Prevalence, genetic diversity and co-infection patterns of selected tick-borne haemoparasites infecting cattle in Karamoja region, northeastern Uganda
Authors: Etiang Patrick , Kamusiime Maureen , Wamala Henry , Nkamwesiga Joseph , Ainebyoona Solomon , Abizera Harriet , Kakuru Mesearch , Byaruhanga Charles , Amanyire Wilson , Mugimba Kizito Kahoza , Mayanja Maureen Nanziri , Biryomumaisho Savino , Tweyongyere Robert , Muhanguzi Dennis 
Published: November 2024

Abstract

Background:
Bovine theileriosis, babesiosis, anaplasmosis and ehrlichiosis are the most important tick-borne diseases (TBD) of cattle in Karamoja region where they constitute a major constraint to livestock health and productivity. The semi-arid region presents with factors that favor the proliferation of ticks and transmission of TBD. Few studies on the occurrence / distribution of TBD and the host-parasite interactions in the region exist. Understanding host parasite interactions paves way for the design of effective control strategies.
Methods:
Blood was randomly collected on FTA cards from 3,540 cattle spread across four districts in each of the dry (November 2022 to February 2023) and wet (July to August 2023) seasons making a total of 7,080 samples. The blood samples were screened for tick-borne protozoan and rickettsial haemoparasites (TBH) using conventional PCR, followed by Sanger sequencing of representative PCR amplicons. The prevalence of different tick-borne haemoparasites was determined as the proportion of the positive samples within the total samples screened. Logistic regression models were fit to explain the most important predictors of being positive for the screened pathogens.
Results
The overall prevalence of infection with at least one of the screened TBH was 39.2% (CI: 37.6–40.9; n = 3,540) and 39.0% (CI: 37.3–40.6; n = 3,540) in the dry and wet seasons respectively. A difference that was not statistically significant (p > 0.05). In the dry season, Amudat [72.9%; CI: 68.3–77.1; n = 420] and Kaabong [26.7%; CI: 24.4–29.0; n = 480] had the highest and the lowest overall infection rates with at least one of the screened TBHs, while in the wet season, it was Moroto [44.7%; CI: 41.8–47.7; n = 1,440] and Amudat [34.3%; CI: 29.8–39; n = 420] that had the highest and the lowest rates. The overall prevalence of infection with the individual TBH in the dry season in descending order was: - B. bigemina 11.8% (CI: 10.8–12.9), B. bovis 11.8% (CI: 10.8–12.9), A. marginale 9.2% (CI: 8.2–10.2), E. ruminantium 5.1% (CI: 4.4–5.8) and T. parva 1.3% (CI: 1.0-1.8). In the wet season, the prevalence for different TBHs was: - T. parva 22.6% (CI: 21.3–24), A. marginale 13.6% (CI: 12.5–14.8), B. bigemina 12.7% (CI: 11.6–13.8), E. ruminantium 1.4% (CI: 1.1–1.9) and B. bovis 0.3% (CI: 0.1–0.5). The prevalence of infection with the individual TBHs within districts varied in the two sample collections. In the dry season, the ranges across the study districts were: A. marginale 6.7–11.2%, E. ruminantium 2.3–7.1%, T. parva 0.1–6.0%, B. bovis 7.7–16% and B. bigemina 3.3–39%, while in the wet season, the ranges across the study districts were; A. marginale 3.1–27.9%, E. ruminantium 0.5–2.4%, T. parva 16.7–25.2%, B. bovis 0.0–0.4% and B. bigemina 6.1–18.3%. Geospatial location, increasing age, sex, overnight stay in cattle kraals and cattle breeds were significant predictors for testing positive for at least one of the TBH during the survey. The co-occurrence of B. bovis and B. bigemina (2.74%; CI: 2.23–3.33) was the most frequent and the least was for E. ruminantium and T. parva (0.14%; CI: 0.05–0.33) in the dry season. On the other hand, co-occurrence of A. marginale and E. ruminantium (1.64%; CI: 1.25–2.11) was the most frequent while that of B. bovis and E. ruminantium was the least recorded in the rain season (0%; CI: 0–0.1). Phylogenetic analyses of the selected TBH species genes revealed a high genetic similarity in the sequences of A. marginale, B. bigemina and B. bovis, and subgrouping of the obtained sequences with the previously published sequences from other parts of the world.
Conclusion:
This study demonstrates high TBH infection and co-infection rates in cattle in Karamoja region. Babesia bovis was reported for the first time infecting cattle in the region. Geospatial location, increasing age, sex, overnight stay in cattle kraals and cattle breeds were significant predictors for testing positive for at least one of the TBHs. Variations in the TBH prevalence, co-infection rates and the significance of predictors were recorded in the two season surveys. There was a high genetic similarity in the sequences of A. marginale, B. bigemina and B. bovis. This information can be used in the design of cost-effective area and season specific control strategies for combating TBDs in the region.