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      The impact of migration and antimicrobial resistance on the transmission dynamics of typhoid fever in Kathmandu, Nepal: A mathematical modelling study

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          Abstract

          Background

          A substantial proportion of the global burden of typhoid fever occurs in South Asia. Kathmandu, Nepal experienced a substantial increase in the number of typhoid fever cases (caused by Salmonella Typhi) between 2000 and 2003, which subsequently declined but to a higher endemic level than in 2000. This epidemic of S. Typhi coincided with an increase in organisms with reduced susceptibility against fluoroquinolones, the emergence of S. Typhi H58, and an increase in the migratory population in Kathmandu.

          Methods

          We devised a mathematical model to investigate the potential epidemic drivers of typhoid in Kathmandu and fit this model to weekly data of S. Typhi cases between April 1997 and June 2011 and the age distribution of S. Typhi cases. We used this model to determine if the typhoid epidemic in Kathmandu was driven by heightened migration, the emergence of organisms with reduced susceptibility against fluoroquinolones or a combination of these factors.

          Results

          Models allowing for the migration of susceptible individuals into Kathmandu alone or in combination with the emergence of S. Typhi with reduced susceptibility against fluoroquinolones provided a good fit for the data. The emergence of organisms with reduced susceptibility against fluoroquinolones organisms alone, either through an increase in disease duration or increased transmission, did not fully explain the pattern of S. Typhi infections.

          Conclusions

          Our analysis is consistent with the hypothesis that the increase in typhoid fever in Kathmandu was associated with the migration of susceptible individuals into the city and aided by the emergence of reduced susceptibility against fluoroquinolones. These data support identifying and targeting migrant populations with typhoid immunization programmes to prevent transmission and disease.

          Author summary

          Typhoid fever is endemic in Nepal, with Kathmandu coined “the typhoid capital of the world”. We developed a mathematical model to assess the importance of migration and antimicrobial resistance on the transmission of typhoid fever in Kathmandu, Nepal from April 1997 to June 2011. During this period, the burden of typhoid fever increased markedly from January 2000 to December 2003, after which the epidemic declined, but to a higher endemic level than in 2000. Our findings are consistent with the hypothesis that migration of susceptible individuals into Kathmandu played an important role in the epidemic, and may have been further aided by the emergence of typhoid fever with reduced susceptibility against fluoroquinolones. This study showed that identifying and targeting migrant populations with control efforts could be an important avenue to prevent typhoid transmission and disease.

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          Most cited references 29

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          Typhoid fever and paratyphoid fever: Systematic review to estimate global morbidity and mortality for 2010

          Background Typhoid and paratyphoid fever remain important causes of morbidity worldwide. Accurate disease burden estimates are needed to guide policy decisions and prevention and control strategies. Methods We conducted a systematic literature review of the PubMed and Scopus databases using pre-defined criteria to identify population-based studies with typhoid fever incidence data published between 1980 and 2009. We also abstracted data from annual reports of notifiable diseases in countries with advanced surveillance systems. Typhoid and paratyphoid fever input data were grouped into regions and regional incidence and mortality rates were estimated. Incidence data were extrapolated across regions for those lacking data. Age-specific incidence rates were derived for regions where age-specific data were available. Crude and adjusted estimates of the global typhoid fever burden were calculated. Results Twenty-five studies were identified, all of which contained incidence data on typhoid fever and 12 on paratyphoid fever. Five advanced surveillance systems contributed data on typhoid fever; 2 on paratyphoid fever. Regional typhoid fever incidence rates ranged from <0.1/100 000 cases/y in Central and Eastern Europe and Central Asia to 724.6/100 000 cases/y in Sub-Saharan Africa. Regional paratyphoid incidence rates ranged from 0.8/100 000 cases/y in North Africa/Middle East to 77.4/100 000 cases/y in Sub-Saharan Africa and South Asia. The estimated total number of typhoid fever episodes in 2010 was 13.5 million (interquartile range 9.1–17.8 million). The adjusted estimate accounting for the low sensitivity of blood cultures for isolation of the bacteria was 26.9 million (interquartile range 18.3–35.7 million) episodes. These findings are comparable to the most recent analysis of global typhoid fever morbidity, which reported crude and adjusted estimates of 10.8 million and 21.7 million typhoid fever episodes globally in 2000. Conclusion Typhoid fever remains a significant health burden, especially in low- and middle-income countries. Despite the availability of more recent data on both enteric fevers, additional research is needed in many regions, particularly Africa, Latin America and other developing countries.
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            Typhoid fever in children aged less than 5 years.

            Calculation of the incidence of typhoid fever during preschool years is important to define the optimum age of immunisation and the choice of vaccines for public-health programmes in developing countries. Hospital-based studies have suggested that children younger than 5 years do not need vaccination against typhoid fever, but this view needs to be re-examined in community-based longitudinal studies. We undertook a prospective follow-up study of residents of a low-income urban area of Delhi, India, with active surveillance for case detection. A baseline census was undertaken in 1995. Between Nov 1, 1995, and Oct 31, 1996, we visited 8172 residents of 1820 households in Kalkaji, Delhi, twice weekly to detect febrile cases. Blood samples were obtained from febrile patients, and those who tested positive for Salmonella typhi were treated with ciprofloxacin. 63 culture-positive typhoid fever cases were detected. Of these, 28 (44%) were in children aged under 5 years. The incidence rate of typhoid per 1000 person-years was 27.3 at age under 5 years, 11.7 at 5-19 years, and 1.1 between 19 and 40 years. The difference in the incidence of typhoid fever between those under 5 years and those aged 5-19 years (15.6 per 1000 person-years [95% CI 4.7-26.5]), and those aged 19-40 years (26.2 [16.0-36.3]) was significant (p<0.001 for both). The difference between the incidence of typhoid at 5-19 years and the incidence at 19-40 years was also significant (10.6 [6.3-14.8], p<0.001). Morbidity in those under 5 and in older people was similar in terms of duration of fever, signs and symptoms, and need for hospital admission. Our findings challenge the common view that typhoid fever is a disorder of school-age children and of adults. Typhoid is a common and significant cause of morbidity between 1 and 5 years of age. The optimum age of typhoid immunisation and the choice of vaccines needs to be reassessed.
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              Current concepts in the diagnosis and treatment of typhoid fever.

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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
                5 May 2017
                May 2017
                : 11
                : 5
                Affiliations
                [1 ]Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, Connecticut, United States of America
                [2 ]David Geffen School of Medicine, University of California Los Angeles, Los Angeles, California, United States of America
                [3 ]Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America
                [4 ]Fogarty International Center, Bethesda, Maryland, United States of America
                [5 ]Oxford University Clinical Research Unit, Patan Academy of Health Sciences, Kathmandu, Nepal
                [6 ]Centre for Tropical Medicine and Global Health, University of Oxford, Oxford, United Kingdom
                [7 ]The Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
                Georgia Southern University Jiann-Ping Hsu College of Public Health, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: NJS BB SB BTG VEP.

                • Formal analysis: NJS CCB VEP.

                • Funding acquisition: NJS BB SB BTG VEP.

                • Investigation: CCB BB AA SD AK SB.

                • Methodology: NJS CCB BTG VEP.

                • Resources: CCB BB AA SD AK SB.

                • Software: NJS CCB BTG VEP.

                • Writing – original draft: NJS VEP.

                • Writing – review & editing: NJS CCB BTG BB AA SD AK SB VEP.

                Article
                PNTD-D-16-02140
                10.1371/journal.pntd.0005547
                5435358
                28475605

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Page count
                Figures: 4, Tables: 2, Pages: 16
                Product
                Funding
                This work was supported by a Belgian American Educational Foundation Postdoctoral Fellowship ( www.baef.be) (NJS), the Wellcome Trust (Strategic Award 106158/Z/14/Z, http://www.wellcome.ac.uk) (NJS, BB, AA, SD, AK, SB, VEP), and the Bill and Melinda Gates Foundation (OPP1141321, http://www.gatesfoundation.org/). 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
                Salmonella
                Salmonella Typhi
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Salmonella
                Salmonella Typhi
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Salmonella
                Salmonella Typhi
                Biology and Life Sciences
                Organisms
                Bacteria
                Enterobacteriaceae
                Salmonella
                Salmonella Typhi
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Typhoid
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Fevers
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Fevers
                People and Places
                Geographical Locations
                Asia
                Nepal
                People and Places
                Population Groupings
                Age Groups
                People and Places
                Demography
                Age Distribution
                Medicine and Health Sciences
                Epidemiology
                Infectious Disease Epidemiology
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Epidemiology
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Salmonellosis
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-05-17
                Data is available as supplementary information.

                Infectious disease & Microbiology

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