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      The spatial-temporal distribution of soil-transmitted helminth infections in Guangdong Province, China: A geostatistical analysis of data derived from the three national parasitic surveys

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          Abstract

          Background

          The results of the latest national survey on important human parasitic diseases in 2015–2016 showed Guangdong Province is still a moderately endemic area, with the weighted prevalence of soil-transmitted helminths (STHs) higher than the national average. High-resolution age- and gender-specific spatial-temporal risk maps can support the prevention and control of STHs, but not yet available in Guangdong.

          Methodology

          Georeferenced age- and gender-specific disease data of STH infections in Guangdong Province was derived from three national surveys on important human parasitic diseases, conducted in 1988–1992, 2002–2003, and 2015–2016, respectively. Potential influencing factors (e.g., environmental and socioeconomic factors) were collected from open-access databases. Bayesian geostatistical models were developed to analyze the above data, based on which, high-resolution maps depicting the STH infection risk were produced in the three survey years in Guangdong Province.

          Principal findings

          There were 120, 31, 71 survey locations in the first, second, and third national survey in Guangdong, respectively. The overall population-weighted prevalence of STH infections decreased significantly over time, from 68.66% (95% Bayesian credible interval, BCI: 64.51–73.06%) in 1988–1992 to 0.97% (95% BCI: 0.69–1.49%) in 2015–2016. In 2015–2016, only low to moderate infection risk were found across Guangdong, with hookworm becoming the dominant species. Areas with relatively higher risk (>5%) were mostly distributed in the western region. Females had higher infection risk of STHs than males. The infection risk of A. lumbricoides and T. trichiura were higher in children, while middle-aged and elderly people had higher infection risk of hookworm. Precipitation, elevation, land cover, and human influence index (HII) were significantly related with STH infection risk.

          Conclusions/Significance

          We produced the high-resolution, age- and gender-specific risk maps of STH infections in the three national survey periods across nearly 30 years in Guangdong Province, which can provide important information assisting the control and prevention strategies.

          Author summary

          Even though the overall infection risk of soil-transmitted helminths (STHs) in Guangdong Province decreased over time, it is still higher than the national average. Risk maps can assist spatial-targeting control and intervention. We developed Bayesian geostatistical models based on the data derived from three national surveys on important human parasitic diseases in Guangdong, conducted in 1988–1992, 2002–2003, and 2015–2016, respectively. Based on these, high-resolution, age- and gender-specific infection risk maps were produced. We found that the overall STH infection risk sharply decreased over time, from 68.66% to 0.97%. We identified that moderately endemic risk (>5%) mostly distributed in small areas of western Guangdong, and prevalence in all other areas was below 5% in 2015–2016. The higher infection risk of STHs was found among females. Children were most likely to be infected with A. lumbricoides and T. trichiura, however, middle-aged and elderly people had higher infection risk of hookworm. Therefore, results of this study suggested that the government can pay more attention to people in western Guangdong, especially middle-aged and elderly people engaged in farming. As such, the government may continue to strengthen the monitoring net in the historical endemic areas to avoid the re-infection.

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          Most cited references69

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          Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017

          Summary Background How long one lives, how many years of life are spent in good and poor health, and how the population’s state of health and leading causes of disability change over time all have implications for policy, planning, and provision of services. We comparatively assessed the patterns and trends of healthy life expectancy (HALE), which quantifies the number of years of life expected to be lived in good health, and the complementary measure of disability-adjusted life-years (DALYs), a composite measure of disease burden capturing both premature mortality and prevalence and severity of ill health, for 359 diseases and injuries for 195 countries and territories over the past 28 years. Methods We used data for age-specific mortality rates, years of life lost (YLLs) due to premature mortality, and years lived with disability (YLDs) from the Global Burden of Diseases, Injuries, and Risk Factors Study (GBD) 2017 to calculate HALE and DALYs from 1990 to 2017. We calculated HALE using age-specific mortality rates and YLDs per capita for each location, age, sex, and year. We calculated DALYs for 359 causes as the sum of YLLs and YLDs. We assessed how observed HALE and DALYs differed by country and sex from expected trends based on Socio-demographic Index (SDI). We also analysed HALE by decomposing years of life gained into years spent in good health and in poor health, between 1990 and 2017, and extra years lived by females compared with males. Findings Globally, from 1990 to 2017, life expectancy at birth increased by 7·4 years (95% uncertainty interval 7·1–7·8), from 65·6 years (65·3–65·8) in 1990 to 73·0 years (72·7–73·3) in 2017. The increase in years of life varied from 5·1 years (5·0–5·3) in high SDI countries to 12·0 years (11·3–12·8) in low SDI countries. Of the additional years of life expected at birth, 26·3% (20·1–33·1) were expected to be spent in poor health in high SDI countries compared with 11·7% (8·8–15·1) in low-middle SDI countries. HALE at birth increased by 6·3 years (5·9–6·7), from 57·0 years (54·6–59·1) in 1990 to 63·3 years (60·5–65·7) in 2017. The increase varied from 3·8 years (3·4–4·1) in high SDI countries to 10·5 years (9·8–11·2) in low SDI countries. Even larger variations in HALE than these were observed between countries, ranging from 1·0 year (0·4–1·7) in Saint Vincent and the Grenadines (62·4 years [59·9–64·7] in 1990 to 63·5 years [60·9–65·8] in 2017) to 23·7 years (21·9–25·6) in Eritrea (30·7 years [28·9–32·2] in 1990 to 54·4 years [51·5–57·1] in 2017). In most countries, the increase in HALE was smaller than the increase in overall life expectancy, indicating more years lived in poor health. In 180 of 195 countries and territories, females were expected to live longer than males in 2017, with extra years lived varying from 1·4 years (0·6–2·3) in Algeria to 11·9 years (10·9–12·9) in Ukraine. Of the extra years gained, the proportion spent in poor health varied largely across countries, with less than 20% of additional years spent in poor health in Bosnia and Herzegovina, Burundi, and Slovakia, whereas in Bahrain all the extra years were spent in poor health. In 2017, the highest estimate of HALE at birth was in Singapore for both females (75·8 years [72·4–78·7]) and males (72·6 years [69·8–75·0]) and the lowest estimates were in Central African Republic (47·0 years [43·7–50·2] for females and 42·8 years [40·1–45·6] for males). Globally, in 2017, the five leading causes of DALYs were neonatal disorders, ischaemic heart disease, stroke, lower respiratory infections, and chronic obstructive pulmonary disease. Between 1990 and 2017, age-standardised DALY rates decreased by 41·3% (38·8–43·5) for communicable diseases and by 49·8% (47·9–51·6) for neonatal disorders. For non-communicable diseases, global DALYs increased by 40·1% (36·8–43·0), although age-standardised DALY rates decreased by 18·1% (16·0–20·2). Interpretation With increasing life expectancy in most countries, the question of whether the additional years of life gained are spent in good health or poor health has been increasingly relevant because of the potential policy implications, such as health-care provisions and extending retirement ages. In some locations, a large proportion of those additional years are spent in poor health. Large inequalities in HALE and disease burden exist across countries in different SDI quintiles and between sexes. The burden of disabling conditions has serious implications for health system planning and health-related expenditures. Despite the progress made in reducing the burden of communicable diseases and neonatal disorders in low SDI countries, the speed of this progress could be increased by scaling up proven interventions. The global trends among non-communicable diseases indicate that more effort is needed to maximise HALE, such as risk prevention and attention to upstream determinants of health. Funding Bill & Melinda Gates Foundation.
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            Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.

            The three main soil-transmitted helminth infections, ascariasis, trichuriasis, and hookworm, are common clinical disorders in man. The gastrointestinal tract of a child living in poverty in a less developed country is likely to be parasitised with at least one, and in many cases all three soil-transmitted helminths, with resultant impairments in physical, intellectual, and cognitive development. The benzimidazole anthelmintics, mebendazole and albendazole, are commonly used to remove these infections. The use of these drugs is not limited to treatment of symptomatic soil-transmitted helminth infections, but also for large-scale prevention of morbidity in children living in endemic areas. As a result of data showing improvements in child health and education after deworming, and the burden of disease attributed to soil-transmitted helminths, the worldwide community is awakening to the importance of these infections. Concerns about the sustainability of periodic deworming with benzimidazole anthelmintics and the emergence of resistance have prompted efforts to develop and test new control tools.
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              Global numbers of infection and disease burden of soil transmitted helminth infections in 2010

              Background Quantifying the burden of parasitic diseases in relation to other diseases and injuries requires reliable estimates of prevalence for each disease and an analytic framework within which to estimate attributable morbidity and mortality. Here we use data included in the Global Atlas of Helminth Infection to derive new global estimates of numbers infected with intestinal nematodes (soil-transmitted helminths, STH: Ascaris lumbricoides, Trichuris trichiura and the hookworms) and use disability-adjusted life years (DALYs) to estimate disease burden. Methods Prevalence data for 6,091 locations in 118 countries were sourced and used to estimate age-stratified mean prevalence for sub-national administrative units via a combination of model-based geostatistics (for sub-Saharan Africa) and empirical approaches (for all other regions). Geographical variation in infection prevalence within these units was approximated using modelled logit-normal distributions, and numbers of individuals with infection intensities above given thresholds estimated for each species using negative binomial distributions and age-specific worm/egg burden thresholds. Finally, age-stratified prevalence estimates for each level of infection intensity were incorporated into the Global Burden of Disease Study 2010 analytic framework to estimate the global burden of morbidity and mortality associated with each STH infection. Results Globally, an estimated 438.9 million people (95% Credible Interval (CI), 406.3 - 480.2 million) were infected with hookworm in 2010, 819.0 million (95% CI, 771.7 – 891.6 million) with A. lumbricoides and 464.6 million (95% CI, 429.6 – 508.0 million) with T. trichiura. Of the 4.98 million years lived with disability (YLDs) attributable to STH, 65% were attributable to hookworm, 22% to A. lumbricoides and the remaining 13% to T. trichiura. The vast majority of STH infections (67%) and YLDs (68%) occurred in Asia. When considering YLDs relative to total populations at risk however, the burden distribution varied more considerably within major global regions than between them. Conclusion Improvements in the cartography of helminth infection, combined with mathematical modelling approaches, have resulted in the most comprehensive contemporary estimates for the public health burden of STH. These numbers form an important benchmark upon which to evaluate future scale-up of major control efforts.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Project administrationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                18 July 2022
                July 2022
                : 16
                : 7
                : e0010622
                Affiliations
                [1 ] Department of Medical Statistics, School of Public Health, Sun Yat-sen University, Guangzhou, People’s Republic of China
                [2 ] Sun Yat-sen Global Health Institute, Sun Yat-sen University, Guangzhou, People’s Republic of China
                [3 ] Center for Disease Control and Prevention of Guangdong Province, Guangzhou, People’s Republic of China
                Seoul National University College of Medicine, REPUBLIC OF KOREA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0003-4324-5465
                Article
                PNTD-D-22-00428
                10.1371/journal.pntd.0010622
                9333454
                35849623
                6ed23615-aee6-48b1-bf24-b9d4f3fd87c6
                © 2022 Huang 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
                : 2 April 2022
                : 29 June 2022
                Page count
                Figures: 6, Tables: 4, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 82073665
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003453, Natural Science Foundation of Guangdong Province;
                Award ID: 2022A1515010042
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100012151, Sanming Project of Medicine in Shenzhen;
                Award ID: SZSM201803061
                Award Recipient :
                Funded by: Fundamental Research Funds for the Central Universities, Sun Yat-sen University
                Award ID: 22qntd4201
                Award Recipient :
                YSL was financial supported by the National Natural Science Foundation of China (Grant No. 82073665, https://www.nsfc.gov.cn/), and by the Natural Science Foundation of Guangdong Province (Grant No. 2022A1515010042, http://gdstc.gd.gov.cn/), and by the Sanming Project of Medicine in Shenzhen (Grant No. SZSM201803061), and by the Fundamental Research Funds for the Central Universities, Sun Yat-sen University (Grant No. 22qntd4201). 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
                Epidemiology
                Medical Risk Factors
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Helminth Infections
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Hookworms
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Helminths
                Hookworms
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Ascaris Lumbricoides
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Helminths
                Ascaris Lumbricoides
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Ascaris
                Ascaris Lumbricoides
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Nematoda
                Ascaris
                Ascaris Lumbricoides
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Helminth Infections
                Soil-Transmitted Helminthiases
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Soil-Transmitted Helminthiases
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Biology and Life Sciences
                Population Biology
                Population Dynamics
                Geographic Distribution
                People and Places
                Population Groupings
                Age Groups
                Custom metadata
                vor-update-to-uncorrected-proof
                2022-07-28
                The disease data cannot be shared publicly because of the confidentiality required by Guangdong Provincial Center for Disease Control and Prevention. Researchers can contact Guangdong Provincial Center for Disease Control and Prevention at +86-020-31051692 or sjkzxjfs@ 123456gd.gov.cn to apply for the data. All other data are available from the open-access databases.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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