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      A retrospective epidemiological analysis of human Cryptosporidium infection in China during the past three decades (1987-2018)

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          Abstract

          Background

          Cryptosporidiosis is an emerging infectious disease of public health significance worldwide. The burden of disease caused by Cryptosporidium varies between and within countries/areas. To have a comprehensive understanding of epidemiological status and characteristics of human Cryptosporidium infection in China since the first report in 1987, a retrospective epidemiological analysis was conducted by presenting differences in the prevalence of Cryptosporidium by province, year, population, living environment and season and possible transmission routes and risk factors as well as genetic characteristics of Cryptosporidium in humans.

          Methodology/Principal findings

          A systematic search was conducted to obtain epidemiological papers of human Cryptosporidium infection/cryptosporidiosis from PubMed and Chinese databases. Finally, 164 papers were included in our analysis. At least 200,054 people from 27 provinces were involved in investigational studies of Cryptosporidium, with an average prevalence of 2.97%. The prevalence changed slightly over time. Variable prevalences were observed: 0.65–11.15% by province, 1.89–47.79% by population, 1.77–12.87% and 0–3.70% in rural and urban areas, respectively. The prevalence peak occurred in summer or autumn. Indirect person-to-person transmission was documented in one outbreak of cryptosporidiosis in a pediatric hospital. 263 Cryptosporidium isolates were obtained, and seven Cryptosporidium species were identified: C. hominis (48.3%), C. andersoni (22.43%), C. parvum (16.7%), C. meleagridis (8.36%), C. felis (3.04%), C. canis (0.76%) and C. suis (0.38%).

          Conclusions/Significances

          This systematic review reflects current epidemiological status and characteristics of Cryptosporidium in humans in China. These data will be helpful to develop efficient control strategies to intervene with and prevent occurrence of human Cryptosporidium infection/cryptosporidiosis in China as well as have a reference effect to other countries. Further studies should focus on addressing a high frequency of C. andersoni in humans and a new challenge with respect to cryptosporidiosis with an increasing population of elderly people and patients with immunosuppressive diseases.

          Author summary

          Cryptosporidium is a major cause of diarrheal disease in humans globally. Due to the lack of effective drug treatment and vaccine prevention against cryptosporidiosis, it is particularly important to develop efficient control strategies to intervene with and prevent Cryptosporidium infection in humans. The present review presented and analyzed epidemiological status and characteristics of Cryptosporidium infection in humans in China since the first report in 1987. To date, epidemiological investigations of Cryptosporidium infecion have been carried out in different populations in 27 provinces, autonomous regions, and municipalities. Average prevalence of Cryptosporidium was 2.97% (5,933/200,054). Like other infectious disease, due to poor sanitation conditions in rural areas, people living in rural areas had a significantly higher prevalence of Cryptosporidium (1.77–12.87%) than those living in urban areas (0–3.70%). Seven Cryptosporidium species were identified, including C. hominis, C. andersoni, C. parvum, C. meleagridis, C. felis, C. canis and C. suis. This retrospective epidemiological analysis indicates wide geographical distribution of human Cryptosporidium infection/cryptosporidiosis in China.

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          Cryptosporidium species in humans and animals: current understanding and research needs.

          Cryptosporidium is increasingly recognized as one of the major causes of moderate to severe diarrhoea in developing countries. With treatment options limited, control relies on knowledge of the biology and transmission of the members of the genus responsible for disease. Currently, 26 species are recognized as valid on the basis of morphological, biological and molecular data. Of the nearly 20 Cryptosporidium species and genotypes that have been reported in humans, Cryptosporidium hominis and Cryptosporidium parvum are responsible for the majority of infections. Livestock, particularly cattle, are one of the most important reservoirs of zoonotic infections. Domesticated and wild animals can each be infected with several Cryptosporidium species or genotypes that have only a narrow host range and therefore have no major public health significance. Recent advances in next-generation sequencing techniques will significantly improve our understanding of the taxonomy and transmission of Cryptosporidium species, and the investigation of outbreaks and monitoring of emerging and virulent subtypes. Important research gaps remain including a lack of subtyping tools for many Cryptosporidium species of public and veterinary health importance, and poor understanding of the genetic determinants of host specificity of Cryptosporidium species and impact of climate change on the transmission of Cryptosporidium.
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            Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010.

            The present update gives a comprehensive review of worldwide waterborne parasitic protozoan outbreaks that occurred and were published globally between January 2004 and December 2010. At least one hundred and ninety-nine outbreaks of human diseases due to the waterborne transmission of parasitic protozoa occurred and were reported during the time period from 2004 to 2010. 46.7% of the documented outbreaks occurred on the Australian continent, 30.6% in North America and 16.5% in Europe. Cryptosporidium spp. was the etiological agent in 60.3% (120) of the outbreaks, Giardia lamblia in 35.2% (70) and other protozoa in 4.5% (9). Four outbreaks (2%) were caused by Toxoplasma gondii, three (1.5%) by Cyclospora cayetanensis. In two outbreaks (1%) Acanthamoeba spp. was identified as the causative agent. In one outbreak, G. lamblia (in 17.6% of stool samples) and Cryptosporidium parvum (in 2.7% of stool samples) as well as Entamoeba histolytica (in 9.4% of stool samples) and Blastocystis hominis (in 8.1% of stool samples) were detected. In those countries that are likely affected most a lack of surveillance systems is noticeable. However, countries that established surveillance systems did not establish an international standardization of reporting systems. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt.

              At least 325 water-associated outbreaks of parasitic protozoan disease have been reported. North American and European outbreaks accounted for 93% of all reports and nearly two-thirds of outbreaks occurred in North America. Over 30% of all outbreaks were documented from Europe, with the UK accounting for 24% of outbreaks, worldwide. Giardia duodenalis and Cryptosporidium parvum account for the majority of outbreaks (132; 40.6% and 165; 50.8%, respectively), Entamoeba histolytica and Cyclospora cayetanensis have been the aetiological agents in nine (2.8%) and six (1.8%) outbreaks, respectively, while Toxoplasma gondii and Isospora belli have been responsible for three outbreaks each (0.9%) and Blastocystis hominis for two outbreaks (0.6%). Balantidium coli, the microsporidia, Acanthamoeba and Naegleria fowleri were responsible for one outbreak, each (0.3%). Their presence in aquatic ecosystems makes it imperative to develop prevention strategies for water and food safety. Human incidence and prevalence-based studies provide baseline data against which risk factors associated with waterborne and foodborne transmission can be identified. Standardized methods are required to maximize public health surveillance, while reporting lessons learned from outbreaks will provide better insight into the public health impact of waterborne pathogenic protozoa.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: Data curationRole: Validation
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Validation
                Role: MethodologyRole: Validation
                Role: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                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
                30 March 2020
                March 2020
                : 14
                : 3
                : e0008146
                Affiliations
                [1 ] Department of Parasitology, Harbin Medical University, Harbin, Heilongjiang, China
                [2 ] National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention; Chinese Center for Tropical Diseases Research; WHO Collaborating Center`for Tropical Diseases; National Center for International Research on Tropical Diseases, Ministry of Science and Technology; Key Laboratory of Parasite and Vector Biology, MOH; Shanghai, China
                University of North Carolina at Chapel Hill, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-8525-500X
                http://orcid.org/0000-0002-1974-0047
                Article
                PNTD-D-19-00751
                10.1371/journal.pntd.0008146
                7145189
                32226011
                62920074-74d2-4bd6-a1e3-7d6d0e8941c2
                © 2020 Liu 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
                : 16 May 2019
                : 17 February 2020
                Page count
                Figures: 5, Tables: 1, Pages: 19
                Funding
                This work was partially supported by the National Science and Technology Major Program of China (No. 2018ZX10713001-004 to YS), the National Natural Science Foundation of China (No. 81772225 to JC) and the Chinese Special Program for Scientific Research of Public Health (No. 201502021 to JC). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. All the authors thank reviewers for their positive and constructive comments on the submitted manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Cryptosporidium
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Cryptosporidium
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Cryptosporidium
                Cryptosporidium Parvum
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Cryptosporidium
                Cryptosporidium Parvum
                Medicine and Health Sciences
                Parasitic Diseases
                Cryptosporidiosis
                People and Places
                Geographical Locations
                Asia
                China
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Cardiobacterium Hominis
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Cardiobacterium Hominis
                Ecology and Environmental Sciences
                Natural Resources
                Water Resources
                Medicine and Health Sciences
                Gastroenterology and Hepatology
                Diarrhea
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Diarrhea
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Diarrhea
                Biology and Life Sciences
                Parasitology
                Parasite Groups
                Apicomplexa
                Oocysts
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-04-09
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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