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Rift Valley Fever Virus Circulation in Livestock and Wildlife, and Population Dynamics of Potential Vectors, in Northern Kwazulu- Natal, South Africa

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Rift Valley Fever Virus Circulation in Livestock and Wildlife, and Population Dynamics of Potential Vectors, in Northern Kwazulu- Natal, South Africa Rift Valley fever virus circulation in livestock and wildlife, and population dynamics of potential vectors, in northern KwaZulu- Natal, South Africa by CARIEN VAN DEN BERGH Submitted in partial fulfilment of the requirements for the degree Doctor of Philosophy in the Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria Promoter: Prof EH Venter Co-promoter: Prof PN Thompson Co-promoter: Prof R Swanepoel August 2019 i DECLARATION I, Carien van den Bergh, student number 28215461 hereby declare that this dissertation, “Rift Valley fever virus circulation in livestock and wildlife, and population dynamics of potential vectors, in northern KwaZulu-Natal, South Africa.”, submitted in accordance with the requirements for the Doctor of Philosophy (Veterinary Science) degree at University of Pretoria, is my own original work and has not previously been submitted to any other institution of higher learning. All sources cited or quoted in this research paper are indicated and acknowledged with a comprehensive list of references. ............................................................. Carien van den Bergh August 2019 ii ACKNOWLEDGEMENTS I would like to express my sincere gratitude to the following people: My supervisors, Prof Estelle Venter, Prof Peter Thompson and Prof Bob Swanepoel for their guidance and support. Prof Peter Thompson, Ginette Thompson, Dannet Geldenhuys, Yusuf Ngoshe and Bruce Hay for accompanying me to Ndumo for sample collections. Prof Paulo Almeida and Dr Louwtjie Snyman, for their assistance with the mosquito identification. Ms Karen Ebersohn for assisting me with laboratory work. I would like to acknowledge the kindness and patience of the farmers and herders in the study area, as well as the generous assistance of the State Veterinarian and the Animal Health Technicians of the KwaZulu-Natal Department of Agriculture and Rural Development, Jozini District, and Ezemvelo KZN Wildlife. We thank Ezemvelo KZN Wildlife for supplying the weather data Centers for Disease Control and Prevention, Meat Industry Trust, Cape Wools South Africa and AgriSETA for the funds to do the project. Francois van Niekerk, my husband and my mother Ina Muller for their help and support. The results of this research have been published and reported at conferences: Van den Bergh C., Venter E.H.; Swanepoel R., Thompson P.N (2019). High seroconversion rate to Rift Valley fever virus in cattle and goats in far northern KwaZulu-Natal, South Africa, in the absence of reported outbreaks. PLOS Neglected Tropical Diseases 13(5): e0007296. https://doi.org/10.1371/journal.pntd.0007296 Poster for Faculty day Delegate at Southern African Society for Veterinary Epidemiology and Preventative Medicine Delegate at the 15th International Symposium of Veterinary Epidemiology and Economics iii ABBREVIATIONS AIC Akaike information criterion Ae. Aedes An. Anopheles BHK21 Baby hamster kidney 21 CHIKV Chikungunya virus CI Confidence interval CPE Cytopathic effects Cx. Culex ELISA Enzyme-linked immunosorbent assay FMD Foot and mouth disease IEP Inter-epidemic period IgG Immunoglobulin G IgM Immunoglobulin M KNP Kruger National Park KZN KwaZulu-Natal L Large M Medium MIR Maximum Infection Rate MP12 Rift Valley fever MP12 vaccine strain N Nucleocapsid NGR Ndumo Game reserve NSm Non-structural protein coded by the M-segment NSs Non-structural protein coded by the S-segment OBP Onderstepoort Biological Products OD Optical density OIE World Organisation for Animal Health OR Odds Ratio PBS Phosphate buffered saline PCR Polymerase chain reaction PP Positive percentage qRT-PCR Real-Time Quantitative reverse transcriptase PCR iv RdRp RNA dependant RNA polymerase RK13 Rabbit kidney 13 RNP Ribonucleocapsid rNP Recombinant nucleoprotein RT-PCR Reverse transcriptase polymerase chain reaction RVF Rift Valley fever RVFV Rift Valley fever virus S Small SA South Africa spp. Species SINV Sindbis virus SNT Serum neutralizing test TCID Tissue culture infective dose TEP Tembe Elephant Park v TABLE OF CONTENTS DECLARATION ii ACKNOWLEDGEMENTS iii LIST OF ABBREVIATIONS iv TABLE OF CONTENTS vi LIST OF TABLES x LIST OF FIGURES xi SUMMARY xiv CHAPTER 1: Literature Review…………………………………………………. 1 1.1 INTRODUCTION……………….………….……………………………………. 1 1.2 THE AETIOLOGICAL AGENT………………………………………………… 2 1.2.1 Structure……………………..……………….………………………………. 2 1.2.2 Pathogenesis………………………..………………………………………… 4 1.2.3 Clinical signs……………….…………….……………………………………. 5 1.2.4 Immune response…………………………..………………………………… 6 1.2.5 Control…………………………………………………………………………. 7 1.2.6 Diagnosis……………….……………………………………………………… 8 1.3 EPIDEMIOLOGY…………….………………………………………………….. 10 1.3.1 Hosts……………………………………………………………………………. 10 1.3.2 Vectors…………………………….……………………………………………. 11 1.3.3 Transmission………………………...………………………………………… 16 1.3.4 Occurrences……………………………………………………………………. 17 1.3.5 Inter-epidemic period………………………………………………………….. 19 1.3.6 Rift Valley fever in South Africa…………...…………………………………. 21 1.4 STUDY AREA …………………………………………………………………… 24 1.5 THESIS OUTLINE.………………………………………………… …………… 27 REFERENCES………………………..……………………………………………… 28 vi CHAPTER 2: High seroconversion rate to RVFV in cattle and goats in the far northern KwaZulu-Natal, in the absence of reported outbreaks……………………………………………………………………………... 38 2.1 INTRODUCTION…………………………………………….…..………………. 39 2.2 MATERIALS AND METHODS……………….………………………..……….. 42 2.2.1 Study area……..……………………….………………………………………. 42 2.2.2 Study design and sampling…………………………………………………… 45 2.2.3 Serology…………………...……………………………………………………. 46 2.2.4 Statistical analysis……...……………………………………………………… 47 2.3 RESULTS…..…………………………………………………………………….. 49 2.3.1 Seroprevalence…….………………………………………………………….. 49 2.3.2 Seroconversion rate…………………………………………………………… 52 2.4 DISCUSSION…………………………………………………………………….. 58 2.5 CONCLUSION…………………………………………………………………… 62 REFERENCES…..…………………………………………………………………… 63 CHAPTER 3: Neutralizing antibodies against Rift Valley fever virus in wild antelope in far northern KwaZulu-Natal, South Africa, indicate recent viral circulation……………………………………………………………. 67 3.1 INTRODUCTION…………………………………………………………………. 68 3.2 MATERIALS AND METHODS………………………………………………….. 71 3.2.1 Ethical approval………………………………………………..………………. 71 3.2.2 Study area………………………………………………………………………. 71 3.2.3 Sampling and laboratory testing……………………………………………… 72 3.2.4 Statistical analysis……………………………...……………………………… 73 3.3 RESULTS……………………………..………………………………………….. 73 3.4 DISCUSSION…………………………………………………………………….. 77 3.5 CONSCLUSION…………………………………………………………………. 80 REFERENCES………………………………………………………………….……. 81 vii CHAPTER 4: Population dynamics of Rift Valley fever virus vectors in circulation in northern KwaZulu-Natal, South Africa, 2017– 2018………………………………………………………………………………….. 84 4.1 INTRODUCTION…….…………………………………………………………. 84 4.2 MATERIALS AND METHODS…………………………….………………….. 87 4.2.1 Study area…………………………………………………………………….. 87 4.2.2 Collection sites……………………………….………………………………. 87 4.2.3 Collection method……………………………………………………………. 90 4.2.4 Viral screening. ………………………………………………………………. 91 4.2.5 Statistical analysis………………………………………………………..….. 91 4.3 Results……………………………………………………...…………………… 92 4.4 DISCUSSION…………………………………………………………………… 100 REFERENCES……………………...……………….……………………………… 105 CHAPTER 5: Detection of Rift Valley fever, Chikungunya and Sindbis viruses in Aedes (Aedimorphus) durbanensis from northern KwaZulu- Natal, South Africa……………………………………….………………….…… 108 5.1 INTRODUCTION……………..…………………………………………….…. 108 5.2 MATERIALS AND METHODS…………………………………………….…. 112 5.2.1 Mosquito trapping and processing…………………………………….….. 112 5.2.2 Real-time reverse transcriptase polymerase chain reaction……….….. 113 5.2.3 Phylogenetic analysis………………………………………………….…… 114 5.3 RESULTS…………………………………………………………………….… 120 5.4 DISCUSSION………………………………………………………………….. 125 REFERENCES………………………………………………………………….…. 129 CHAPTER 6: GENERAL CONCLUSION ………………………………………. 135 REFERENCES……………………………………………………………………… 141 viii Annexure AEC Approval confirmation letter……………………………………………………………………………….………….143 Section 20………………………………………………………………….………………………………………………………….144 ix List of Tables Table 1.1 Mosquito species from which RVFV has been isolated previously. 13 Table 2.1 Rift Valley fever seroprevalence in cattle at diptanks in far northern KwaZulu-Natal, June 2016. 50 Table 2.2 Rift Valley fever seroprevalence in goats in far northern KwaZulu- Natal, February-April 2017. 51 Table 2.3 Incidence rate of seroconversion* to Rift Valley fever virus in cattle and goats in far northern KwaZulu-Natal between June 2016 and June 53 2018, expressed as numbers of seroconversions per animal-year Table 2.4 Factors associated with incidence rate of seroconversion to Rift Valley fever virus in cattle and goats in far northern KwaZulu-Natal between 57 June 2016 and June 2018. Table 3.1 Seroprevalence of Rift Valley fever virus in wild antelope in far northern KwaZulu-Natal: descriptive statistics and univariate 75 associations. Table 3.2 Factors associated with seropositivity to Rift Valley fever virus in wild antelope in far northern KwaZulu-Natal: multivariable logistic 76 regression model. Table 4.1 Mosquito species and the total numbers of mosquitoes collected over the three areas in the study period. 93 Table 4.2 Associations of total rainfall, and average minimum and maximum temperatures 30 days prior to collection on the Aedes and Culex genera and the total number of mosquitoes collected per trap-night at 99 three sites in northern KwaZulu-Natal, using a negative binomial regression model. Table 5.1 Chikungunya virus, complete genome sequences with accession
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