1921
Volume 100, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Although vaccination is effective in preventing infection, pertussis remains endemic worldwide, including China. To lead better targeted prevention strategies, we examined dynamics of spatial and temporal patterns of pertussis transmission in Shandong, China, from 2009 to 2017. We used space-time cluster analysis, logistic regression analysis, and regression tree model to detect the changes in spatial patterns of pertussis infections in Shandong Province, China, between periods (2009–2011, 2012–2014, and 2015–2017). The yearly pertussis incidence rates dramatically increased by 16.8 times from 2009 to 2017. Shifting patterns of peaks of pertussis infections were observed over both time (from June–July to August–September) and space (from Linyi to Jinan), with increasing RR from 4.1 (95% CI: 2.3–7.4) (2009–2011) to 6.1 (95% CI: 5.6–6.7) (2015–2017) and obvious coincidence of peak time. West Shandong had larger odds of increased infections over the study period (odds ratio: 1.52 [95% CI: 1.05–2.17]), and pertussis had larger odds of spreading to east (odds ratio: 2.32 [95% CI: 1.63–3.31]) and north (odds ratio: 1.69 [95% CI: 1.06–2.99]) over time. Regression tree model indicated that the mean difference in yearly average pertussis incidence between 2009–2011 and 2015–2017 increased by more than 4-fold when the longitudes of counties are < 118.0°E. The geographic expansion of pertussis infection may increase the risk of epidemic peaks, coinciding with increased infections in the future. The findings might offer evidence for targeting preventive measures to the areas most in need to minimize the impact of the disease.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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References

  1. Marzouqi I, Richmond P, Fry S, Wetherall J, Mukkur T, , 2010. Development of improved vaccines against whooping cough: current status. Hum Vaccin 6: 543553. [Google Scholar]
  2. Fennelly NK, Sisti F, Higgins SC, Ross PJ, van der Heide H, Mooi FR, Boyd A, Mills KH, , 2008. Bordetella pertussis expresses a functional type III secretion system that subverts protective innate and adaptive immune responses. Infect Immun 76: 12571266. [Google Scholar]
  3. Schmidtke AJ, Boney KO, Martin SW, Skoff TH, Tondella ML, Tatti KM, , 2012. Population diversity among Bordetella pertussis isolates, United States, 1935–2009. Emerg Infect Dis 18: 12481255. [Google Scholar]
  4. Kamiya H, 2012. Transmission of Bordetella holmesii during pertussis outbreak, Japan. Emerg Infect Dis 18: 11661169. [Google Scholar]
  5. Octavia S, Sintchenko V, Gilbert GL, Lawrence A, Keil AD, Hogg G, Lan R, , 2012. Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008–2010. J Infect Dis 205: 12201224. [Google Scholar]
  6. Guo B, Page A, Wang H, Taylor R, McIntyre P, , 2013. Systematic review of reporting rates of adverse events following immunization: an international comparison of post-marketing surveillance programs with reference to China. Vaccine 31: 603617. [Google Scholar]
  7. Huang H, 2015. Epidemiological features of pertussis resurgence based on community populations with high vaccination coverage in China. Epidemiol Infect 143: 19501956. [Google Scholar]
  8. World Health Organization, 2018. WHO Vaccine-Preventable Diseases: Monitoring System. 2018 Global Summary. Available at: http://apps.who.int/immunization_monitoring/globalsummary/countries?countrycriteria%5Bcountry%5D%5B%5D=CHN&commit=OK. Accessed January 31, 2019. [Google Scholar]
  9. Zeng Q, Li D, Huang G, Xia J, Wang X, Zhang Y, Tang W, Zhou H, , 2016. Time series analysis of temporal trends in the pertussis incidence in Mainland China from 2005 to 2016. Sci Rep 6: 32367. [Google Scholar]
  10. Wang Y, Xu C, Wang Z, Zhang S, Zhu Y, Yuan J, , 2018. Time series modeling of pertussis incidence in China from 2004 to 2018 with a novel wavelet based SARIMA-NAR hybrid model. PLoS ONE 13: e0208404. [Google Scholar]
  11. Yang Y, Yao K, Ma X, Shi W, Yuan L, Yang Y, , 2015. Variation in Bordetella pertussis susceptibility to erythromycin and virulence-related genotype changes in China (1970–2014). PLoS One 10: e0138941. [Google Scholar]
  12. Meng Q, Li L, Shi W, Wang Q, Ding M, Liu Y, Ma X, Yao K, , 2018. Seroprevalence of diphtheria and pertussis immunoglobulin G among children with pneumonia in Ji’nan, China. BMC Pediatr 18: 383. [Google Scholar]
  13. Grassly NC, Fraser C, , 2006. Seasonal infectious disease epidemiology. Proc Biol Sci 273: 25412550. [Google Scholar]
  14. de Greeff SC, Dekkers AL, Teunis P, Rahamat-Langendoen JC, Mooi FR, de Melker HE, , 2009. Seasonal patterns in time series of pertussis. Epidemiol Infect 137: 13881395. [Google Scholar]
  15. Zhang Y, Milinovich G, Xu Z, Bambrick H, Mengersen K, Tong S, Hu W, , 2017. Monitoring pertussis infections using internet search queries. Sci Rep 7: 10437. [Google Scholar]
  16. Skowronski DM, De Serres G, MacDonald D, Wu W, Shaw C, Macnabb J, Champagne S, Patrick DM, Halperin SA, , 2002. The changing age and seasonal profile of pertussis in Canada. J Infect Dis 185: 14481453. [Google Scholar]
  17. Fine PE, Clarkson JA, , 1986. Seasonal influences on pertussis. Int J Epidemiol 15: 237247. [Google Scholar]
  18. Rushton G, Elmes G, McMaster R, , 2000. Considerations for improving geographic information system research in public health. URISA J 12: 3150. [Google Scholar]
  19. Varga C, Pearl DL, McEwen SA, Sargeant JM, Pollari F, Guerin MT, , 2013. Evaluating area-level spatial clustering of Salmonella enteritidis infections and their socioeconomic determinants in the greater Toronto area, Ontario, Canada (2007–2009): a retrospective population-based ecological study. BMC Public Health 13: 1078. [Google Scholar]
  20. National Statistics Bureau of China, 2010. The Sixth National Population Census data. Available at: http://data.stats.gov.cn/. Accessed December 25, 2018. [Google Scholar]
  21. Zhang J, Su Y, Wu J, Liang H, , 2015. GIS based land suitability assessment for tobacco production using AHP and fuzzy set in Shandong Province of China. Comput Electron Agr 114: 202211. [Google Scholar]
  22. Zhang Q, Han F, Nie Q, Ren H, Zhang B, Liu Q, He Q, Shao Z, , 2011. Seroprevalence of antibodies to pertussis and diphtheria among healthy adults in China. J Infect 63: 441446. [Google Scholar]
  23. National Health Commission of the PRC, 2007. Pertussis Diagnostic Criteria. Available at: http://www.nhfpc.gov.cn/zwgkzt/s9491/201410/52040bc16d3b4eecae56ec28b3358666.shtml. Accessed December 20, 2018. [Google Scholar]
  24. Lee HS, Nguyen-Viet H, Nam VS, Lee M, Won S, Duc PP, Grace D, , 2017. Seasonal patterns of dengue fever and associated climate factors in 4 provinces in Vietnam from 1994 to 2013. BMC Infect Dis 17: 218. [Google Scholar]
  25. Ke G, Hu Y, Huang X, Peng X, Lei M, Huang C, Gu L, Xian P, Yang D, , 2016. Epidemiological analysis of hemorrhagic fever with renal syndrome in China with the seasonal-trend decomposition method and the exponential smoothing model. Sci Rep 6: 39350. [Google Scholar]
  26. Cherry JD, , 2005. The epidemiology of pertussis: a comparison of the epidemiology of the disease pertussis with the epidemiology of Bordetella pertussis infection. Pediatrics 115: 14221427. [Google Scholar]
  27. Wu J, Tschakert P, Klutse E, Ferring D, Ricciardi V, Hausermann H, Oppong J, Smithwick EA, , 2015. Buruli ulcer disease and its association with land cover in southwestern Ghana. PLoS Negl Trop Dis 9: e0003840. [Google Scholar]
  28. Seixas R, Nunes T, Machado J, Tavares L, Owen S, Bernardo F, Oliveira M, , 2018. Demographic characterization and spatial cluster analysis of human Salmonella 1, 4,[5], 12: i:-infections in Portugal: a 10 year study. J Infect Public Health 11: 178182. [Google Scholar]
  29. Kulldorff M, Nagarwalla N, , 1995. Spatial disease clusters: detection and inference. Stat Med 14: 799810. [Google Scholar]
  30. Wu S, Wu F, Hong R, He J, , 2012. Incidence analyses and space-time cluster detection of hepatitis C in Fujian province of China from 2006 to 2010. PLoS One 7: e40872. [Google Scholar]
  31. Prates MO, Kulldorff M, Assunção RM, , 2014. Relative risk estimates from spatial and space–time scan statistics: are they biased? Stat Med 33: 26342644. [Google Scholar]
  32. Dunn CE, Kingham SP, Rowlingson B, Bhopal RS, Cockings S, Foy CJ, Acquilla SD, Halpin J, Diggle P, Walker D, , 2001. Analysing spatially referenced public health data: a comparison of three methodological approaches. Health Place 7: 112. [Google Scholar]
  33. De’ath G, Fabricius KE, , 2000. Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81: 31783192. [Google Scholar]
  34. Breiman L, Friedman JH, Olshen RA, Stone CJ, , 1984. Classification and Regression Trees. Monterey, CA: Wadsworth & Brooks. [Google Scholar]
  35. Zhang Q, Li M, Wang L, Xin T, He Q, , 2013. High-resolution melting analysis for the detection of two erythromycin-resistant Bordetella pertussis strains carried by healthy schoolchildren in China. Clin Microbiol Infect 19: E260E262. [Google Scholar]
  36. Wang Z, Cui Z, Li Y, Hou T, Liu X, Xi Y, Liu Y, Li H, He Q, , 2014. High prevalence of erythromycin-resistant Bordetella pertussis in Xi’an, China. Clin Microbiol Infect 20: O825O830. [Google Scholar]
  37. Zhang L, 2010. Effect of vaccination on Bordetella pertussis strains, China. Emerg Infect Dis 16: 16951701. [Google Scholar]
  38. Spokes PJ, Quinn HE, McAnulty JM, , 2010. Review of the 2008–2009 pertussis epidemic in NSW: notifications and hospitalisations. NSW Public Health Bull 21: 167173. [Google Scholar]
  39. Sheridan SL, Ware RS, Grimwood K, Lambert SB, , 2012. Number and order of whole cell pertussis vaccines in infancy and disease protection. JAMA 308: 454456. [Google Scholar]
  40. Paget J, Marquet R, Meijer A, van der Velden K, , 2007. Influenza activity in Europe during eight seasons (1999–2007): an evaluation of the indicators used to measure activity and an assessment of the timing, length and course of peak activity (spread) across Europe. BMC Infect Dis 7: 141. [Google Scholar]
  41. Choisy M, Rohani P, , 2012. Changing spatial epidemiology of pertussis in continental USA. Proc Biol Sci 279: 45744581. [Google Scholar]
  42. Huang X, Lambert S, Lau C, Magalhaes RS, Marquess J, Rajmokan M, Milinovich G, Hu W, , 2017. Assessing the social and environmental determinants of pertussis epidemics in Queensland, Australia: a Bayesian spatio-temporal analysis. Epidemiol Infect 145: 12211230. [Google Scholar]
  43. Jackson D, Rohani P, , 2014. Perplexities of pertussis: recent global epidemiological trends and their potential causes. Epidemiol Infect 142: 672684. [Google Scholar]
  44. Yin H, Kong F, Zhang X, , 2011. Changes of residential land density and spatial pattern from 1989 to 2004 in Jinan City, China. Chin Geogr Sci 21: 619628. [Google Scholar]
  45. Yip W, Subramanian S, Mitchell AD, Lee DT, Wang J, Kawachi I, , 2007. Does social capital enhance health and well-being? Evidence from rural China. Soc Sci Med 64: 3549. [Google Scholar]
  46. Broutin H, Elguero E, Simondon F, Guégan J, , 2004. Spatial dynamics of pertussis in a small region of Senegal. Proc Biol Sci 271: 20912098. [Google Scholar]
  47. Artois J, Jiang H, Wang X, Qin Y, Pearcy M, Lai S, Shi Y, Zhang J, Peng Z, Zheng J, , 2018. Changing geographic patterns and risk factors for avian influenza A (H7N9) infections in humans, China. Emerg Infect Dis 24: 8794. [Google Scholar]
  48. Zhang Y, Bambrick H, Mengersen K, Tong S, Hu W, , 2018. Using Google trends and ambient temperature to predict seasonal influenza outbreaks. Environ Int 117: 284291. [Google Scholar]
  49. Martens P, Hall L, , 2000. Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis 6: 103109. [Google Scholar]
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Supplemental material

  • Received : 08 Jan 2019
  • Accepted : 20 Feb 2019
  • Published online : 05 Jun 2019

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