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      Changing seroprevalence of schistosomiasis japonica in China from 1982 to 2020: A systematic review and spatial analysis

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          Abstract

          Background

          Schistosomiasis is a global public health issue. In China, while the seroprevalence of Schistosomiasis japonica has currently reduced to a relatively low level, risk of infection still exists in certain areas. However, there has been a lack of comprehensive research on the long-term trends of national seroprevalence, changes across age groups, and characteristics in spatial distribution, which is crucial for effectively targeting interventions and achieving the goal of eliminating schistosomiasis by 2030. Our study aimed to address this gap by analyzing the long-term trends of Schistosomiasis japonica seroprevalence in China from 1982 to 2020 based on the data from diverse sources spanning a period of 39 years.

          Methodology

          Seroprevalence data were collected from literature databases and national schistosomiasis surveillance system. Meta-analysis was conducted to estimate the seroprevalence. Joinpoint model was used to identify changing trend and inflection point. Inverse distance weighted interpolation was used to determine the spatial distribution of seroprevalence.

          Principal findings

          The seroprevalence decreased from 34.8% in 1982 to 2.4% in 2020 in China. Before 2006, the seroprevalence was higher in the middle age group, and a pattern of increasing with age was observed afterwards. The areas with high seroprevalence existed in Dongting Lake, Poyang Lake, Jianghan Plain, the Anhui branch of the Yangtze River and some localized mountainous regions in Sichuan and Yunnan provinces.

          Conclusions/Significance

          There was a significant decline in the seroprevalence of Schistosomiasis japonica from 1982 to 2020 in China. Nevertheless, schistosomiasis has not been eradicated; thus, implementing precise and personalized monitoring measures is crucial for the elimination of schistosomiasis, especially in endemic areas and with a particular focus on the elderly.

          Author summary

          Serological immunological testing is a crucial means of monitoring schistosomiasis. In China, while the seroprevalence of Schistosomiasis japonica has currently reduced to a relatively low level, risk of infection still exists in certain areas. Achieving the goal of eliminating schistosomiasis by 2030 necessitates more precise and effective prevention and control measures. Our study intended to figure out the long-term trends of Schistosomiasis japonica seroprevalence in China from 1982 to 2020, focusing on age and spatial variations to identify high-risk areas and populations. We expect that the results can inform the development of targeted measures for schistosomiasis elimination.

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          Most cited references53

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          Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010.

          Measuring disease and injury burden in populations requires a composite metric that captures both premature mortality and the prevalence and severity of ill-health. The 1990 Global Burden of Disease study proposed disability-adjusted life years (DALYs) to measure disease burden. No comprehensive update of disease burden worldwide incorporating a systematic reassessment of disease and injury-specific epidemiology has been done since the 1990 study. We aimed to calculate disease burden worldwide and for 21 regions for 1990, 2005, and 2010 with methods to enable meaningful comparisons over time. We calculated DALYs as the sum of years of life lost (YLLs) and years lived with disability (YLDs). DALYs were calculated for 291 causes, 20 age groups, both sexes, and for 187 countries, and aggregated to regional and global estimates of disease burden for three points in time with strictly comparable definitions and methods. YLLs were calculated from age-sex-country-time-specific estimates of mortality by cause, with death by standardised lost life expectancy at each age. YLDs were calculated as prevalence of 1160 disabling sequelae, by age, sex, and cause, and weighted by new disability weights for each health state. Neither YLLs nor YLDs were age-weighted or discounted. Uncertainty around cause-specific DALYs was calculated incorporating uncertainty in levels of all-cause mortality, cause-specific mortality, prevalence, and disability weights. Global DALYs remained stable from 1990 (2·503 billion) to 2010 (2·490 billion). Crude DALYs per 1000 decreased by 23% (472 per 1000 to 361 per 1000). An important shift has occurred in DALY composition with the contribution of deaths and disability among children (younger than 5 years of age) declining from 41% of global DALYs in 1990 to 25% in 2010. YLLs typically account for about half of disease burden in more developed regions (high-income Asia Pacific, western Europe, high-income North America, and Australasia), rising to over 80% of DALYs in sub-Saharan Africa. In 1990, 47% of DALYs worldwide were from communicable, maternal, neonatal, and nutritional disorders, 43% from non-communicable diseases, and 10% from injuries. By 2010, this had shifted to 35%, 54%, and 11%, respectively. Ischaemic heart disease was the leading cause of DALYs worldwide in 2010 (up from fourth rank in 1990, increasing by 29%), followed by lower respiratory infections (top rank in 1990; 44% decline in DALYs), stroke (fifth in 1990; 19% increase), diarrhoeal diseases (second in 1990; 51% decrease), and HIV/AIDS (33rd in 1990; 351% increase). Major depressive disorder increased from 15th to 11th rank (37% increase) and road injury from 12th to 10th rank (34% increase). Substantial heterogeneity exists in rankings of leading causes of disease burden among regions. Global disease burden has continued to shift away from communicable to non-communicable diseases and from premature death to years lived with disability. In sub-Saharan Africa, however, many communicable, maternal, neonatal, and nutritional disorders remain the dominant causes of disease burden. The rising burden from mental and behavioural disorders, musculoskeletal disorders, and diabetes will impose new challenges on health systems. Regional heterogeneity highlights the importance of understanding local burden of disease and setting goals and targets for the post-2015 agenda taking such patterns into account. Because of improved definitions, methods, and data, these results for 1990 and 2010 supersede all previously published Global Burden of Disease results. Bill & Melinda Gates Foundation. Copyright © 2012 Elsevier Ltd. All rights reserved.
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            Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk.

            An estimated 779 million people are at risk of schistosomiasis, of whom 106 million (13.6%) live in irrigation schemes or in close proximity to large dam reservoirs. We identified 58 studies that examined the relation between water resources development projects and schistosomiasis, primarily in African settings. We present a systematic literature review and meta-analysis with the following objectives: (1) to update at-risk populations of schistosomiasis and number of people infected in endemic countries, and (2) to quantify the risk of water resources development and management on schistosomiasis. Using 35 datasets from 24 African studies, our meta-analysis showed pooled random risk ratios of 2.4 and 2.6 for urinary and intestinal schistosomiasis, respectively, among people living adjacent to dam reservoirs. The risk ratio estimate for studies evaluating the effect of irrigation on urinary schistosomiasis was in the range 0.02-7.3 (summary estimate 1.1) and that on intestinal schistosomiasis in the range 0.49-23.0 (summary estimate 4.7). Geographic stratification showed important spatial differences, idiosyncratic to the type of water resources development. We conclude that the development and management of water resources is an important risk factor for schistosomiasis, and hence strategies to mitigate negative effects should become integral parts in the planning, implementation, and operation of future water projects.
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              Human schistosomiasis.

              Human schistosomiasis--or bilharzia--is a parasitic disease caused by trematode flukes of the genus Schistosoma. By conservative estimates, at least 230 million people worldwide are infected with Schistosoma spp. Adult schistosome worms colonise human blood vessels for years, successfully evading the immune system while excreting hundreds to thousands of eggs daily, which must either leave the body in excreta or become trapped in nearby tissues. Trapped eggs induce a distinct immune-mediated granulomatous response that causes local and systemic pathological effects ranging from anaemia, growth stunting, impaired cognition, and decreased physical fitness, to organ-specific effects such as severe hepatosplenism, periportal fibrosis with portal hypertension, and urogenital inflammation and scarring. At present, preventive public health measures in endemic regions consist of treatment once every 1 or 2 years with the isoquinolinone drug, praziquantel, to suppress morbidity. In some locations, elimination of transmission is now the goal; however, more sensitive diagnostics are needed in both the field and clinics, and integrated environmental and health-care management will be needed to ensure elimination. Copyright © 2014 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Methodology
                Role: ConceptualizationRole: Data curationRole: Methodology
                Role: ConceptualizationRole: Methodology
                Role: ConceptualizationRole: Methodology
                Role: ConceptualizationRole: Methodology
                Role: ConceptualizationRole: Methodology
                Role: Conceptualization
                Role: Conceptualization
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administration
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: Project administrationRole: Writing – original draftRole: 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
                3 September 2024
                September 2024
                : 18
                : 9
                : e0012466
                Affiliations
                [1 ] School of Public Health, Fudan University, Shanghai, China
                [2 ] Key Laboratory of Public Health Safety, Fudan University, Ministry of Education, Shanghai, China
                [3 ] Fudan University Center for Tropical Disease Research, Shanghai, China
                [4 ] Hunan Institute for Schistosomiasis Control, Yueyang, Hunan Province, China
                [5 ] School of Epidemiology and Public Health, Faculty of Medicine, University of Ottawa, Ottawa, Canada
                Federal University of Agriculture Abeokuta, NIGERIA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-4635-0802
                Article
                PNTD-D-24-00174
                10.1371/journal.pntd.0012466
                11398675
                39226311
                4945130b-a99f-48d2-ac53-636c1ce83ca2
                © 2024 Zhou 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
                : 3 February 2024
                : 17 August 2024
                Page count
                Figures: 5, Tables: 0, Pages: 14
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Research Article
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Helminth Infections
                Schistosomiasis
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Schistosomiasis
                People and Places
                Population Groupings
                Age Groups
                People and Places
                Geographical Locations
                Asia
                China
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Helminth Infections
                Schistosomiasis
                Schistosomiasis Japonica
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Schistosomiasis
                Schistosomiasis Japonica
                Physical Sciences
                Mathematics
                Numerical Analysis
                Interpolation
                Medicine and Health Sciences
                Pharmaceutics
                Drug Therapy
                Chemotherapy
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Immune Cells
                Antigen-Presenting Cells
                Biology and Life Sciences
                Immunology
                Immune Cells
                Antigen-Presenting Cells
                Medicine and Health Sciences
                Immunology
                Immune Cells
                Antigen-Presenting Cells
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Serology
                Custom metadata
                vor-update-to-uncorrected-proof
                2024-09-13
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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