Landscape of emerging and re-emerging infectious diseases in China: impact of ecology, climate, and behavior

Abstract

For the past several decades, the infectious disease profile in China has been shifting with rapid developments in social and economic aspects, environment, quality of food, water, housing, and public health infrastructure. Notably, 5 notifiable infectious diseases have been almost eradicated, and the incidence of 18 additional notifiable infectious diseases has been significantly reduced. Unexpectedly, the incidence of over 10 notifiable infectious diseases, including HIV, brucellosis, syphilis, and dengue fever, has been increasing. Nevertheless, frequent infectious disease outbreaks/events have been reported almost every year, and imported infectious diseases have increased since 2015. New pathogens and over 100 new genotypes or serotypes of known pathogens have been identified. Some infectious diseases seem to be exacerbated by various factors, including rapid urbanization, large numbers of migrant workers, changes in climate, ecology, and policies, such as returning farmland to forests. This review summarizes the current experiences and lessons from China in managing emerging and re-emerging infectious diseases, especially the effects of ecology, climate, and behavior, which should have merits in helping other countries to control and prevent infectious diseases.

Keywords

infectious disease profile / emerging infectious diseases / influence factor

References

[1] Tong MX, Hansen A, Hanson-Easey S, Cameron S, Xiang J, Liu Q, Sun Y, Weinstein P, Han GS, Williams C, Bi P. Infectious diseases, urbanization and climate change: challenges in future China. Int J Environ Res Public Health 2015; 12(9): 11025–11036

[2] Xu JG. Behavioral and ecological infectious diseases: from SARS to H7N9 avian influenza outbreak in China. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi ) 2013; 34(5): 417–418 (in Chinese)

[3] Lu J, Milinovich GJ, Hu W. A brief historical overview of emerging infectious disease response in China and the need for a One Health approach in future responses. One Health 2016; 2: 99–102

[4] Yang S, Wu J, Ding C, Cui Y, Zhou Y, Li Y, Deng M, Wang C, Xu K, Ren J, Ruan B, Li L. Epidemiological features of and changes in incidence of infectious diseases in China in the first decade after the SARS outbreak: an observational trend study. Lancet Infect Dis 2017; 17(7): 716–725

[5] Yang W, Li Z, Lan Y, Wang J, Ma J, Jin L, Sun Q, Lv W, Lai S, Liao Y, Hu W. A nationwide web-based automated system for early outbreak detection and rapid response in China. Western Pac Surveill Response J 2011; 2(1): 10–15

[6] Luo HM, Zhang Y, Wang XQ, Yu WZ, Wen N, Yan DM, Wang HQ, Wushouer F, Wang HB, Xu AQ, Zheng JS, Li DX, Cui H, Wang JP, Zhu SL, Feng ZJ, Cui FQ, Ning J, Hao LX, Fan CX, Ning GJ, Yu HJ, Wang SW, Liu DW, Wang DY, Fu JP, Gou AL, Zhang GM, Huang GH, Chen YS, Mi SS, Liu YM, Yin DP, Zhu H, Fan XC, Li XL, Ji YX, Li KL, Tang HS, Xu WB, Wang Y, Yang WZ. Identification and control of a poliomyelitis outbreak in Xinjiang, China. N Engl J Med 2013; 369(21): 1981–1990

[7] Stone R. China. Race to contain plague in quake zone. Science 2010; 328(5978): 559

[8] Yu D. Prevention of plague in China in last 50 years. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2000; 21(4): 300–303 (in Chinese)

[9] Liang X, Bi S, Yang W, Wang L, Cui G, Cui F, Zhang Y, Liu J, Gong X, Chen Y, Wang F, Zheng H, Wang F, Guo J, Jia Z, Ma J, Wang H, Luo H, Li L, Jin S, Hadler SC, Wang Y. Evaluation of the impact of hepatitis B vaccination among children born during 1992–2005 in China. J Infect Dis 2009; 200(1): 39–47

[10] Xiao J, Lin H, Liu T, Zeng W, Li X, Shao X, Tan Q, Xu Y, Xu X, Zheng H, Ma W. Disease burden from hepatitis B virus infection in Guangdong Province, China. Int J Environ Res Public Health 2015; 12(11): 14055–14067

[11] Yezhou L. The National Immunization Plan: China. Australas Med J 2010; 3(7): 375–379

[12] Luo HM, Zhang Y, Wang XQ, Yu WZ, Wen N, Yan DM, Wang HQ, Wushouer F, Wang HB, Xu AQ, Zheng JS, Li DX, Cui H, Wang JP, Zhu SL, Feng ZJ, Cui FQ, Ning J, Hao LX, Fan CX, Ning GJ, Yu HJ, Wang SW, Liu DW, Wang DY, Fu JP, Gou AL, Zhang GM, Huang GH, Chen YS, Mi SS, Liu YM, Yin DP, Zhu H, Fan XC, Li XL, Ji YX, Li KL, Tang HS, Xu WB, Wang Y, Yang WZ. Identification and control of a poliomyelitis outbreak in Xinjiang, China. N Engl J Med 2013; 369(21): 1981–1990

[13] Zhang S, Li RT, Wang Y, Liu Q, Zhou YH, Hu Y. Seroprevalence of hepatitis B surface antigen among pregnant women in Jiangsu, China, 17 years after introduction of hepatitis B vaccine. Int J Gynaecol Obstet 2010; 109(3): 194–197

[14] Lin H, Zou H, Wang Q, Liu C, Lang L, Hou X, Li Z. Short-term effect of El Niño-Southern Oscillation on pediatric hand, foot and mouth disease in Shenzhen, China. PLoS One 2013; 8(7): e65585

[15] Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A, Zhang Y, Yan D, Li Q, Dong X, Zhang J, Zhao Y, Wan J, Feng Z, Sun J, Wang S, Li D, Xu W. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J 2010; 7(1): 94

[16] Ding ZS. An outbreak of water-borne infection by viral hepatitis A. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 1982; 3(2): 80–83 (in Chinese)

[17] Yan YC. Preliminary investigation on the etiology and host animals of epidemic hemorrhagic fever in Honan. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 1982; 3(4): 197–200 (in Chinese)

[18] Hung T, Chen GM, Wang CG, Yao HL, Fang ZY, Chao TX, Chou ZY, Ye W, Chang XJ, Den SS, . Waterborne outbreak of rotavirus diarrhoea in adults in China caused by a novel rotavirus. Lancet 1984; 1(8387): 1139–1142

[19] Lin H, Zhang Z, Lu L, Li X, Liu Q. Meteorological factors are associated with hemorrhagic fever with renal syndrome in Jiaonan County, China, 2006–2011. Int J Biometeorol 2014; 58(6): 1031–1037

[20] Zhang ZF. Investigation of Lyme disease in northeast of China. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 1989; 10(5): 261–264 (in Chinese)

[21] Wang HY. Investigation of an outbreak of HNANB[E] in Shufu County, Xinjiang. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 1989; 10(5): 270–273 (in Chinese)

[22] Zeng Y. HIV infection and AIDS in China. Arch AIDS Res 1992; 6(1-2): 1–5

[23] Zhang TC. Epidemiologic studies of enteritis caused by Campylobacter jejuni. IV. A study of the principal reservoir hosts. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 1985; 6(1): 26–28 (in Chinese)

[24] Deng C. A report on investigation of an outbreak of Legionnaires’ disease in a hotel in Beijing. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 1993; 14(2): 78–80 (in Chinese)

[25] Qu M, Xu J, Ding Y, Wang R, Liu P, Kan B, Qi G, Liu Y, Gao S. Molecular epidemiology of Vibrio cholerae O139 in China: polymorphism of ribotypes and CTX elements. J Clin Microbiol 2003; 41(6): 2306–2310

[26] Hu X, Zhu F, Wang H, Chen S, Wang G, Sun J, Hua C, Yang H. Studies on human streptococcal infectious syndrome caused by infected pigs. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2000; 34(3): 150–152 (in Chinese)

[27] Xu J, Cheng B, Feng L, Jing H, Yang J, Zhao G, Wang H, Li H. Serological investigations on patients with hemolytic uremic syndromes due to enterohemorrhagic Escherichia coli O157:H7 infection. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2002; 23(2): 114–118 (in Chinese)

[28] Enserink M. SARS in China. China’s missed chance. Science 2003; 301(5631): 294–296

[29] Shao Z, Li W, Ren J, Liang X, Xu L, Diao B, Li M, Lu M, Ren H, Cui Z, Zhu B, Dai Z, Zhang L, Chen X, Kan B, Xu J. Identification of a new Neisseria meningitidis serogroup C clone from Anhui Province, China. Lancet 2006; 367(9508): 419–423

[30] Ye C, Zhu X, Jing H, Du H, Segura M, Zheng H, Kan B, Wang L, Bai X, Zhou Y, Cui Z, Zhang S, Jin D, Sun N, Luo X, Zhang J, Gong Z, Wang X, Wang L, Sun H, Li Z, Sun Q, Liu H, Dong B, Ke C, Yuan H, Wang H, Tian K, Wang Y, Gottschalk M, Xu J. Streptococcus suis sequence type 7 outbreak, Sichuan, China. Emerg Infect Dis 2006; 12(8): 1203–1208

[31] Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang XW, Zhang XL, Zhao D, Wang G, Feng Y, Ma J, Liu W, Wang J, Gao GF. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 2005; 309(5738): 1206

[32] Zhang L, Liu Y, Ni D, Li Q, Yu Y, Yu XJ, Wan K, Li D, Liang G, Jiang X, Jing H, Run J, Luan M, Fu X, Zhang J, Yang W, Wang Y, Dumler JS, Feng Z, Ren J, Xu J. Nosocomial transmission of human granulocytic anaplasmosis in China. JAMA 2008; 300(19): 2263–2270

[33] Cao B, Li XW, Mao Y, Wang J, Lu HZ, Chen YS, Liang ZA, Liang L, Zhang SJ, Zhang B, Gu L, Lu LH, Wang DY, Wang C; National Influenza A Pandemic (H1N1) 2009 Clinical Investigation Group of China. Clinical features of the initial cases of 2009 pandemic influenza A (H1N1) virus infection in China. N Engl J Med 2009; 361(26): 2507–2517

[34] Zhang YZ, Zhou DJ, Xiong Y, Chen XP, He YW, Sun Q, Yu B, Li J, Dai YA, Tian JH, Qin XC, Jin D, Cui Z, Luo XL, Li W, Lu S, Wang W, Peng JS, Guo WP, Li MH, Li ZJ, Zhang S, Chen C, Wang Y, de Jong MD, Xu J. Hemorrhagic fever caused by a novel tick-borne Bunyavirus in Huaiyangshan, China. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2011; 32(3): 209–220 (in Chinese)

[35] Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, Zhang L, Zhang QF, Popov VL, Li C, Qu J, Li Q, Zhang YP, Hai R, Wu W, Wang Q, Zhan FX, Wang XJ, Kan B, Wang SW, Wan KL, Jing HQ, Lu JX, Yin WW, Zhou H, Guan XH, Liu JF, Bi ZQ, Liu GH, Ren J, Wang H, Zhao Z, Song JD, He JR, Wan T, Zhang JS, Fu XP, Sun LN, Dong XP, Feng ZJ, Yang WZ, Hong T, Zhang Y, Walker DH, Wang Y, Li DX. Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 2011; 364(16): 1523–1532

[36] Xu B, Liu L, Huang X, Ma H, Zhang Y, Du Y, Wang P, Tang X, Wang H, Kang K, Zhang S, Zhao G, Wu W, Yang Y, Chen H, Mu F, Chen W. Metagenomic analysis of fever, thrombocytopenia and leukopenia syndrome (FTLS) in Henan Province, China: discovery of a new bunyavirus. PLoS Pathog 2011; 7(11): e1002369

[37] Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 2013; 368(20): 1888–1897

[38] Xu L, Stige LC, Chan KS, Zhou J, Yang J, Sang S, Wang M, Yang Z, Yan Z, Jiang T, Lu L, Yue Y, Liu X, Lin H, Xu J, Liu Q, Stenseth NC. Climate variation drives dengue dynamics. Proc Natl Acad Sci USA 2017; 114(1): 113–118

[39] Lu Z, Fu SH, Cao L, Tang CJ, Zhang S, Li ZX, Tusong M, Yao XH, Zhang HL, Wang PY, Wumaier M, Yuan XY, Li MH, Zhu CZ, Fu LP, Liang GD. Human infection with West Nile Virus, Xinjiang, China, 2011. Emerg Infect Dis 2014; 20(8): 1421–1423

[40] Deng YQ, Zhao H, Li XF, Zhang NN, Liu ZY, Jiang T, Gu DY, Shi L, He JA, Wang HJ, Sun ZZ, Ye Q, Xie DY, Cao WC, Qin CF. Isolation, identification and genomic characterization of the Asian lineage Zika virus imported to China. Sci China Life Sci 2016; 59(4): 428–430

[41] Ling Y, Chen J, Huang Q, Hu Y, Zhu A, Ye S, Xu L, Lu H. Yellow fever in a worker returning to China from Angola, March 2016. Emerg Infect Dis 2016; 22(7): 1317–1318

[42] Liu W, Sun FJ, Tong YG, Zhang SQ, Cao WC. Rift Valley fever virus imported into China from Angola. Lancet Infect Dis 2016; 16(11): 1226

[43] Wu J, Yi L, Zou L, Zhong H, Liang L, Song T, Song Y, Su J, Ke C. Imported case of MERS-CoV infection identified in China, May 2015: detection and lesson learned. Euro Surveill 2015; 20(24): 21158

[44] Li H, Zheng YC, Ma L, Jia N, Jiang BG, Jiang RR, Huo QB, Wang YW, Liu HB, Chu YL, Song YD, Yao NN, Sun T, Zeng FY, Dumler JS, Jiang JF, Cao WC. Human infection with a novel tick-borne Anaplasma species in China: a surveillance study. Lancet Infect Dis 2015; 15(6): 663–670

[45] Ye C, Lan R, Xia S, Zhang J, Sun Q, Zhang S, Jing H, Wang L, Li Z, Zhou Z, Zhao A, Cui Z, Cao J, Jin D, Huang L, Wang Y, Luo X, Bai X, Wang Y, Wang P, Xu Q, Xu J. Emergence of a new multidrug-resistant serotype X variant in an epidemic clone of Shigella flexneri. J Clin Microbiol 2010; 48(2): 419–426

[46] Lu Z, Lu XJ, Fu SH, Zhang S, Li ZX, Yao XH, Feng YP, Lambert AJ, Ni X, Wang FT, Tong SX, Nasci RS, Feng Y, Dong Q, Zhai YG, Gao XY, Wang HY, Tang Q, Liang GD. Tahyna virus and human infection, China. Emerg Infect Dis 2009; 15(2): 306–309

[47] Jiang JF, Zheng YC, Jiang RR, Li H, Huo QB, Jiang BG, Sun Y, Jia N, Wang YW, Ma L, Liu HB, Chu YL, Ni XB, Liu K, Song YD, Yao NN, Wang H, Sun T, Cao WC. Epidemiological, clinical, and laboratory characteristics of 48 cases of “Babesia venatorum” infection in China: a descriptive study. Lancet Infect Dis 2015; 15(2): 196–203

[48] Jia N, Jiang JF, Huo QB, Jiang BG, Cao WC. Rickettsia sibirica subspecies sibirica BJ-90 as a cause of human disease. N Engl J Med 2013; 369(12): 1176–1178

[49] Liu W, Li H, Lu QB, Cui N, Yang ZD, Hu JG, Fan YD, Guo CT, Li XK, Wang YW, Liu K, Zhang XA, Yuan L, Zhao PY, Qin SL, Cao WC. Candidatus Rickettsia tarasevichiae infection in Eastern Central China: a case series. Ann Intern Med 2016; 164(10): 641–648

[50] Jia N, Zheng YC, Ma L, Huo QB, Ni XB, Jiang BG, Chu YL, Jiang RR, Jiang JF, Cao WC. Human infections with Rickettsia raoultii, China. Emerg Infect Dis 2014; 20(5): 866–868

[51] Ni XB, Jia N, Jiang BG, Sun T, Zheng YC, Huo QB, Liu K, Ma L, Zhao QM, Yang H, Wang X, Jiang JF, Cao WC. Lyme borreliosis caused by diverse genospecies of Borrelia burgdorferi sensu lato in northeastern China. Clin Microbiol Infect 2014; 20(8): 808–814

[52] Pan H, Li X, Ge D, Wang S, Wu Q, Xie W, Jiao X, Chu D, Liu B, Xu B, Zhang Y. Factors affecting population dynamics of maternally transmitted endosymbionts in Bemisia tabaci. PLoS One 2012; 7(2): e30760

[53] Walsh MP, Seto J, Jones MS, Chodosh J, Xu W, Seto D. Computational analysis identifies human adenovirus type 55 as a re-emergent acute respiratory disease pathogen. J Clin Microbiol 2010; 48(3): 991–993

[54] Shi Q, Zhou W, Chen C, Gao C, Xiao K, Wang J, Zhang BY, Wang Y, Zhang F, Dong XP. Quality evaluation for the surveillance system of human prion diseases in China based on the data from 2010 to 2016. Prion 2016; 10(6): 484–491

[55] Zhang YZ, He YW, Dai YA, Xiong Y, Zheng H, Zhou DJ, Li J, Sun Q, Luo XL, Cheng YL, Qin XC, Tian JH, Chen XP, Yu B, Jin D, Guo WP, Li W, Wang W, Peng JS, Zhang GB, Zhang S, Chen XM, Wang Y, Li MH, Li Z, Lu S, Ye C, de Jong MD, Xu J. Hemorrhagic fever caused by a novel Bunyavirus in China: pathogenesis and correlates of fatal outcome. Clin Infect Dis 2012; 54(4): 527–533

[56] Zhu B, Xu Z, Du P, Xu L, Sun X, Gao Y, Shao Z. Sequence type 4821 clonal complex serogroup B Neisseria meningitidis in China, 1978–2013. Emerg Infect Dis 2015; 21(6): 925–932

[57] Du P, Zheng H, Zhou J, Lan R, Ye C, Jing H, Jin D, Cui Z, Bai X, Liang J, Liu J, Xu L, Zhang W, Chen C, Xu J. Detection of multiple parallel transmission outbreak of Streptococcus suis human infection by use of genome epidemiology, China, 2005. Emerg Infect Dis 2017; 23(2): 204–211

[58] Ye C, Zheng H, Zhang J, Jing H, Wang L, Xiong Y, Wang W, Zhou Z, Sun Q, Luo X, Du H, Gottschalk M, Xu J. Clinical, experimental, and genomic differences between intermediately pathogenic, highly pathogenic, and epidemic Streptococcus suis. J Infect Dis 2009; 199(1): 97–107

[59] Xiong Y, Wang P, Lan R, Ye C, Wang H, Ren J, Jing H, Wang Y, Zhou Z, Bai X, Cui Z, Luo X, Zhao A, Wang Y, Zhang S, Sun H, Wang L, Xu J. A novel Escherichia coli O157:H7 clone causing a major hemolytic uremic syndrome outbreak in China. PLoS One 2012; 7(4): e36144

[60] Zhang N, Lan R, Sun Q, Wang J, Wang Y, Zhang J, Yu D, Hu W, Hu S, Dai H, Du P, Wang H, Xu J. Genomic portrait of the evolution and epidemic spread of a recently emerged multidrug-resistant Shigella flexneri clone in China. J Clin Microbiol 2014; 52(4): 1119–1126

[61] Lu QB, Tong YG, Wo Y, Wang HY, Liu EM, Gray GC, Liu W, Cao WC. Epidemiology of human adenovirus and molecular characterization of human adenovirus 55 in China, 2009–2012. Influenza Other Respir Viruses 2014; 8(3): 302–308

[62] Chen M, Zhu Z, Huang F, Liu D, Zhang T, Ying D, Wu J, Xu W. Adenoviruses associated with acute respiratory diseases reported in Beijing from 2011 to 2013. PLoS One 2015; 10(3): e0121375

[63] Huang G, Yao W, Yu W, Mao L, Sun H, Yao W, Tian J, Wang L, Bo Z, Zhu Z, Zhang Y, Zhao Z, Xu W. Outbreak of epidemic keratoconjunctivitis caused by human adenovirus type 56, China, 2012. PLoS One 2014; 9(10): e110781

[64] Mei YF, Skog J, Lindman K, Wadell G. Comparative analysis of the genome organization of human adenovirus 11, a member of the human adenovirus species B, and the commonly used human adenovirus 5 vector, a member of species C. J Gen Virol 2003; 84(8): 2061–2071

[65] Zhang YZ, Xu J. The emergence and cross species transmission of newly discovered tick-borne Bunyavirus in China. Curr Opin Virol 2016; 16: 126–131

[66] Dong X, Chen XP, Liu N, Dumler SJ, Zhang YZ. Co-circulation of multiple species of Rickettsiales bacteria in one single species of hard ticks in Shenyang, China. Ticks Tick Borne Dis 2014; 5(6): 727–733

[67] Li K, Lin XD, Wang W, Shi M, Guo WP, Zhang XH, Xing JG, He JR, Wang K, Li MH, Cao JH, Jiang ML, Holmes EC, Zhang YZ. Isolation and characterization of a novel arenavirus harbored by rodents and shrews in Zhejiang Province, China. Virology 2015; 476: 37–42

[68] Blasdell KR, Duong V, Eloit M, Chretien F, Ly S, Hul V, Deubel V, Morand S, Buchy P. Evidence of human infection by a new mammarenavirus endemic to Southeastern Asia. eLife 2016; 5: e1313519

[69] Zhang JZ, Fan MY, Bi DZ, Cui WF, Han YF. Genotypic identification of three new strains of spotted fever group rickettsiae isolated in China. Acta Virol 1996; 40(4): 215–219

[70] Chen XP, Dong YJ, Guo WP, Wang W, Li MH, Xu J, Dumler JS, Zhang YZ. Detection of Wolbachia genes in a patient with non-Hodgkin’s lymphoma. Clin Microbiol Infect 2015; 21(2):182 e181–184

[71] Fang LQ, Liu K, Li XL, Liang S, Yang Y, Yao HW, Sun RX, Sun Y, Chen WJ, Zuo SQ, Ma MJ, Li H, Jiang JF, Liu W, Yang XF, Gray GC, Krause PJ, Cao WC. Emerging tick-borne infections in mainland China: an increasing public health threat. Lancet Infect Dis 2015; 15(12): 1467–1479

[72] Lu L, Lin H, Tian L, Yang W, Sun J, Liu Q. Time series analysis of dengue fever and weather in Guangzhou, China. BMC Public Health 2009; 9(1): 395

[73] Lin H, Liu T, Song T, Lin L, Xiao J, Lin J, He J, Zhong H, Hu W, Deng A, Peng Z, Ma W, Zhang Y. Community involvement in Dengue outbreak control: an integrated rigorous intervention strategy. PLoS Negl Trop Dis 2016; 10(8): e0004919

[74] Lai S, Zhou H, Xiong W, Gilbert M, Huang Z, Yu J, Yin W, Wang L, Chen Q, Li Y, Mu D, Zeng L, Ren X, Geng M, Zhang Z, Cui B, Li T, Wang D, Li Z, Wardrop NA, Tatem AJ, Yu H. Changing epidemiology of human brucellosis, China, 1955–2014. Emerg Infect Dis 2017; 23(2): 184–194

[75] Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. The new global map of human brucellosis. Lancet Infect Dis 2006; 6(2): 91–99

[76] Kan B, Wang M, Jing H, Xu H, Jiang X, Yan M, Liang W, Zheng H, Wan K, Liu Q, Cui B, Xu Y, Zhang E, Wang H, Ye J, Li G, Li M, Cui Z, Qi X, Chen K, Du L, Gao K, Zhao YT, Zou XZ, Feng YJ, Gao YF, Hai R, Yu D, Guan Y, Xu J. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. J Virol 2005; 79(18): 11892–11900

[77] Wang M, Yan M, Xu H, Liang W, Kan B, Zheng B, Chen H, Zheng H, Xu Y, Zhang E, Wang H, Ye J, Li G, Li M, Cui Z, Liu YF, Guo RT, Liu XN, Zhan LH, Zhou DH, Zhao A, Hai R, Yu D, Guan Y, Xu J. SARS-CoV infection in a restaurant from palm civet. Emerg Infect Dis 2005; 11(12): 1860–1865

[78] Wang M, Di B, Zhou DH, Zheng BJ, Jing H, Lin YP, Liu YF, Wu XW, Qin PZ, Wang YL, Jian LY, Li XZ, Xu JX, Lu EJ, Li TG, Xu J. Food markets with live birds as source of avian influenza. Emerg Infect Dis 2006; 12(11): 1773–1775

[79] Xu J, Lu S, Wang H, Chen C. Reducing exposure to avian influenza H7N9. Lancet 2013; 381(9880): 1815–1816

[80] Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, Wu P, Zhou H, Lau EH, Guo D, Ni MY, Peng Z, Feng L, Jiang H, Luo H, Li Q, Feng Z, Wang Y, Yang W, Leung GM. Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet 2014; 383(9916): 541–548

[81] Pang B, Jing H, Zheng H, Sun H, Zhao A, Xu J. Molecular typing of Shiga-toxin producing Escherichia coli O157:H7 isolated in China with pulsed field gel electrophresis. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2002; 23(2): 123–126 (in Chinese)

[82] Meng Q, Xiong Y, Lan R, Ye C, Wang T, Qi T, Wang Y, Wang H, Bai X, Bai X, Ji S, Jin D, Yuan X, Zhao A, Sun H, Jing H, Xu J. SNP genotyping of enterohemorrhagic Escherichia coli O157:H7 isolates from China and genomic identity of the 1999 Xuzhou outbreak. Infect Genet Evol 2013; 16: 275–281

[83] Xia N, Zhang J, Li S, Ge S, Wu T, Zheng Z, Wu W, Shi W. Advances in research on HEV. J Xiamen Univ (Natural Science Edition) (Xiamen Da Xue Xue Bao (Zi Ran Ke Xue Ban)) 2011; 50(2): 431–436 (in Chinese)

[84] Zhang W, He Y, Wang H, Shen Q, Cui L, Wang X, Shao S, Hua X. Hepatitis E virus genotype diversity in eastern China. Emerg Infect Dis 2010; 16(10): 1630–1632

[85] Ning H, Niu Z, Yu R, Zhang P, Dong S, Li Z. Identification of genotype 3 hepatitis E virus in fecal samples from a pig farm located in a Shanghai suburb. Vet Microbiol 2007; 121(1-2): 125–130

[86] Liu P, Li L, Wang L, Bu Q, Fu H, Han J, Zhu Y, Lu F, Zhuang H. Phylogenetic analysis of 626 hepatitis E virus (HEV) isolates from humans and animals in China (1986–2011) showing genotype diversity and zoonotic transmission. Infect Genet Evol 2012; 12(2): 428–434

[87] Kyle JL, Harris E. Global spread and persistence of dengue. Annu Rev Microbiol 2008; 62(1): 71–92

[88] Wang L, Zhou P, Fu X, Zheng Y, Huang S, Fang B, Zhang G, Jia K, Li S. Yellow fever virus: Increasing imported cases in China. J Infect 2016; 73(4): 377–380

[89] Xiang B, Gao P, Kang Y, Ren T. Importation of Zika Virus in China: a significant risk in southern China. J Infect 2017; 74(3): 328–330

[90] Song T, Kang M, Zhang Y, Liang L, Lin H. Elements of successful management of an imported Middle East respiratory syndrome case in Guangdong, China. Western Pac Surveill Response J 2015; 6(4): 33–34

[91] Lin H, Lu L, Tian L, Zhou S, Wu H, Bi Y, Ho SC, Liu Q. Spatial and temporal distribution of falciparum malaria in China. Malar J 2009; 8(1): 130

[92] Sang S, Chen B, Wu H, Yang Z, Di B, Wang L, Tao X, Liu X, Liu Q. Dengue is still an imported disease in China: a case study in Guangzhou. Infect Genet Evol 2015; 32:178–190

[93] Li X, Liu T, Lin L, Song T, Du X, Lin H, Xiao J, He J, Liu L, Zhu G, Zeng W, Guo L, Cao Z, Ma W, Zhang Y. Application of the analytic hierarchy approach to the risk assessment of Zika virus disease transmission in Guangdong Province, China. BMC Infect Dis 2017; 17(1): 65

[94] Liu AY, Zang WJ, Yuan LL, Chai YL, Wang S. Latent syphilis among inpatients in an urban area of China. Glob J Health Sci 2014; 7(3): 249–253

[95] Wu Z, Rou K, Detels R. Prevalence of HIV infection among former commercial plasma donors in rural eastern China. Health Policy Plan 2001; 16(1): 41–46

[96] Chen ZQ, Zhang GC, Gong XD, Lin C, Gao X, Liang GJ, Yue XL, Chen XS, Cohen MS. Syphilis in China: results of a national surveillance programme. Lancet 2007; 369(9556): 132–138

[97] Tan NX, Messina JP, Yang LG, Yang B, Emch M, Chen XS, Cohen MS, Tucker JD. A spatial analysis of county-level variation in syphilis and gonorrhea in Guangdong Province, China. PLoS One 2011; 6(5): e19648

[98] Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P. Host and viral traits predict zoonotic spillover from mammals. Nature 2017; 546(7660): 646–650

[99] Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 2015;4:e05378.

[100] Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ. Redefining the invertebrate RNA virosphere. Nature 2016; 540(7634): 539–543

[101] Meng X, Lu S, Yang J, Jin D, Wang X, Bai X, Wen Y, Wang Y, Niu L, Ye C, Rosselló-Móra R, Xu J. Metataxonomics reveal vultures as a reservoir for Clostridium perfringens. Emerg Microbes Infect 2017; 6(2): e9

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (Nos. L1522033, 81290340, and 81290345) and the National Key Research and Development Program of China (No. 2016YFC1201903). We thank the two anonymous reviewers for the improvement of this study. We also extend our gratitude to Dr. Hualiang Lin and Prof. Xinhe Lai for the revision and discussion.

Compliance with ethics guidelines

Qiyong Liu, Wenbo Xu, Shan Lu, Jiafu Jiang, Jieping Zhou, Zhujun Shao, Xiaobo Liu, Lei Xu, Yanwen Xiong, Han Zheng, Sun Jin, Hai Jiang, Wuchun Cao, and Jianguo Xu declare that they have no financial conflicts of interest. This manuscript is a review article and does not involve a research protocol requiring approval by a relevant institutional review board or ethics committee.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11684-017-0605-9 and is accessible for authorized users.

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