Definition
Nairobi sheep disease (NSD) is a noncontagious, tick-borne, viral
infection of sheep and goats characterized by hemorrhagic gastroenteritis and high
mortality.
Etiology
Nairobi sheep disease virus (NSDV) is transmitted primarily by the
brown tick, Rhipicephalus appendiculatus. The causative agent is an RNA-containing
virus having structural and chemical characteristics common within the Bunyaviridae viruses (16). However, it is antigenically independent of this group but is closely
related to the Ganjam virus of goats in India (7). Ganjam virus is antigenically related
to Dugbe virus isolated from cattle in west Africa. A new genus, Nairovirus, has
been proposed for these three viruses (19).
Host Range
Laboratory and domesticated animals other than sheep and goats are
resistant to infection with NSDV (17). Davies (5) was unable to isolate NSDV from blood or
tissues of a wide range of wild ruminants and rodents. However, it has been suggested (4)
that the African field rat (Arvicathus abysinicus nubilans) might be a reservoir
host.
Geographic Distribution
Nairobi sheep disease is usually confined to countries in east
Africa, where the principal vector, R. appendiculatus, is endemic. The disease has
been reported most frequently in Kenya in Kikuyu country between Nairobi and Mount Kenya
as well as in Uganda, Tanzania, and Somalia (1). A disease similar to NSD called Kisenyi
sheep disease has been described in the Republic of the Congo (3). Sera positive for NSDV
antibody were confirmed in an outbreak in haired sheep in Harar Province of Ethiopia.
Transmission
Nairobi sheep disease is not contagious and is only transmitted by
ticks. Transmission by contact does not occur. Experimentally, NSD can be transmitted by
the inoculation of infectious blood, serum, or organ suspensions into susceptible animals.
Large doses (50 cc) of virulent blood or serum given to sheep by mouth may also cause
infection.
The major vector of NSD is R. appendiculatus and is
generally thought to be the only species of tick in which transovarial transmission of NSD
is known to occur; however, there is firm evidence that a population of R. pulchellus in Somalia also transovarially transmits the virus. The African bont tick (Amblyomma
variegatum) is believed to have been responsible for one large outbreak of NSD in
Kenya (3). However, in a laboratory investigation, A. variegatum was found to be a
less efficient vector than R. appendiculatus (4). More recently in Kenya, a closer
correlation has been shown to exist between the presence of NSD antibody in sheep and
goats and infestations with R. appendiculatus than with A. variegatum (14).
Of eight species of ticks representing three genera (Amblyomma, Hyalomma,
and Rhipicephalus) collected in Kenya, NSDV was isolated only from R.
appendiculatus (5). Unfed adult ticks are infective for over 2 years. It has
previously been stated by Daubney and Hudson (3) that infected R. appendiculatus lose their infectivity when allowed to feed on immune sheep or on nonsusceptible animals;
however, this was later shown not to be the case (11).
Incubation Period
The incubation period in natural infections is 4 to 15 days.
Experimental inoculation of sheep and goats with virus results in a shorter incubation
period of 1 to 3 days (19).
Clinical Signs
Nairobi sheep disease is characterized by an acute hemorrhagic
gastroenteritis (17). Clinical signs of NSD begin with a temperature rise to 40 to 41° C
(104 to 106° F) and, during this stage, a prominent clinical depression develops followed
by a temperature decline and diarrhea. There is an abundant mucopurulent nasal discharge,
and breathing may become rapid and painful. Leukopenia is prominent during the period of
hyperthermia (18). Initially the feces are thin and watery but later they may contain
mucus and blood. In less acute cases the course of the disease is slower, and sheep become
anorexic, weak, and recumbent with signs of diarrhea. There may be abortions. In
hyperacute infections there is a sudden rise in body temperature that abruptly declines on
the third to the sixth day followed by collapse and death within a few hours.
Gross Lesions
The most obvious lesions are those associated with hemorrhagic
gastroenteritis. The abomasal mucosa is hyperemic and may be covered with petechial
hemorrhages. Intestinal lesions are most severe in the cecum and the anterior part of the
colon. Hemorrhages in the mucosa of the large intestine are numerous, and the intestinal
contents are blood stained.
There is nonspecific congestion and petechial and ecchymotic
hemorrhages in most organs and tissues.
Generalized hyperplasia of lymphoid tissue is a prominent lesion.
Lymph nodes are enlarged and edematous. The spleen may be several times its normal size
and engorged with blood.
In pregnant ewes, the genital tract may be very hyperemic, which
is indicative of inflammation, and fetal membranes may be swollen and edematous, and
contain hemorrhages. The aborted fetus has numerous hemorrhages in its tissues and organs.
Morbidity and Mortality
Early studies (17) revealed that sheep and goats resident in
endemic areas were generally immune, whereas severe outbreaks occurred in susceptible
animals moved into these region. Davies (5) in a 9-year study discovered that NSD
outbreaks were mainly associated with the trading of livestock in the vicinity of Kenya's
major cities. Sporadic outbreaks in nonendemic regions were usually preceded by excessive
amounts of rainfall and the appearance of the tick vector.
Prognosis in susceptible sheep and goats is poor, although mild
infection may occur. Mortality in Merino and Merino crossbreds is about 40 percent, but
mortality in Masai sheep is much higher.
Diagnosis
Field Diagnosis
An outbreak of NSD is nearly always associated with movement of
susceptible animals into an endemic area where R. appendiculatus is abundant. When
recently introduced small ruminants become ill with signs of severe enteritis and nasal
discharge within an NSD endemic area and sheep native to the area do not, it is a likely
assumption that NSD is the current problem. This is particularly true if the incidence of
illness in sheep is high, is low in goats, and is absent in cattle and other animals.
Susceptibility of goats may depend on breed (6).
Specimens for Laboratory
Heparinized blood is the best source of NSDV during the febrile
stage. During later stages of illness, when body temperature has declined or is normal and
the amount of virus in the blood stream is low or absent, spleen and mesenteric lymph
nodes are the best tissues for virus isolation (2,17). Also submit serum, preferably
paired specimens, for serology.
Laboratory Diagnosis
Laboratory confirmation is necessary for a definitive diagnosis.
Inoculation of cell culture with suspensions of infected organs or plasma and subsequent
staining of the cell culture by the direct (FAT) or indirect fluorescein conjugated
antibody test (IFAT) provide the most reliable means of identifying NSDV. The use of a
fluorescein conjugated antibody test allows detection virus in 24 to 48 hours after
inoculation of cell cultures and thus is not dependent on cytopathogenic effects in tissue
culture cells (10).
Intracerebral inoculation of suckling mice is an excellent method
of isolating NSDV. The brain material from infected mice can be used as a source of viral
antigen, and its identity can be determined by FAT or a complement fixation test (10).
Differential Diagnosis
The disease must be differentiated from heartwater, Rift Valley
fever, anthrax, some types of plant and heavy metal poisoning, peste des petits ruminants,
and coccidiosis.
Differentiation from other viral or rickettsial diseases is based
on geographic location of the outbreak, species of animal affected, cross-immunity
studies, serologic investigations, and viral isolation.
The following criteria may be of assistance in arriving at a
diagnosis:
1. Nairobi sheep disease
a. Nairobi sheep disease causes severe illness in sheep — an
affliction that is characterized by diarrhea, often hemorrhagic.
b. There is high mortality in Masai sheep, low mortality in Merino
or Merino crosses, low mortality in goats, and no mortality in other ruminants, including
wildlife.
c. R. appendiculatus ticks are abundant in the region.
d. Intracerebral inoculation of mice with blood or tissue
suspensions causes rodent death.
e. The Nairobi sheep disease virus can be isolated and propagated
in tissue culture.
f. The fluorescein antibody test and serum neutralization and
complement fixation tests will identify the causative agent.
2. Heartwater
a. Heartwater causes severe illness in sheep and is characterized
by CNS signs followed by death. Pulmonary edema and an abundance of fluid in the
pericardial sac and pleural cavities may be seen in the more prolonged cases.
Gastroenteritis is rare.
b. There is a high incidence of illness and mortality in exotic
breeds of sheep, goats, and cattle in contrast to a lower incidence and mortality in
indigenous breeds.
c. Amblyomma hebraeum or A. variegatum ticks are
abundant in the affected area.
d. The rickettsia may be passaged in mice, often without any
evidence of illness in the affected mice.
e. Cowdria ruminantium, a rickettsia, can be demonstrated
in endothelial cells of capillaries found in brain smears and endothelial cells of large
blood vessels stained with Giemsa.
f. The rickettsia cannot be isolated easily in tissue culture.
3. Rift Valley Fever (RVF)
a. In cattle, sheep, goats, and man, RVF is a very acute disease.
b. Rift Valley fever is characterized by a rapid course of
infection, severe depression, diarrhea, massive liver necrosis, and widespread abortion.
c. The illness appears after periods of heavy rainfall when there
is an abundance of mosquitoes, the arthropod vectors of the virus.
d. Ticks are not vectors of RVF and may be absent from the area of
infection.
e. Mice, tissue cultures, and embryonated hen's eggs can be
infected, and the isolated virus can be identified by serologic and immunologic methods.
4. Anthrax
a. Many species of mammals may be affected.
b. The most prominent lesions are multiple hemorrhages,
hemorrhagic enteritis, and prominent swelling of the spleen with failure of blood to clot.
c. Blood or tissue smears stained with Giemsa reveal numerous
encapsulated rod-shaped bacteria arranged in chains.
d. Inoculated laboratory animals die, have numerous hemorrhages,
and have an abundance of encapsulated bacteria in their tissues.
e. Bacillus anthracis can be grown and identified on
laboratory media.
5. Arsenic poisoning (from dips)
a. Many species of animals may be affected.
b. Signs: Profuse watery diarrhea, sometimes blood tinged, severe
colic, dehydration, depression, weakness, and CNS signs; high fatality rates.
c. Lesions: Edema and necrosis of gastric and intestinal
epithelium and subepithelium. Diffuse degeneration of liver and other abdominal viscera.
d. Arsenic detected in tissues.
6. Coccidiosis
a Signs: Diarrhea (sometimes bloody), dehydration, fever,
anorexia, and anemia.
The disease can be fatal — especially in lambs.
b. Lesions: Edema, inflammation, and mucosal hemorrhage
predominantly in the ileum, cecum, and upper colon.
c. Thick white patches of oocysts may develop in small intestine.
These oocysts can be demonstrated microscopically.
Treatment
There is no specific treatment for NSD. Supportive treatment,
protection from climatic adversities, and availability of good quality feed may reduce the
mortality rate.
Vaccination
Recovery from NSD leads to lifelong immunity. Because sheep and
goats in endemic areas are constantly exposed to ticks carrying virus, they maintain good
immunity and have no clinical signs of illness. It has been suggested (14) that lambs and
kids are protected by colosteral antibody until they can acquire an active immunity
through infection.
The Nairobi sheep disease virus can be propagated in cell culture
(goat testes, goat kidneys, and hamster kidneys). When cell culture virus is attenuated,
it is capable of protecting sheep and goats from NSD (9). The Entebbe strain of NSDV
passaged 140 to 150 times through mouse brain is also used as vaccine. However, because of
variability of breed responses to modified live virus vaccines and their adverse effects,
they are generally not recommended.
Control and Eradication
Susceptible sheep and goats must be protected from the vector by
weekly acaricide dipping and spraying. Movement of animals into endemic areas must be
controlled unless sheep and goats are naturally immune or have been vaccinated.
Because the infection is not transmitted by contact, there is
little need for strict quarantine procedures. Dead sheep should be buried or incinerated.
Livestock on the premises should be dipped or sprayed with acaricides to reduce the
existing tick population.
Public Health
Antibodies against NSDV have been detected in human blood serum,
but it is not known if these antibodies are the result of NSDV infection or have been
caused by a yet unidentified agent. An apparently naturally acquired clinical case was
reported from Uganda in which a young man from whom virus was isolated experienced
transient clinical signs (15). However no serological conversion has been demonstrated in
investigators working with the virus (6).
GUIDE TO THE LITERATURE
1. BUGYAKI, L. 1957. "Kisenyi sheep disease"—A
viral infection transmitted by arthropoda (summary). Bull. Epiz. Dis. Afr., 5:467.
2. DAUBNEY, R., and HUDSON, J.R. 1934. Nairobi sheep disease.
Parasit., 23:507.
3. DAUBNEY, R., and HUDSON, J.R. 1934. Nairobi sheep disease:
Natural and experimental transmission by ticks other than Rhipicephalus appendiculatus.
Parasit., 26:496.
4. DAVIES, F.G. 1978. A survey of Nairobi sheep disease antibody
in sheep and goats, wild ruminants and rodents within Kenya. J. Hyg. Camb., 81:251.
5. DAVIES, F.G. 1978. Nairobi sheep disease Kenya. The isolation
of virus from sheep and goats, ticks, and possible maintenance hosts. J. Hyg. Camb.,
81:259.
6. DAVIES, F.G. 1989. Nairobi Sheep Disease. In The Arboviruses. Epidemiology
and Ecology, Monath. ed. Vol. lll. Chap 33. pp. 191.
7. DAVIES, F. G., CASALS, J., JESSET, D.M., and OCHIENG, P. 1978.
The serological relationships of Nairobi sheep disease virus. J. Comp. Path., 88:519.
8. DAVIES, F. G., JESSET, D.M. and OTIENA, S. 1976. The
antibody
response of sheep following infection with Nairobi sheep disease virus. J. Comp. Path.,
86:497.
9. DAVIES, F. G., MUNGAI, J. N., and SHAW, T. 1974. A Nairobi
sheep disease vaccine. Vet. Rec., 94:128.
10. DAVIES, F.G., MUNGAI, J.W., and TAYLOR, M. 1977. The
laboratory diagnosis of Nairobi Sheep Disease. Trop. Anim. Hlth. Prod., 9:75.
11. DAVIES, F.G., and MWAKIMA, F. (1982). Qualitative studies of
the transmission of Nairobi sheep disease virus by Rhipicephalus appendiculatus. J.
Comp. Path., 92:15.
12. ELDELSTEN, R.M. 1975. The distribution and prevalence of
Nairobi sheep disease and other tick-borne infections of sheep and goats in northern
Somalia. Trop. Anim. Hlth. Prod ,7:29.
13. HENNING, M.W. 1956. Animal Diseases in South Africa. 3d
ed., Johannesburg. Republic of South Africa:Central News Agency, Ltd., p. 1122.
14. HOWARTH, J.A., and TERPSTRA, C. 1965. The propagation of
Nairobi sheep virus in goat testes, goat kidneys and hamster kidneys. J. Comp. Path.,
75:437.
15. KIRYA, G.B., TUKEI, P.M., LULE, M., and MUJOMBA, E. Nairobi
Sheep Disease in man. East Africa Virus Research Institute, Rep., 284.
16. MELNICK, J.L 1973. Classification and Nomenclature of Viruses:
In Ultrastructure of Animal Viruses and Bacteriophages. An Atlas. A.J. Dalton, and
F. Haguenau, eds). Chap. 5:1.
17. MONTGOMERY, R.E. 1917. On a tick-borne gastroenteritis of
sheep and goats occurring in British East Africa. J. Comp. Path., 30:28.
18. MUGERA, G.M., and CHEMA, S. 1967. Nairobi sheep disease: A
study of its pathogenesis in sheep, goats and suckling mice. Bull. Epiz. Dis. Afr.,
15:337.
19. PORTERFIELD, J.S., and DELLA-PORTA, A.J. 1981. Bunyaviridae:
Infections and Diagnosis. In Comparative Diagnosis of Viral Diseases IV. New
York:Acad. Press.. Chap 10. pp. 479.
C.M. Groocock, D.V.M., Ph.D., USDA-APHIS-IS, Vienna, Austria
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