks of life (Palfi et al., 1980). Suc-
cessful vaccination of lambs using U.V. inactivated virus adsorbed onto alu-
minium hydroxide has been reported but the immune response was signifi-
cantly reduced by the presence of colostral antibody (Palfi et al., 1980).
5. Economic significance.
At present the importance of adenovirus infections in sheep is not known.
The work of Davies et al. (1980) suggests that adenovirus causes varying
degrees of pneumonia and could therefore result in economically significant
loss of productivity.
6. Infection of sheep with bovine adenovirus.
The isolation of a type 2 bovine adenovirus from sheep has been reported
(Belak and Palfi, 1974b). This virus was isolated from lambs with enteritis
and pneumonia, some of which died. Inoculation of the virus into lambs pro-
duced clinical respiratory disease and enteritis, similar to the disease seen in
the original outbreak (Belak et al., 1975).
7. Adenovirus infections of goats.
Two serologically different adenoviruses have been isolated from goats
with « peste des petits ruminants » in Nigeria. These isolates are not related