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Semi-Arid Regions: a Case Study in Ningxia, China Jie Li1,2†, Xiangxue Zhang3,4†, Li Wang5,6, Chengdong Xu4*, Gexin Xiao7*, Ran Wang1, Fang Zheng1,2 and Fang Wang1,2

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Semi-Arid Regions: a Case Study in Ningxia, China Jie Li1,2†, Xiangxue Zhang3,4†, Li Wang5,6, Chengdong Xu4*, Gexin Xiao7*, Ran Wang1, Fang Zheng1,2 and Fang Wang1,2 Li et al. BMC Public Health (2019) 19:1482 https://doi.org/10.1186/s12889-019-7758-1 RESEARCH ARTICLE Open Access Spatial-temporal heterogeneity of hand, foot and mouth disease and impact of meteorological factors in arid/ semi-arid regions: a case study in Ningxia, China Jie Li1,2†, Xiangxue Zhang3,4†, Li Wang5,6, Chengdong Xu4*, Gexin Xiao7*, Ran Wang1, Fang Zheng1,2 and Fang Wang1,2 Abstract Background: The incidence of hand, foot and mouth disease (HFMD) varies over space and time and this variability is related to climate and social-economic factors. Majority of studies on HFMD were carried out in humid regions while few have focused on the disease in arid/semi-arid regions, more research in such climates would potentially make the mechanism of HFMD transmission clearer under different climate conditions. Methods: In this paper, we explore spatial-temporal distribution of HFMD in Ningxia province, which has an arid/semi- arid climate in northwest China. We first employed a Bayesian space-time hierarchy model (BSTHM) to assess the spatial-temporal heterogeneity of the HFMD cases and its relationship with meteorological factors in Ningxia from 2009 to 2013, then used a novel spatial statistical software package GeoDetector to test the spatial-temporal heterogeneity of HFMD risk. Results: The results showed that the spatial relative risks in northern part of Ningxia were higher than those in the south. The highest temporal risk of HFMD incidence was in fall season, with a secondary peak in spring. Meteorological factors, such as average temperature, relative humidity, and wind speed played significant roles in the spatial-temporal distribution of HFMD risk. Conclusions: The study provide valuable information on HFMD distribution in arid/semi-arid areas in northwest China and facilitate understanding of the concentration of HFMD. Keywords: Hand,Footandmouthdisease,Spatial-temporalvariation,GeoDetector;Bayesianspace-timehierarchical model, Ningxia Background since the early 1970s, while the largest outbreaks of Hand, foot and mouth disease (HFMD) is a common in- HFMD happened in the Asia-Pacific region, for reasons fectious disease, affecting mainly children under 5 years not completely clear [1–3]. HFMD endemic has been re- of age, which is caused by a group of enteroviruses, in ported in Japan since 1967 [4]. In Singapore, nationwide particular Coxsackievirus A16 and Enterovirus 71. Many epidemics occurred periodically with the annual inci- widespread epidemics have been reported worldwide dence rate per 100,000 population increasing from 125.5 in 2001 to 435.9 in 2007 [5]. In China, HFMD preva- * Correspondence: [email protected]; [email protected] lence has been reported from 2007, when several large †Jie Li and Xiangxue Zhang contributed equally to this work. outbreaks of HFMD had occurred [6]. Since 2009, over 4 State Key Laboratory of Resources and Environmental Information System, one million cases of HFMD occurred on a yearly basis Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, 11A, Datun Road, Beijing 100101, China and keeps being one of the most infected diseases in 7China National Center for Food Safety Risk Assessment, Beijing 100022, China. Environmental risk factors such as climatological China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Li et al. BMC Public Health (2019) 19:1482 Page 2 of 11 factors, population factors and economic condition may Methods affect the incidence of HFMD [7]. Study region The occurrence of HFMD showed apparent seasonal- Ningxia Hui Autonomous Region (henceforth Ningxia) ity in countries or regions with distinct climate condi- is located in northwest China (Fig. 1). It has an area of tions. In country level, previous studies demonstrated 66,400 km2 and total population of about 6.82 million in that HFMD incidence showed apparent seasonal vari- 2017. The province is mountainous in the south and ation across China, while HFMD cases were prevalent gradually transforms to flat plain terrain in the north, throughout the year. In Northern Thailand, HFMD oc- which has elevation of slight over 1000 m. Ningxia has a curred throughout the year but peaked in the rainy and typical continental semi-arid climate with annual rainfall cold seasons [8]. In regional level, peaks of HFMD were around 300 mm and evaporation over 1000 mm. The observed in spring and summer (March to July) in rainy season is from June to September. Winter in Henan province (located in eastern central China) [9]. In Ningxia is long and cold, while summer is short and hot, Yixing city (one of the biggest cities in southern China with average annual temperature ranges from 5 to 9 °C. in Jiangsu province) HFMD were also found to be most The areas with flat terrain in the north are more eco- prevalent in summer [10]. nomically developed and industrialized, while in the Most of the previous studies concentrated in areas southern mountainous areas most counties are under- with high HFMD incidence, which are often charac- developed, some of which are even listed as state poverty terized by high population density [11]. Climate in counties of China. high incidence areas are often temperate to humid, such as Hunan, Guangdong, Guangxi and Henan Data provinces [12–20]. On the other hand, HFMD in Data on HFMD were provided by the Chinese Centre arid/semi-arid areas were seldomly studied. To date for Disease Control and Prevention (CDC). As HFMD is (May 2019), only one relevant paper was retrieved by listed as a category C infectious disease, HFMD inci- searching “hfmd arid semi-arid” on Pubmed. Similar dence in China was reported to the CDC via an to other studies, the retrieved paper found that wea- internet-based reporting system, the national disease re- ther factor such as average temperature and relative port system, by the physicians treating the disease and humidity have significant effect on HFMD [21]. In public health personnel. The data for this study included general, the study on HFMD in arid and semi-arid the number of people diagnosed of HFMD in each regions is still limited, more research in such climates county during 1st January 2009 to 31 December 2013 on would potentially make the mechanism of HFMD a monthly basis in Ningxia (Fig. 2). transmission clearer under different climate Monthly meteorological data in the same period were conditions. obtained from China’s Meteorological Data Sharing Ser- Moreover, many previous studies have considered the vice System (http://data.cma.gov.cn/), which included effect of meteorological factors on HFMD in either tem- average temperature, precipitation, relative humidity, air poral or spatial domain in isolation [11, 22]. However, pressure, wind speed, and hours of sunshine based on the spatial and temporal effects are often combined in surveillance stations within Ningxia (Fig. 3). determining the incidence of HFMD. Understanding of spatial-temporal heterogeneity and the combined effects GeoDetector that influence HFMD occurrence would be beneficial for In this study, the spatial and temporal heterogeneity of controlling its incidence and spread. HFMD risk was calculated by GeoDetector q statistic In this study, we analyze the spatial-temporal het- [23–25], as following: erogeneity of HFMD and its relationship with me- XL 1 2 teorological factors in Ningxia province, which is q ¼ 1− N hσh; ð1Þ Nσ2 h¼1 located in northwest China having a semi-arid climate to shed more light on the mechanisms of HFMD where q indicates the level of spatial stratified heterogen- transmission in semi-arid regions. The objectives of eity. q ranges from zero to one, with zero indicates ran- this study are: (1) to map county-level spatial- dom distribution and one indicates strong heterogeneity temporal heterogeneity and variation of HFMD risks between strata. in Ningxia; (2) to detect areas with high incidences of HFMD (hot spots) and areas with low incidences Bayesian space-time hierarchy model (cold spots) and quantify their changes in spatial and In Bayesian space-time hierarchy model (BSTHM), temporal dimension; and (3) to explore the associ- the number of cases yit was modeled by the Poisson ation of meteorological factors with HFMD incidence and log link regression functions, nit was the risk in semi-arid areas. population [26, 27], following as: Li et al. BMC Public Health (2019) 19:1482 Page 3 of 11 Fig. 1 Location of Ningxia province in China and its monthly HFMD incidence (The administrative map in the figure was obtained from the Resource and Environment Data Cloud Platform (http://www.resdc.cn)) y ∼PoissonðÞ n u whereas less than 0.20, was regarded as a cold spot. The it it it X Ã Ã N n other regions were regarded as neither hot nor cold logðÞ¼rit a þ si þ ðÞþb t þ vt b it þ β xnit þ εit; 0 1 n¼1 spots. Then, the regions were further divided depending ð2Þ on the posterior probability p (b1i >0 |hi, data) of local slope b1i [27] bli. If a region that the value was greater where rit represents the relative risk (RR) of HFMD in than 0.8, a faster increasing trend compared with the region i (i =1,2, …, 22) and month t (t =1,2, …,60).α overall trend, was assumed.
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