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Epidemiology of peste des petits ruminants in selected districts of Borena zone, Ethiopia

BMC Veterinary Research volume 20, Article number: 451 (2024) Cite this article

Abstract

Background

Peste des petits ruminant (PPR) is a contagious disease caused by the peste des petits ruminants virus (PPRV). The disease poses a significant economic threat to small ruminant production in Ethiopia, particularly to the striving pastoral production system. A cross-sectional study was conducted to estimate the seroprevalence and associated risk factors of PPR in the small ruminants of the Borena Zone. A total of 384 serum samples were collected randomly from sheep and goats and examined for the presence of PPRV antibodies using competition enzyme-linked immune sorbent assay (c-ELISA). Additionally, a retrospective analysis of five years of outbreak data was performed to provide insight into the spatial and temporal distribution of the disease.

Results

The seroprevalence of PPRV antibodies in nonvaccinated, vaccinated, and unknown vaccination status of small ruminants in this study was found to be 32.1%, 68.8%, and 45.5%, respectively. Multivariable logistic analysis revealed a statistically significant association between PPRV seropositivity and several factors, including age, animal origin, flock size, and veterinary services status. A retrospective analysis revealed 53 PPR outbreaks in the Borena Zone from 2018 to 2022, exacerbated by low vaccination coverage relative to the at-risk animal population.

Conclusion

The study revealed significant gaps in current vaccination efforts, with herd immunity levels falling below the FAO-WOAH recommended threshold of 80%. Despite Ethiopia’s ambitious goal to eradicate PPR by 2027, the frequent outbreaks and insufficient herd immunity highlight the inadequacy of the existing strategies. To effectively move toward eradication, Ethiopia must align its approach with the global PPR eradication framework, which emphasizes a comprehensive strategy that includes diagnostics, surveillance, prevention, and the establishment of a robust veterinary regulatory system, rather than relying solely on vaccination. Overcoming logistical challenges, improving vaccination coverage, and optimizing the timing of vaccination campaigns, especially in hard-to-reach areas, will be crucial for reducing outbreaks and making progress toward eradication.

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Background

Peste des petits ruminant (PPR), a viral disease, caused by the peste des petits ruminants virus (PPRV), that affects goats, sheep, other domestic animals, and wild species. The virus belongs to the Paramyxoviridae family and the Morbillivirus genus. This genus includes notable viruses such as Rinderpest Virus (RPV), Canine Distemper Virus (CD), and Phocine Distemper Virus (PDV), which affect cattle, dogs, and seals, respectively [1]. The disease causes pyrexia, nasal and ocular discharge, breathing difficulties, ulcers, necrosis, and erosive alterations in the mucosal lining of the digestive system. As the disease progresses, it can lead to pneumonia, severe diarrhea, and abortion. It induces immunosuppression, with secondary bacterial infections exacerbating the condition in affected animals [2].

Currently, PPR poses a significant economic threat to small ruminant producers in the developing world. In naive small ruminant population, the morbidity rates could reach up to 100% [3], and mortality rates range from 50 to 80% [4, 5]. The disease has a significant impact on food security [6] and restricts the international trade of animals and animal products [7, 8]. In Ethiopia, different studies conducted on PPR showed a prevalence ranging from 5.7 to 28.1% in the unvaccinated small ruminant population [9,10,11,12]. Although these studies were conducted in different parts of the country, many data gaps still exist especially in pastoral production systems. Thus, more investigation needs to be done to better understand the epidemiology of the PPR in different geographical settings and in relation to the vaccination status of small ruminants.

Given its endemic status in most of Africa, including Ethiopia, substantial efforts are being directed toward its eradication [13, 14]. The control and prevention of PPR require the immunization of susceptible animals at the appropriate times [15]. Recently, live attenuated PPR vaccines for small ruminants have been shown to establish lifetime immunity against all lineages [16]. In addition to vaccination, surveillance through systematic monitoring and diagnostic testing plays a crucial role in tracing the spread of diseases and in the effective control of PPR [17].

Borena zone is well known for its pastoral livestock production. Small ruminants’ production supports the livelihood of most pastoralists and contributes to food security in the area. Thus, any outbreak of livestock disease, including PPR, would have a high impact on the social fabric of the community. Additionally, the risk of disease transmission is considered high due to seasonal animal movement within the area [18]. Borena zone also shares an international border with Kenya and Somalia, and seasonal movement of livestock among countries can contribute to disease spread. Ethiopia has been implementing the national progressive PPR control and eradication strategy and a risk-based vaccination campaign is ongoing in different parts of the country including the Borena zone. Despite the vaccination campaign in the zone, limited vaccine coverage, uncontrolled animal movement, drought, and feed shortages may contribute spread of the PPR. Thus, the present study aimed to provide epidemiological insights that support the ongoing PPR control and eradication program in Borena zone and beyond.

Materials and methods

Study area

A cross-sectional study was conducted in three selected districts of Oromia region, Borena zone, namely Dubluk, Elweye, and Yabelo. In contrast, the retrospective study encompassed the entirety of the Borena zone. The Borena zone is located in the southern part of Ethiopia in Oromia Regional State (Fig. 1).

Fig. 1
figure 1

Map of the study area. The study was conducted in the Borena zone, with the seroprevalence study specifically targeting three districts: Elweye, Dubluk, and Yabelo. In contrast, the retrospective study covered the entire Borena zone

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Study population and study design

The study population consists of sheep and goats owned by pastoral communities in the southern lowlands of Ethiopia (Borana zone). The sheep and goats are reared on pasture and they are local breeds. These animals grazed on communal pastures and used communal public water sources.

Both cross-sectional and retrospective study designs were used in this study. The cross-sectional study was conducted from December 2022 to June 2023 to determine the seroprevalences of PPRV antibodies among nonvaccinated and vaccinated small ruminants. In addition, a retrospective analysis of five years of outbreak data was performed to provide insight into the spatial and temporal distribution of the disease.

Sample size determination

The sample size required for the study of seroprevalence was computed according to the formula given by Thrusfield [19], with a 50% expected prevalence, 95% confidence interval, and 5% of absolute precision. Hence, according to the formula, a minimum sample size of 384 small ruminants was required.

Sampling strategies

Herd size and study unit profiling

The herds were divided into small (less than 40 animals), medium (40–75 animals), and large herds > 75 animals) [20]. The age of the study animals was determined based on dentition according to ESGPIP [21] and divided into young animals (less than 1 year), adult animals (1–3 years), and old animals (older than 3 years). The body condition of the animals was recorded and classified as poor, medium, or good according to ESGPIP [22].

Districts were chosen through a careful evaluation of factors such as small ruminant population (Table 1), accessibility, and safety considerations related to travel, taking into account information on security concerns. The lists of village administrations (kebeles) in the districts were obtained from the agricultural offices of respective districts, and two kebeles were randomly selected from each district, making a total of six kebeles. Kebeles, households, and small ruminants were selected randomly from available lists.

Table 1 Sample size of small ruminants and number of interviewed participants
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Data collection

Sample collection and transportation

Blood was collected from the jugular vein of sheep and goats using plain vacutainer tubes. During blood collection, data on risk factors such as body condition, species, age, sex, herd size, introduction of new animals, water sources, market access, veterinary services, and vaccination status were recorded (Suplementary file 1). District, kebele and sample codes were properly labeled. Formal records of vaccination status are not maintained by pastoralists. However, they have detailed knowledge of their animals’ vaccination history. During data collection, pastoralists were asked if their animals had been vaccinated in the past three years; this oral confirmation was used to establish vaccination status. Additionally, local agricultural offices were consulted to confirm any previous vaccination campaigns in the Kebele.

Blood samples were left in a slanted position overnight for serum separation. The separated serum was decanted and aliquoted into 2 ml cryovial tube at Yabelo Pastoral and Dryland Agriculture Research Center and then stored at -20 °C until transportation. The samples were then transported to the Animal Health Institute (AHI) using an ice box with cold packs for serological analysis.

Serological analysis

Antibodies against PPRV were detected using the ID Screen® PPR Competition ELISA kit from ID.vet (manufactured in 310, rue Louis Pasteur-34790 Grabels- Francesensitivity = 94.5%, specificity = 99.4%) according to the protocol recommended by Libeau et al. [23]. The optical densities (ODs) were measured at a wavelength of 450 nm using an ELx800 BioTeK ELISA reader. The results were expressed as the sample negativity percentage (S/N%).

Samples with S/N% <=50% were considered positive, those > 60% were considered negative; and values between 50% and 60% were considered doubtful. OD values were converted to S/N% using the following formula:

S/N % = [OD sample / OD NC] X 100.

Retrospective PPR Outbreaks Data

Data for the five-year retrospective (2018–2022) of PPR outbreaks collected through DOVAR-II, which is part of routine passive surveillance, was obtained from the Ministry of Agriculture. DOVAR-II is a real-time, web-based reporting system where animal health staff (DOVAR-II focal personnel) in the districts collect and complete information. The report contains outbreak data organized by month, year, regional states, zones, and districts, as well as the number of cases, deaths due to PPR, and vaccine doses used.

Data management and analysis

Field data, retrospective data and laboratory findings were collected and organized in Microsoft Excel 2010 and coded for subsequent analysis. All data analyses were performed using STATA statistical software (version 14.0, STATA Corp., College Station, Texas, 77845, USA). The proportion of seroprevalence was calculated for the fixed explanatory variables examined in the study. Univariable logistic regression was used to assess the association of risk factors with disease, and significant associations (P value < 0.05) were further tested by a multivariable logistic regression model. In this study, a calculated P-value of less than 0.05 was considered statistically significant at a 95% confidence interval and a 5% level of precision.

Results

Seroprevalence of PPR

The seroprevalence of PPRV antibody was 32.1% in non-vaccinated and 45.5% in small ruminants with unknown vaccination history. In addition, 68.8% seroconversion rate was recorded among small ruminants with a history of vaccination against PPRV (Table 2).

Table 2 Seroprevalence of PPR in sheep and goats by vaccination status
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Risk factors of PPR seroprevalence in nonvaccinated populations

A univariable logistic regression was performed to determine the possible individual risk factors for seropositivity against PPRV antibodies. According to the results, the proportion of seropositive is significantly associated with veterinary services status, the origin of the animals, age groups, and flock size (Table 3).

Table 3 Univariable logistic analysis of risk factors for PPR in nonvaccinated populations
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Those variables that differed significantly in the univariable logistic analysis (P-value < 0.05) were further investigated using a multivariable logistic regression model. Consequently, factors such as animal origin, age, flock size, and veterinary services status were identified as statistically significant risk factors for PPR (P < 0.05). Accordingly, older animals were 7.3 times more likely to be seropositive for PPRV infection (OR: 7.3; 95%CI: 2.7–19.4; P = 0.000) compared to adult animals. Compared to born small ruminants, the probability of being seropositive for PPRV antibodies was 4 times higher in purchased animals (OR: 4; 95%CI: 1.4–11.3; P = 0.008) and 8.3 times higher in gifted small ruminants (OR: 8.3; 95%CI: 2.1–32.6; P = 0.003). Sheep and goats kept in medium-sized flocks were more likely to test seropositive for PPR (OR = 15.4, 95% CI: 3.1–77.3; P = 0.001). In addition, small ruminants from areas with poor access to veterinary services were 2.6 times more likely to be seropositive (OR: 2.6; 95%CI: 1.2–5.7; P = 0.019) than those from areas with adequate access to veterinary care (Table 4).

Table 4 Multivariable logistic regression analysis of risk factors associated with PPR positivity in nonvaccinated population
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Seroconversion and risk factors of PPR antibody

Out of 128 small ruminants that had been vaccinated in the past, the overall seroprevalence was 68.8%. Seroconversion was statistically significant (P < 0.05) with animal species, sex, age and body condition (Table 5).

Table 5 Univariable logistic analysis of seroconversion in vaccinated sheep and goats
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The multivariable logistic regression model revealed that both animal species and body condition of the animal had statistically significant effects on PPRV seroconversion (Table 6). Accordingly, the probability of seroconversion was 3.1 times higher in PPRV-vaccinated goats compared to vaccinated sheep (OR: 3.1; 95% CI: 1–8.9; P = 0.041). In addition, animals in poor body condition were 5.5 times more likely to test positive for PPRV antibodies than animals in good body condition (OR: 5.5; 95% CI: 1.1–28.7; P = 0.043).

Table 6 Multivariable logistic regression analysis of factors in PPR positivity in the vaccinated population
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A retrospective epidemiological analysis of PPR outbreaks

Spatial distributions of PPR disease outbreaks

The retrospective data shows that PPR outbreaks from the Borena zone were reported in the districts of Dhas, Arero, Dillo, Dirre, Dubluk, Elwaye, Gomole, Guchi, Moyale and Yabello (Fig. 2). Higher number of outbreaks were recorded in Arero (n = 21; 39.6%), followed by Dhas district (n = 11; 20.8%).

Fig. 2
figure 2

Number of PPR outbreaks Borena zone by district from 2018 to 2022

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Temporal distributions of PPR outbreaks in Borena Zone

The result of retrospective outbreak data analysis at the national level showed that a total of 554 outbreaks were recorded in Ethiopia. Of the total, 9.6% (53 outbreaks) and 692 small ruminant deaths were recorded in the Borena zone between 2018 and 2022. Yearly analysis of the PPR outbreak in Borana showed that most of the outbreaks were reported in 2019 (Fig. 3).

Fig. 3
figure 3

Annual number of PPR outbreaks in Borena zone

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A monthly variation was observed in the frequency of outbreaks, with most outbreaks occurring in January (20.8%), followed by December (Fig. 4). In October and May, there were fewer outbreaks (1.9%) than in all other months.

Fig. 4
figure 4

Monthly number of PPR outbreaks in Borena zone

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Vaccination in Borena Zone

From 2018 to 2022, a total of 10,000 vaccine doses were deployed to manage PPRV in Borena zone. The reported at-risk animal population in the region was 397,189. Notably, the vaccination effort in the Borena zone represented 0.7% of the overall vaccine doses administered nationwide.

Discussion

The study found a seroprevalence of 32.1% in unvaccinated animals in the study area, which is consistent with previous reports from other pastoral areas of Ethiopia [10, 24,25,26]. Nevertheless, the seroprevalence reported in the current study was found to be lower when compared to investigations conducted by Dubie et al. [5], Senbeto [27], and Yalew et al. [28] across various small ruminant production systems in Ethiopia. In contrast, the current seroprevalence was higher than the reports of [11, 29, 30] in Ethiopia. The difference in seroprevalence might be due to varied geographical locations, seasonal and uncontrolled movement of animals, small ruminant population density, management strategies, and migration of animals within and between countries.

The current study identified age as a significant risk factor. The likelihood of being seropositive for PPRV infection in older animals was 7.3 times higher when compared to adult small ruminants. Similar findings were reported by [6, 11, 27, 28, 31,32,33], who identified age as a potential risk factor for PPRV. In contrast, Shuaib et al. [34]. found a non-significant association between age and positivity for serum levels of PPRV, which might be due to the immunogenic nature of PPRV, long-term seropositivity, and high mortality rate of highly susceptible animals.

In this study, animal origin was also identified as a risk factor. The probability of testing positive for PPR was four times higher among animals purchased from markets and 8.3 times higher for gifted small ruminants compared to those born within the flocks. These findings align with a study by Abesha et al. [26], which reported a 2.7 times higher likelihood of seropositivity in animals brought from other locations as opposed to those born within the flocks. Additionally, research by Alemu [11], Hailegebreal [35], and Singh et al. [36] indicated that animals newly acquired from markets or other places were identified as potential sources of the disease.

Moreover, our study revealed that sheep and goats raised in medium-sized flocks had higher seropositivity. This observation is consistent with previous researches [11, 26, 35] where flock size was identified as a risk factor associated with PPR.

The antibody level of PPRV in vaccinated animals was significantly higher in goats than in sheep. As a result, antibodies generated in response to natural PPR infection differences in species and additional vaccination might trigger a considerably stronger immunologic response in the target species. Mebrahtu et al. [25] reported a higher seropositivity in goats when compared with sheep.

Our study demonstrated that sheep and goats raised in medium-sized flocks exhibited higher seropositivity rates, which aligns with previous research identifying flock size as a significant risk factor for Peste des petits ruminants (PPR) [11, 26, 35]. Importantly, we observed that antibody levels against PPRV in vaccinated animals were significantly higher in goats than in sheep. Although our study did not reveal a statistically significant difference in seroprevalence between the two species, prior research by Mebrahtu et al. [25 indicated higher seropositivity in goats compared to sheep.

Additionally, it is crucial to consider that the severity of PPR can be influenced by the circulating lineage or strain of the virus. Sheep and goats may respond differently to various strains, which could affect disease outcomes. For instance, certain strains may exhibit heightened virulence in goats, leading to more severe clinical manifestations, while others may be less pathogenic in sheep [37]. This aspect underscores the need for further studies to explore the interactions between host species and the specific strains of PPRV, as understanding these relationships will be vital for developing effective control measures and vaccination strategies. Notably, lineage IV is the predominant lineage circulating in Ethiopia, which further emphasizes the importance of monitoring this strain’s impact on both sheep and goat populations in the region [33, 38].

Herd immunity was assessed in 128 small ruminants with a history of vaccination, revealing a protection level of 68.8% against PPR. This finding aligns with the results of Alemu [11], who reported a 64.5% herd immunity rate in vaccinated small ruminants from the eastern Amhara region bordering the Afar region, and Faris et al. [39], who observed a 61% seroconversion level in the Awash Fentale district of the Afar Region, Ethiopia. These studies, along with our current findings, suggest a consistent range of herd immunity levels across different regions of Ethiopia. These seroconversion rates are below the FAO-WOAH recommended threshold of 80% herd immunity [40]. This shortfall may be due to logistical challenges in vaccination efforts, such as inadequate cold chain management, poor vaccine handling, and distribution practices, as well as insufficient awareness and communication during vaccination campaigns.

However, a notably higher seroconversion rate of 93.9% was reported by Yirga et al. [41] in the Metema district of northwest Ethiopia. This exceptional level of herd immunity was achieved through good vaccine management practices, including strict adherence to cold chain protocols and effective vaccination delivery. The success in Metema demonstrates that with proper vaccine quality control, cold chain maintenance, and effective vaccination delivery, higher seroconversion rates are attainable.

To address the low seroconversion rates in other parts of the country, adopting the strategies used in Metema could be highly beneficial. This would involve improving cold chain management to ensure vaccine potency, enhancing training for vaccination personnel, and increasing awareness among pastoralists about the importance of adhering to vaccination schedules. By replicating the best practices observed in Metema, other regions could potentially improve their herd immunity levels, thereby enhancing the overall effectiveness of PPR vaccination campaigns in Ethiopia.

Our retrospective data analysis identified 53 outbreak reports from the Borena zone over the past five years. Despite Ethiopia’s ambitious goal of eradicating PPR by 2027, ahead of the global target of 2030 [17], these outbreaks highlight gaps in the effectiveness of current control strategies. To meet the 2027 target, Ethiopia should have transitioned from Phase Two (eradication) to Phase Three (accreditation). However, this has not occurred, and the country continues to experience PPR outbreaks. From 2018 to 2022, a total of 10,000 vaccine doses were deployed to manage PPRV in the Borena Zone, which has an at-risk animal population of 397,189. The low vaccination coverage relative to the size of the at-risk population, combined with inadequate seroconversion rates that fail to ensure sufficient herd immunity, may contribute to the high number of observed outbreaks. This suggests a need to critically review and strengthen Ethiopia’s PPR eradication measures, particularly focusing on improving diagnostics, surveillance, and vaccination protocols.

The analysis also showed that PPR outbreaks occur throughout the year, with a peak during the dry season. This pattern is consistent with findings by Alemu [11], Senbeto [27], and Abraham et al. [9], who noted increased disease incidence due to animal movement in search of resources and weakened resistance from poor nutrition. To address these seasonal outbreaks, vaccination campaigns should be better timed to maximize their effectiveness. Additionally, vaccination efforts should be supported by other PPR eradication strategies outlined in the global PPR eradication plan.

Additionally, a disproportionately high number of PPR outbreaks were reported in the districts of Arero and Dhas. These areas face significant challenges related to accessibility, which complicates the implementation of effective vaccination campaigns. To address these issues, it is essential to assess and address accessibility barriers to prevent these regions from becoming persistent focal points for the disease. Improving infrastructure and logistical support in these hard-to-reach areas will be crucial for enhancing vaccination coverage and controlling future outbreaks.

Conclusions

The study reveals a high seroprevalence of PPR in unvaccinated sheep and goats in the Borena zone and inadequate herd immunity in vaccinated animals. The high number of outbreaks reported highlight significant shortcomings in the current eradication strategies. Achieving Ethiopia’s goal of eradicating PPR by 2027 appears highly unlikely under the present approach. Therefore, a comprehensive reassessment and restructuring of the eradication plan is necessary. To meet the goal of PPR eradication, the Ethiopian government should align its strategies with the global eradication framework, which includes five key cornerstones: diagnostics, surveillance, prevention and control, the development of a regulatory framework that strengthens veterinary services, and stakeholder engagement, rather than focusing solely on vaccination.

Data availability

The datasets for this study are available on request to the corresponding author.

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Acknowledgements

The authors would like to thank Ministry of Agriculture (MOA), Yabelo Pastoral and Dryland Agriculture Research Center, Animal Health Institute (AHI) and Yabelo Regional Laboratory. We would like to thank also Dr. Dereje Teshome, Mr. Beshir Hussein and Dr. Golo Dabasa.

Funding

This study received financial support from Addis Ababa University under Thematic Project Number: LT/PY-114/2022. The funder had no role in the conception, design of the study, data collection, analysis, and interpretation of the data reported in this manuscript.

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Authors and Affiliations

  1. Yabello Pastoral and Dryland Agriculture Research Center, Oromia Agricultural Research Institute, P.O. Box 85, Yabello, Ethiopia

    Adem Kumbe

  2. College of Veterinary Medicine and Agriculture, Addis Ababa University, P.O. Box 34, Bishoftu, Ethiopia

    Haileleul Negussie, Yitbarek Getachew, Sisay Girma, Hika Waktole & Samson Leta

  3. Animal and Human Health Program, International Livestock Research Institute, Addis Ababa, Ethiopia

    Biruk Alemu & Gezahagn Alemayehu

  4. Animal Health Institute, P.O. Box 04, Sebeta, Ethiopia

    Demeke Sibhatu & Kemal Emiyu

  5. Laboratory of Host-Pathogen Interaction in Livestock, Division of Animal and Human Health Engineering, Department of Biosystems, KU Leuven, Leuven, 3001, Belgium

    Samson Leta

  6. Institute for Microbiology, University of Veterinary Medicine Hannover, Hannover, Germany

    Sisay Girma

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  1. Adem Kumbe
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  2. Haileleul Negussie
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Contributions

AK, YG, HN, SL, HW contributed to the development of the proposal, design, collecting of field and lab data, writing up, and revising of the paper. GA, DS, SG, BA, KE and SL contributed in the laboratory, manuscript edition, and reviews. The final manuscript was read and approved by all authors.

Corresponding author

Correspondence to Samson Leta.

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Ethical approval

The study was carried out in accordance with the Animal Research Ethics Review Committee of the College of Veterinary Medicine and Agriculture of Addis Ababa University and ethical approval for the study was ensured by the approval certificate with reference number VM/ERC/04/15/2022. All methods were performed by skilled experts with relevant guidelines and regulation listed by ethical committee. Safety, welfare and wellbeing of the study animals were secured during the study. Informed consent for study participation was obtained from all animal owners before blood sample collection.

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Not applicable.

Competing interests

The authors declare no competing interests.

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Kumbe, A., Negussie, H., Getachew, Y. et al. Epidemiology of peste des petits ruminants in selected districts of Borena zone, Ethiopia. BMC Vet Res 20, 451 (2024). https://doi.org/10.1186/s12917-024-04312-4

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BMC Veterinary Research

ISSN: 1746-6148

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