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Transmission Ecology of Old World Arenaviruses in Natural Populations of Their Reservoir Hosts

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Transmission Ecology of Old World Arenaviruses in Natural Populations of Their Reservoir Hosts Faculteit Wetenschappen Biologie TRANSMISSION ECOLOGY OF OLD WORLD ARENAVIRUSES IN NATURAL POPULATIONS OF THEIR RESERVOIR HOSTS TRANSMISSIE-ECOLOGIE VAN OUDE WERELD ARENAVIRUSSEN IN NATUURLIJKE POPULATIES VAN HUN PRIMAIRE GASTHEREN Proefschrift voorgelegd tot het behalen van de graad van doctor in de wetenschappen aan de Universiteit Antwerpen te verdedigen door Joachim Mariën Promotors: Prof. dr. Herwig Leirs dr. Jonas Reijniers Antwerpen, 2018 Internal PhD committee Prof dr. Erik Matthysen Prof dr. Kris Vissenberg Prof dr. Niel Hens External PhD committee Prof dr. Stephanie Kramer-Schadt (Leibniz-Institut for Zoo- and wildlife research & Technische Universität, Berlin, Germany) Prof. dr. Steven Belmain (University of Greenwich, London, United-Kingdom) Supervisors Work related to Morogoro virus: dr. Benny Borremans (University of California Los Angeles, Los Angeles, USA) Work related to Lassa virus: dr. Elisabeth Fichet-Calvet (Bernhard-Nocht institute for tropical medicine, Hamburg, Germany) “Since the soldier did not speak English, the accompanying medic translated his story for us. Four days prior, the soldier had been sleeping in his tent when he awoke to feel something crawling on his shoulder. He had grabbed what turned out to be a rat and flung it across the room, but not before the rodent managed to bite him. The soldier dutifully showed us the healing puncture wound on his hands. The soldier had not thought much of the incident until he developed a fever and a cough three days later. The soldier had then talked to the medic of his battalion, who discussed the issue up the chain of command and eventually decided to bring the man to the Lassa ward. We had him describe the rat for us and lamented that he had thrown away the carcass. It sounded like a Mastomys natalensis (the species that transmits Lassa), but it was impossible to be sure. After some debate, Dr. Conteh decided to err on the side of safety and start the soldier on a prophylactic regimen of ribavirin. We put the unfortunate man in his room, away from the other patients. His case was a reminder that in Africa, the majority of wartime deaths are not directly from bullets or bombs, but from the spread of infectious disease that historically accompany a society’s breakdown.” Excerpt from the diary of Dr. Ross I. Donaldson The Lassa ward (2003) A Natal multimammate mouse (Mastomys natalensis) Table of contents Summary 1 Samenvatting 4 Chapter 1 7 Introduction Chapter 2 21 No measurable adverse effects of Lassa, Morogoro and Gairo arenaviruses on their rodent reservoir host in natural conditions Chapter 3 39 Arenavirus infection correlates with lower survival of its natural rodent host in a long-term capture-mark-recapture study Chapter 4 55 Arenavirus dynamics in experimentally and naturally infected rodent hosts Chapter 5 77 Seasonal host dynamics translate into density-dependent arenavirus cycles Chapter 6 101 Movement patterns of small rodents in Lassa fever-endemic villages in Guinea Chapter 7 118 Evaluation of rodent control to fight Lassa fever based on field data and mathematical modelling Chapter 8 138 Discussion Dankwoord – Acknowledgements 148 References 152 Summary Summary In West Africa, the multimammate mouse (Mastomys natalensis) is the primary reservoir of Lassa virus (LASV), an arenavirus that causes severe haemorrhagic fever in humans. It is estimated that this virus affects between 200.000 and 300.000 people yearly with a fatality rate of 1-2%. Humans get infected by close direct or indirect contact with the rodent or its excretions, which can be through contaminated food or water, direct consumption of the rodent, or inhalation of excretion particles. Because no vaccine for use in humans exists and therapeutic options are limited to the broad-spectrum antiviral ribavirin, rodent control is currently assumed to be the only feasible option to control Lassa fever. However, no solid information exists on how effective rodent control really is or which control strategies would be most effective to reduce spillover. Mastomys natalensis also hosts several other arenaviruses such as Morogoro virus (MORV), which occurs in rodent populations in Tanzania. Because the ecology of Tanzanian M. natalensis is well known and MORV is not pathogenic for humans, MORV-M. natalensis is considered a suitable model for examining arenavirus-host interactions in general. The model is especially considered a safe substitute for studying closely related but pathogenic arenaviruses like LASV. This thesis has two main objectives. The first is to improve our understanding of how arenaviruses can persist in rodent populations. Therefore, we will study the transmission dynamics of MORV in highly fluctuating populations of M. natalensis in Tanzania. The second is to explore which rodent control strategies are efficient to control LASV in Guinea. To achieve this, we will use data from different field experiments performed in Guinea, together with information derived from studying the first objective. How can arenaviruses persist in populations of their reservoir host? Seasonal variation in rainfall causes M. natalensis population densities to fluctuate heavily in Tanzania. When densities become very low, they may result in the extinction of parasites because transmission may cease due to lack of contacts between hosts. However, MORV seems to persist in such low densities regardlessly. As a first step to explore how this is possible we investigated the virulence of MORV in M. natalensis. This would indicate whether MORV causes adverse effects in its host, which if true, would be an additional factor that could limit the virus’ persistence probability. In contrast, based on morphological characteristics (chapter 1 Summary 2) and survival data (chapter 3), we showed that MORV causes no or only mild adverse effects in its host. This could be an adaptation of the virus to persist during the yearly host population bottlenecks and is in line with the ‘parasite trade-off hypothesis’, which balances virulence and host survival so that transmission is maximized over the lifetime of infection. Understanding parasite persistence in wildlife populations relies on a correct interpretation of the infection patterns. These patterns are well-investigated for MORV in laboratory conditions, where M. natalensis was inoculated intraperitoneally and followed for several weeks. However, important differences may occur when animals become infected in natural conditions due to circumstances that were not accounted for in the lab (e.g. due to differences in genetic strains, stress levels, infection dose or life histories). In order to validate these laboratory results, we compared MORV infection patterns between naturally and experimentally infected multimammate mice, using blood and excretion samples that were collected during a three- month capture-mark-recapture (CMR) study (chapter 4). We found a good match between the field and laboratory data for 52% of the naturally infected animals. Mismatches could be explained by infection patterns that were not yet tested in the lab, such as maternal antibodies or an antibody detection limit. An interesting result related to the persistence of MORV was that some animals in the field (16% of infected) showed signs of chronic or latent infections, while it was previously assumed that MORV infections in M. natalensis are predominantly acute. The transmission dynamics of MORV in populations of M. natalensis were investigated by comparing model simulations to serological data of a ten-year CMR time series (chapter 5). In this dataset, we observed that seropositive animals were continuously present (indicating no extinction of the virus) and that seroprevalence peaks after the high-density season of the host. This seasonal pattern could be best approximated by mathematical models that included a combination of vertical and density-dependent horizontal transmission while a small number of animals had to be chronically infected to ensure viral persistence. To further investigate whether chronically infected individuals are indeed present in natural conditions, we performed a small lab experiment in which wild-caught rodents were caged for eight weeks, sampled each week and afterwards dissected. In agreement with the previous short CMR-study (chapter 4) and the model simulations, we observed that a low number of animals (8%) showed signs of chronic MORV infections. 2 Summary How effective is rodent control to reduce LASV spillover risk in Guinea? After investigating how MORV can persist in populations of M. natalensis in Tanzania, we moved our focus to the transmission of LASV in rodent populations in Guinea. Little attention has been paid to the ecology of M. natalensis in West Africa and in order to better understand how LASV spreads on a local scale, we first investigated the movement patterns of M. natalensis in Lassa fever-endemic villages (chapter 6). By performing several CMR and dyed bait (Rhodamine B) experiments in different villages in Guinea, we observed that M. natalensis easily moves between the fields and the houses in the village. This observation supports the hypothesis that rodents move from the fields to the houses to search for food during the dry season, which might explain the higher incidence of human Lassa fever cases during this period. Information derived from these experiments was also used to inform a mathematical model for LASV transmission (discussed in the next chapter), as it provided an estimate of the population density and
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