Detection of peste des petits ruminants and concurrent secondary diseases in sheep and goats in Ngorongoro district, Tanzania

Small ruminants contribute significantly to the economy of most rural communities in developing countries. Though small ruminants contribute towards alleviation of poverty, their productivity is hampered by, among other things, infectious diseases and poor husbandry practices (FAO and OIE 2016). Compared with cattle, there are limited studies on small ruminants’ health and the information available is fragmented and sometimes incomplete (Farougou et al. 2013). One area which is poorly documented is the magnitude of multiple infections, by different types of pathogens such as viruses, bacteria, and parasites, in sheep and goats that result in respiratory diseases (Settypalli et al. 2016). Some clinical signs associated with respiratory diseases of small ruminants include ocular and nasal discharges, lesions in the oral and nasal mucus membranes, cough, pneumonia, diarrhea, and severe dehydration (Kul et al. 2015; Roeder and Obi 1999).

One important respiratory disease affecting small ruminants currently worldwide is peste des petits ruminants, PPR. Peste des petits ruminants is a viral disease of small ruminants first reported in West Africa in the early 1940s and later recognized as endemic in both West and Central Africa (Parida et al. 2015; Gargadennec and Lalanne 1942). The disease is caused by small ruminant morbillivirus (SRMV), formerly peste des petits ruminants virus (PPRV), a member of the genus Morbillivirus of the Paramyxoviridae family (ICTV 2016). Currently, PPR is prevalent in Central, Eastern, and Western Africa, Asia, and the near and Middle East (Libeau et al. 2014). In East Africa, PPR was detected in Kenya and Uganda in 2007, while in Tanzania, it was officially confirmed in 2008 (Kivaria et al. 2009; Swai et al. 2009). The disease is considered endemic in Tanzanian domestic sheep and goat populations (Torsson et al. 2017; Kgotlele et al. 2016).

Other respiratory diseases of economic importance affecting small ruminants include contagious caprine pleuropneumonia (CCPP), pasturella, sheeppox, and goatpox (Kul et al. 2015; Emikpe et al. 2010; Brown et al. 1991; Ugochukwu and Agwu 1991). Mycoplasma capricolum subspecies capripneumoniae (Mccp) is the causative agent of CCPP, a highly contagious disease of goats first described in 1873 in Algeria (OIE 2014). The disease was later described in 1976 in Kenya by MacOwan and Minette (1976), followed by subsequent isolations in several African countries including Tanzania (Kusiluka et al. 2000a, b; Bölske et al. 1995). Sheep poxvirus and goat poxvirus, which belong to the Capripoxvirus genus, are responsible for pox diseases in sheep and goats. These occur in several parts of Africa, Asia, the Middle East, and India (Spickler 2015). Pasteurella multocida (P. multocida) is also isolated from cases of respiratory diseases in sheep, goats, pigs, and cattle, often causing pneumonia either alone or as an opportunist with other respiratory pathogens (Settypalli et al. 2016). Pneumonic pasteurellosis is one of the most economically important infectious diseases of ruminants with a wide prevalence throughout the continents (Mohammed and Abdelsalam 2008). The similarity in the signs caused by these pathogens, and their co-localization in nearly the same endemic areas, calls for appropriate differential diagnostic testing to accurately identify the responsible pathogen(s) (Settypalli et al. 2016). In this study, the aim was to investigate the etiological cause of a respiratory disease outbreak in sheep and goats in Loliondo area in Ngorongoro district of Arusha region in Tanzania.

Clinical signs observed in the examined animals were nasal discharges and diarrhea. These clinical signs are expressed in many infectious diseases of small ruminants. Infectious diseases that present similar observed clinical signs include PPR, pneumonic pasteurellosis, and CCPP for nasal discharges; PPR, coccidiosis, or gastro-intestinal helminth infestations for diarrhea; and contagious ecthyma, sheep pox, and goat pox for nodular lesions (Zro et al. 2014; Munir et al. 2009; Diallo et al. 2007; Roeder and Obi 1999). In Tanzania, difficulty in differentiating clinical signs in sheep and goats has been mentioned as a major limiting factor in diagnosis especially for PPR and CCPP (Mbyuzi et al. 2014). In such cases where specific manifestations of the diseases are absent, reliable laboratory tests are needed.

The overall seroprevalence of PPR in this study was 74.6%. This seroprevalence is in line with findings from a recent study that analyzed samples from 14 regions of Tanzania, with Arusha region having an overall seroprevalence of 71.1% (Kgotlele et al. 2016). Other studies done in northern Tanzania have found PPR seroprevalence of 45.5% in 2008 (Swai et al. 2009) and 22.1% in 2008–2009 (Kivaria et al. 2013). This variation over the years may be due to uncontrolled animal movement that spread PPR in the sheep and goat population reared without proper vaccination. In this study, presence of antibodies to SRMV was most likely caused by natural exposure as none of the animals were vaccinated according to records from the District Veterinary Office. The animals in this study were grazed in communal pastures, which could be where they encounter infected animals. Intermingling of animals in communal grazing lands has been found to facilitate spread of infectious diseases such as PPR, CCPP, contagious ecthyma, and goat and sheep pox (Kusiluka and Kambarage 1996).

There was statistical diference between animals under 2 years more likely to be seropositive than those above 2 years. The differences noted between the age groups are most likely due to younger animals loosing their aquired passive immunity after 3 months and the older ones having life long immunity after survival of infection (Kul et al. 2015). In this study, there was no statistical difference between males and females. This finding is different from another study done in Tanzania where females were more likely to be seropositive than males (Torsson et al. 2017). It is believed that females are used in reproduction hence kept longer in the herd than males, therefore, have a longer risk period for exposure in the herd. Stress associated with pregnancy and milk production could also predispose them to infection (Aziz-ul- et al., 2016).

All four pathogens investigated in this study were detected from nasal swabs, including co-infections of SRMV and Mccp, SRMV and CaPV, SRMV and P. multocida, and Mccp and CaPV. Co-association of SRMV with other viral and bacterial infections in small ruminants has been demonstrated before in other studies in different parts of the world (Kul et al. 2015). Viral diseases with co-association with SRMV include sheep and goat pox virus, while co-associations with bacterial pathogens include Pasteurella spp., Mccp, and Mannheimia haemolytica (Malik et al. 2011; Emikpe et al. 2010; Brown et al. 1991; Ugochukwu and Agwu 1991). The co-infections detected in this study may have provided complications during field diagnosis that resulted in the persistence and severity in the affected flock. Thus, laboratory confirmation is critical for appropriate interventions to be made for the different diseases of sheep and goats especially regarding PPR. Development and use of specific diagnostic tests that can distinguish PPR from diseases with similar signs has helped unquestionably to improve knowledge and understanding in geographical distribution and spread of the disease in specific areas (Libeau 2015). This is critical as PPR has been identified as the next animal disease to be eradicated after rinderpest. One of the factors identified in the PPR Global Control and Eradication Strategy (PPR GCES) that make eradication possible is availability of appropriate diagnostic tests and protocols for surveillance (FAO and OIE 2016). Thus, help attain one of the objectives to progressively reduce the incidence and spread of PPR and ultimately eradicate.

In conclusion, SRMV, Mccp, CaPV, and P. multocida were detected in sheep and goats in Ngorongoro district. The study also confirmed occurrence of co-infection of pathogens that are associated with respiratory distress in sheep and goats in Tanzania, an important factor for consideration in small ruminant disease diagnosis and control strategies especially for PPR.