Introduction
Peste des petits ruminants (PPRs) is an acute and highly contagious viral disease of small ruminants, characterized by high fever, ocular and nasal discharges, pneumonia, necrosis and ulceration of the mucous membrane, and gastroenteritis leading to severe diarrhea [1]. Although the disease may affect wild ungulates from the families Gazellinae, Caprinae, and Hippotraginae, it is particularly severe in sheep and goats, leading to nearly 90% morbidity and 100% mortality in unvaccinated flocks [2]. The disease has also been observed in camels, cattle, and buffaloes [3].
PPR virus (PPRV) is an extremely pleomorphic enveloped RNA virus that belongs to the family Paramyxoviridae in the genus Morbillivirus. The virus shares genetic ancestry with the viruses that cause rinderpest, canine distemper, measles, and dolphin distemper. In particular, PPRV and rinderpest virus are so closely related that the tissue culture rinderpest vaccine was generally employed in the early control of PPR and was only discontinued as a result of the global rinderpest eradication program. Similar to most paramyxoviruses, the genome of PPRV is approximately 15.9 kb negative-stranded RNA encoding nucleoprotein (N), phosphoprotein (P), matrix protein (M), fusion protein (F), hemagglutinin protein (H), and large protein (L) [4]. These are often used to classify PPRV isolates into various lineages. To date, four lineages have been discovered and epidemiologically linked to the geographic spread of PPRV. Interestingly, lineage IV, which emerged in new hosts and geographical areas, has higher evolutionary adaptation to sheep and goats than the other three lineages [5].
The disease can be diagnosed by identifying the PPRV antigen using antigen-capture enzyme-linked immunosorbent assays (ELISAs), antibodies by antibody-detection ELISAs, and PPRV RNA by reverse transcription polymerase chain reaction [6].
PPR camel outbreaks have been observed in Iran [7] and Kenya [8]. PPR in Nigeria has been documented as far back as 1976 by Hamdy and Dardiri [9], and the illness continues to be widespread in the nation, causing significant financial losses in the small ruminant industry. PPR has recently been reported in various regions of the nation by Luka et al. [10] and El-Yuguda et al. [11]. There is also evidence of natural infection of camels with PPR in Sokoto [12]. However, there is little information about the possible roles of transmission between camels, sheep, and goats and the characterization of the virus in camels in the study area. Investigating the precise role camels may play in the epidemiology in the impacted zones is necessary in light of the recent disease outbreaks. The camels stand out among the PPRV atypical hosts, such as pigs, buffaloes, and wild animals, because they are geographically distributed throughout the PPR endemic regions of the world, herded with the typical host, small ruminants, in most of Africa and Asia, and their numbers are steadily rising [13].
PPR results in the death of livestock that is usually owned by poor people in developing countries; it poses a threat to food security and the worldwide trade of cattle and livestock products. PPR is one of the diseases now being targeted for eradication, presumably by the year 2030 [14]. Determining whether PPRV infection exists in other hosts herded with sheep and goats is crucial since it will affect eradication efforts. Therefore, this study was carried out to determine the seroprevalence of the disease and some risk factors for the occurrence of the disease in camels in Sokoto State, Nigeria.
Materials and Methods
Study area
Sokoto is located at the coordinates 13°05’N and 05°15’E in the extreme northwest of Nigeria. It covers an area of approximately 25,973 square kilometers (Fig. 1). The last national census in 2006 reported the state human population to be 3,702,676, with an annual rainfall of between 500 mm and 1,300 mm and humidity varying from 10% to 90% [15]. The state has livestock resources with an estimated 3 million cattle, 3 million sheep, 5 million goats, 4,600 camels, and a host of other local and exotic poultry species [16].
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Figure 1.
Map of Sokoto state [MOCIT, 2002].
Study design
A systematic random sampling technique was employed to obtain whole blood from camels and the samples were obtained from herds and abattoirs inclusion criteria. Both apparently healthy and sick camels were sampled.
Sample collection, transport, and storage
Five milliliters of blood samples each were collected from camels (both young and adult) and transported in ice packs to the Central Research Laboratory, Faculty of Veterinary Medicine, Usmanu Danfodiyo University, Sokoto. The blood samples were centrifuged at 5,000 g for 5 minutes, sera were separated/ harvested and kept at −20°C. A total number of 60 samples were collected out of which 26 were from males and 34 were from females. The samples were obtained in the rainy, harmattan, and dry seasons (8 in the rainy, 16 in harmattan, and 36 in the dry) from August 2023 to May, 2024. Forty-two of the samples were obtained from the abattoir while 18 were obtained from different herds. The samples from the abattoir were obtained from Sokoto’s main abattoir while the other samples from herds were obtained from local governments in each of the senatorial zones.
Enzyme-linked immunosorbent assay
A competitive ELISA kit with a sensitivity of 92% and specificity of 76.36% for the detection of anti-PPRV nucleoprotein antibodies in goat serum obtained from ID. Vet Innovative Diagnostics Grabels, France, was used to test serum samples for the presence of PPRV antibodies at the Central Research Laboratory, Faculty of Veterinary Medicine, Usmanu Danfodiyo University Sokoto. Briefly, the wells were coated with purified recombinant PPR nucleoprotein (NP). The samples were to be tested and the controls were added to the microwells. Anti-NP formed an antibody-antigen complex which masked the NP epitopes. An anti-NP-peroxidase (HRP) conjugate was added to the microwells. It is bound to the remaining free NP epitopes, forming an antigen-conjugate-HRP complex. After washing to eliminate the excess conjugate, the substrate solution, tetramethylbenzidine was added. The resulting coloration was dependent on the quantity of specific antibodies present in the sample tested. In the absence of antibodies, a blue coloration appeared which became yellow after the addition of the stop solution. In the presence of antibodies, no coloration appeared. The microplate was read at 450 nm.
Data analysis
The data obtained from the study were subjected to both descriptive and inferential statistics to determine the association of the variables (age, sex, location, and season) with the presence of PPRV antibodies. Z-test was used to determine the proportions between the age groups and sexes while chi-square was used to determine the association between ages, sexes, and seasons.
The value of p < 0.05 was considered significant in the studies and statistical software ‘SPSS’ version 22.0 was used for the analysis.
Results
A total of 60 samples obtained from camels were collected and screened for the presence of PPR antibodies using an indirect ELISA kit from Idvet®. Among them, 11 were positive constituting an overall seroprevalence of 18.3%.
The Z-Test for proportions of samples by sex, location, age, and season is shown in Table 1. No statistically significant association was found between sex, location, and age. However, a statistically significant association (p < 0.05) was found with prevalence and season.
The chi-square test for positive versus negative cases of PPR in Camels by sex, location, age, and Season is shown in Table 2. No statistically significant association was found between the variables and the occurrence of the infection in camels.
Table 1.
Z-test for proportions of samples by sex, location, age, and season.
| Variable | Comparison | Z-value | p-value |
|---|---|---|---|
| Sex | Male versus female | 0.8304 | p ˃ 0.05 |
| Location | Abattoir versus herds | −1.2377 | p ˃ 0.05 |
| Age | Young (Less than 2 years) versus adult (Above 2 years) | 0.5235 | p ˃ 0.05 |
| Season | Dry versus harmattan | 1.2529 | p ˃ 0.05 |
| Dry versus rainy | −1.0570 | p ˃ 0.05 | |
| Harmattan versus Rainy | −1.9365 | p ˂ 0.05 |
Note: Significant results are marked with p < 0.05.
Table 2.
Chi-square test for positive versus negative cases in camels by sex, location, age, and season.
| Variable | Group | Positive | Negative | Chi-square (X2) | (X2)Yates | p-value |
|---|---|---|---|---|---|---|
| Sex | Male | 6 | 20 | 0.6,896 | 0.2,438 | p > 0.05 |
| Female | 5 | 29 | ||||
| Location | Abattoir | 6 | 36 | 1.5,319 | 0.7,633 | p > 0.05 |
| Herd | 5 | 13 | ||||
| Age | Young | 9 | 43 | 0.2,740 | 0.0,011 | p > 0.05 |
| Adult | 2 | 6 | ||||
| Season | Dry | 7 | 27 | 3.5,380 | 1.5,883 | p > 0.05 |
| Harmattan | 1 | 15 | ||||
| Rainy | 3 | 5 |
Note: All results are marked as insignificant (p > 0.05), indicating no significant association in these categories.
Discussion
Findings from this study revealed an overall seroprevalence rate of 18.3% for PPR antibodies in camels in Sokoto State, Nigeria. This finding is particularly important given the context in which camels interact with small ruminants, the primary hosts for PPR. Despite the absence of overt clinical signs, the detection of antibodies suggests that camels can serve as incidental hosts, which may play a role in the epidemiology of PPR in mixed-species farming systems [17]. Camels, while not primary hosts, can contribute to the maintenance of the virus within the ecosystem, particularly in environments where they coexist with infected sheep and goats [18]. Such dynamics necessitate the incorporation of camels into PPR surveillance and control programs, as their presence could indirectly influence the incidence of PPR in economically important small ruminant populations [19].
Similar seroprevalence rates have been reported in other studies across Africa; for example, in Sudan, a study found a seroprevalence of 17% in camels [3]. This study’s findings align with previous research, highlighting the consistent presence of PPR antibodies in camels in Africa [20].
The prevalence obtained in this study is lower than that obtained by El-Yuguda et al. [11], who reported a prevalence of 27.8% in the semi-arid region of Northern Nigeria. This difference was attributed to the higher number of camels sampled in their study. In other parts of Africa, research conducted in Ethiopia revealed higher seroprevalence rates of 31% in camels than the prevalence obtained in this study. This difference was attributed to higher livestock density and movement patterns that facilitate disease transmission [21].
However, the prevalence found in this study is higher than that of some other studies. In Nigeria, Daneji et al. [12] reported a seroprevalence rate of 4% from 250 sampled camels using the agar-gel precipitation test. A prevalence of 3.36% was obtained from four northern states in Nigeria [22]. These differences were also attributed to the number of camels sampled in the different studies and to the possibility of more small ruminants being herded along camels due to dwindling economic fortunes, and the detection tests employed. ELISA used in this study is a more sensitive technique and can detect low levels of antibodies compared to other techniques like the agar-gel precipitation test.
In other parts of Africa, Omani et al. [8] conducted a study in Kenya that documented a seroprevalence of 5.5% in camels, which is lower than the prevalence observed in this study. Their research highlighted that the seroprevalence was linked to proximity to small ruminant populations, reinforcing that camels may acquire antibodies through contact with infected hosts.
Beyond Africa, studies in other regions, including the Middle East and South Asia, have similarly reported low seroprevalence rates in camels, ranging from 2% to 8% [23].
The disparities in seroprevalence across studies may be influenced by factors such as local climate conditions, variations in herd management practices, and differences in vaccination coverage against PPR. In Nigeria, a comprehensive review highlighted that factors such as vaccination history, age, and sex influence PPR seroprevalence, reinforcing the need for tailored control measures [24].
Our findings suggest a statistically significant variation in seroprevalence across seasons, with higher rates observed in the rainy season. This could be attributed to the fact that microorganisms tend to replicate more in wet conditions. This seasonal influence corroborates previous studies in Bangladesh that reported remarkable susceptibility to the infection in the rainy season compared to other seasons [25]. Understanding these dynamics is essential for planning vaccination campaigns and implementing biosecurity measures at critical times, particularly in areas prone to seasonal outbreaks.
No significant association in seroprevalence was observed across age, sex, and location. This lack of variability suggests a relatively uniform infection risk across these categories in camels. This is also similar to the findings of Woma et al. [22], who reported no significant difference between the sexes of the camel and the seroprevalence.
Findings from this study indicated a higher number of young animals were positive compared to older animals. This was attributed to the number of camels sampled during the sampling period, where young camels were sampled more than adults. There was no statistically significant association between age and seropositivity. This finding is in line with reports that camels’ exposure to PPR does not strongly correlate with age or sex, possibly due to their generally lower susceptibility and longer lifecycle compared to small ruminants [26]. However, other studies conducted have indicated significant age-related differences in PPR seroprevalence. Woma et al. [22] reported a statistically significant difference between camels that were less than or equal to 5 years and those above 5 years of age. At the same time, another study by Rahman et al. [20] in Pakistan reported a higher prevalence in younger camels compared to adults. This could be due to the fact that younger animals might have lower immunity due to lack of exposure to pathogens. The seroprevalence observed in this study implies the urgent need for inclusive vaccination campaigns targeting not only sheep and goats but also camels, particularly in Sokoto State, where mixed-species farming is prevalent.
Conclusion
This study reveals a significant seroprevalence of PPR antibodies in camels within Sokoto State, Nigeria signifying their potential role as incidental hosts in the transmission of PPR. Although camels are not primary hosts, their presence in mixed-species farming systems with small ruminants like sheep and goats can influence disease persistence and spread. The observed seroprevalence, coupled with seasonal variations, emphasizes that PPR transmission is complex, involving interspecies interactions, environmental conditions, and management practices. These findings suggest that camels, even without showing clinical signs, may contribute to maintaining the virus, especially in areas with frequent camel-small ruminant interactions. It was recommended that the possibility of including camels in vaccination efforts to substantially reduce the risk of cross-species transmission should be looked into. Further research to determine the role of camels in the transmission dynamics of the disease should be carried out toward global eradication of PPR by the year 2030.
