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Herd and animal level seroprevalence and associated risk factors of Leptospira interrogans sensu lato serovar Hardjo in cattle in southwest Ethiopia

BMC Veterinary Research volume 20, Article number: 553 (2024) Cite this article

Abstract

Leptospirosis is a significant zoonotic disease that causes high economic losses in cattle production due to its association with abortions, stillbirths, infertility, and reduced milk yields. However, the epidemiology of bovine leptospirosis in Ethiopia is poorly understood. From October 2020 to October 2021, a cross-sectional study was conducted to investigate the seroprevalence of serovar Hardjo in cattle in southwest Ethiopia, as well as the associated risk factors. To test for the existence of L. Hardjo antibodies, blood samples were taken from 461 cattle. Indirect ELISA was used to identify the presence of antibodies against L. Hardjo in sera samples. We conducted a multivariable random-effect logistic regression analysis to identify potential risk factors associated with L. Hardjo seropositivity. An overall L. Hardjo seroprevalence of 24.7% (95% CI: 20.2–48.8) and 53.5% (95% CI: 45.7–90.5) was recorded at the animal level and the herd level, respectively, in the study areas. This study revealed six factors influencing L. Hardjo seropositivity in cattle herds. Large herds had twice the odds of seropositivity (OR = 2.0, 95% CI: 1.1–3.8) compared to small herds. Co-grazing cattle exhibited higher odds (OR = 2.2, 95% CI: 1.2–4.1) of seropositivity. Extensive management systems significantly increased the odds (OR = 10.3, 95% CI: 1.7–61.8) compared to semi-intensive systems. Highland cattle had higher odds (OR = 3.7, 95% CI: 1.4–10.3) than lowland cattle. Older cattle (OR = 4.6, 95% CI: 2.4–8.9) were more likely to be seropositive. At the herd level, extensive management (OR = 2.8, 95% CI: 1.3–5.8) and large herds (OR = 2.5, 95% CI: 1.3–4.7) increased the risk of seropositivity. Herds with sheep/goats (OR = 2.3, 95% CI: 1.3–4.1) were also at higher risk, highlighting significant L. Hardjo seropositivity risk factors in cattle herds. The study findings showed that leptospirosis was highly prevalent across the study areas. As a result, use proper management, raise zoonotic awareness for leptospirosis, and conduct molecular bovine leptospirosis research in study areas were recommended.

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Introduction

Leptospirosis is a globally distributed and emerging zoonotic disease caused by spirochete bacteria of the genus Leptospira, which affects a wide range of mammals, including livestock such as cattle [1, 2]. More than 300 serovars of pathogenic Leptospira species have been recognized according to serological classification [3]. Among the numerous serovars of Leptospira, Leptospira serovar Hardjo is of particular concern due to its role in causing reproductive disorders, such as abortions and reduced fertility, leading to economic losses in the livestock industry [4,5,6]. Cattle have been adapted as a maintenance or reservoir host for Leptospira interrogans serovar sensu lato serovar Hardjo, leading to subclinical infection in the majority of cases [7]. Leptospirosis is a neglected disease that causes serious illness among farmers, farm workers, and other individuals employed in the livestock sector [2, 8, 9]. Even though maintenance hosts and the serovars they harbor may vary across the globe, a fundamental knowledge of serovars and their maintenance hosts is necessary to comprehend the epidemiology of leptospirosis in a particular area [10].

Epidemiological information on leptospirosis is the most important step in implementing and designing interventions for reducing the risk of the disease in cattle [11, 12]. The occurrence of L. Hardjo in cattle is influenced by factors related to management, host, and environment [13]. Age of cattle, herd size, common grazing, the introduction of new cattle, mixing of cattle with pigs or sheep and the use of the infected bulls are the risk factors of leptospirosis in cattle [14, 15]. Infected or carrier animals or contaminated objects can spread the disease through direct or indirect contact. Urine, aborted materials, birth products, normal fetuses, and vaginal discharges are the main source of leptospirosis in cattle [11, 16].

The availability of samples and the stage of the disease have an impact on leptospirosis diagnosis. Serology is the most often used diagnostic approach for leptospirosis, and it aids in the study of the disease’s epidemiology [17,18,19]. ELISA is a widely utilized serological approach in which antigen-antibody reactions occur and an enzyme report system monitors the analysis of concern [20]. This method demonstrates the potential as a viable alternative to MAT, given that numerous laboratories in tropical regions possess the necessary infrastructure for conducting this test [21, 22]. Notably, ELISA exhibits superior sensitivity compared to MAT, particularly during the acute phase, making it suitable for the early diagnosis of leptospirosis [23]. Unlike MAT, ELISA can distinguish between immunoglobulin classes, allowing it to detect infections in their early stages as well as older ones [17, 24].

Bovine leptospirosis is a significant concern in Sudan, Uganda, Kenya, Eritrea, and Somalia. The prevalence and serovar distribution vary across these countries, but the impact of disease on cattle health and the potential for zoonotic transmission make it a priority for research, control, and public health efforts [25, 26]. In Ethiopia, serological studies on leptospirosis in cattle have been conducted in Jimma town and in various agro-ecological zones of southwest Ethiopia [27, 28]. These studies have indicated that leptospirosis has a significant impact on cattle reproductive efficiency, and the disease is the leading cause of cattle abortion in the country. Another study has also identified leptospirosis as one of the five zoonotic diseases that are most urgently needed to be controlled in the country [29]. However, these works have been limited to addressing the epidemiology of leptospirosis in rural areas where people live in close contact with animals, particularly in southwest Ethiopia. Southwest Ethiopia has been known to be where large forest exists in the country and the areas have a warm, high rainfall, and humid environment. Thus, the areas are favorable for the occurrence and transmission of leptospirosis among cattle herds and humans [13, 30]. To control the disease and design the control strategy, it is essential to know the epidemiology of L. Hardjo in areas. Therefore, the objective of this study was to ascertain the seroprevalence of serovar Hardjo in cattle in southwest Ethiopia and the related risk factors.

Materials and methods

Ethics and consent

This study was conducted in accordance with the principles of the National Institutes of Health Guide for the Care and Use of Laboratory Animals and was approved by the Institutional Animal Care and Use Committee at Ethiopian Institute of Agricultural Research (EIAR). All efforts were made to minimize animal suffering and to reduce the number of animals used. The animals used in this study were obtained from Semen Bench, Shei Bench, Sheko, Meinet Shasha, and Meinet Goldiya districts. Prior to their use in the study, written informed consent was obtained from the owners of the animals. The consent form explained the purpose of the study, the procedures that would be performed on the animals, and any potential risks or discomforts associated with the study. The owners were also informed that they had the right to withdraw their consent at any time and that their animals would be provided with appropriate care and treatment regardless of their decision. In addition to obtaining informed consent from the owners, all animals were cared for in accordance with established guidelines for animal care and use.

Study areas

Five districts in the Bench-Sheko and West Omo zones of southwest Ethiopia where the study was carried out were Semen Bench, Shei Bench, Sheko, Meinet Shasha, and Meinet Goldiya. These areas can be found between latitudes 5° 52’ 48” N and 7° 12’ 36” N and longitude 34° 52’ 48” E and 36° 8’ 24” (Fig. 1). The zones are situated between 500 and 3000 m above sea level (m asl). The zones’ annual temperatures range from 15.1ºC to 27ºC, and they receive 400–2000 mm of rain on average each year. According to Ethiopian agro-ecology [31], the zones are divided as lowland (1500 m asl), mid-altitude (1500–2300 m asl), and highland (> 2300 m asl). Thus, selected districts were divided into lowland (Meinet Shasha), mid-altitude (Sheko and Shei Bench) and highland (Semen Bench and Meinet Goldiya) agro-ecology zones. In the research areas were 71,047 goats, 73,384 sheep and 1,596,803 cattle [32]. Local cattle breeds (Zebu and Sheko breed) are the most prevalent, followed by a few Holstein-Friesian crosses. The study area has extensive (crop-livestock production) and semi-intensive (urban production) management methods.

Fig. 1
figure 1

Map showing study districts in southwest Ethiopia

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Study design and population

In the study conducted from October 2020 to October 2021, we employed a cross-sectional study design to determine the seroprevalence and associated risk factors of serovar Hardjo in cattle. The study population was cattle with age of six months and above that was kept in Semen Bench, Shei Bench, Sheko, Meinet Goldiya, and Meinet Shasha districts of Bench-Sheko and West Omo zones. Cattle in various age groups, body conditions, breeds, agro-ecologies, and management system made up the study population.

Sampling procedure and sample size determination

A multistage sampling method was used, at each stage, sampling units were selected randomly [33]. The study zones were selected purposively due to the zones having a huge cattle population and the zones have high rainfall and a humid environment which is suitable for leptospirosis occurrence and transmission. However, districts, kebeles (the small administrative unit in the district), villages, and herds were selected by a proportional simple random sampling technique. The sampling frames of sampling units were taken from the respective sampling stages. Five districts namely, Semen Bench, Shei Bench, Sheko, Meinet Shasha, and Meinet Goldiya were selected by lottery method from a total of fifteen districts in the zones. Similarly, twenty-eight kebeles were selected from these districts by a simple random sampling method. Based on the number of villages in the kebeles, a simple random selection approach was used to choose 84 villages from those kebeles. A proportional simple random sampling technique was employed to select a total of 202 herds. Similarly, herds were chosen from the selected villages using a simple random sampling approach, which involved a lottery method. The number of animals sampled from each herd could vary depending on the cattle population of the herd. Since no previous study had been conducted on leptospirosis in cattle in the study areas, we determined the sample size for this study by applying Thrusfield [34], formula. The calculation was based on a desired absolute precision of 5% and a 95% confidence interval (CI) to estimate a prevalence of 50%. Consequently, 384 cattle were needed for this study. To account for variations among clusters, the sample size was adjusted by multiplying it by the design effect (D), using the formula D = ρ (n − 1) + 1, where ‘n’ represents the average number of cattle in a cluster (2). An intra-cluster correlation value of ρ = 0.20 was obtained for infection disease [35], resulting in a calculated design effect (D) of 1.20. In this study, the design effect of 1.20 was applied to the original sample size of 384, resulting in a total of 461 cattle being used in this study.

Blood sample collection

Using sterilized needles and plain vacutainer containers, blood samples of around ten milliliters were taken from each cattle’s jugular vein. The tubes were then labeled with a unique identification number of cattle and kept in a slant position overnight at room temperature and then the sera were separated. The codes for the animals were transferred to the cryovials into which the serum was decanted, and sera samples were stored at -200C [36] in the Mizan Regional Veterinary Laboratory until they were brought to the National Veterinary Institute, Bishoftu, using an icebox for laboratory analysis.

Serological test procedure

The PrioCHECK® L. Hardjo Ab (PrioCHECK®, Lelystad, Netherlands) is an indirect ELISA designed to identify antibodies against serovar Hardjo in cattle serum [37] and the manufacturer’s guidelines were followed when preparing and testing serum samples. First, 100 µl of ELISA buffer was dispensed into the test plate’s wells A1 and B1 (blacks), followed by 90 µl of ELISA buffer into wells C1 through H1. Then, in wells C1 and D1, 10 µl of 1:20 diluted reference serum1 (positive control) was dispensed. In wells E1 and F1, ten microliters of 1:20 diluted reference serum2 (negative control) were dispensed. In wells G1 and H1, 10 µl of 1:20 diluted reference serum3 (weak positive control) was dispensed. The remaining wells were then dispensed with 90 µl of ELISA buffer. In each of these wells, ten microliters of 1:20 diluted test sera were dispensed, resulting in a final serum dilution of 1:200. Titration of serum samples was accomplished by doing a two-fold serial dilution in dilution buffer. The test plate was sealed, lightly shaken, and incubated at 37ºC for 60 min. The content was discarded after one hour, and the test plate was rinsed six times with washing solution before being dried again. The test plate was then covered and incubated for one hour at 37ºC with 100 µl of the diluted conjugate dispensed in all wells. A washing solution was used to wash the test plate six times after 60 min. All wells received 100 µl of the chromogen (TMB) substrate, which was incubated for 15 min at 220C. The wells were then filled with 100 µl of stop solution, and the test plate was stirred to mix the contents of the wells. Within 15 min of terminating the color development, the color change was detected and the optical density (OD) of the wells was measured at 450 nm. The mean OD450 value of the blanks (wells A1 and B1) was computed, as well as the corrected OD450 value of all samples. According to Ko et al. [38] the formula below, the percentage positivity (PP) of the reference samples 2, 3, and test samples were calculated.

$${\rm PP} = \:\left[\frac{\text{c}\text{o}\text{r}\text{r}\text{e}\text{c}\text{t}\text{e}\text{d}\:\text{O}\text{D}450\:\text{t}\text{e}\text{s}\text{t}\:\text{s}\text{a}\text{m}\text{p}\text{l}\text{e}}{\text{c}\text{o}\text{r}\text{r}\text{e}\text{c}\text{t}\text{e}\text{d}\:\text{O}\text{D}450\:\text{r}\text{e}\text{f}\text{e}\text{r}\text{e}\text{n}\text{c}\text{e}\:\text{s}\text{e}\text{r}\text{u}\text{m}1}\right] \times 100$$

For specific antibodies to L. Hardjo, serum samples with PP of 20%, 20–40%, and > 45% were termed negative, inconclusive (antibodies may be present), and positive, respectively. Sera samples with inconclusive antibody titers were retested, and if the results were still inconclusive, they were classified as negative in the data analysis.

Data collection

A total of 461 cattle were selected and their owners were contacted to acquire information on individual animals, management and environmental related factors. These factors were recorded on the data collection formats. Data was recorded on various aspects of individual animals, including parity, breed, age, pregnancy status, and a history of abortion. Furthermore, aspects such as herd size, species composition, the introduction of new animals, agro-ecology, livestock management, co-grazing practices, water sources, feed storage, and wildlife contact were also noted. According to how well the ribs and vertebral spinous processes looked, the body condition score of cattle was categorized as poor (scores 1 and 2), medium (scores 3), and good (scores 4 and 5) [39]. Small (> 15 heads of cattle), medium (15–30 heads of cattle), and large (> 30 heads of cattle) were the three categories used to categorize herd sizes. According to Richard [40] criteria, the livestock management system was classified as either extensive or semi-intensive. Since the age at first calving for cattle in tropical conditions was thought to be between two and three years [41], the age of cattle was divided into three categories: <3, 3–6, and > 6 years. Similar to this, cattle parity was divided into three categories: nulliparous (zero parity), monoparous (one parity), and pluriparous (two parities or more) [42]. The term “abortion” refers to the termination of a pregnancy between forty-five and two hundred sixty days gestation [43, 44].

Data management and analysis

The laboratory data was recorded, saved, and analyzed using STATA version 14.0 for Windows (Stata Corp. College Station, TX, USA) after being imported into Microsoft® Excel for Windows 2010. The number of positive animals divided by the total number of animals tested was used to calculate the seroprevalence of L. Hardjo at the animal level. Number of positive herds containing at least one infected cattle divided by the total number of sampled herds was used to determined seroprevalence of L. Hardjo at the herd level. The 95% confidence interval (CI) for each seroprevalence was calculated using Epitool’s binomial exact method. Seroprevalence at the animal level was obtained after adjusting for sample weight. Associations between L. Hardjo seropositivity and explanatory variables were analysed using a logistic regression model for both positive animals and herds. In this analysis, variables such as parity, breed, age, a history of abortion, herd size, species composition, the introduction of new animals, agro-ecology, livestock management, type of grazing, water source, feed storage, pregnancy status and accessibility to wild animals were taken into account. The variables that have a P ≤ 0.25 in the univariable analyses were further examined in a mulitvariable analysis. In this analysis we have added village and herd as random effects in the herd and individual animal models, respectively. To test for multicollinearity in the final multivariable models, generalized variable inflation factors (GVIF) were used. Variables having a GVIF^ (1/2*Df) of greater than 2 were eliminated. With respect to the variables in the final model, a test for biologically significant two-way interactions was also conducted. Modeling the effects of possible risk variables for L. Hardjo seropositivity was done using multivariable mixed effects logistic regression analysis (herd and individual animal). The components in the overall model that were not significant at a p-value of less than or equal to 0.05 were removed using the backward elimination procedure. The Hosmer-Lemeshow test was used to determine the model fit and variables that were maintained in the model after being determined to be significant at P ≤ 0.05. When a covariate changed the estimated risks OR by more than 25% [33] in the study, it was regarded as a confounder and added to the model. The probability level of 0.05 was set for a significant difference.

Results

Animal-level and herd-level seroprevalence of serovar Hardjo

Out of a total of 461 examined cattle, 24.7% of them were positive for L. Hardjo antibody by using indirect ELISA at the individual animal level. The highest (61.4%) and lowest (17.5%) seroprevalence of L. Hardjo was recorded in Semen Bench and Sheko districts at the individual animal level, respectively. However, the highest (61.4%) and lowest (35.5%) herd-level seroprevalence of L. Hardjo was recorded in Sheko and Meinet Goldiya districts respectively with an overall of 53.5% seroprevalence. A statistically significant difference (P < 0.05) was observed among study areas both at herd-level and animal-level (Table 1).

Table 1 Distribution of L. Hardjo seroprevalence at animal-level and herd-level in cattle of southwest Ethiopia
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Herd-level potential risk factors of serovar Hardjo

A higher seroprevalence of L. Hardjo was recorded in extensive (55.0%) than semi-intensive (47.6%) management systems and the difference was statistically significant (P < 0.05) in univariable and multivariable analysis. Furthermore, the multivariable logistic regression model’s results showed that the size of the herd and the species composition had a significant (P < 0.05) impact on the seroprevalence of L. Hardjo in the cattle herd. However, agro-ecology, co-grazing, water source, accessibility to wild animals as well as the new cattle introduced were not substantially associated (P > 0.05) with herd-level seroprevalence of L. Hardjo (Table 2). No evidence of multicollinearity or significant interactions between the variables was found. A Hosmer-Lemeshow goodness-of-fit value (χ2 = 3.55, P = 0.615) indicated that the model adequately explained the data.

Table 2 Potential L. Hardjo risk factors at the herd level in cattle in southwest Ethiopia using both univariate and multivariate methods
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Animal-level potential risk factors of serovar Hardjo

The highest (27.1%) seroprevalence of L. Hardjo was recorded in cattle from highland areas. The result of the univariable analysis revealed that agro-ecology was related (P < 0.05) with seropositivity of L. Hardjo in cattle. Cattle from the highland had 3.9 times more odds of L. Hardjo seropositivity than those in the lowland. Similarly, a statistically significant difference (P < 0.05) was observed between the seroprevalence of L. Hardjo and the management system with the cattle managed under extensive management was 7.9 times higher odds of L. Hardjo seropositivity than those kept under a sem-intensive management system. In the present result age was associated (P < 0.05) with seroprevalence of L. Hardjo. Cattle aged greater than 6 and 3–6 years were 4.6 and 2.0 times respectively higher odds of L. Hardjo seropositivity compared to cattle aged less than 3 years. Moreover, higher odds of L. Hardjo seropositivity were observed in monoparous and pluriparous cattle than in nulliparous cattle with a statistically significant difference (P < 0.05). Similarly, a statistically significant difference (P < 0.05) was observed between the seropositivity of L. Hardjo and the history of abortion. Cattle with a history of abortion had higher odds of L. Hardjo seropositivity than those which did not. The univariable analysis did not show any significant difference (P > 0.05) between seropositivity of L. Hardjo and variables such as herd size, co-grazing, water source, feed storage, accessibility to wild animals, the introduction of new animals, breed, body condition score and pregnancy status (Table 3).

Table 3 Single-variable logistic regression analysis of assumed risk factors of L. Hardjo seropositivity in cattle of southwest Ethiopia
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Multivariable logistic regression analysis has shown that age, agro-ecology, management system, herd size, and co-grazing were related with the seroprevalence of L. Hardjo in cattle (Table 4). No significant difference (P < 0.05) was found among the variables in terms of interaction and multicollinearity. The model successfully fit the data, as demonstrated by Hosmer and Lemeshow’s test (χ2 = 5.94, P = 0.547).

Table 4 Multivariable logistic regression analysis of possible risk factors of L. Hardjo seropositivity in cattle of southwest Ethiopia
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Discussion

This study provided preliminary serological evidence of Leptospira interrogans sensu lato serovar Hardjo in cattle for the first time in the studied area. Even though L. Hardjo infection in adult cattle can be asymptomatic, it also can result in abortion, stillbirth, infertility, and reduced milk yield, causing high economic losses [5, 6]. This study can help in the application of management techniques to control and prevent leptospirosis in cattle. It provided sero-epidemiological information on the occurrence of Leptospira infection in the studied areas. The current study result revealed 24.7% and 53.5% seroprevalence of L. Hardjo at animal-level and herd-level, respectively. Moreover, the seroprevalence of L. Hardjo was influenced by age, agro-ecology, herd size, management system, and co-grazing, at the animal level. Similarly, herd size, management system, and species composition have an impact on the seroprevalence of L. Hardjo at the herd level.

In the present study, an overall 24.7% seroprevalence of L. Hardjo was documented at the animal level in the study areas. This high seroprevalence of L. Hardjo in study areas could be due to the fact that vaccination against leptospirosis is not used in the areas and even not in the country. Cattle that have been naturally exposed to Leptospira spp serovar Hardjo had circulating antibodies. This is in good agreement with the finding of Desa et al. [27], who found a 24.5% seroprevalence of L. Hardjo in Jimma town, Ethiopia. A similar level of seroprevalence of L. Hardjo was also reported by Balamurugan et al. [45] 23.7% in India, Ismail et al. [46] 26.3% in Jordan, Schoonman and Swai [47] 30.3% in Tanzania, Gamage et al. [48] 20.3% in Sri Lanka and Taddei et al. [49] 19.3% in Colombia. However, higher seroprevalence than the current result was reported by Joel et al. [50] 88.2% in Mexico, Natarajaseenivasan et al. [51] 87% in India, Parver et al. [52] 42.3% in Pakistan, and 81.7% in Malaysia [53]. This result was higher than the previous studies conducted in other countries, for instance, 13.90% in Madagascar [54], 13.0% in India [55], 8.4% in Iran [56] and 14.2% in Malaysia [57]. The difference in seroprevalence of L. Hardjo in various study areas could be due to the variation in agro-ecology, management system, reservoirs host, and animal breed.

Vaccine strategies for leptospirosis in cattle can vary significantly between countries due to variations in disease prevalence and the specific Leptospira serovars present [58]. Countries experiencing higher leptospirosis prevalence often adopt more targeted vaccination approaches, taking into account the regional variations in serovars. The selection of the appropriate serovar is crucial and is influenced by geographic differences. Local factors such as climate conditions and reservoir hosts play a significant role in determining disease prevalence [59, 60]. Tailoring vaccines for leptospirosis in cattle to specific countries is essential to ensure that they address prevalent serovars and regional epidemiology. Customizing strategies for each country is vital due to the diverse challenges and characteristics they present [61, 62].

Herd-level seroprevalence (53.5%) of L. Hardjo recorded in the present study concurs well with the result of Desa et al. [27] and Schafbauer et al. [54], who stated seroprevalence of 74.0% in Jimma town, Ethiopia and 74% in Madagascar, respectively. Nevertheless, the seroprevalence noted in this finding was lower than the findings of the value by Campos et al. [63] 100% in Brazil, Ruano et al. [64] 98.2% in Ecuador, and Ismail et al. [46] 92.3% in Jordan. On the other hand, the current result was higher than seroprevalence 31.3% reported in Algeria [65] and 28.6% in Thailand [66]. Cattle herds that included sheep and/or goats were two times (OR = 2.3) more likely to have L. Hardjo seropositivity than cattle-only herds. In agreement with the finding of Schoonman and Swai [47] and Yupiana et al. [67] who demonstrated that the presence of sheep and/or goats in cattle herds was a risk factor for L. Hardjo. This may be due to sheep and goats being reservoir hosts for serovar Hardjo and serve as a source by this serovar infection [5, 68]. Moreover, the interspecies transmission of leptospirosis may also occur in herds [69].

In the present study, the highest (27.1%) seroprevalence of L. Hardjo was recorded in cattle from highland followed by midland (26.9%) and lowland (8.8%). Interestingly, the variation in agro-ecologies was strongly related to the presence of serovar L. Hardjo in cattle. In comparison to cattle from the lowland, highland cattle were around four times (OR = 3.7) more likely to be seropositivity with L. Hardjo. This could be due to the total amount of rainfall that these agro-ecologies receive. Districts with highland agro-ecologies often had greater yearly rainfall than districts with midland and lowland agro-ecologies. Because of the moist climate, this most likely helps Leptospira persist in the environment. High rainfall has been identified to potentially create the right conditions for Leptospira to persist for lengthy durations, assuring a steady supply of infection for susceptible populations [70, 71]. The highest seroprevalence of L. Hardjo was observed in Semen Bench (61.4%) and Meinet Goldiya (80.3%) districts at animal-level and herd-level respectively with significant differences (P < 0.05). It was noted that the distribution of Leptospira spp depends on the geographical location, and environmental and socioeconomic characteristics [72].

The management system was significantly associated (P < 0.05) with the seropositivity of L. Hardjo in cattle in the present study. Cattle managed under an extensive management system were ten times (OR = 10.3) more likely to be seropositive for L. Hardjo compared to semi-intensive. This may be due to poor husbandry practices in the extensive management system, and serovar L. Hardjo-infected cattle increase the risk of contaminating the environment during co-grazing. Moreover, an extensive management system increases the probability to contact with infected or carrier animals [73]. It is also reported sharing common pasture was increase the risk of Leptospira infection transmission in cattle as has been reported in the current study and previous one [63]. Our findings are consistent with previous results from Ethiopia [27] and Thailand [66], which have shown that cattle managed under an extensive management system are associated with seropositivity for L. Hardjo. Likewise, the herd-level seroprevalence of L. Hardjo was also associated with a management system with a herd managed under an extensive management system was more odds of L. Hardjo seropositivity.

According to the current research, cattle were more likely to be seropositive for L. Hardjo as they aged. The older cattle (> 6 years) were about five times more likely to have L. Hardjo seropositivity than the younger ones (< 3 years) (OR = 4.6). This may be due to the prolonged exposure of older cattle to leptospirosis, their poor immune response, and the persistence of antibodies in cattle [11, 74, 75]. These results support previous findings [27, 76] that have stated age as an important risk factor associated with L. Hardjo seropositivity in cattle in Ethiopia and Australia. These results also align with the findings of Talebkhan et al. [77], Hassanpour et al. [78], Rajala et al. [79], and Kelly et al. [80], who have indicated that increasing age is associated with an increased risk of seropositivity of L. Hardjo in cattle.

In this study cattle utilizing, co-grazing had more odds (OR = 2.2) of showing Hardjo seropositivity compared to those not using co-grazing. The co-grazing maybe increases the frequency of contact among the cattle, resulting in favorable conditions for the transmission of L. Hardjo infection in the herd. This is in agreement with the finding of Robi et al. [81], who reported that co-grazing increased the risk of leptospirosis incidence in cattle. Rodents (permanent carrier) are an important source of Leptospira spp and grazing areas or water sources may get contaminated. Leptospira spp can persisted in the environment from hours to 193 days [82]. The persistence of this pathogen in the environment can affect the indirect transmission of leptospirosis [83] and common grazing may increase the direct transmission of leptospirosis among cattle [84]. This study showed that common grazing was an important risk factor associated with Leptospira seropositivity in cattle, which is agrees with the findings of Mthiwa et al. [26] in Kenya and Rajala et al. [79] in low-income countries.

This study also demonstrated a strong association between herd size and the seropositivity of L. Hardjo in cattle. The odds of L. Hardjo seropositivity in large herd sizes were about two times higher than those from small herd sizes. This may be associated with an increased risk of contact, spread, the persistence of leptospirosis, and increased contact in large size herds [85, 86]. In agreement with this result, several authors in different countries [27, 56, 64, 87] have also reported a higher seropositivity of L. Hardjo in large-sized herds. Similarly, other authors, like Mthiwa et al. [26], Oliveira et al. [88] and Ryan et al. [89] also stated that there was a positive association between herd size and seropositivity of Leptospira serovar Hardjo in cattle. Moreover, herd size was also a risk factor for the occurrence of L. Hardjo seropositivity at the herd level with the large size herd having about three times (OR = 2.5) more odds of L. Hardjo seropositivity compared to small size herd. This may be because a large herd size increases the risk of contact with the pathogen, rendering conditions for an easier transmission of the infection and persistence of Leptospira for longer periods in the herd [85, 90]. Our result agrees with the previous findings [89, 91, 92] which indicated that herd size was associated with seropositivity of serovar Hardjo at the herd level.

In the present study, the history of abortion was considerably related to seroprevalence of Hardjo in female cattle, with cattle that had a history of abortion having two times (OR = 2.1) more probability to possess to be seropositive to Hardjo than those had no history of abortion. This corroborates with the finding of Mthiwa et al. [26] in Kenya and also confirms our previous findings [80, 93], stating that leptospirosis is one of the most important causes of cattle abortion in Ethiopia. Aborting cattle maintained in the herds can also act as a source of infection in future parturitions through reproduction track discharge [94].

The limitation of this study is its exclusive focus on detecting Leptospira serovar Hardjo exposure in cattle through ELISA. We recommend conducting further investigations to identify potential, overlooked serovars in cattle populations in southwest Ethiopia that may be prevalent. Cattle that testing positive for antibodies does not necessarily signify that they were infected at the time of sampling. This was also another limitation of this study. Thus, Leptospira isolation and molecular characterization should be conducted for the confirmation of the presence of infecting serovar. Moreover, the current study’s cross-section study design does not allow to access how these infections’ incidence patterns would change over time.

Conclusion

Antibodies to L. Hardjo were found to be high at both the animal and herd level in southwest Ethiopia, according to the findings of this study. Cattle from large-sized herds, co-grazing, an extensive management system, highland areas, as well as older cattle, were risk factors associated with seropositivity to L. Hardjo at the animal level. Leptospira Hardjo seropositivity was associated with an extensive management system, a large herd size, and the presence of sheep and/or goats in the herd at the herd level. This study demonstrated the widespread prevalence of leptospirosis among cattle in the studied areas. As a result, this study suggests that a suitable management approach should be developed, as well as raising awareness of the zoonotic significance of leptospirosis. In addition, further research should be undertaken on the molecular epidemiology of bovine leptospirosis in study areas.

Data availability

The corresponding author will provide the data used in the current study upon reasonable request.

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Acknowledgements

We appreciate the financial assistance provided by the Ethiopian Institute of Agricultural Research (EIAR). The National Veterinary Institute (NVI) and Mizan regional veterinary laboratory provided logistic support to the authors. In addition, we appreciate the assistance provided by the Bench-Sheko and West Omo zones offices during fieldwork.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not for profit sectors.

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  1. Ethiopian Institute of Agricultural Research, Tepi Agricultural Research Center, P.O Box: 34, Tepi, Ethiopia

    Dereje Tulu Robi & Melkam Aleme

  2. Ethiopian Institute of Agricultural Research, Holeta Agricultural Research Center, P.O. Box 2003, Holeta, Ethiopia

    Ararsa Bogale & Beksisa Urge

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Contributions

1. Dereje Tulu Robi: Conceived and designed the study. 2. Dereje Tulu Robi, Ararsa Bogale: Analyzed and interpreted the data. 3. Dereje Tulu Robi: Writing – original draft. 4. Dereje Tulu Robi, Ararsa Bogale, Melkam Aleme: Performed the field investigation. 5. Beksisa Urge, project administration and supervision.

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Correspondence to Dereje Tulu Robi.

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The Ethiopian Institute of Agricultural Research (EIAR) carried out all techniques in accordance with experimental standards and procedures that were approved by the ethical committee of the EIAR animal health research program (reference number EIAR-2662/2010) regarding animal welfare and ethical issues. These procedures were in line with international standards for animal welfare. This study was conducted in accordance with the principles of the National Institutes of Health Guide for the Care and Use of Laboratory Animals and was approved by the Institutional Animal Care and Use Committee at the Ethiopian Institute of Agricultural Research (EIAR).

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The authors declare no competing interests.

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Robi, D.T., Bogale, A., Aleme, M. et al. Herd and animal level seroprevalence and associated risk factors of Leptospira interrogans sensu lato serovar Hardjo in cattle in southwest Ethiopia. BMC Vet Res 20, 553 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12917-024-04418-9

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12917-024-04418-9

Keywords

BMC Veterinary Research

ISSN: 1746-6148

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