Geographic and climatic characteristics of Uganda

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Background Livestock are the main source of wealth for pastoralists in eastern Africa, in addition to their social and cultural functions (Onono et al., 2015). However, tick-borne diseases (TBDs) inflict substantial economic losses on livestock production and resource use, thereby impacting the livelihoods of pastoralists (Kivaria, 2006; Ocaido et al., 2009a; Marcellino et al., 2011; Kasozi et al., 2014; Laisser et al., 2015).
Losses directly attributed to TBDs include mortality, production losses, and costs of diagnosis, treatment and tick control (Kivaria, 2006; Jonsson et al., 2008; Ocaido et al., 2009a). In Tanzania, for example, the total annual national loss due to TBDs was estimated to be US $364 million, including an estimated mortality of 1.3 million cattle (Kivaria, 2006). In Uganda, 75.4% of losses in cattle were attributable to ticks and TBDs (Ocaido et al., 2009b), and the costs for controlling ticks and TBDs in cattle constituted 86% of the total disease control costs (Ocaido et al., 2009a). Tick-borne diseases also constrain the improvement of the local breeds of cattle in Africa because of the high levels of mortality in exotic (Bos taurus) and crossbred cattle (Uilenberg, 1995; Minjauw and McLeod, 2003; Muhanguzi et al., 2010b).
The most important TBDs that affect cattle in eastern Africa are theileriosis, anaplasmosis, babesiosis and ehrlichiosis (Kivaria, 2006; Gachohi et al., 2010; Kasozi et al., 2014; Laisser et al., 2015). Theileriosis is caused by parasites of the genus Theileria, which are obligate intracellular protozoa that belong to the phylum Apicomplexa, order Piroplasmida and family Theileriidae (Levine et al., 1980; Norval et al., 1992). The most pathogenic and economically important Theileria species in cattle are T. parva and T. annulata (Norval et al., 1992). Benign forms of theileriosis are caused by T. mutans, T. taurotragi and T. velifera, which occur mainly in Africa, while T. sergenti, T. buffeli and T. orientalis occur worldwide (Uilenberg, 1981). Theileria parva causes East Coast fever (ECF), Corridor disease and January disease in eastern, central and southern Africa, and is transmitted by the ticks Rhipicephalus appendiculatus, R. zambeziensis and R. duttoni (Lawrence et al., 2004a; Lawrence et al., 2004b). In eastern Africa, T. parva is transmitted between infected and susceptible cattle by R. appendiculatus. The infection causes an acute, usually fatal lymphoproliferative disease, ECF (Norval et al., 1992; Oura et al., 2011; Muhanguzi et al., 2014). The disease is more severe in exotic and crossbred cattle, but also in indigenous calves and adult cattle in endemically unstable areas (Perry and Young, 1995). Cattle often become long-term asymptomatic carriers of T. parva following treatment or spontaneous recovery, thereby maintaining the parasite population (Dolan, 1986; Kariuki et al., 1995; Kabi et al., 2014).
The genus Anaplasma (phylum Proteobacteria, order Rickettsiales, family Anaplasmataceae) contains obligate intracellular organisms that include pathogens of ruminants: Anaplasma marginale (the type species), A. marginale subsp. centrale, A. bovis and A. ovis (Dumler et al., 2001; Aubry and Geale, 2011). Anaplasma marginale subsp. centrale is usually considered a separate species and referred to as A. centrale. Also included in the genus Anaplasma are A. phagocytophilum, which infects a wide range of hosts including humans, rodents, birds, dogs and ruminants (Dumler et al., 2001; Hoar et al., 2008; Yang et al., 2013), and A. platys, which infects dogs (Dumler et al., 2001). Anaplasma marginale, a gram-negative intra-erythrocytic rickettsia, is the main cause of anaplasmosis in cattle (Theiler, 1910; Dumler et al., 2001), and is endemic across much of the globe in tropical and subtropical regions (Kocan et al., 2010). Bovine anaplasmosis is a haemolytic disease that results in considerable economic losses to both dairy and beef industries (Kocan et al., 2010). Anaplasma marginale can be transmitted biologically by ticks, mechanically by haematophagous arthropods or infected blood in fomites, and transplacentally from dams to calves (Aubry and Geale, 2011). Infected cattle often remain persistently infected (life-long carriers) regardless of the disease state (Richey and Palmer, 1990; Radostitis et al., 2007; Aubry and Geale, 2011). Although the carrier status provides immunity to clinical disease, it is a source of infection for naïve cattle (Kocan et al., 2010). All cattle are susceptible to infection, but those over two years of age exhibit severe disease with mortality risks of 29% to 49% (Aubry and Geale, 2011).
Anaplasma centrale (Theiler, 1911) is a less pathogenic organism, and is used as a live vaccine in Israel, South Africa, Australia and South America to provide a certain degree of protection against A. marginale (Aubry and Geale, 2011). In eastern Africa, A. marginale is transmitted mainly by the tick Rhipicephalus decoloratus (Chenyambuga et al., 2010; Magona et al., 2011a; Magona et al., 2011b). Previous studies in Uganda show that A. marginale is distributed in various parts of the country (Oura et al., 2004; Kabi et al., 2008; Muhanguzi et al., 2010a; Magona et al., 2011a; Magona et al., 2011b). World strains of A. marginale which vary in genotype, antigenic composition, morphology and infectivity for ticks have been identified using the major surface protein 1a (msp1α) gene of the pathogen (de la Fuente et al., 2007; Cabezas- Cruz et al., 2013; Pohl et al., 2013; Mutshembele et al., 2014; Silva et al., 2015). Anaplasma marginale surface protein 1a (MSP1a) is a model molecule for classification studies because it serves as a marker for strain identity. The molecule is both an adhesin necessary for infection of cells and an immune-reactive protein, and is also an indicator of the evolution of strain diversity (Cabezas-Cruz and de la Fuente, 2015). The genus Ehrlichia (phylum Proteobacteria, order Rickettsiales, family Anaplasmataceae) includes the obligate rickettsial intracellular pathogen E. ruminantium (formerly Cowdria ruminantium) that causes heartwater or cowdriosis in some wild, and all domestic, ruminants (Allsopp, 2010). The disease is also a potential emerging zoonosis (Allsopp et al., 2005). The genus also includes E. canis and E. chaffeensis, which mainly affect canids and humans, respectively, producing a monocytic ehrlichiosis or subclinical infections (Dumler et al., 2001). Other Ehrlichia species are E. ewingi, E. muris and E. ovina (Allsopp et al., 2004). Heartwater is severe in small ruminants, exotic breeds of cattle, and stressed or naïve local cattle (Minjauw and McLeod, 2003). The disease is endemic to all of sub-Saharan Africa and several islands in the Caribbean (Maillard and Maillard, 1998; Molia et al., 2008), where it poses a threat of spread to the American mainland (Burridge et al., 2002). Ten species of Amblyomma ticks are capable of transmitting E. ruminantium in Africa (Allsopp et al., 2004), the most important being A. variegatum and A. hebraeum (Bezuidenhout, 1987; Walker and Olwage, 1987). Amblyomma variegatum is reportedly the tick vector for heartwater in Uganda (Magona et al., 2011b; Nakao et al., 2012).

TABLE OF CONTENTS :

• DECLARATION
• ACKNOWLEDGEMENTS
• TABLE OF CONTENTS
• LIST OF FIGURES
• LIST OF TABLES
• LIST OF ABBREVIATIONS
• THESIS SUMMARY
• CHAPTER General Introduction
  • 1.1 Background
  • 1.2 Problem Statement and Justification
  • 1.3 Objectives of the study
  • 1.4 Thesis overview
  • 1.5 References
• CHAPTER Literature Review
  • 2.1 Geographic and climatic characteristics of Uganda
  • 2.2 Livestock production and management practices in Uganda
  • 2.3 Transhumant pastoralism
  • 2.4 Karamoja Region and livestock production
  • 2.5 Important tick-borne diseases of livestock in sub-Saharan Africa
    • 2.5.1 Theileriosis
      • 2.5.1.1 Aetiology
      • 2.5.1.2 Transmission
      • 2.5.1.3 Pathogenesis and clinical signs
    • 2.5.2 Anaplasmosis
      • 2.5.2.1 Aetiology
      • 2.5.2.2 Transmission
      • 2.5.2.3 Pathogenesis and clinical signs
      • 2.5.2.4 Genetic diversity of Anaplasma marginale
    • 2.5.3 Heartwater
      • 2.5.3.1 Aetiology
      • 2.5.3.2 Transmission
      • 2.5.3.3 Pathogenesis and clinical signs
      • 2.5.3.4 Carrier state
    • 2.5.4 Babesiosis
      • 2.5.4.1 Aetiology
      • 2.5.4.2 Transmission
      • 2.5.4.3 Pathogenesis, clinical signs and pathology
      • 2.5.4.4 Carrier state
  • 2.6 Epidemiology of tick-borne diseases
    • 2.6.1 Livestock-wildlife interface and tick-borne diseases
    • 2.6.2 Climatic factors, seasonal changes, vegetation and ecology
    • 2.6.3 Production system, management practices and control strategies
    • 2.6.4 Breed of cattle
    • 2.6.5 Age of cattle
    • 2.6.6 Cattle movements and population dynamics
    • 2.6.7 Physiological state
    • 2.6.8 Morphological and behavioural traits
    • 2.6.9 Endemic stability
    • 2.6.10 Co-infection with tick-borne haemoparasites
    • 2.6.11 Vector and pathogen factors
    • 2.6.12 Life cycle of ticks
  • 2.7 Participatory epidemiology
  • 2.8 Diagnosis of tick-borne diseases
    • 2.8.1 Clinical examination, the use of epidemiological information and xenodiagnosis
    • 2.8.2 Microscopic examination
    • 2.8.3 Serological methods
      • 2.8.3.1 Indirect fluorescent antibody test
      • 2.8.3.2 Enzyme-linked immunosorbent assay
      • 2.8.3.3 Card agglutination test
    • 2.8.4 DNA-based methods
      • 2.8.4.1 Isothermal amplification
      • 2.8.4.2 Conventional polymerase chain reaction (PCR)
      • 2.8.4.3 Reverse line blot hybridisation
      • 2.8.4.4 Real-time polymerase chain reaction
  • 2.9 Control of tick-borne diseases
  • 2.9.1 Tick control
  • 2.9.2 Chemotherapy and chemoprophylaxis
  • 2.9.3 Vaccination
  • 2.9.4 Animal genetics
  • 2.9.5 Integrated control
  • 2.10 References
• CHAPTER Using participatory epidemiology to investigate management options and relative importance of tick-borne diseases among transhumant Zebu cattle in Karamoja Region,
  • Uganda
  • 3.1 Abstract
  • 3.2 Introduction
  • 3.3 Materials and Methods
    • 3.3.1 Study area
    • 3.3.2 Selection of study locations
    • 3.3.3 Data collection
      • 3.3.3.1 Clearance, training and administration for the study
      • 3.3.3.2 Participatory epidemiology tools
    • 3.3.4 Statistical analyses
    • 3.4 Results
    • 3.4.1 Composition of the groups
    • 3.4.2 Grazing systems and water sources
    • 3.4.3 Cattle diseases
      • 3.4.3.1 Description of cattle diseases
      • 3.4.3.2 Most important cattle diseases as determined from pairwise ranking
      • 3.4.3.3 Matrix scoring for cattle diseases
    • 3.4.3.4 Incidence of cattle diseases
    • 3.4.4 Control of ticks and tick-borne diseases
      • 3.4.4.1 Tick control practices
      • 3.4.4.2 Drugs and drug use practices in treating TBDs
      • 3.4.4.3 Constraints to the control of ticks and TBDs
    • 3.4.5 Key informant interviews, review of surveillance data, direct observations, and clinical
  • examinations of animals
  • 3.5 Discussion
  • 3.6 Conclusions
  • 3.7 References
• CHAPTER Endemic status of tick-borne infections and tick species diversity among transhumant Zebu cattle in Karamoja Region, Uganda
  • 4.1 Abstract
  • 4.2 Introduction
  • 4.3 Materials and Methods
    • 4.3.1 Ethics approval
    • 4.3.2 Study design and sample size methodology
    • 4.3.3 Semi-structured interviews for management practices and proportional piling exercises
    • 4.3.4 Clinical examinations, field observations, and collection and identification of ticks
    • 4.3.5 Serological analysis
    • 4.3.6 Statistical analyses
  • 4.4 Results
    • 4.4.1 Management practices and age distribution of TBD cases
    • 4.4.2 Clinical findings and tick infestation
    • 4.4.3 Theileria parva and Anaplasma marginale seroprevalences and risk factors for seropositivity
  • 4.5 Discussion
  • 4.6 Conclusions
  • 4.7 References
• CHAPTER Molecular investigation of tick-borne haemoparasite infections among transhumant Zebu cattle in Karamoja Region, Uganda
  • 5.1 Abstract
  • 5.2 Introduction
  • 5.3 Materials and Methods
    • 5.3.1 Ethics statement
    • 5.3.2 Study area
    • 5.3.3 Study design and study animals
    • 5.3.4 Blood sample collection and DNA extraction
    • 5.3.5 Reverse line blot (RLB) hybridisation assay
    • 5.3.6 Quantitative real-time PCR (qPCR) assays
    • 5.3.7 Amplification, cloning and sequencing of the 18S rRNA gene of Theileria and Babesia species
  • 5.3.8 Sequence and phylogenetic analyses
  • 5.3.9 Nucleotide sequence accession numbers and statistical analysis
  • 5.4 Results
  • 5.4.1 Distribution of sampled cattle by location, sex and age group
  • 5.4.2 Tick-borne haemoparasite prevalence by RLB hybridisation assay
  • 5.4.3 Comparison between RLB and qPCR results
  • 5.4.4 18S rRNA gene sequence analysis
  • 5.4.5 Phylogenetic analyses
  • 5.5 Discussion
  • 5.6 Conclusions
  • 5.7 References
• CHAPTER Phylogeny of Anaplasma species and sequence analysis of Anaplasma marginale amon cattle from a pastoral area of Karamoja, Uganda
  • 6.1 Abstract
  • 6.2 Introduction
  • 6.3 Materials and Methods
    • 6.3.1 Ethics approval
    • 6.3.2 Study area
    • 6.3.3 Blood samples and DNA extraction
    • 6.3.4 Duplex quantitative real-time polymerase chain reaction (qPCR)
    • 6.3.5 PCR amplification of 16S rRNA and msp1α genes
    • 6.3.6 Cloning and sequencing of PCR products
    • 6.3.7 Sequence and phylogenetic analyses
    • 6.3.8 Nucleotide sequence accession numbers
    • 6.3.9 Statistical analyses
  • 6.4 Results
    • 6.4.1 Prevalence of A. marginale and A. centrale
    • 6.4.2 PCR amplification and cloning of 16S rRNA and msp1α genes
    • 6.4.3 16S rRNA gene sequence analysis
    • 6.4.4 16S rRNA phylogenetic analyses
    • 6.4.5 Anaplasma marginale msp1α tandem repeats
  • 6.5 Discussion
  • 6.6 Conclusions
  • 6.7 References
• CHAPTER General Discussion, Conclusions and Recommendations
  • 7.1 Discussion
  • 7.2 Conclusions
  • 7.3 Recommendations
  • 7.4 References
  • APPENDICES
  • LIST OF PUBLICATIONS

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