Nairobi sheep disease
- Host Animals
- Hosts/Species Affected
- Systems Affected
- Distribution Table
- List of Symptoms/Signs
- Disease Course
- Impact: Economic
- Zoonoses and Food Safety
- Disease Treatment
- Prevention and Control
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Nairobi sheep disease
International Common Names
- English: Kisanyi goat disease; nairobi sheep disease, kisanyi goat disease- exotic
OverviewTop of page
Nairobi sheep disease (NSD) was identified as a problem in sheep and goats in Kenya in 1910 (Annual Report Agricultural Department, Kenya, 1913). The disease was characterized by the sudden onset of pyrexia with prostration, followed by a profuse foetid diarrhoea. NSD has a high mortality rate in susceptible sheep and goats. An important study was published in 1917 by R.E. Montgomery, who was working at the Veterinary Research Laboratory, Kabete, in Kenya, which showed that NSD was caused by a tick-transmitted virus (Montgomery, 1917). This was a classical early work, which demonstrated the trans-ovarial and trans-stadial transmission of the virus in the Ixodid tick, Rhipicephalus appendiculatus. He also showed that the pathogenicity of the virus appeared to be restricted to sheep and goats, and other domestic animals were refractory to infection with NSD.
The virus is a member of the genus Nairovirus of the family Bunyaviridae. Other members of the genus include Ganjam, Dugbe, Congo-Crimean haemorrhagic fever (CCHF) and Hazara viruses. These are transmitted by Ixodid ticks. Davies et al. (1978) observed that NSD appeared to be serologically identical with Ganjam virus isolated in several states in India, and subsequently in Sri Lanka. Further genetic and serological analyses have demonstrated that Ganjam virus is an Asian variant of NSD virus (Marczinke and Nichol, 2002; Yadav et al., 2011; Kuhn et al., 2016). Ganjam virus is transmitted by Haemaphysalis intermedia and probably other tick species, and has caused disease in man and also produces an NSD-like syndrome in sheep (Dandawate et al., 1969).
The virus is not readily communicable to man (Davies, 1988), but human infections have been previously documented. Human sera has been shown to contain antibodies in India (Dandawate et al., 1969, Joshi et al., 1998), Uganda (Weinbren, 1959), Kenya (Morrill et al., 1991), and Sri Lanka (Perera et al., 1996). Cases of laboratory-acquired infections have been reported (Banerjee et al., 1979; Rao et al., 1981).
The range of NSD may be greater than that already described. It can persist in a state of enzootic stability with no manifestation of clinical disease problems until susceptible animals are introduced. NSD occurs in those eco-climatic zones where continuous life cycles of the tick are possible, and not in the drier zones, where only single generations of the tick can occur. The range of the principal tick vector R. appendiculatus includes parts of the southern Sudan, Botswana, Mozambique, Zambia and South Africa. In many of these places, Rhipicephalus zambeziensis (a closely related species) predominates, and R. appendiculatus is less common in these drier areas. In addition, Haemaphysalis longicornis has recently been identified as a vector for NSD in China (Gong et al., 2015). This tick is present throughout the world, including eastern Asia, the USA, Australia, and New Zealand, and recent modelling work predicts its range could be even more extensive (Zhao et al., 2020).
The disease causes periodic epizootics in most of the affected countries, which result in 50-75% losses in the flocks of the pastoralists involved. This has considerable socio-economic impact, for many groups rely almost entirely on the sale of small ruminants for their income. The epizootics appear to be triggered by climatic changes, which alter the microclimate in favour of increases in the tick vector populations.
This disease is on the list of diseases notifiable to the World Organisation for Animal Health (OIE). The distribution section contains data from OIE's WAHID database on disease occurrence. For further information from OIE, see www.oie.int.
Host AnimalsTop of page
Hosts/Species AffectedTop of page
The principal hosts for NSD are sheep and goats, and goats may be slightly less susceptible than sheep. There is considerable variation in the susceptibility of different breeds and strains of sheep and goats. The East African hair sheep breeds are highly susceptible to NSD virus and 75-95% mortality has been encountered in the field and after laboratory infections. The imported breeds of wool sheep, such as the Corriedale, have a lower mortality rate of 30-60% in laboratory studies. Terpstra (1969) observed an 88% mortality rate in goats in West Nile Province of Uganda, but in Kenya the Masai-type goats have a 10-40% mortality. All age groups remain highly susceptible to NSD. Nomadic pastoralists with their large flocks of small ruminants are at greatest risk from epizootic NSD. Settled agricultural and livestock farming in enzootic areas generally allows small ruminants to develop immunity at an early age and NSD presents no disease problems.
Weinbren (1959) isolated NSD virus from blue duikers at the Entebbe zoo. No disease syndrome has ever been identified elsewhere in wild ruminant species and these are remarkably free from antibody to NSD virus. This may be due to the origin of the samples tested, which were collected from the drier zones where NSD is not enzootic (Davies, 1978a, 1978b).
Cattle are not susceptible to NSD and neither are horses, donkeys, pigs, poultry, and dogs (Montgomery, 1917). Suckling mice are susceptible to NSD when inoculated by the intra-cerebral (ic) and intra-peritoneal (ip) routes, and older mice are susceptible to intra-cerebral inoculations. Rabbits, guinea pigs, hamsters and rats were refractory to intra-peritoneal and intra-cerebral inoculations. The wild rat Arvicanthus niloticus developed a viraemia of 105 mouse LD50 after intra-peritoneal inoculation.
There have been many reports of NSD and Ganjam infections in man (Weinbren, 1959; Tukei, personal communication). Reports of NSD have been entirely from Uganda and were reported at the East African Virus Research Institute at Entebbe. Some of the laboratory staff had antibody to NSD virus on mouse serum-virus neutralization tests. These tests are notoriously unreliable. No human NSD virus infections have been identified in Kenya, nor have any laboratory infections occurred. Staff who worked with NSD for more than 20 years and handled sick and dead sheep, NSD-infected mouse tissues and cultures, all remained sero-negative to the virus. Ganjam infections in man have been acquired in the laboratory (Banerjee et al., 1979; Rao et al., 1981). Human infections show a febrile reaction with headaches, shivering and muscle pains. These usually disappear after 3 days.
Systems AffectedTop of page
digestive diseases of small ruminants
multisystemic diseases of small ruminants
reproductive diseases of small ruminants
respiratory diseases of small ruminants
DistributionTop of page
The disease has been found to coincide with the distribution of R. appendiculatus throughout Kenya, with virus and antibody occurring throughout the highland areas, the Lake Victoria basin and the coastal zone (Davies, 1978 a, 1978b). The disease is found wherever animal movements occur from the non-endemic to the endemic areas. These are typically when trade movement occurs from the semi-arid zones to the centres of population such as Nairobi and Mombasa. Wherever small ruminants are held outside the cities for any length of time, high mortality may follow. Sheep and goats moved from semi-arid areas into the Taita Hills of Kenya to feed troops during the First World War suffered high mortality from NSD. Similar disease problems have been encountered in Uganda with movements of small stock to Entebbe or to experimental farm units, and in Rwanda when they are moved to the shore of Lake Kivu, from the hill country.
The disease was reported clinically as early as 1931-33 in Entebbe and also in 1940. Virus was first isolated in Uganda from two blue duikers (Cephalophus caerulis) at the Entebbe zoo in 1957 (East African Virus Research Institute Reports, 1958) and subsequently encountered as a disease in sheep and goats in Entebbe in 1955 (Weinbren et al., 1958) and West Nile Province in 1963 (Terpstra, 1969), when exotic sheep were being introduced to improve production. Subsequently, NSD or antibody to the virus was found throughout most of the country apart from the arid and semi-arid zones to the north and north-east (Terpstra, 1969). The distribution was closely related to that of R. appendiculatus.
The disease was first identified in Somalia in 1938 by Pavalglia, in imported Karakul sheep (quoted by Pellegrini, 1950). Pellegrini (1950) made a study of the transmission of NSD in Somalia in 1950 and suggested that Rhipicephalus pulchellus was the likeliest vector in the Horn of Africa. It is by far the most common tick in this part of the Horn of Africa (Pegrum, 1976). Edelesten (1975) described an outbreak of NSD in the north of Somalia and also in the Ogaden of Ethiopia. All these workers identified a highly fatal clinical disease in sheep and goats, which was attributed to the virus. The Kenyan race of this tick was capable of transmitting NSD, but was shown to be an inefficient vector compared with R. appendiculatus.
Bugyaki (1955) has presented evidence of a tick-borne virus disease like NSD near Kisenyi, along the shores of Lake Kivu in Rwanda. R. appendiculatus was shown to be the vector and the disease was clinically the same. The disease has been reported from Tanzania and antibody to the virus has been found in sheep and goats throughout north Tanzania (Jesset, 1978). Virus was isolated from sick sheep in north Tanzania in 1977. The distribution of antibody to NSD in Tanzania is closely related to that of the tick vector, R. appendiculatus.
There is no evidence for NSD occurring as a disease in the south of Africa. Only very few sera with low titres of antibody have been found in limited serological surveys in Zambia and Botswana. Some 450 sera were examined from Botswana and 300 from Zambia. These were considered likely to be due to cross relationships with other Nairoviruses such as Crimean-Congo haemorrhagic fever. No clinical disease syndrome that might be NSD has ever been identified south of Tanzania. It is unlikely that the Veterinary Services in countries such as Zambia, Zimbabwe, Malawi, Mozambique, Botswana and South Africa would have failed to identify the presence of such a highly pathogenic virus. Ganjam virus was first isolated on the Asian continent in 1954 from H. intermedia in India (Dandawate and Shah, 1969) and Sri Lanka in 1996 (Perera et al., 1996). Most recently in 2013, NSD virus has been isolated from H. longicornis in China (Gong et al., 2015).
A systematic review completed by Krasteva et al. (2020) compiled and georeferenced all known occurrences of NSD and Ganjam virus in the literature (see: https://www.frontiersin.org/articles/10.3389/fvets.2020.00419/full#supplementary-material). These occurrences have also been mapped (see pictures) to show spread of the disease over time from the African continent to parts of Asia.
For current information on disease incidence, see OIE's World Animal Health Information System (OIE-WAHIS).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 10 Jan 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Algeria||Absent, No presence record(s)|
|Benin||Absent, No presence record(s)|
|Burundi||Absent, No presence record(s)|
|Cabo Verde||Absent, No presence record(s)|
|Cameroon||Absent, No presence record(s)|
|Central African Republic||Absent, No presence record(s)|
|Djibouti||Absent, No presence record(s)|
|Egypt||Absent, No presence record(s)|
|Eswatini||Absent, No presence record(s)|
|Ethiopia||Absent, No presence record(s)|
|Kenya||Absent, No presence record(s)||2003|
|Lesotho||Absent, No presence record(s)|
|Libya||Absent, No presence record(s)|
|Madagascar||Absent, No presence record(s)|
|Mauritius||Absent, No presence record(s)|
|Morocco||Absent, No presence record(s)|
|Mozambique||Absent, No presence record(s)|
|Nigeria||Absent, No presence record(s)|
|Réunion||Absent, No presence record(s)|
|São Tomé and Príncipe||Absent, No presence record(s)|
|South Africa||Absent, No presence record(s)|
|Sudan||Absent, No presence record(s)|
|Tunisia||Absent, No presence record(s)|
|Zambia||Absent, No presence record(s)|
|Zimbabwe||Absent, No presence record(s)|
|Armenia||Absent, No presence record(s)|
|Azerbaijan||Absent, No presence record(s)|
|Bahrain||Absent, No presence record(s)|
|Bangladesh||Absent, No presence record(s)|
|Bhutan||Absent, No presence record(s)|
|Brunei||Absent, No presence record(s)|
|China||Absent, No presence record(s)|
|Georgia||Absent, No presence record(s)|
|India||Absent, No presence record(s)|
|Indonesia||Absent, No presence record(s)|
|Iran||Absent, No presence record(s)|
|Iraq||Absent, No presence record(s)|
|Israel||Absent, No presence record(s)|
|Japan||Absent, No presence record(s)|
|Jordan||Absent, No presence record(s)|
|Kazakhstan||Absent, No presence record(s)|
|Kuwait||Absent, No presence record(s)|
|Kyrgyzstan||Absent, No presence record(s)|
|Laos||Absent, No presence record(s)|
|Lebanon||Absent, No presence record(s)|
|Malaysia||Absent, No presence record(s)|
|-Peninsular Malaysia||Absent, No presence record(s)|
|-Sabah||Absent, No presence record(s)|
|-Sarawak||Absent, No presence record(s)|
|Myanmar||Absent, No presence record(s)|
|North Korea||Absent, No presence record(s)|
|Oman||Absent, No presence record(s)|
|Pakistan||Absent, No presence record(s)|
|Philippines||Absent, No presence record(s)|
|Singapore||Absent, No presence record(s)|
|South Korea||Absent, No presence record(s)|
|Sri Lanka||Absent, No presence record(s)|
|Syria||Absent, No presence record(s)|
|Taiwan||Absent, No presence record(s)|
|Tajikistan||Absent, No presence record(s)|
|Turkmenistan||Absent, No presence record(s)|
|United Arab Emirates||Absent, No presence record(s)|
|Uzbekistan||Absent, No presence record(s)|
|Vietnam||Absent, No presence record(s)|
|Albania||Absent, No presence record(s)|
|Andorra||Absent, No presence record(s)|
|Belarus||Absent, No presence record(s)|
|Belgium||Absent, No presence record(s)|
|Bosnia and Herzegovina||Absent, No presence record(s)|
|Bulgaria||Absent, No presence record(s)|
|Croatia||Absent, No presence record(s)|
|Cyprus||Absent, No presence record(s)|
|Czechia||Absent, No presence record(s)|
|Denmark||Absent, No presence record(s)|
|Estonia||Absent, No presence record(s)|
|Finland||Absent, No presence record(s)|
|France||Absent, No presence record(s)|
|Germany||Absent, No presence record(s)|
|Greece||Absent, No presence record(s)|
|Hungary||Absent, No presence record(s)|
|Iceland||Absent, No presence record(s)|
|Ireland||Absent, No presence record(s)|
|Isle of Man||Absent, No presence record(s)|
|Jersey||Absent, No presence record(s)|
|Latvia||Absent, No presence record(s)|
|Liechtenstein||Absent, No presence record(s)|
|Lithuania||Absent, No presence record(s)|
|Luxembourg||Absent, No presence record(s)|
|Malta||Absent, No presence record(s)|
|Moldova||Absent, No presence record(s)|
|Montenegro||Absent, No presence record(s)|
|Netherlands||Absent, No presence record(s)|
|North Macedonia||Absent, No presence record(s)|
|Norway||Absent, No presence record(s)|
|Poland||Absent, No presence record(s)|
|Portugal||Absent, No presence record(s)|
|Romania||Absent, No presence record(s)|
|Russia||Absent, No presence record(s)|
|Serbia and Montenegro||Absent, No presence record(s)|
|Slovakia||Absent, No presence record(s)|
|Slovenia||Absent, No presence record(s)|
|Spain||Absent, No presence record(s)|
|Sweden||Absent, No presence record(s)|
|Switzerland||Absent, No presence record(s)|
|Ukraine||Absent, No presence record(s)|
|United Kingdom||Absent, No presence record(s)|
|-Northern Ireland||Absent, No presence record(s)|
|Barbados||Absent, No presence record(s)|
|Belize||Absent, No presence record(s)|
|Bermuda||Absent, No presence record(s)|
|British Virgin Islands||Absent, No presence record(s)|
|Canada||Absent, No presence record(s)|
|Cayman Islands||Absent, No presence record(s)|
|Costa Rica||Absent, No presence record(s)|
|Cuba||Absent, No presence record(s)|
|Curaçao||Absent, No presence record(s)|
|Dominica||Absent, No presence record(s)|
|Dominican Republic||Absent, No presence record(s)|
|El Salvador||Absent, No presence record(s)|
|Greenland||Absent, No presence record(s)|
|Guatemala||Absent, No presence record(s)|
|Haiti||Absent, No presence record(s)|
|Honduras||Absent, No presence record(s)|
|Mexico||Absent, No presence record(s)|
|Nicaragua||Absent, No presence record(s)|
|Panama||Absent, No presence record(s)|
|Saint Kitts and Nevis||Absent, No presence record(s)|
|Saint Vincent and the Grenadines||Absent, No presence record(s)|
|Trinidad and Tobago||Absent, No presence record(s)|
|United States||Absent, No presence record(s)|
|Australia||Absent, No presence record(s)|
|French Polynesia||Absent, No presence record(s)|
|New Caledonia||Absent, No presence record(s)|
|New Zealand||Absent, No presence record(s)|
|Samoa||Absent, No presence record(s)|
|Vanuatu||Absent, No presence record(s)|
|Argentina||Absent, No presence record(s)|
|Bolivia||Absent, No presence record(s)|
|Brazil||Absent, No presence record(s)|
|Chile||Absent, No presence record(s)|
|Colombia||Absent, No presence record(s)|
|Ecuador||Absent, No presence record(s)|
|Falkland Islands||Absent, No presence record(s)|
|French Guiana||Absent, No presence record(s)|
|Guyana||Absent, No presence record(s)|
|Paraguay||Absent, No presence record(s)|
|Peru||Absent, No presence record(s)|
|Uruguay||Absent, No presence record(s)|
|Venezuela||Absent, No presence record(s)|
PathologyTop of page
The first laboratory evidence of NSD infection is a markedly depressed total white-cell-count to 1-2 million per cubic millimetre. Animals which die at the early febrile stage of the disease show no signs that might be identifiable as characteristic of NSD. There will be a congestion of the carcass with lymphadenitis; usually the pre-scapular lymph node on one side will be notably enlarged and oedematous, with subcapsular haemorrhages. There will be petechial and ecchymotic haemorrhages, particularly on the serosal surfaces and epicardium and throughout the carcass.
Later in the course of the disease, when deaths follow the onset of diarrhoea, there will be catarrhal mucoid enteritis to a severe haemorrhagic form with extensive ulceration in the folds of the abomasum, duodenum, ileocaecal valve, caecum and colon, often with zebra striping in the rectal folds. Oedema of the lungs with froth in the trachea and bronchi is found in many cases. Extensive petechial and ecchymotic haemorrhages occur, usually in the subcapsular or serosal areas of the parenchymatous organs and lymph nodes, which are enlarged and hyperaemic. There will be haemorrhages on the epicardium with some pericardial fluid. The kidney may show some subcapsular haemorrhages. The urogenital tract may show infection and haemorrhage after abortions, with some bladder haemorrhages. The spleen usually shows some subcapsular haemorrhage and may or may not be enlarged.
The pathology of NSD has been described by Daubney and Hudson (1931), Weinbren et al. (1958), and Mugera and Chema (1967). The lesions in most of the tissues and organs are those associated with the haemorrhage, together with some inflammatory changes with cellular infiltration. The spleen and lymph nodes usually show some hyperplasia of the germinal centres. The most significant and specific lesions of NSD are of a glomerular-tubular nephritis. There is severe congestion associated with the glomeruli, and peri-vascular cuffing with plasma and other inflammatory cells. The nuclei of the endothelial cells of the glomeruli become swollen and the cytoplasm swollen, vacuolated and granular. Degenerative changes occur in the glomeruli and convoluted and other tubules. Casts of desquamated cells appear in the lumen with much granular hyaline material. In the medullary area of the kidney, there is much congestion and swelling but the tubules themselves are not as severely affected as elsewhere. These kidney lesions are highly specific for NSD in enzootic areas, for no other virus disease produces anything similar. Recovered animals show severe interstitial fibrosis with greatly compromised kidney function.
DiagnosisTop of page
The clinical signs are similar in both sheep and goats. The onset of fever 2-8 days after either movement to a new area or introductions from elsewhere, is a common history. Ixodid ticks infest the animals. The fever is high, 40-41.5°C and persists for at least 3 days and often longer. The fever is accompanied by severe depression, partial or total anorexia, a disinclination to move and often some respiratory distress. The superficial lymph nodes will be enlarged. There is usually conjunctival injection and a sero-sanguineous nasal discharge. Diarrhoea occurs within 36-48 hours of the onset of fever and this may be accompanied by abdominal pain and colic, with tenesmus and grunting. The diarrhoea is profuse and watery at first and later may become mucoid and haemorrhagic. Abortion will occur in affected pregnant females. The total white-cell-count will be found to be below 1-2 million per cubic millimetre. All age groups may be affected in a totally susceptible population group. The disease occurs in dramatic epidemic form, if there has been movement of animals from non-enzootic to NSD-enzootic zones, where the vector ticks are present.
Post-mortem signs are not helpful in the early stages of the disease, when only non-specific signs of an acute septicaemic or viral disease may be seen. This is likely to be the case in many NSD outbreak situations. Later in the course of the disease, the alimentary signs with zebra striping in the large bowel and abomasal haemorrhage may be helpful.
Diagnosis may be made by identification of the NSD viral antigen by agar-gel diffusion tests, which can be performed at any laboratory or by isolation of the causal virus. Plasma taken from a sheep with high fever or spleen and/or mesenteric lymph node tissue may be used as the optimal samples for virus isolation (Davies et al., 1977). This may be accomplished readily by the inoculation of suckling mice of 2-4 days of age by the intra-cerebral route or by the direct inoculation of tissue cultures. Cultures of lamb kidney or testis, or the cell lines such as BHK 21 C 13 and Vero cells may be used for primary isolation. Blind passage is advisable in both systems. In tissue cultures, blind passage is necessary in most cases before cytopathic effects become obvious, but the viral antigen may be readily detected at 56-72 h post inoculation by fluorescent antibody staining of the infected cultures. Cover-slip or slide-well cultures are recommended for this purpose. Deaths occur in infant mice at 5-10 days after inoculation. The virus may be identified by the preparation of an antigen for agar gel or complement fixation tests (CFT), sub-inoculation into tissue cultures or by a capture ELISA.
Staining of infected cultures with haematoxylin and eosin shows the interesting form of the inclusion bodies produced by NSD. These are of pleomorphic eosinophilic bodies with spindle or other irregular shape or as an irregular ring surrounding the nucleus. Fluorescent staining shows small granules of fluorescent antigen in the cytoplasm.
Serological diagnosis may be made with acute and convalescent sera using any of the older assay methods, which have included CFT, indirect FAT or indirect haem-agglutination. Neutralization tests have proved to be of no value, for both pre- and post-inoculation sera give similar endpoints in mouse or tissue culture assay systems. It has been suggested that the neutralization may be complement dependent and the addition of complement to the virus/serum mixtures may give different results. ELISA systems have been developed and used in the laboratory (Munz et al., 1983), but have not been extensively used in the field. All serological systems suffer the disadvantage that there are cross relationships with other members of the Nairovirus group. These are, however, at a much lower level than the specific NSD response. In the fluorescent assays for example, endpoints of 1/2500-1/10,000 may be obtained with specific sera and less than 1/100 with the non-specific cross relationships. Similar results have been obtained with indirect IHA, CFT and other test systems and cut-off points determined. The ELISA test systems need to be evaluated against field sera that are positive to other Nairovirus group members.
Emphasis should be made again of the difficulty of making any diagnosis purely on post-mortem evidence. Suspicion should be high, if there are large numbers of deaths in small ruminants caused by a disease with high fever in animals obviously infested with Ixodid ticks. The AGDP test can be performed in remote laboratory situations and is a low-cost test system. It is valuable in many areas where NSD is enzootic. Accurate diagnosis requires more sophisticated systems, which are only available in the National Reference laboratories in NSD-enzootic countries and not always there. Simpler pen-side tests would be most valuable for NSD.
Immunology of NSD
Recovered animals remain immune for life. The antibody response may be detected after 3-5 days and for 6-9 months by CFT and for at least 2-3 years by the fluorescent antibody and indirect haemagglutination tests (Davies et al., 1976). The ELISA test has not been systematically evaluated over long periods of time.
Several vaccines have been developed against NSD. A strain has been attenuated by passage in adult mouse brain, and this has proved to be too pathogenic for field use. A strain was developed by passage in suckling mouse brain and this gave promising results in Uganda (Terpstra, 1969). Later reports from Uganda suggested that it was not a good immunogen and it has not been widely used. An inactivated vaccine was prepared at Kabete, Kenya from high titre tissue culture fluids and this gave protection after two inoculations given with adjuvant (Davies et al., 1977). It was prepared for use in valuable imported stock but was little used. Most indigenous animals in NSD-enzootic areas are immune and this stable enzootic state ensures there is little call for any intervention.
List of Symptoms/SignsTop of page
|Cardiovascular Signs / Pulse deficiency, deficit||Sheep & Goats:All Stages||Sign|
|Cardiovascular Signs / Tachycardia, rapid pulse, high heart rate||Sheep & Goats:All Stages||Diagnosis|
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Sheep & Goats:All Stages||Diagnosis|
|Digestive Signs / Bloody stools, faeces, haematochezia||Sheep & Goats:All Stages||Diagnosis|
|Digestive Signs / Diarrhoea||Sheep & Goats:All Stages||Diagnosis|
|Digestive Signs / Excessive salivation, frothing at the mouth, ptyalism||Sheep & Goats:All Stages||Diagnosis|
|Digestive Signs / Grinding teeth, bruxism, odontoprisis||Sheep & Goats:All Stages||Sign|
|Digestive Signs / Hepatosplenomegaly, splenomegaly, hepatomegaly||Sheep & Goats:All Stages||Sign|
|Digestive Signs / Unusual or foul odor, stools, faeces||Sheep & Goats:All Stages||Diagnosis|
|General Signs / Dehydration||Sheep & Goats:All Stages||Sign|
|General Signs / Fever, pyrexia, hyperthermia||Sheep & Goats:All Stages||Diagnosis|
|General Signs / Generalized weakness, paresis, paralysis||Sheep & Goats:All Stages||Sign|
|General Signs / Haemorrhage of any body part or clotting failure, bleeding||Sheep & Goats:All Stages||Sign|
|General Signs / Inability to stand, downer, prostration||Sheep & Goats:All Stages||Diagnosis|
|General Signs / Lymphadenopathy, swelling, mass or enlarged lymph nodes||Sheep & Goats:All Stages||Diagnosis|
|General Signs / Pale mucous membranes or skin, anemia||Sheep & Goats:All Stages||Sign|
|General Signs / Reluctant to move, refusal to move||Sheep & Goats:All Stages||Diagnosis|
|General Signs / Sudden death, found dead||Sheep & Goats:All Stages||Sign|
|General Signs / Swelling mass vagina||Sign|
|General Signs / Swelling mass, vulva, clitoris||Other:Adult Female||Sign|
|General Signs / Tenesmus, straining, dyschezia||Sheep & Goats:All Stages||Diagnosis|
|General Signs / Weight loss||Sheep & Goats:All Stages||Sign|
|Nervous Signs / Coma, stupor||Sheep & Goats:All Stages||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Sheep & Goats:All Stages||Sign|
|Ophthalmology Signs / Conjunctival, scleral, injection, abnormal vasculature||Sheep & Goats:All Stages||Diagnosis|
|Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes||Sheep & Goats:All Stages||Diagnosis|
|Ophthalmology Signs / Purulent discharge from eye||Sign|
|Pain / Discomfort Signs / Colic, abdominal pain||Sheep & Goats:All Stages||Diagnosis|
|Reproductive Signs / Abortion or weak newborns, stillbirth||Sheep & Goats:Gimmer,Sheep & Goats:Mature female||Diagnosis|
|Reproductive Signs / Agalactia, decreased, absent milk production||Sign|
|Respiratory Signs / Abnormal lung or pleural sounds, rales, crackles, wheezes, friction rubs||Sheep & Goats:All Stages||Sign|
|Respiratory Signs / Dull areas on percussion of chest, thorax||Sheep & Goats:All Stages||Sign|
|Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping||Sign|
|Respiratory Signs / Epistaxis, nosebleed, nasal haemorrhage, bleeding||Sign|
|Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea||Sheep & Goats:All Stages||Sign|
|Respiratory Signs / Mucoid nasal discharge, serous, watery||Sheep & Goats:All Stages||Sign|
|Respiratory Signs / Purulent nasal discharge||Sign|
|Skin / Integumentary Signs / Warm skin, hot, heat||Sheep & Goats:All Stages||Sign|
|Urinary Signs / Glucosuria||Sheep & Goats:All Stages||Sign|
|Urinary Signs / Proteinuria, protein in urine||Sheep & Goats:All Stages||Sign|
Disease CourseTop of page
The incubation period for NSD is of 1-5 days after parenteral inoculation and will vary with the genotype of the animal, amount of virus inoculum and route of inoculation. Tick infections usually follow within 3-7 days of application and attachment. The initial signs are of a febrile reaction from 40 to 41.5°C, which may persist for 3-8 days and occasionally longer. The viraemia is correlated with the febrile reaction and subsequently virus may be isolated from the spleen and carcass lymph nodes for 10-15 days. A lymphadenitis may be detected at this stage and usually one of the pre-scapular lymph nodes is enlarged and is related to the site of attachment and feeding of the infected tick. During this period, the animal is extremely depressed with anorexia and disinclined to move; typically it stands with its head held down. There may be a sero-sanguineous nasal discharge with injection of the conjunctiva and some lachrymation. A foul-smelling diarrhoea usually develops 1-3 days after the onset of fever. At first this is watery green in colour and later may become mucoid and blood-stained. Abdominal colic and tenesmus with groaning may accompany this. An increased respiratory rate develops progressively during the course of the disease and respiratory distress is a common terminal sign. Pregnant animals may abort at this stage or later. Deaths may occur early after the onset of the febrile reaction and then for up to 12 days afterwards.
Mortality rates vary with the genotype of the animals affected and may vary from 15-30% to 95% of those infected. General observations suggest that those sheep indigenous to East Africa may be more susceptible than the exotic imported breeds. This is different from the mortality to other African virus diseases such as Rift Valley fever, when the reverse is the case. Some goat breeds appear relatively resistant to NSD with low mortality rates of 15-30%, in others 90% mortality occurs (Terpstra, 1969).
EpidemiologyTop of page
In Enzootic Areas
NSD virus can remain cryptic in enzootic areas for years, in ongoing tick-host-tick cycles and be maintained by trans-ovarial transmission with no manifestation of any disease problem. Young animals are challenged when they have maternal antibody and develop an active immune response. The small-ruminant populations show high levels of immunity (Davies, 1978a). This situation prevails throughout the enzootic areas for NSD in East Africa. Disease is signalled whenever susceptible breeds of sheep and goats are introduced into the enzootic areas to improve the production potential of the indigenous breeds. This has happened in Uganda (Terpstra, 1969), in Kenya and in Somalia (Pavalglia, 1938; quoted by Pellegrini, 1950), when Karakul sheep were brought from Italy. Disease also follows the movement of sheep and goats from non-enzootic semi-arid zones to the centres of population for trade purposes. Any attempts at tick control in the small-ruminant populations may allow the development of susceptible population groups, which are at risk when the tick control activities cease or fail for any reason. The levels of flock immunity remain high, wherever high levels of larval survival ensure persistent populations of the tick vectors. This happens wherever there are two wet, or continuous wet with only short dry seasons. It is possible that there are such enzootic areas in the south of Sudan, where R. appendiculatus occurs, in Uganda and in parts of the Congo.
In Epizootic Areas
Pastoralists in areas that are non-enzootic for NSD have described epizootics that kill most of their sheep (Lewis, 1934). This is in areas where the tick vector may be present, but in only extremely small numbers, which is typically in the Acacia savannahs of agroclimatic zone III in East Africa. These populations have, however, been seen to increase dramatically following the periodic changes in rainfall pattern, when for 6-18 months there may be prolonged and heavy rainfall with heavy cloud cover. This results in the development of more ground vegetation, which allows huge increases in the tick populations to occur. Where previously, one R. appendiculatus tick may be found after examining 10 animals, after these changes hundreds may be found on a single animal. In such conditions epizootics of NSD have been seen with high mortality rates in the non-immune sheep and goat populations. Such climatic conditions have occurred in 7-15 year cycles, but may become more frequent following the changes induced by the El Nino/Southern Ocean Oscillation effects (ENSO).
The history of epizootic NSD in Somalia suggests a similar epidemiological basis. The outbreaks have followed periods of severe drought, which resulted in much movement of livestock. The mortality was occurring in these migratory flocks, which moved, presumably into NSD-enzootic areas.
The enzootic areas for NSD are in the moist-forest-derived or natural grasslands and in the contiguous moist bushed and wooded grasslands. These are in Eco-climatic Zones II & III in most classifications for Africa. Zone IV, which include the drier Acacia grasslands, are generally too dry for the tick vector, other than when associated with the riverine woodland zones. These have a higher water table and allow the persistence of R. appendiculatus in Zone IV; these populations increase hugely in favourable conditions.
Temperatures of 15-30°C are optimal for the maturation of the various stages of this tick species. A relative humidity of greater than 45%RH is necessary for maturation and development of the tick vector. Lower levels have a negative effect upon the larval and nymphal stages; higher levels have a positive effect. Such conditions are available in most of the NSD-enzootic areas of East Africa, where continuous life cycles are possible.
Environmental modelling developed by Krasteva et al. (2020) has shown that minimum temperature is one of the most important variables predicting suitable areas of spread for tick species capable of spreading NSD, followed by humidity and livestock density. This is significant considering that global warming will continue to cause changes in severe temperatures and will force species to modify their current distributions to novel environments. Their work also identified countries with suitable environmental conditions were NSD could circulate and pose a transmission risk, including Ethiopia, Malawi, Zimbabwe, Southeastern China, Taiwan, and Vietnam. Additionally, they identified areas that would be unsuitable, including the Democratic Republic of Congo, Zambia, and Southern Somalia.
The principal vector of NSD in Kenya and Uganda has been shown to be Rhipicephalus appendiculatus (Montgomery, 1917; Daubney and Hudson, 1931; Terpstra, 1969; Davies, 1978a, 1978b). Amblyomma variegatum has also been shown to transmit NSD, but is a less efficient vector than R. appendiculatus. Amblyomma gemma, R. simus and R. pulchellus have been described as "occasional vectors" in Kenya Departmental reports.
In Somalia, Pellegrini (1950) showed that R. pulchellus was capable of trans-ovarial and trans-stadial transmission of NSD virus. Similar experiments with the Kenyan race of R. pulchellus were not successful (Daubney and Hudson, 1934; Davies, unpublished data). Most subsequent attempts to transmit NSD with R. pulchellus have also failed, although there was a report from Kabete in 1948 that a successful transmission of NSD had occurred. The virus has not been isolated from pools of this tick species. The distribution of the tick does not coincide with that of NSD virus or antibody in Kenya.
Bugyaki (1955) found that R. appendiculatus was the vector of the NSD-like disease he described at Kisenyi on the shores of Lake Kivu in Rwanda.
R. appendiculatus was originally a tick species found on wild Bovidae. It has adapted to most domestic ruminant species and will feed upon domestic bovids, sheep and goats. Small ruminants are, however, less favoured hosts than cattle. Bos indicus cattle carry fewer ticks than the exotic Bos taurus breeds. The tick feeds in large numbers, particularly upon buffalo and waterbuck, with lower infestation rates on other wild ruminants (Walker, 1967). Populations of the tick are greatest where the temperature and humidity are optimal and where suitable hosts are available in large numbers, and this is further supported by ecological niche modeling (Krasteva et al., 2020). Larval survival rates may be high in optimal conditions and large populations of ticks develop with ongoing life cycles throughout the year. In less favourable conditions, which are drier with perhaps a single short wet season and prolonged dry conditions with fewer available host species, larval survival rates and tick populations are much lower. The NSD virus has been shown to survive in a single adult for 871 days, in larvae for 144 and nymphs for 138 (Lewis, 1946).
Rhipicephalus pulchellus is a tick species most commonly found on black cotton soils in East Africa. It is by far the most common tick species infesting cattle, sheep and goats in those parts of Somalia, where NSD has been identified (Pegrum 1976). The populations have been found to increase "40 fold" after the rains in the "haud" of north-west Somalia.
Ganjam virus has been isolated in India from Haemaphysalis intermedia and this is considered to be the most important vector species. It has also been isolated from Haemaphysalis wellingtonii and once from mosquitoes Culex vishnui (complex). In Sri Lanka, Haemaphysalis ticks also appear to be the main vectors.
Most recently in China, H. longicornis has been identified as a new vector for NSD (Gong et al., 2015).
A classical work by Dr Aneurin Lewis at the Veterinary Research Laboratory at Kabete, examined the tick/vector relationships in detail (Lewis, 1947). He was able to show that individual adult ticks could retain NSD infection for at least 871 days, and that larvae remained infective for 144 and nymphs at least 138 days. This, together with the original evidence from Montgomery (1917) and Daubney and Hudson (1931), who demonstrated the trans-ovarial transmission of the virus, explains the long-term persistence of NSD in the enzootic areas. This happens when no manifestation of disease has ever been recorded. Davies (1978a) found evidence of high antibody levels in sheep populations, where no disease had been reported for more than 50 years.
Daubney and Hudson (1931) suggested that feeding resulted in sterilization of infected ticks, which then lost the ability to transmit at a subsequent feed. This point was studied in a series of experiments by Davies and Mwakima (1982). They showed that feeding a vertically infected tick population upon susceptible, immune or unsusceptible hosts did not result in their sterilization with regard to NSD virus. This is important because R. appendiculatus populations feed predominantly upon unsusceptible host species such as cattle and wild bovids. Tick populations would gradually become free from NSD if each feed resulted in sterilization. Field evidence suggested that it was not happening and the laboratory experiments confirmed this.
Little work has been done on the infection rates in tick populations but Davies (unpublished work) found that this was below 1% of the population he examined. It is possible that the assay systems he used were insensitive. Work done at the NERC, Oxford has shown that guinea pigs could pick up a nairovirus from ticks, when no viraemia had been detected (Jones et al., 1987). Transmission experiments that suggest that R. appendiculatus is probably the most important vector, have been carried out in Kenya, Uganda and Rwanda. R. pulchellus appears to be the important vector in north Somalia and probably in region V of Ethiopia. Other ticks, notably Amblyomma varieagatum, can transmit the virus, but less efficiently than R. appendiculatus. R. simus, Amblyomma gemma and possibly other Ixodid ticks may also be able to transmit NSD on occasion (Kenya Veterinary Department Annual Reports, 1948).
Impact: EconomicTop of page
NSD is an extremely pathogenic virus disease for sheep and goats. It is the most pathogenic virus disease of small ruminants in East Africa, with mortality rates in indigenous animals of 70-95%. No other disease shows such dramatic mortality: hundreds of animals may die over a period of 2-6 weeks when introduced into an enzootic area from a non-enzootic zone. Losses in the quarantine area outside Nairobi were extremely high until the animals were transported straight for slaughter.
The extensions in the range of the tick vector, which follow the periodic periods of prolonged and heavy rainfall, also result in huge losses in these extension zones. The pastoralists have reported losing from 50 to 75% of their flocks during such periods, which has considerable socio-economic consequences. Similar losses have been sustained in these population groups in Somalia.
Introductions of exotic breeds are hazardous in enzootic areas, because losses due to NSD will be high. Vaccines have been developed for use in such circumstances, but these are not usually available. There is no treatment for the disease.
Zoonoses and Food SafetyTop of page
No human disease problems have been encountered amongst the pastoral and other populations in the NSD enzootic areas, which might be due to NSD. Small ruminants are being killed throughout the year and ticks are regularly removed from individual animals and killed by squeezing between finger and thumb. This can create an aerosol, which is infected with NSD if the ticks are contaminated with the virus. Such pastoral populations suffer from Rift Valley fever (RVF) contracted after slaughter of their livestock during RVF epizootics. They do not appear to identify a disease syndrome, which could be NSD, and which follows killing and butchering their stock. This is not the case with another Nairovirus, Crimean Congo haemorrhagic fever, which can be transmitted in an identical manner.
The virus may persist in a carcass until such time as the pH falls 8-12 h after death; the virus is destroyed at low pH. It is not considered to present a risk to personnel at any point in the food chain. NSD-infected carcasses in a slaughter-house may be condemned as fevered or diseased. They would not present any food safety hazard if they passed through the system at an early stage of incubation.
NSD is on the Office International des Epizooties (OIE) list of notifiable diseases and is therefore a reportable disease; it is on the list of exotic diseases of the USDA. Its occurrence in a new country should be followed by immediate slaughter of all affected and in-contact animals. Extensive tick surveys should then be carried out to eliminate the imported infected ticks and their hosts to prevent the disease becoming established.
There is a danger that NSD might be introduced to a new continent or country with the importation of animals infested with the vector tick and virus. Any importations of wild or domestic Bovidae and other species which are parasitized by the tick, should be treated on at least two occasions with acaricides and be subject to detailed inspection for ticks before export. Trade in wild ruminant and other species presents the greatest possibility for this to happen. The virus does not persist in infected animals for longer than the febrile period and no transmission is likely to occur from infected tissues. Most importing countries require a period of quarantine greater than the possible danger period for NSD.
There is a theoretical possibility that the virus could be transferred with Palearctic bird species in their migration from Africa north into Europe and Eurasia. This appears not to have occurred thus far, but remains a possibility. Birds are frequently seen to have Rhipicephalus larvae or nymphs when trapped on migration northward.
Disease TreatmentTop of page
No drug therapy is currently available that could be of any value in the treatment of NSD other than ribavirin. Ribavirin is used successfully in the treatment of other Bunyavirus diseases in humans, such as Rift Valley fever. It has an important role in human disease control and there is no doubt that any case of human NSD would benefit from early administration of this anti-viral agent. It is not available for use in animals and in the present situation cannot be a cost-effective option.
Prevention and ControlTop of page
The use of vaccines for the prophylaxis of NSD has been suggested whenever valuable small ruminants are being imported into an enzootic area. Vaccines have been developed which showed considerable promise when tested in the laboratory, but there is no demand for these in the field. The steady enzootic state ensures that high levels of immunity are present in the small-ruminant populations at risk. No interventions such as vaccination, nor tick control are indicated.
This enzootic state can be altered by tick control practices, which may then lapse, and most importantly by extension in the range of the tick. The current ENSO activity (El Nino Southern Oscillation) results in periods of greater drought and greater rainfall. The latter is important as the cause of extensions in the range of the tick beyond the enzootic zones. Such changes can be predicted using serology and the CLIMEX data (CSIRO, Australia) for R. appendiculatus as a basis for defining enzootic areas and monitoring the data generated by ARTEMIS (African Real Time Environmental Monitoring Information Service). This provides data on the changes in vegetation, which develop following prolonged and heavy rainfall and favour extension and the development of large tick populations in hitherto clean areas. Short-term tick control or vaccination may then be instituted in these extension zones. The availability of 'pour on' acaricides (permethrin and cypermethrin) provide a cost-effective means of controlling the tick infestations during the critical periods, when these extensions occur.
The pastoralists themselves are aware of the dangers presented by areas infested with the vector tick, which also transmits a serious disease of cattle (Lewis, 1934). They are able to identify such problem areas and avoid grazing them at times when a danger is perceived.
The broad level of flock immunity which prevails throughout the enzootic areas for NSD in East African countries, and the awareness of the dangers of movement into enzootic areas from the arid and semi-arid zones, leads to a successful 'laissez faire' approach to NSD. Traders are aware of the problems and no national policies have been generated for control of the disease, for the scientific evidence supports a non-interventional approach. The dangers of extensions into agro-climatic zone IV following climatic changes remains and predictive epidemiology, as is now being used for Rift Valley fever, should be adopted to define and monitor the danger zones.
ReferencesTop of page
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ContributorsTop of page
07/04/2021 Updated by:
Stephanie Krasteva and Gustavo Machado, North Carolina State University