Urbanization prolongs hantavirus epidemics in cities

Significance Urbanization reduces exposure risk to many wildlife parasites and in general, improves overall health. However, our study importantly shows the complicated relationship between the diffusion of zoonotic pathogens and urbanization. Here, we reveal an unexpected relationship between hemorrhagic fever with renal syndrome incidence caused by a severe rodent-borne zoonotic pathogen worldwide and the process of urbanization in developing China. Our findings show that the number of urban immigrants is highly correlated with human incidence over time and also explain how the endemic turning points are associated with economic growth during the urbanization process. Our study shows that urbanizing regions of the developing world should focus their attention on zoonotic diseases. Urbanization and rural–urban migration are two factors driving global patterns of disease and mortality. There is significant concern about their potential impact on disease burden and the effectiveness of current control approaches. Few attempts have been made to increase our understanding of the relationship between urbanization and disease dynamics, although it is generally believed that urban living has contributed to reductions in communicable disease burden in industrialized countries. To investigate this relationship, we carried out spatiotemporal analyses using a 48-year-long dataset of hemorrhagic fever with renal syndrome incidence (HFRS; mainly caused by two serotypes of hantavirus in China: Hantaan virus and Seoul virus) and population movements in an important endemic area of south China during the period 1963–2010. Our findings indicate that epidemics coincide with urbanization, geographic expansion, and migrant movement over time. We found a biphasic inverted U-shaped relationship between HFRS incidence and urbanization, with various endemic turning points associated with economic growth rates in cities. Our results revealed the interrelatedness of urbanization, migration, and hantavirus epidemiology, potentially explaining why urbanizing cities with high economic growth exhibit extended epidemics. Our results also highlight contrasting effects of urbanization on zoonotic disease outbreaks during periods of economic development in China.

[1]  N. Stenseth,et al.  Interannual cycles of Hantaan virus outbreaks at the human–animal interface in Central China are controlled by temperature and rainfall , 2017, Proceedings of the National Academy of Sciences.

[2]  Bing Xu,et al.  Anthropogenically driven environmental changes shift the ecological dynamics of hemorrhagic fever with renal syndrome , 2017, PLoS pathogens.

[3]  Bing Xu,et al.  Changes in Rodent Abundance and Weather Conditions Potentially Drive Hemorrhagic Fever with Renal Syndrome Outbreaks in Xi’an, China, 2005–2012 , 2015, PLoS neglected tropical diseases.

[4]  G. Chowell,et al.  Time-Specific Ecologic Niche Models Forecast the Risk of Hemorrhagic Fever with Renal Syndrome in Dongting Lake District, China, 2005–2010 , 2014, PloS one.

[5]  Zijian Feng,et al.  Epidemic characteristics of hemorrhagic fever with renal syndrome in China, 2006–2012 , 2014, BMC Infectious Diseases.

[6]  M. Nawaz,et al.  Analysis of an Outbreak of Hemorrhagic Fever with Renal Syndrome in College Students in Xi’an, China , 2014, Viruses.

[7]  B. Grenfell,et al.  Animal Reservoir, Natural and Socioeconomic Variations and the Transmission of Hemorrhagic Fever with Renal Syndrome in Chenzhou, China, 2006–2010 , 2014, PLoS neglected tropical diseases.

[8]  S. Weaver Urbanization and geographic expansion of zoonotic arboviral diseases: mechanisms and potential strategies for prevention. , 2013, Trends in Microbiology.

[9]  Lidong Gao,et al.  Ecology and geography of hemorrhagic fever with renal syndrome in Changsha, China , 2013, BMC Infectious Diseases.

[10]  B. Cazelles,et al.  Atmospheric Moisture Variability and Transmission of Hemorrhagic Fever with Renal Syndrome in Changsha City, Mainland China, 1991–2010 , 2013, PLoS neglected tropical diseases.

[11]  D. Patrick,et al.  Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. , 2013, Vector borne and zoonotic diseases.

[12]  Shiwen Wang,et al.  Changes in age distribution of hemorrhagic fever with renal syndrome: an implication of China’s expanded program of immunization , 2013, BMC Public Health.

[13]  J. Zhao,et al.  Environmental variability and the transmission of haemorrhagic fever with renal syndrome in Changsha, People's Republic of China , 2012, Epidemiology and Infection.

[14]  Ying Liang,et al.  Investigation of an outbreak of cutaneous anthrax in Banlu village, Lianyungang, China, 2012. , 2012, Western Pacific surveillance and response journal : WPSAR.

[15]  S. Magle,et al.  Wild Birds as Sentinels for Multiple Zoonotic Pathogens Along an Urban to Rural Gradient in Greater Chicago, Illinois , 2012, Zoonoses and public health.

[16]  Yves Rosseel,et al.  lavaan: An R Package for Structural Equation Modeling , 2012 .

[17]  Verena D. Schmittmann,et al.  Qgraph: Network visualizations of relationships in psychometric data , 2012 .

[18]  Lei Yan,et al.  Epidemiologic characteristics of haemorrhagic fever with renal syndrome in Mainland China from 2006 to 2010. , 2012, Western Pacific surveillance and response journal : WPSAR.

[19]  Francis L Martin,et al.  Understanding and harnessing the health effects of rapid urbanization in China. , 2011, Environmental science & technology.

[20]  François Chappuis,et al.  Urbanisation and infectious diseases in a globalised world , 2011, The Lancet Infectious Diseases.

[21]  Mercedes Pascual,et al.  Forcing Versus Feedback: Epidemic Malaria and Monsoon Rains in Northwest India , 2010, PLoS Comput. Biol..

[22]  L. Fang,et al.  Spatiotemporal Trends and Climatic Factors of Hemorrhagic Fever with Renal Syndrome Epidemic in Shandong Province, China , 2010, PLoS neglected tropical diseases.

[23]  A. Plyusnin,et al.  Hantavirus Infections in Humans and Animals, China , 2010, Emerging infectious diseases.

[24]  S. Liang,et al.  Urbanisation and health in China , 2010, The Lancet.

[25]  Colleen B. Jonsson,et al.  A Global Perspective on Hantavirus Ecology, Epidemiology, and Disease , 2010, Clinical Microbiology Reviews.

[26]  W. Liu,et al.  Climate Variability and Hemorrhagic Fever with Renal Syndrome Transmission in Northeastern China , 2010, Environmental health perspectives.

[27]  L. Fang,et al.  Spatiotemporal Dynamics of Hemorrhagic Fever with Renal Syndrome, Beijing, People’s Republic of China , 2009, Emerging infectious diseases.

[28]  Wei Liu,et al.  Predicting the risk of hantavirus infection in Beijing, People's Republic of China. , 2009, The American journal of tropical medicine and hygiene.

[29]  Ming-hui Li,et al.  Seoul Virus and Hantavirus Disease, Shenyang, People’s Republic of China , 2009, Emerging infectious diseases.

[30]  Yuanli Liu,et al.  China's health system performance , 2008, The Lancet.

[31]  Sarah Cook,et al.  Internal migration and health in China , 2008, The Lancet.

[32]  Zhe Dun,et al.  Seoul virus in patients and rodents from Beijing, China. , 2008, The American journal of tropical medicine and hygiene.

[33]  Christopher Dye,et al.  Health and Urban Living , 2008, Science.

[34]  Dennis Normile,et al.  China's Living Laboratory in Urbanization , 2008, Science.

[35]  Wu-Chun Cao,et al.  Landscape Elements and Hantaan Virus–related Hemorrhagic Fever with Renal Syndrome, People’s Republic of China , 2007, Emerging infectious diseases.

[36]  Heikki Haario,et al.  DRAM: Efficient adaptive MCMC , 2006, Stat. Comput..

[37]  J. Klingström,et al.  Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. , 2006, The Journal of general virology.

[38]  N. McIntyre,et al.  From patterns to emerging processes in mechanistic urban ecology. , 2006, Trends in ecology & evolution.

[39]  A. Fauci,et al.  The challenge of emerging and re-emerging infectious diseases , 2004, Nature.

[40]  Jonathan A. Patz,et al.  Unhealthy Landscapes: Policy Recommendations on Land Use Change and Infectious Disease Emergence , 2004, Environmental health perspectives.

[41]  M. McKinney,et al.  Urbanization, Biodiversity, and Conservation , 2002 .

[42]  Jonathan A. Patz,et al.  Using remotely sensed data to identify areas at risk for hantavirus pulmonary syndrome. , 2000, Emerging infectious diseases.

[43]  P. Daszak,et al.  Emerging infectious diseases of wildlife--threats to biodiversity and human health. , 2000, Science.

[44]  Roger C.K. Chan,et al.  Urbanization and sustainable metropolitan development in China: Patterns, problems and prospects* , 1999 .

[45]  G. Song Epidemiological progresses of hemorrhagic fever with renal syndrome in China. , 1999, Chinese medical journal.

[46]  A Iwamoto,et al.  Emerging and Re-emerging Infectious Diseases , 2003, National Institute of Allergy and Infectious Diseases, NIH.

[47]  T. Harpham Urbanisation and health in transition , 1997, The Lancet.

[48]  B. Hjelle,et al.  Hantaviruses: a global disease problem. , 1997, Emerging infectious diseases.

[49]  J. Scholefield,et al.  A randomised, prospective, double-blind, placebo-controlled trial of glyceryl trinitrate ointment in treatment of anal fissure , 1997, The Lancet.

[50]  P. Petraitis,et al.  Inferring multiple causality : the limitations of path analysis , 1996 .

[51]  J. Besag,et al.  On conditional and intrinsic autoregressions , 1995 .

[52]  S. Chib,et al.  Understanding the Metropolis-Hastings Algorithm , 1995 .

[53]  Z. Lei GEOGRAPHY-INCLUDED REGIONAL ECONOMIC GROWING MODEL AND CASE STUDY , 2012 .

[54]  Fan Jing-chun Vector surveillance and control in emergencies in China: proceedings and perspectives , 2011 .

[55]  Bruce Morley Causality between economic growth and immigration: An ARDL bounds testing approach , 2006 .

[56]  P. Atkinson,et al.  Opinion — tropical infectious diseases: Urbanization, malaria transmission and disease burden in Africa , 2005, Nature Reviews Microbiology.