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      Significance of major international seaports in the distribution of murine typhus in Taiwan

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          Abstract

          Background

          International seaports are hotspots for disease invasion and pathogens can persist in seaports even after ports are abandoned. Transmitted by fleas infected by Rickettsia typhi, murine typhus, a largely neglected and easily misdiagnosed disease, is known to occur primarily in large seaports. However, the significance of seaports in the occurrence of murine typhus has never been validated quantitatively.

          Methodology/Principal findings

          We studied the spatial distribution of murine typhus, a notifiable disease, in Taiwan. We investigated whether risk of infection was correlated with distance to international seaports and a collection of environmental and socioeconomic factors, using a Bayesian negative binomial conditionally autoregressive model, followed with geographically weighted regression. Seaports that are currently in use and those that operated in the 19 th century for trade with China, but were later abandoned due to siltation were analyzed. A total of 476 human cases of murine typhus were reported during 2000–2014 in the main island of Taiwan, with spatial clustering in districts in southwest and central-west Taiwan. A higher incidence rate (case/population) was associated with a smaller distance to currently in-use international seaports and lower rainfall and temperature, but was uncorrelated with distance to abandoned ports. Geographically weighted regression revealed a geographic heterogeneity in the importance of distance to in-use seaports near the four international seaports of Taiwan.

          Conclusions/Significance

          Our study suggests that murine typhus is associated with international seaports, especially for those with large trading volume. Thus, one of the costs of global trade in Taiwan might be elevated risks of murine typhus. Globalization has accelerated the spread of infectious diseases, but the burden of disease varies geographically, with regions surrounding major international seaports warranting particular surveillance.

          Author summary

          Globalization has hastened the spread of infectious diseases, with seaports as hotspots for disease invasion. Transmitted by fleas infected with the rickettsia Rickettsia typhi, murine typhus occurs worldwide, but its significance as a common causative agent of illness in tropical regions remains largely neglected. Although it is recognized that murine typhus is prevalent primarily in large seaports, the significance of seaports in the occurrence of murine typhus has never been validated quantitatively. We thus investigated whether distribution of murine typhus in Taiwan was associated with international seaports. Notably, abandoned international seaports (abandoned in the 19 th century due to siltation) were also studied to see whether the causative agent of murine typhus might still circulate around the ports even after being abandoned. We found that infection risk of murine typhus was negatively associated with distance to operating seaports but was uncorrelated with nearness to abandoned seaports. In addition, the importance of distance to operating seaports for risk of murine typhus infection varied spatially. Our study highlights elevated disease risk as a cost of international trade and suggests particular surveillance in regions surrounding major international seaports.

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          Most cited references58

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          The mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), originally indigenous to South-east Asia, islands of the Western Pacific and Indian Ocean, has spread during recent decades to Africa, the mid-east, Europe and the Americas (north and south) after extending its range eastwards across Pacific islands during the early 20th century. The majority of introductions are apparently due to transportation of dormant eggs in tyres. Among public health authorities in the newly infested countries and those threatened with the introduction, there has been much concern that Ae. albopictus would lead to serious outbreaks of arbovirus diseases (Ae. albopictus is a competent vector for at least 22 arboviruses), notably dengue (all four serotypes) more commonly transmitted by Aedes (Stegomyia) aegypti (L.). Results of many laboratory studies have shown that many arboviruses are readily transmitted by Ae. albopictus to laboratory animals and birds, and have frequently been isolated from wild-caught mosquitoes of this species, particularly in the Americas. As Ae. albopictus continues to spread, displacing Ae. aegypti in some areas, and is anthropophilic throughout its range, it is important to review the literature and attempt to predict whether the medical risks are as great as have been expressed in scientific journals and the popular press. Examination of the extensive literature indicates that Ae. albopictus probably serves as a maintenance vector of dengue in rural areas of dengue-endemic countries of South-east Asia and Pacific islands. Also Ae. albopictus transmits dog heartworm Dirofilaria immitis (Leidy) (Spirurida: Onchocercidae) in South-east Asia, south-eastern U.S.A. and both D. immitis and Dirofilaria repens (Raillet & Henry) in Italy. Despite the frequent isolation of dengue viruses from wild-caught mosquitoes, there is no evidence that Ae. albopictus is an important urban vector of dengue, except in a limited number of countries where Ae. aegypti is absent, i.e. parts of China, the Seychelles, historically in Japan and most recently in Hawaii. Further research is needed on the dynamics of the interaction between Ae. albopictus and other Stegomyia species. Surveillance must also be maintained on the vectorial role of Ae. albopictus in countries endemic for dengue and other arboviruses (e.g. Chikungunya, EEE, Ross River, WNV, LaCrosse and other California group viruses), for which it would be competent and ecologically suited to serve as a bridge vector.
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            Nonindigenous vectors that arrive, establish, and spread in new areas have fomented throughout recorded history epidemics of human diseases such as malaria, yellow fever, typhus, and plague. Although some vagile vectors, such as adults of black flies, biting midges, and tsetse flies, have dispersed into new habitats by flight or wind, human-aided transport is responsible for the arrival and spread of most invasive vectors, such as anthropophilic fleas, lice, kissing bugs, and mosquitoes. From the fifteenth century to the present, successive waves of invasion of the vector mosquitoes Aedes aegypti, the Culex pipiens Complex, and, most recently, Aedes albopictus have been facilitated by worldwide ship transport. Aircraft have been comparatively unimportant for the transport of mosquito invaders. Mosquito species that occupy transportable container habitats, such as water-holding automobile tires, have been especially successful as recent invaders. Propagule pressure, previous success, and adaptations to human habits appear to favor successful invasions by vectors.
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              Mammal invaders on islands: impact, control and control impact.

              The invasion of ecosystems by exotic species is currently viewed as one of the most important sources of biodiversity loss. The largest part of this loss occurs on islands, where indigenous species have often evolved in the absence of strong competition, herbivory, parasitism or predation. As a result, introduced species thrive in those optimal insular ecosystems affecting their plant food, competitors or animal prey. As islands are characterised by a high rate of endemism, the impacted populations often correspond to local subspecies or even unique species. One of the most important taxa concerning biological invasions on islands is mammals. A small number of mammal species is responsible for most of the damage to invaded insular ecosystems: rats, cats, goats, rabbits, pigs and a few others. The effect of alien invasive species may be simple or very complex, especially since a large array of invasive species, mammals and others, can be present simultaneously and interact among themselves as well as with the indigenous species. In most cases, introduced species generally have a strong impact and they often are responsible for the impoverishment of the local flora and fauna. The best response to these effects is almost always to control the alien population, either by regularly reducing their numbers, or better still, by eradicating the population as a whole from the island. Several types of methods are currently used: physical (trapping, shooting), chemical (poisoning) and biological (e.g. directed use of diseases). Each has its own set of advantages and disadvantages, depending on the mammal species targeted. The best strategy is almost always to combine several methods. Whatever the strategy used, its long-term success is critically dependent on solid support from several different areas, including financial support, staff commitment, and public support, to name only a few. In many cases, the elimination of the alien invasive species is followed by a rapid and often spectacular recovery of the impacted local populations. However, in other cases, the removal of the alien is not sufficient for the damaged ecosystem to revert to its former state, and complementary actions, such as species re-introduction, are required. A third situation may be widespread: the sudden removal of the alien species may generate a further disequilibrium, resulting in further or greater damage to the ecosystem. Given the numerous and complex population interactions among island species, it is difficult to predict the outcome of the removal of key species, such as a top predator. This justifies careful pre-control study and preparation prior to initiating the eradication of an alien species, in order to avoid an ecological catastrophe. In addition, long-term monitoring ofthe post-eradication ecosystem is crucial to assess success and prevent reinvasion.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                6 March 2017
                March 2017
                : 11
                : 3
                : e0005430
                Affiliations
                [1 ]Department of Life Science, National Taiwan Normal University, Taipei, Taiwan
                [2 ]Geography and Environment, University of Southampton, Southampton, United Kingdom
                [3 ]Department of Geography, National Taiwan University, Taipei, Taiwan
                [4 ]Center for Diagnostics and Vaccine Development, Centers for Disease Control, Ministry of Health and Welfare, Taipei, Taiwan
                [5 ]Faculty of Science and Technology, Lancaster University, Lancaster, United Kingdom
                [6 ]School of Geography, Archaeology and Palaeoecology, Queen's University Belfast, Belfast, Northern Ireland, United Kingdom
                Fondation Raoul Follereau, FRANCE
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: CCK.

                • Data curation: CCK NW.

                • Formal analysis: CCK.

                • Investigation: CCK NW CTC HCW PMA.

                • Methodology: CCK NW.

                • Resources: CCK NW CTC HCW PMA.

                • Software: CCK NW.

                • Validation: CCK.

                • Visualization: CCK.

                • Writing – original draft: CCK.

                • Writing – review & editing: CCK NW CTC HCW PMA.

                Author information
                http://orcid.org/0000-0002-1892-6712
                Article
                PNTD-D-16-01943
                10.1371/journal.pntd.0005430
                5354449
                28264003
                59816141-8422-497a-a79f-556da9897493
                © 2017 Kuo et al

                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
                : 26 October 2016
                : 23 February 2017
                Page count
                Figures: 6, Tables: 1, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: 105-2811-H-002 -024
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: 105-2410-H-002 -218 -MY3
                Award Recipient :
                This work was funded by Taiwan Ministry of Science and Technology (MOST 105-2811-H-002-024, 105-2410-H-002-218-MY3 to CT Chang). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Typhus
                Murine Typhus
                People and Places
                Geographical Locations
                Asia
                Taiwan
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Fleas
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Rodents
                Biology and Life Sciences
                Organisms
                Bacteria
                Rickettsia
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Rickettsia
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Rickettsia
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Cats
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-03-16
                The data have been permanently deposited in figshare: https://doi.org/10.6084/m9.figshare.4698091.v1.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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