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      Frequency‐dependent transmission of Batrachochytrium salamandrivorans in eastern newts

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          Abstract

          Transmission is the fundamental process whereby pathogens infect their hosts and spread through populations, and can be characterized using mathematical functions. The functional form of transmission for emerging pathogens can determine pathogen impacts on host populations and can inform the efficacy of disease management strategies. By directly measuring transmission between infected and susceptible adult eastern newts ( Notophthalmus viridescens) in aquatic mesocosms, we identified the most plausible transmission function for the emerging amphibian fungal pathogen Batrachochytrium salamandrivorans ( Bsal). Although we considered a range of possible transmission functions, we found that Bsal transmission was best explained by pure frequency dependence. We observed that >90% of susceptible newts became infected within 17 days post‐exposure to an infected newt across a range of host densities and initial infection prevalence treatments. Under these conditions, we estimated R 0 = 4.9 for Bsal in an eastern newt population. Our results suggest that Bsal has the capability of driving eastern newt populations to extinction and that managing host density may not be an effective management strategy. Intervention strategies that prevent Bsal introduction or increase host resistance or tolerance to infection may be more effective. Our results add to the growing empirical evidence that transmission of wildlife pathogens can saturate and be functionally frequency‐dependent.

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          Covid-19 — Navigating the Uncharted

          The latest threat to global health is the ongoing outbreak of the respiratory disease that was recently given the name Coronavirus Disease 2019 (Covid-19). Covid-19 was recognized in December 2019. 1 It was rapidly shown to be caused by a novel coronavirus that is structurally related to the virus that causes severe acute respiratory syndrome (SARS). As in two preceding instances of emergence of coronavirus disease in the past 18 years 2 — SARS (2002 and 2003) and Middle East respiratory syndrome (MERS) (2012 to the present) — the Covid-19 outbreak has posed critical challenges for the public health, research, and medical communities. In their Journal article, Li and colleagues 3 provide a detailed clinical and epidemiologic description of the first 425 cases reported in the epicenter of the outbreak: the city of Wuhan in Hubei province, China. Although this information is critical in informing the appropriate response to this outbreak, as the authors point out, the study faces the limitation associated with reporting in real time the evolution of an emerging pathogen in its earliest stages. Nonetheless, a degree of clarity is emerging from this report. The median age of the patients was 59 years, with higher morbidity and mortality among the elderly and among those with coexisting conditions (similar to the situation with influenza); 56% of the patients were male. Of note, there were no cases in children younger than 15 years of age. Either children are less likely to become infected, which would have important epidemiologic implications, or their symptoms were so mild that their infection escaped detection, which has implications for the size of the denominator of total community infections. On the basis of a case definition requiring a diagnosis of pneumonia, the currently reported case fatality rate is approximately 2%. 4 In another article in the Journal, Guan et al. 5 report mortality of 1.4% among 1099 patients with laboratory-confirmed Covid-19; these patients had a wide spectrum of disease severity. If one assumes that the number of asymptomatic or minimally symptomatic cases is several times as high as the number of reported cases, the case fatality rate may be considerably less than 1%. This suggests that the overall clinical consequences of Covid-19 may ultimately be more akin to those of a severe seasonal influenza (which has a case fatality rate of approximately 0.1%) or a pandemic influenza (similar to those in 1957 and 1968) rather than a disease similar to SARS or MERS, which have had case fatality rates of 9 to 10% and 36%, respectively. 2 The efficiency of transmission for any respiratory virus has important implications for containment and mitigation strategies. The current study indicates an estimated basic reproduction number (R0) of 2.2, which means that, on average, each infected person spreads the infection to an additional two persons. As the authors note, until this number falls below 1.0, it is likely that the outbreak will continue to spread. Recent reports of high titers of virus in the oropharynx early in the course of disease arouse concern about increased infectivity during the period of minimal symptoms. 6,7 China, the United States, and several other countries have instituted temporary restrictions on travel with an eye toward slowing the spread of this new disease within China and throughout the rest of the world. The United States has seen a dramatic reduction in the number of travelers from China, especially from Hubei province. At least on a temporary basis, such restrictions may have helped slow the spread of the virus: whereas 78,191 laboratory-confirmed cases had been identified in China as of February 26, 2020, a total of 2918 cases had been confirmed in 37 other countries or territories. 4 As of February 26, 2020, there had been 14 cases detected in the United States involving travel to China or close contacts with travelers, 3 cases among U.S. citizens repatriated from China, and 42 cases among U.S. passengers repatriated from a cruise ship where the infection had spread. 8 However, given the efficiency of transmission as indicated in the current report, we should be prepared for Covid-19 to gain a foothold throughout the world, including in the United States. Community spread in the United States could require a shift from containment to mitigation strategies such as social distancing in order to reduce transmission. Such strategies could include isolating ill persons (including voluntary isolation at home), school closures, and telecommuting where possible. 9 A robust research effort is currently under way to develop a vaccine against Covid-19. 10 We anticipate that the first candidates will enter phase 1 trials by early spring. Therapy currently consists of supportive care while a variety of investigational approaches are being explored. 11 Among these are the antiviral medication lopinavir–ritonavir, interferon-1β, the RNA polymerase inhibitor remdesivir, chloroquine, and a variety of traditional Chinese medicine products. 11 Once available, intravenous hyperimmune globulin from recovered persons and monoclonal antibodies may be attractive candidates to study in early intervention. Critical to moving the field forward, even in the context of an outbreak, is ensuring that investigational products are evaluated in scientifically and ethically sound studies. 12 Every outbreak provides an opportunity to gain important information, some of which is associated with a limited window of opportunity. For example, Li et al. report a mean interval of 9.1 to 12.5 days between the onset of illness and hospitalization. This finding of a delay in the progression to serious disease may be telling us something important about the pathogenesis of this new virus and may provide a unique window of opportunity for intervention. Achieving a better understanding of the pathogenesis of this disease will be invaluable in navigating our responses in this uncharted arena. Furthermore, genomic studies could delineate host factors that predispose persons to acquisition of infection and disease progression. The Covid-19 outbreak is a stark reminder of the ongoing challenge of emerging and reemerging infectious pathogens and the need for constant surveillance, prompt diagnosis, and robust research to understand the basic biology of new organisms and our susceptibilities to them, as well as to develop effective countermeasures.
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            Superspreading and the effect of individual variation on disease emergence

            Coughs and sneezes... From Typhoid Mary to SARS, it has long been known that some people spread disease more than others. But for diseases transmitted via casual contact, contagiousness arises from a plethora of social and physiological factors, so epidemiologists have tended to rely on population averages to assess a disease's potential to spread. A new analysis of outbreak data shows that individual differences in infectiousness exert powerful influences on the epidemiology of ten deadly diseases. SARS and measles (and perhaps avian influenza) show strong tendencies towards ‘superspreading events’ that can ignite explosive epidemics — but this same volatility makes outbreaks more likely to fizzle out. Smallpox and pneumonic plague, two potential bioterrorism agents, show steadier growth but still differ markedly from the traditional average-based view. These findings are relevant to how emerging diseases are detected and controlled. Supplementary information The online version of this article (doi:10.1038/nature04153) contains supplementary material, which is available to authorized users.
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              COVID-19: what is next for public health?

              The WHO Scientific and Technical Advisory Group for Infectious Hazards (STAG-IH), working with the WHO secretariat, reviewed available information about the outbreaks of 2019 novel coronavirus disease (COVID-19) on Feb 7, 2020, in Geneva, Switzerland, and concluded that the continuing strategy of containment for elimination should continue, and that the coming 2–3 weeks through to the end of February, 2020, will be crucial to monitor the situation of community transmission to update WHO public health recommendations if required. Genetic analysis early in the outbreak of COVID-19 in China revealed that the virus was similar to, but distinct from, severe acute respiratory syndrome coronavirus (SARS-CoV), but the closest genetic similarity was found in a coronavirus that had been isolated from bats. 1 As there was in early January, 2020, scarce information available about the outbreak, knowledge from outbreaks caused by the SARS-CoV and Middle East respiratory syndrome coronavirus (MERS-CoV) formed the basis for WHO public health recommendations in mid-January. 2 However, the availability of more evidence in the past month has shown major differences between the outbreaks and characteristics of COVID-19 compared with those of SARS-CoV. Recognising the Wuhan-focused and nationwide outbreak responses in China, WHO has encouraged countries with heavy air travel exchange with Wuhan to take precautionary public health measures 2 and, if there is imported infection, to undertake activities that could lead to the elimination of the virus in human populations as occurred during the 2003 SARS outbreak. 3 After the SARS outbreak, a few follow-on outbreaks occurred, including accidents in laboratories researching SARS-CoV. 4 SARS-CoV is thought to have been eliminated from human populations during 2003, and there have been no reports in the medical literature about SARS-CoV circulation in human populations since then. The 2003 SARS outbreaks are thought to have originated from the spillover of a mutated coronavirus from animals sold in a live animal market in Guangdong province in China to a few humans, and it then surfaced as a large cluster of pneumonia in health-care settings in Guangdong province. 5 Although the causative agent was then unknown, an infected medical doctor who had been treating patients in Guangdong province travelled to Hong Kong when he became ill and became an index case for hospital-associated and community outbreaks in Hong Kong and in three countries outside of China. The causative agent was later identified as a coronavirus and named SARS-CoV. The SARS outbreaks were at times characterised by several superspreading events—eg, hotel-based transmission from one infected hotel guest to others who travelled to Canada, Singapore, and Vietnam. 6 One large apartment complex-based outbreak of SARS was later found to be caused by aerosolisation of virus contaminated sewage. 6 COVID-19 is thought to have been introduced to human populations from the animal kingdom in November or December, 2019, as suggested by the phylogeny of genomic sequences obtained from early cases. 7 The genetic epidemiology suggests that from the beginning of December, 2019, when the first cases were retrospectively traced in Wuhan, the spread of infection has been almost entirely driven by human-to-human transmission, not the result of continued spillover. There was massive transmission in a matter of weeks in Wuhan, and people in the resulting chains of transmission spread infection by national and international travel during the Chinese New Year holidays. COVID-19 seems to have different epidemiological characteristics from SARS-CoV. COVID-19 replicates efficiently in the upper respiratory tract and appears to cause less abrupt onset of symptoms, similar to conventional human coronaviruses that are a major cause of common colds in the winter season. 8 Infected individuals produce a large quantity of virus in the upper respiratory tract during a prodrome period, are mobile, and carry on usual activities, contributing to the spread of infection. By contrast, transmission of SARS-CoV did not readily occur during the prodromal period when those infected were mildly ill, and most transmission is thought to have occurred when infected individuals presented with severe illness, thus possibly making it easier to contain the outbreaks SARS-CoV caused, unlike the current outbreaks with COVID-19. 6 © 2020 Kyodo News/Contributor/Getty Images 2020 Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active. COVID-19 also has affinity for cells in the lower respiratory tract and can replicate there, causing radiological evidence of lower respiratory tract lesions in patients who do not present with clinical pneumonia. 8 There seem to be three major patterns of the clinical course of infection: mild illness with upper respiratory tract presenting symptoms; non-life-threatening pneumonia; and severe pneumonia with acute respiratory distress syndrome (ARDS) that begins with mild symptoms for 7–8 days and then progresses to rapid deterioration and ARDS requiring advanced life support (WHO EDCARN clinical telephone conference on COVID-19, personal communication with Myoung-don Oh [Seoul National University Hospital] and Yinzhong Shen [Shanghai Public Health Clinical Center]) The case fatality ratio with COVID-19 has been difficult to estimate. The initial case definition in China included pneumonia but was recently adjusted to include people with milder clinical presentation and the current estimate is thought to be about 1–2%, which is lower than that for SARS (10%). 9 The actual case fatality ratio of infection with COVID-19 will eventually be based on all clinical illness and at the time of writing information on subclinical infection is not available and awaits the development of serological tests and serosurveys. Presently COVID-19 seems to spread from person to person by the same mechanism as other common cold or influenza viruses—ie, face to face contact with a sneeze or cough, or from contact with secretions of people who are infected. The role of faecal–oral transmission is yet to be determined in COVID-19 but was found to occur during the SARS outbreak. 10 The lock-down of Wuhan City seems to have slowed international spread of COVID-19; however, the effect is expected to be short-lived (WHO modelling group). Efforts are currently underway in China, in the 24 countries to which infected persons have travelled, and in public conveyances, such as cruise ships, to interrupt transmission of all existing and potential chains of transmission, with elimination of COVID-19 in human populations as the final goal. This WHO-recommended strategy is regularly assessed each week by STAG-IH on the basis of daily risk assessments by WHO as information becomes available from outbreak sites. A plausible scenario based on the available evidence now is that the newly identified COVID-19 is causing, like seasonal influenza, mild and self-limiting disease in most people who are infected, with severe disease more likely among older people or those with comorbidities, such as diabetes, pulmonary disease, and other chronic conditions. Health workers and carers are at high risk of infection, and health-care-associated amplification of transmission is of concern as is always the case for emerging infections. People in long-term care facilities are also at risk of severe health consequences if they become infected. Non-pharmaceutical interventions remain central for management of COVID-19 because there are no licensed vaccines or coronavirus antivirals. If the situation changes towards much wider community transmission with multiple international foci, the WHO strategy of containment for elimination could need to be adjusted to include mitigation strategies combined with the following activities currently recommended by STAG-IH on the WHO website. First, close monitoring is needed of changes in epidemiology and of the effectiveness of public health strategies and their social acceptance. Second, continued evolution is needed of enhanced communication strategies that provide general populations and vulnerable populations most at risk with actionable information for self-protection, including identification of symptoms, and clear guidance for treatment seeking. Third, continued intensive source control is needed in the epicentre in China—ie, isolation of patients and persons testing positive for COVID-19, contact tracing and health monitoring, strict health facility infection prevention and control, and use of other active public health control interventions with continued active surveillance and containment activities at all other sites where outbreaks are occurring in China. Fourth, continued containment activities are needed around sites outside China where there are infected people and transmission among contacts, with intensive study to provide information on transmissibility, means of transmission, and natural history of infection, with regular reporting to WHO and sharing of data. Fifth, intensified active surveillance is needed for possible infections in all countries using the WHO-recommended surveillance case definition. 11 Sixth, preparation for resilience of health systems in all countries is needed, as is done at the time of seasonal influenza, anticipating severe infections and course of disease in older people and other populations identified to be at risk of severe disease. Seventh, if widespread community transmission is established, there should then be consideration of a transition to include mitigation activities, especially if contact tracing becomes ineffective or overwhelming and an inefficient use of resources. Examples of mitigation activities include cancelling public gatherings, school closure, remote working, home isolation, observation of the health of symptomatic individuals supported by telephone or online health consultation, and provision of essential life support such as oxygen supplies, mechanical ventilators and extracorporeal membrane oxygenation (ECMO) equipment. Eighth, serological tests need to be developed that can estimate current and previous infections in general populations. Finally, continued research is important to understand the source of the outbreak by study of animals and animal handlers in markets to provide evidence necessary for prevention of future coronavirus outbreaks.
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                Author and article information

                Contributors
                mgray11@utk.edu
                Journal
                Transbound Emerg Dis
                Transbound Emerg Dis
                10.1111/(ISSN)1865-1682
                TBED
                Transboundary and Emerging Diseases
                John Wiley and Sons Inc. (Hoboken )
                1865-1674
                1865-1682
                09 March 2021
                March 2022
                : 69
                : 2 ( doiID: 10.1111/tbed.v69.2 )
                : 731-741
                Affiliations
                [ 1 ] Center for Wildlife Health Department of Forestry, Wildlife, and Fisheries University of Tennessee Institute of Agriculture Knoxville TN USA
                [ 2 ] Institute of Infection, Veterinary and Ecological Sciences University of Liverpool Liverpool UK
                [ 3 ] Department of Ecology, Evolution and Marine Biology University of California‐Santa Barbara Santa Barbara CA USA
                Author notes
                [*] [* ] Correspondence

                Matthew J. Gray, Center for Wildlife Health, Department of Forestry, Wildlife, and Fisheries, University of Tennessee Institute of Agriculture, Knoxville, Tennessee, USA.

                Email: mgray11@ 123456utk.edu

                Author information
                https://orcid.org/0000-0001-8243-9217
                Article
                TBED14043
                10.1111/tbed.14043
                9290712
                33617686
                a565b98a-39b6-410c-9f4c-a91a4c768036
                © 2021 The Authors. Transboundary and Emerging Diseases published by Wiley‐VCH GmbH.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 February 2021
                : 07 December 2020
                : 19 February 2021
                Page count
                Figures: 4, Tables: 2, Pages: 11, Words: 8470
                Funding
                Funded by: United States National Science Foundation
                Award ID: 1814520
                Award ID: NE/S013369/1
                Funded by: United States Department of Agriculture, National Institute of Food and Agriculture
                Award ID: Hatch Project 1012932
                Funded by: United States Fish and Wildlife Service
                Award ID: TN‐U2‐F19AP00047
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                March 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.7 mode:remove_FC converted:18.07.2022

                Infectious disease & Microbiology
                amphibian,batrachochytrium,density‐dependent transmission,disease,fungus,model

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