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      Changing Patterns of Salmonella enterica Serovar Rissen From Humans, Food Animals, and Animal-Derived Foods in China, 1995–2019

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          Abstract

          Salmonellosis represents a growing threat to global public health. Salmonella enterica remains the leading cause of bacterial foodborne diseases in China. Salmonella enterica serovar Rissen ( S. Rissen) has been recognized as one of the emerging serovars among humans in different countries worldwide. However, knowledge on the prevalence of S. Rissen in China is largely lacking. To address essential epidemiological information for S. Rissen in China, a total of 1,182 S. Rissen isolates recovered from samples across the food chain were collected from 16 provinces or province-level cities between 1995 and 2019. Risk factors due to the consumption of animal-derived food products were also analyzed. We found S. Rissen is widely distributed, especially in the Eastern and Southern parts of China, and there is an increasing frequency in recent years as evidenced by the greater number of isolates recovered in 2016, 2017, and 2018. Interestingly, the majority of S. Rissen isolates recovered in this study were from human samples (63.4%; 749/1182), remarkably, 58.4% (438/749) were from asymptomatic carriers. We obtained most of the S. Rissen isolates from humans from Guangxi (59.5%; 446/749) and Shanghai (29.5%; 221/749). Among 302 human diarrheal isolates (40.3%; 302/749), we found 44.6% (139/311) of S. Rissen in children with diarrhea (age below 10 years old). This is of clinical significance as diarrhea is one of the crucial causes of child mortality globally and our findings here highlighted the importance of Salmonella infections in Chinese children. Additionally, S. Rissen isolates were also found to be associated with pork and poultry products in China. This study projected the most updated national-wide study of S. Rissen isolates obtained from different sources in China over the past two decades. Continued surveillance is warranted to further monitor this emerging serovar in China and elsewhere over the world.

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          Most cited references73

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          The global burden of nontyphoidal Salmonella gastroenteritis.

          To estimate the global burden of nontyphoidal Salmonella gastroenteritis, we synthesized existing data from laboratory-based surveillance and special studies, with a hierarchical preference to (1) prospective population-based studies, (2) "multiplier studies," (3) disease notifications, (4) returning traveler data, and (5) extrapolation. We applied incidence estimates to population projections for the 21 Global Burden of Disease regions to calculate regional numbers of cases, which were summed to provide a global number of cases. Uncertainty calculations were performed using Monte Carlo simulation. We estimated that 93.8 million cases (5th to 95th percentile, 61.8-131.6 million) of gastroenteritis due to Salmonella species occur globally each year, with 155,000 deaths (5th to 95th percentile, 39,000-303,000 deaths). Of these, we estimated 80.3 million cases were foodborne. Salmonella infection represents a considerable burden in both developing and developed countries. Efforts to reduce transmission of salmonellae by food and other routes must be implemented on a global scale.
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            Global burden of childhood pneumonia and diarrhoea

            Summary Diarrhoea and pneumonia are the leading infectious causes of childhood morbidity and mortality. We comprehensively reviewed the epidemiology of childhood diarrhoea and pneumonia in 2010–11 to inform the planning of integrated control programmes for both illnesses. We estimated that, in 2010, there were 1·731 billion episodes of diarrhoea (36 million of which progressed to severe episodes) and 120 million episodes of pneumonia (14 million of which progressed to severe episodes) in children younger than 5 years. We estimated that, in 2011, 700 000 episodes of diarrhoea and 1·3 million of pneumonia led to death. A high proportion of deaths occurs in the first 2 years of life in both diseases—72% for diarrhoea and 81% for pneumonia. The epidemiology of childhood diarrhoea and that of pneumonia overlap, which might be partly because of shared risk factors, such as undernutrition, suboptimum breastfeeding, and zinc deficiency. Rotavirus is the most common cause of vaccine-preventable severe diarrhoea (associated with 28% of cases), and Streptococcus pneumoniae (18·3%) of vaccine-preventable severe pneumonia. Morbidity and mortality from childhood pneumonia and diarrhoea are falling, but action is needed globally and at country level to accelerate the reduction.
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              Epidemiology, Clinical Presentation, Laboratory Diagnosis, Antimicrobial Resistance, and Antimicrobial Management of Invasive Salmonella Infections.

              Salmonella enterica infections are common causes of bloodstream infection in low-resource areas, where they may be difficult to distinguish from other febrile illnesses and may be associated with a high case fatality ratio. Microbiologic culture of blood or bone marrow remains the mainstay of laboratory diagnosis. Antimicrobial resistance has emerged in Salmonella enterica, initially to the traditional first-line drugs chloramphenicol, ampicillin, and trimethoprim-sulfamethoxazole. Decreased fluoroquinolone susceptibility and then fluoroquinolone resistance have developed in association with chromosomal mutations in the quinolone resistance-determining region of genes encoding DNA gyrase and topoisomerase IV and also by plasmid-mediated resistance mechanisms. Resistance to extended-spectrum cephalosporins has occurred more often in nontyphoidal than in typhoidal Salmonella strains. Azithromycin is effective for the management of uncomplicated typhoid fever and may serve as an alternative oral drug in areas where fluoroquinolone resistance is common. In 2013, CLSI lowered the ciprofloxacin susceptibility breakpoints to account for accumulating clinical, microbiologic, and pharmacokinetic-pharmacodynamic data suggesting that revision was needed for contemporary invasive Salmonella infections. Newly established CLSI guidelines for azithromycin and Salmonella enterica serovar Typhi were published in CLSI document M100 in 2015.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                29 July 2021
                2021
                : 12
                : 702909
                Affiliations
                [1] 1Department of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences , Hangzhou, China
                [2] 2Agriculture Research Center, Animal Health Research Institute , Cairo, Egypt
                [3] 3National Institutes for Food and Drug Control , Beijing, China
                [4] 4Department of Microbiology Laboratory, Shanghai Municipal Center for Disease Control and Prevention , Shanghai, China
                [5] 5Hainan Institute of Zhejiang University , Sanya, China
                [6] 6State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, National Medical Center for Infectious Diseases, College of Medicine, The First Affiliated Hospital, Zhejiang University , Hangzhou, China
                [7] 7Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine , Hangzhou, China
                Author notes

                Edited by: Yosra A. Helmy, The Ohio State University, United States

                Reviewed by: Jie Zheng, Center for Food Safety and Applied Nutrition, United States Food and Drug Administration, United States; Claudia Hess, University of Veterinary Medicine Vienna, Austria

                *Correspondence: Min Yue, myue@ 123456zju.edu.cn

                These authors have contributed equally to this work

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2021.702909
                8358327
                34394048
                1ea46adc-5ba7-4833-a743-b6c2f8484044
                Copyright © 2021 Elbediwi, Shi, Biswas, Xu and Yue.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 April 2021
                : 25 June 2021
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 75, Pages: 9, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                salmonella,serovar rissen,emerging serovar,public health,foodborne disease
                Microbiology & Virology
                salmonella, serovar rissen, emerging serovar, public health, foodborne disease

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