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      Associations Between Eight Earth Observation‐Derived Climate Variables and Enteropathogen Infection: An Independent Participant Data Meta‐Analysis of Surveillance Studies With Broad Spectrum Nucleic Acid Diagnostics

      research-article
      1 , 2 , 2 , 3 , 4 , 5 , 6 , 7 , 7 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 1 , 22 , 22 , 23 , 24 , 25 , 1 , 4 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 ,
      GeoHealth
      John Wiley and Sons Inc.
      diarrheal disease, infectious diseases, weather, climate, hydrometeorology, pediatrics

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          Abstract

          Diarrheal disease, still a major cause of childhood illness, is caused by numerous, diverse infectious microorganisms, which are differentially sensitive to environmental conditions. Enteropathogen‐specific impacts of climate remain underexplored. Results from 15 studies that diagnosed enteropathogens in 64,788 stool samples from 20,760 children in 19 countries were combined. Infection status for 10 common enteropathogens—adenovirus, astrovirus, norovirus, rotavirus, sapovirus, Campylobacter, ETEC, Shigella, Cryptosporidium and Giardia—was matched by date with hydrometeorological variables from a global Earth observation dataset—precipitation and runoff volume, humidity, soil moisture, solar radiation, air pressure, temperature, and wind speed. Models were fitted for each pathogen, accounting for lags, nonlinearity, confounders, and threshold effects. Different variables showed complex, non‐linear associations with infection risk varying in magnitude and direction depending on pathogen species. Rotavirus infection decreased markedly following increasing 7‐day average temperatures—a relative risk of 0.76 (95% confidence interval: 0.69–0.85) above 28°C—while ETEC risk increased by almost half, 1.43 (1.36–1.50), in the 20–35°C range. Risk for all pathogens was highest following soil moistures in the upper range. Humidity was associated with increases in bacterial infections and decreases in most viral infections. Several virus species' risk increased following lower‐than‐average rainfall, while rotavirus and ETEC increased with heavier runoff. Temperature, soil moisture, and humidity are particularly influential parameters across all enteropathogens, likely impacting pathogen survival outside the host. Precipitation and runoff have divergent associations with different enteric viruses. These effects may engender shifts in the relative burden of diarrhea‐causing agents as the global climate changes.

          Key Points

          • Many pathogens cause diarrhea in children and are affected in different ways by weather conditions like rainfall, temperature, and humidity

          • Diarrhea‐causing bacteria infections increase in warm, humid weather and when soil is moist, though ETEC is sensitive to rainfall extremes

          • High humidity decreases prevalence of several viruses, though only rotavirus increases in cold weather and following heavy surface runoff

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          Most cited references109

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          Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017

          Summary Background Global development goals increasingly rely on country-specific estimates for benchmarking a nation's progress. To meet this need, the Global Burden of Diseases, Injuries, and Risk Factors Study (GBD) 2016 estimated global, regional, national, and, for selected locations, subnational cause-specific mortality beginning in the year 1980. Here we report an update to that study, making use of newly available data and improved methods. GBD 2017 provides a comprehensive assessment of cause-specific mortality for 282 causes in 195 countries and territories from 1980 to 2017. Methods The causes of death database is composed of vital registration (VR), verbal autopsy (VA), registry, survey, police, and surveillance data. GBD 2017 added ten VA studies, 127 country-years of VR data, 502 cancer-registry country-years, and an additional surveillance country-year. Expansions of the GBD cause of death hierarchy resulted in 18 additional causes estimated for GBD 2017. Newly available data led to subnational estimates for five additional countries—Ethiopia, Iran, New Zealand, Norway, and Russia. Deaths assigned International Classification of Diseases (ICD) codes for non-specific, implausible, or intermediate causes of death were reassigned to underlying causes by redistribution algorithms that were incorporated into uncertainty estimation. We used statistical modelling tools developed for GBD, including the Cause of Death Ensemble model (CODEm), to generate cause fractions and cause-specific death rates for each location, year, age, and sex. Instead of using UN estimates as in previous versions, GBD 2017 independently estimated population size and fertility rate for all locations. Years of life lost (YLLs) were then calculated as the sum of each death multiplied by the standard life expectancy at each age. All rates reported here are age-standardised. Findings At the broadest grouping of causes of death (Level 1), non-communicable diseases (NCDs) comprised the greatest fraction of deaths, contributing to 73·4% (95% uncertainty interval [UI] 72·5–74·1) of total deaths in 2017, while communicable, maternal, neonatal, and nutritional (CMNN) causes accounted for 18·6% (17·9–19·6), and injuries 8·0% (7·7–8·2). Total numbers of deaths from NCD causes increased from 2007 to 2017 by 22·7% (21·5–23·9), representing an additional 7·61 million (7·20–8·01) deaths estimated in 2017 versus 2007. The death rate from NCDs decreased globally by 7·9% (7·0–8·8). The number of deaths for CMNN causes decreased by 22·2% (20·0–24·0) and the death rate by 31·8% (30·1–33·3). Total deaths from injuries increased by 2·3% (0·5–4·0) between 2007 and 2017, and the death rate from injuries decreased by 13·7% (12·2–15·1) to 57·9 deaths (55·9–59·2) per 100 000 in 2017. Deaths from substance use disorders also increased, rising from 284 000 deaths (268 000–289 000) globally in 2007 to 352 000 (334 000–363 000) in 2017. Between 2007 and 2017, total deaths from conflict and terrorism increased by 118·0% (88·8–148·6). A greater reduction in total deaths and death rates was observed for some CMNN causes among children younger than 5 years than for older adults, such as a 36·4% (32·2–40·6) reduction in deaths from lower respiratory infections for children younger than 5 years compared with a 33·6% (31·2–36·1) increase in adults older than 70 years. Globally, the number of deaths was greater for men than for women at most ages in 2017, except at ages older than 85 years. Trends in global YLLs reflect an epidemiological transition, with decreases in total YLLs from enteric infections, respiratory infections and tuberculosis, and maternal and neonatal disorders between 1990 and 2017; these were generally greater in magnitude at the lowest levels of the Socio-demographic Index (SDI). At the same time, there were large increases in YLLs from neoplasms and cardiovascular diseases. YLL rates decreased across the five leading Level 2 causes in all SDI quintiles. The leading causes of YLLs in 1990—neonatal disorders, lower respiratory infections, and diarrhoeal diseases—were ranked second, fourth, and fifth, in 2017. Meanwhile, estimated YLLs increased for ischaemic heart disease (ranked first in 2017) and stroke (ranked third), even though YLL rates decreased. Population growth contributed to increased total deaths across the 20 leading Level 2 causes of mortality between 2007 and 2017. Decreases in the cause-specific mortality rate reduced the effect of population growth for all but three causes: substance use disorders, neurological disorders, and skin and subcutaneous diseases. Interpretation Improvements in global health have been unevenly distributed among populations. Deaths due to injuries, substance use disorders, armed conflict and terrorism, neoplasms, and cardiovascular disease are expanding threats to global health. For causes of death such as lower respiratory and enteric infections, more rapid progress occurred for children than for the oldest adults, and there is continuing disparity in mortality rates by sex across age groups. Reductions in the death rate of some common diseases are themselves slowing or have ceased, primarily for NCDs, and the death rate for selected causes has increased in the past decade. Funding Bill & Melinda Gates Foundation.
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            A modified poisson regression approach to prospective studies with binary data.

            G Zou (2004)
            Relative risk is usually the parameter of interest in epidemiologic and medical studies. In this paper, the author proposes a modified Poisson regression approach (i.e., Poisson regression with a robust error variance) to estimate this effect measure directly. A simple 2-by-2 table is used to justify the validity of this approach. Results from a limited simulation study indicate that this approach is very reliable even with total sample sizes as small as 100. The method is illustrated with two data sets.
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              Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study.

              Diarrhoeal diseases cause illness and death among children younger than 5 years in low-income countries. We designed the Global Enteric Multicenter Study (GEMS) to identify the aetiology and population-based burden of paediatric diarrhoeal disease in sub-Saharan Africa and south Asia. The GEMS is a 3-year, prospective, age-stratified, matched case-control study of moderate-to-severe diarrhoea in children aged 0-59 months residing in censused populations at four sites in Africa and three in Asia. We recruited children with moderate-to-severe diarrhoea seeking care at health centres along with one to three randomly selected matched community control children without diarrhoea. From patients with moderate-to-severe diarrhoea and controls, we obtained clinical and epidemiological data, anthropometric measurements, and a faecal sample to identify enteropathogens at enrolment; one follow-up home visit was made about 60 days later to ascertain vital status, clinical outcome, and interval growth. We enrolled 9439 children with moderate-to-severe diarrhoea and 13,129 control children without diarrhoea. By analysing adjusted population attributable fractions, most attributable cases of moderate-to-severe diarrhoea were due to four pathogens: rotavirus, Cryptosporidium, enterotoxigenic Escherichia coli producing heat-stable toxin (ST-ETEC; with or without co-expression of heat-labile enterotoxin), and Shigella. Other pathogens were important in selected sites (eg, Aeromonas, Vibrio cholerae O1, Campylobacter jejuni). Odds of dying during follow-up were 8·5-fold higher in patients with moderate-to-severe diarrhoea than in controls (odd ratio 8·5, 95% CI 5·8-12·5, p<0·0001); most deaths (167 [87·9%]) occurred during the first 2 years of life. Pathogens associated with increased risk of case death were ST-ETEC (hazard ratio [HR] 1·9; 0·99-3·5) and typical enteropathogenic E coli (HR 2·6; 1·6-4·1) in infants aged 0-11 months, and Cryptosporidium (HR 2·3; 1·3-4·3) in toddlers aged 12-23 months. Interventions targeting five pathogens (rotavirus, Shigella, ST-ETEC, Cryptosporidium, typical enteropathogenic E coli) can substantially reduce the burden of moderate-to-severe diarrhoea. New methods and accelerated implementation of existing interventions (rotavirus vaccine and zinc) are needed to prevent disease and improve outcomes. The Bill & Melinda Gates Foundation. Copyright © 2013 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                mkosek@virginia.edu
                Journal
                Geohealth
                Geohealth
                10.1002/(ISSN)2471-1403
                GH2
                GeoHealth
                John Wiley and Sons Inc. (Hoboken )
                2471-1403
                January 2022
                01 January 2022
                : 6
                : 1 ( doiID: 10.1002/gh2.v6.1 )
                : e2021GH000452
                Affiliations
                [ 1 ] Division of Infectious Diseases and International Health University of Virginia School of Medicine Charlottesville VA USA
                [ 2 ] Department of Earth and Planetary Sciences Johns Hopkins Krieger School of Arts and Sciences Baltimore MA USA
                [ 3 ] Division of Viral Diseases US Centers for Disease Control and Prevention Atlanta GA USA
                [ 4 ] Department of Pediatrics and Child Health Aga Khan University Karachi Pakistan
                [ 5 ] Department of Pediatrics National Academy of Medical Sciences Kanti Children's Hospital Kathmandu Nepal
                [ 6 ] Division of Infectious Diseases Programme for Emerging Infections International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B) Dhaka Bangladesh
                [ 7 ] Department of Infectious Disease Epidemiology Bernhard Nocht Institute for Tropical Medicine (BNITM) Hamburg Germany
                [ 8 ] Centre for Infectious Disease Research in Zambia Lusaka Zambia
                [ 9 ] Department of Pediatrics Vanderbilt University Medical Center Nashville TN USA
                [ 10 ] Centre pour le Développement des Vaccins, Mali Bamako Mali
                [ 11 ] Medical Research Council Unit The Gambia at the London School of Hygiene & Tropical Medicine Banjul The Gambia
                [ 12 ] Epidemiology and Health Economics GSK Vaccine Wavre Belgium
                [ 13 ] Department of Pediatrics and Child Health The Aga Khan University Karachi Pakistan
                [ 14 ] National Institute of Cholera and Enteric Diseases Kolkata India
                [ 15 ] Centro de Investigação em Saúde de Manhiça Manhiça Mozambique
                [ 16 ] Centre for Nutrition & Food Security International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B) Dhaka Bangladesh
                [ 17 ] Department of Pediatrics University of Maryland School of Medicine Baltimore MD USA
                [ 18 ] Departments of Medicine and Pediatrics Center for Vaccine Development and Global Health University of Maryland School of Medicine Baltimore MD USA
                [ 19 ] Global Health Rollins School of Public Health Emory University Atlanta GA USA
                [ 20 ] Kenya Medical Research Institute Center for Global Health Research Kisumu Kenya
                [ 21 ] Centre for Enteric Diseases National Institute for Communicable Diseases Pretoria South Africa
                [ 22 ] Center for Child, Adolescent and Maternal Health Research Tampere University Tampere Finland
                [ 23 ] Department of Child Health Institute of Medicine of Tribhuvan University Kirtipur Nepal
                [ 24 ] Division of Nutrition and Clinical Services International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B) Dhaka Bangladesh
                [ 25 ] Haydom Global Health Institute Haydom Tanzania
                [ 26 ] HIV/AIDS & Global Health Research Programme University of Venda Thohoyandou South Africa
                [ 27 ] Asociacion Benefica PRISMA Iquitos Peru
                [ 28 ] Department of Physiology and Pharmacology Faculty of Medicine Federal University of Ceará Fortaleza Brazil
                [ 29 ] Department of Gastrointestinal Sciences Christian Medical College Vellore India
                [ 30 ] Department of International Health Johns Hopkins Bloomberg School of Public Health Baltimore MA USA
                [ 31 ] Centre for Genomics and Child Health Blizard Institute Queen Mary University of London London UK
                [ 32 ] Zvitambo Institute for Maternal and Child Health Research Harare Zimbabwe
                [ 33 ] Research Institute for Microbial Diseases Osaka University Osaka Japan
                [ 34 ] Department of Medical Sciences National Institute of Health Nonthaburi Thailand
                [ 35 ] Department of Epidemiology Colorado School of Public Health Center for Global Health Aurora CO USA
                [ 36 ] Pediatric Infectious Diseases Hospital Roosevelt Guatemala City Guatemala
                [ 37 ] Children's Hospital Helsinki University Central Hospital Helsinki Finland
                [ 38 ] Hospital Pediátrico David Bernardino Luanda Angola
                [ 39 ] Division of Infectious Diseases and International Health and Public Health Sciences University of Virginia School of Medicine Charlottesville VA USA
                Author notes
                [*] [* ] Correspondence to:

                M. N. Kosek,

                mkosek@ 123456virginia.edu

                Author information
                https://orcid.org/0000-0003-4567-5813
                https://orcid.org/0000-0002-0698-0658
                https://orcid.org/0000-0002-9808-2344
                https://orcid.org/0000-0003-3053-476X
                https://orcid.org/0000-0002-2378-4720
                https://orcid.org/0000-0001-5845-4417
                https://orcid.org/0000-0002-1225-7933
                https://orcid.org/0000-0002-7688-9059
                Article
                GH2300 2021GH000452
                10.1029/2021GH000452
                8729196
                35024531
                990cccd5-c911-4663-bc8d-bbd8cf3f1d33
                © 2021 The Authors. GeoHealth published by Wiley Periodicals LLC on behalf of American Geophysical Union.

                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
                : 12 October 2021
                : 11 May 2021
                : 18 November 2021
                Page count
                Figures: 5, Tables: 1, Pages: 20, Words: 13668
                Funding
                Funded by: NASA's Group on Earth Observations Work Programme
                Award ID: 16‐GEO16‐0047
                Funded by: The Bill and Melinda Gates Foundation
                Award ID: OPP1066146
                Funded by: University of Virginia
                Categories
                Geohealth
                Impacts of Climate Change: Human Health,
                Public Health
                General or Miscellaneous
                Research Article
                Research Article
                Custom metadata
                2.0
                January 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.7.0 mode:remove_FC converted:05.01.2022

                diarrheal disease,infectious diseases,weather,climate,hydrometeorology,pediatrics

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