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Population Based Hospitalization Burden of Laboratory-Confirmed Hand, Foot and Mouth Disease Caused by Multiple Enterovirus Serotypes in Southern China

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Population Based Hospitalization Burden of Laboratory-Confirmed Hand, Foot and Mouth Disease Caused by Multiple Enterovirus Serotypes in Southern China RESEARCH ARTICLE Population based hospitalization burden of laboratory-confirmed hand, foot and mouth disease caused by multiple enterovirus serotypes in Southern China 1☯ 1,2☯ 2☯ 3☯ 4 Shuanbao Yu , Qiaohong Liao , Yonghong Zhou , Shixiong Hu , Qi ChenID , Kaiwei Luo3, Zhenhua Chen5, Li Luo1, Wei Huang3, Bingbing Dai6, Min He6, Fengfeng Liu1, 2 2 7,8 1,2 Qi Qiu , Lingshuang Ren , H. Rogier van Doorn , Hongjie YuID * a1111111111 a1111111111 1 Division of Infectious Disease, Key Laboratory of Surveillance and Early-warning on Infectious Disease, Chinese Center for Disease Control and Prevention, Beijing, China, 2 School of Public Health, Fudan a1111111111 University, Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, China, 3 Hunan a1111111111 Provincial Center for Disease Control and Prevention, Changsha, Hunan Province, China, 4 Hubei Provincial a1111111111 Center for Disease Control and Prevention, Wuhan, Hubei Province, China, 5 Chengdu Center for Disease Control and Prevention, Chengdu, Sichuan Province, China, 6 Anhua County Center for Disease Control and Prevention, Anhua, Hunan Province, China, 7 Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom, 8 Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam OPEN ACCESS ☯ These authors contributed equally to this work. Citation: Yu S, Liao Q, Zhou Y, Hu S, Chen Q, Luo * [email protected] K, et al. (2018) Population based hospitalization burden of laboratory-confirmed hand, foot and mouth disease caused by multiple enterovirus Abstract serotypes in Southern China. PLoS ONE 13(12): e0203792. https://doi.org/10.1371/journal. pone.0203792 Background Editor: MaeÈl Bessaud, Institut Pasteur, FRANCE Hand, foot and mouth disease (HFMD) is spread widely across Asia, and the hospitalization Received: August 23, 2018 burden is currently not well understood. Here, we estimated serotype-specific and age-spe- Accepted: November 30, 2018 cific hospitalization rates of HFMD in Southern China. Published: December 13, 2018 Copyright: © 2018 Yu et al. This is an open access Methods article distributed under the terms of the Creative We enrolled pediatric HFMD patients admitted to 3/3 county-level hospitals, and 3/23 town- Commons Attribution License, which permits unrestricted use, distribution, and reproduction in ship-level hospitals in Anhua county, Hunan (CN). Samples were collected to identify entero- any medium, provided the original author and virus serotypes by RT-PCRs between October 2013 and September 2016. Information on source are credited. other eligible, but un-enrolled, patients were retrospectively collected from the same six hos- Data Availability Statement: All relevant data are pitals. Monthly numbers of all-cause hospitalizations were collected from each of the 23 town- within the manuscript and its Supporting ship-level hospitals to extrapolate hospitalizations associated with HFMD among these. Information files. Funding: This work was supported by grants from Results the National Science Fund for Distinguished Young Scholars (no. 81525023 to Hongjie Yu), the During the three years, an estimated 3,236 pediatric patients were hospitalized with lab-con- National Natural Science Foundation of China (no. firmed HFMD, and among these only one case was severe. The mean hospitalization rate 81473031 to Hongjie Yu), the Li Ka Shing Oxford was 660 (95% CI: 638±684) per 100,000 person-years for lab-confirmed HFMD, with higher Global Health Programme (no. B9RST00-B900.57 to Hongjie Yu), TOTAL foundation (no. 2015±099 rates among CV-A16 and CV-A6 associated HFMD (213 vs 209 per 100,000 person-years), to Hongjie Yu), and Chinese Preventive Medicine and lower among EV-A71, CV-A10 and other enterovirus associated HFMD (134, 39 and 66 PLOS ONE | https://doi.org/10.1371/journal.pone.0203792 December 13, 2018 1 / 15 Hospitalization rates of HFMD in Southern China Association (no. 20101801 to Lidong Gao). The per 100,000 person-years respectively, p<0.001). Children aged 12±23 months had the high- funders had no role in study design, data collection est hospitalization rates (3,594/100,000 person-years), followed by those aged 24±35 months and analysis, decision to publish, or preparation of the manuscript. (1,828/100,000 person-years) and 6±11 months (1,572/100,000 person-years). Compared with other serotypes, CV-A6-associated hospitalizations were evident at younger ages. Competing interests: The authors have declared that no competing interests exist. Conclusions Our study indicates a substantial hospitalization burden associated with non-severe HFMD in a rural county in southern China. Future mitigation policies should take into account the disease burden identified, and optimize interventions for HFMD. Introduction Hand, foot and mouth disease (HFMD) is a common infectious disease that mainly affects children below 5 years of age [1]. HFMD is caused by multiple serotypes of Enterovirus species A, among which enterovirus 71 (EV-A71) and coxsackievirus A16 (CV-A16) are the most fre- quently detected [2]. EV-A71 is of particular concern as it can cause neurological and systemic complications, and even fatal outcomes [2±4]. Coxsackie virus A6 (CV-A6) and Coxsackie virus A10 (CV-A10) have become more prevalent among HFMD outbreaks, with their re- emergence first identified in HFMD cases in Europe and Singapore between 2008 and 2011 [5±8]. These serotypes are also responsible for a considerable proportion of cases of HFMD in China since 2013 [9, 10]. Severe complications associated with CV-A6 and CV-A10 have also been reported [11, 12]. Currently, no specific antiviral treatments are available for HFMD. Three inactivated monovalent EV-A71 vaccines have been licensed in mainland China, with high efficacy (90.0%-97.4%) against EV-A71-HFMD, but no cross-protection against other enterovirus serotype-associated HFMD [13, 14]. Bivalent and multivalent enterovirus vaccines are under development [15, 16]. Since 1997, HFMD has widely spread across Asia, including Malaysia, Japan, Singapore, Vietnam, Cambodia, and China [1, 2, 4, 17±21]. Understanding the age and serotype-specific burden of HFMD, including the hospitalization burden, is valuable in informing healthcare systems, vaccine strategies and other intervention policies. However, the hospitalization bur- den of HFMD has not been thoroughly studied in a well-defined catchment population. Indi- rect estimates of hospitalization rates of HFMD are hampered by limited availability of population-level incidence and unknown hospitalization rates among HFMD cases, however, population-level incidences of HFMD have been estimated in Japan [22], Singapore [23], Malaysia [24], and China [2, 25]. These estimates were based on notifiable surveillance data, which may underestimate the true prevalence. The risk of hospitalization for HFMD varied between 1.3% and 24.3% [26±30], possibly due to patients with distinct severity and different causative serotypes of enterovirus in different studies. The number of people that were included in these studies ranged from 6,027 to 1,081,046 [26±30]. Additionally, there is an increasing threat of enterovirus serotypes of non-EV-A71 among both mild and severe HFMD [7, 11, 25]. Therefore, the specific hospitalization burden of HFMD caused by CV-A6, CV-A10, CV-A16 and other enterovirus serotypes requires further assessment. We aim to estimate population level hospitalization rates of HFMD by age and enterovirus serotype in a well-defined catchment population in China, between October 2013 and Septem- ber 2016. PLOS ONE | https://doi.org/10.1371/journal.pone.0203792 December 13, 2018 2 / 15 Hospitalization rates of HFMD in Southern China Methods Study setting This study was conducted in Anhua County, Yiyang Prefecture, Hunan Province, China [31]. The total population residing in Anhua County was 1,017,463 according to the 2015 census [32]. A total of 165,050 (16%) of the population were children aged <15 years, and of these 61,123 (6%) were aged <5 years [32]. During the study period, there were three county-level hospitals and 23 township-level hospitals in Anhua County where HFMD patients were admit- ted. According to vaccination records, the EV-A71 vaccine was initiated in Anhua County on July 10, 2016. Case definitions A probable case of HFMD was defined as a patient with a rash on their hands, feet, limbs or buttocks, ulcers or vesicles in the mouth, with or without fever. A lab-confirmed case was defined as a probable case with laboratory evidence of enterovirus infection in specimens of stool, rectal swab or throat swab, detected by real-time RT-PCR (reverse transcription-poly- merase chain reaction) or nested RT-PCR. Hospitalized patients were defined as patients admitted to hospital for a period of at least 24 hours. Virological surveillance of HFMD Virological surveillance of HFMD was conducted among six hospitals, including three county- level hospitals and three township-level hospitals between October 2013 and September 2016. The six hospitals selected admitted 87% of the reported HFMD patients from Anhua County during 2010±2012. The methods of virological surveillance have been described elsewhere [31]. Briefly, pediatric patients (aged 0±14 years) who were hospitalized for HFMD, were enrolled after their parents/legal guardians provided verbal consent. Throat swabs and stool samples (rectal swab instead if stool samples were unavailable), were collected within 24 hours of enrollment. A standardized form was used to collect data, including basic demographic information, date of illness onset, types of samples (stool, throat swab, or rectal swab), any complications, and clinical outcome. Swabs were immediately placed in viral transport mediums, and all samples were stored at -70ÊC until testing. Viral RNA was extracted using QIAamp Viral RNA Mini Kit (QIAGEN, Hilden, Germany). RNA from each sample was tested with generic primers and probes target- ing pan-enterovirus conserved regions, and serotype specific primers and probes targeting EV-A71, CV-A16, and CV-A6 (S1 Table). Where a sample tested positive in the generic, but negative in the specific RT-PCRs, nested RT-PCRs were used to amplify VP1 regions.
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