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      Recurrent Anthrax Outbreaks in Humans, Livestock, and Wildlife in the Same Locality, Kenya, 2014–2017

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          Abstract.

          Epidemiologic data indicate a global distribution of anthrax outbreaks associated with certain ecosystems that promote survival and viability of Bacillus anthracis spores. Here, we characterized three anthrax outbreaks involving humans, livestock, and wildlife that occurred in the same locality in Kenya between 2014 and 2017. Clinical and epidemiologic data on the outbreaks were collected using active case finding and review of human, livestock, and wildlife health records. Information on temporal and spatial distribution of prior outbreaks in the area was collected using participatory epidemiology. The 2014–2017 outbreaks in Nakuru West subcounty affected 15 of 71 people who had contact with infected cattle (attack rate = 21.1%), including seven with gastrointestinal, six with cutaneous, and two with oropharyngeal forms of the disease. Two (13.3%) gastrointestinal human anthrax cases died. No human cases were associated with infected wildlife. Of the 54 cattle owned in 11 households affected, 20 died (attack rate = 37%). The 2015 outbreak resulted in death of 10.5% of the affected herbivorous wildlife at Lake Nakuru National Park, including 745 of 4,500 African buffaloes (species-specific mortality rate = 17%) and three of 18 endangered white rhinos (species-specific mortality rate = 16%). The species mortality rate ranged from 1% to 5% for the other affected wildlife species. Participatory epidemiology identified prior outbreaks between 1973 and 2011 in the same area. The frequency and severity of outbreaks in this area suggests that it is an anthrax hotspot ideal for investigating risk factors associated with long-term survival of anthrax spores and outbreak occurrence.

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          Most cited references35

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          The ecology of Bacillus anthracis.

          The global distribution of anthrax is largely determined by soils with high calcium levels and a pH above 6.1, which foster spore survival. It is speculated that the spore exosporium probably plays a key part by restricting dispersal and thereby increasing the probability of a grazing animal acquiring a lethal dose. 'Anthrax Seasons' are characterized by hot-dry weather which stresses animals and reduces their innate resistance to infection allowing low doses of spores to be infective. Necrophagic flies act as case-multipliers and haemophagic flies as space-multipliers; the latter are aided by climatic factors which play a key part in whether epidemics occur. Host death is a function of species sensitivity to the toxins. The major function of scavengers is to open the carcass, spill fluids, and thereby aid bacilli dispersal and initiate sporulation. In the context of landscape ecology viable spore distribution is a function of mean annual temperature, annual precipitation, elevation, mean NDVI, annual NDVI amplitude, soil moisture content, and soil pH.
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            The ecology of anthrax spores: tough but not invincible.

            Bacillus anthracis is the causative agent of anthrax, a serious and often fatal disease of wild and domestic animals. Central to the persistence of anthrax in an area is the ability of B. anthracis to form long-lasting, highly resistant spores. Understanding the ecology of anthrax spores is essential if one hopes to control epidemics. Studies on the ecology of anthrax have found a correlation between the disease and specific soil factors, such as alkaline pH, high moisture, and high organic content. Researchers initially suggested that these factors influenced vegetative anthrax bacilli. However, subsequent research has shown that vegetative cells of B. anthracis have very specific nutrient and physiological requirements and are unlikely to survive outside a host. Review of the properties of spores of B. anthracis and other Bacillus species suggests that the specific soil factors linked to epidemic areas reflect important environmental conditions that aid the anthrax spores in causing epidemics. Specifically, high levels of calcium in the soil may help to maintain spore vitality for prolonged periods, thereby increasing the chance of spores encountering and infecting a new host. Cycles of runoff and evaporation may collect spores dispersed from previous epidemics into storage areas, thereby concentrating them. Uptake of large doses of viable spores from storage areas by susceptible animals, via altered feeding or breeding behavior, may then allow the bacterium to establish infection and cause a new epidemic. Literature search for this review was done by scanning the Life Sciences Collection 1982-1994 using the keywords "anthrax" and "calcium and spore."
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              Predictability of anthrax infection in the Serengeti, Tanzania.

              Anthrax is endemic throughout Africa, causing considerable livestock and wildlife losses and severe, sometimes fatal, infection in humans. Predicting the risk of infection is therefore important for public health, wildlife conservation and livestock economies. However, because of the intermittent and variable nature of anthrax outbreaks, associated environmental and climatic conditions, and diversity of species affected, the ecology of this multihost pathogen is poorly understood.We explored records of anthrax from the Serengeti ecosystem in north-west Tanzania where the disease has been documented in humans, domestic animals and a range of wildlife. Using spatial and temporal case-detection and seroprevalence data from wild and domestic animals, we investigated spatial, environmental, climatic and species-specific associations in exposure and disease.Anthrax was detected annually in numerous species, but large outbreaks were spatially localized, mostly affecting a few focal herbivores.Soil alkalinity and cumulative weather extremes were identified as useful spatial and temporal predictors of exposure and infection risk, and for triggering the onset of large outbreaks.Interacting ecological and behavioural factors, specifically functional groups and spatiotemporal overlap, helped to explain the variable patterns of infection and exposure among species.Synthesis and applications. Our results shed light on ecological drivers of anthrax infection and suggest that soil alkalinity and prolonged droughts or rains are useful predictors of disease occurrence that could guide risk-based surveillance. These insights should inform strategies for managing anthrax including prophylactic livestock vaccination, timing of public health warnings and antibiotic provision in high-risk areas. However, this research highlights the need for greater surveillance (environmental, serological and case-detection-orientated) to determine the mechanisms underlying anthrax dynamics.
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                Author and article information

                Journal
                Am J Trop Med Hyg
                Am. J. Trop. Med. Hyg
                tpmd
                tropmed
                The American Journal of Tropical Medicine and Hygiene
                The American Society of Tropical Medicine and Hygiene
                0002-9637
                1476-1645
                October 2018
                13 August 2018
                13 August 2018
                : 99
                : 4
                : 833-839
                Affiliations
                [1 ]Kenya Zoonotic Disease Unit, Nairobi, Kenya;
                [2 ]Washington State University Global Health Program-Kenya, Washington State University, Pullman, Washington;
                [3 ]Kenya Wildlife Services, Nairobi, Kenya;
                [4 ]Food and Agriculture Organization of the United Nations, Nairobi, Kenya;
                [5 ]Division of Global Health Protection, United States Centers for Disease Control and Prevention, Nairobi, Kenya;
                [6 ]Kenya Directorate of Veterinary Services, Nairobi, Kenya;
                [7 ]International Livestock Research Institute, Nairobi, Kenya
                Author notes
                [* ]Address correspondence to Mathew Muturi, Ministry of Agriculture, Livestock and Fisheries, Directorate of Veterinary Services, Zoonotic Disease Unit P.O. Box 20811-00202, Nairobi, Kenya. E-mail: muturimathew@ 123456gmail.com

                Financial support: Financial support was provided by the United States Defense Threat Reduction Agency; Kenya Ministry of Agriculture, Livestock and Fisheries; Kenya Ministry of Health; and the United States Centers for Disease Control and Prevention.

                Authors’ addresses: Mathew Muturi and Athman Mwatondo, Kenya Zoonotic Disease Unit, Nairobi, Kenya, E-mails: muturimathew@ 123456gmail.com and amwatondo@ 123456yahoo.com . John Gachohi, Eric Osoro, S. Mwangi Thumbi, and M. Kariuki Njenga, Washington State University Global Health Program-Kenya, Washington State University, Pullman, WA, E-mails: john.gachohi@ 123456wsu.edu , eric.osoro@ 123456wsu.edu , thumbi.mwangi@ 123456wsu.edu , and mkariuki.njenga@ 123456wsu.edu . Isaac Lekolool, Francis Gakuya, and Alice Bett, Kenya Wildlife Services, Nairobi, Kenya, E-mails: lekolool@ 123456kws.go.ke , gakuya@ 123456kws.go.ke , and alicebett@ 123456kws.go.ke . Austine Bitek, Food and Agriculture Organization of the United Nations, Nairobi, Kenya, E-mail: austine.bitek@ 123456fao.org . Peninah Munyua, Division of Global Health Protection, U.S. Centers for Disease Control and Prevention, Nairobi, Kenya, E-mail: ikg2@ 123456cdc.gov . Harry Oyas and Obadiah N. Njagi, Department of Veterinary Services, Ministry of Agriculture, Livestock and Fisheries, Kabete, Kenya, E-mails: harryoyas@ 123456yahoo.com and jesse.mwere@ 123456gmail.com . Bernard Bett, International Livestock Research Institute, Nairobi, Kenya, E-mail: b.bett@ 123456cgiar.org .

                Article
                tpmd180224
                10.4269/ajtmh.18-0224
                6159598
                30105965
                083189e8-0b80-440d-b773-33c892b90f12
                © The American Society of Tropical Medicine and Hygiene

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 16 March 2018
                : 15 June 2018
                Page count
                Pages: 7
                Categories
                Articles

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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