Skip to main content
Download PDF

Analysis of the effect of meteorological factors on hemorrhagic fever with renal syndrome in Taizhou City, China, 2008–2020

BMC Public Health volume 22, Article number: 1097 (2022) Cite this article

Abstract

Background

Hemorrhagic fever with renal syndrome (HFRS) is endemic in Zhejiang Province, China, while few studies have concentrated on the influence of meteorological factors on HFRS incidence in the area.

Methods

Data on HFRS and meteorological factors from January 1, 2008 to December 31, 2020 in Taizhou City, Zhejiang Province were collected. Multivariate analysis was conducted to the relationship between meteorological factors including minimum temperatures, relative humidity, and cumulative rainfall with HFRS.

Results

The HFRS incidence peaked in November and December and it was negatively correlated with average and highest average temperatures. Compared with median of meteorological factors, the relative risks (RR) of weekly average temperature at 12 ℃, weekly highest temperature at 18 ℃relative humidity at 40%, and cumulative rainfall at 240 mm were most significant and RRs were 1.41 (95% CI: 1.09–1.82), 1.32 (95% CI: 1.05–1.66), 2.18 (95% CI: 1.16–4.07), and 1.91 (95% CI: 1.16–2.73), respectively. Average temperature, precipitation, relative humidity had interactions on HFRS and the risk of HFRS occurrence increased with the decrease of average temperature and the increase of precipitation.

Conclusion

Our study results are indicative of the association of environmental factors with the HFRS incidence, probable recommendation could be use of environmental factors as early warning signals for initiating the control measure and response. 

Peer Review reports

Background

Climate change, especially extreme weather, not only affect the incidence of acute infectious diseases of the respiratory tract [1,2,3], but also increase the risk of death in patients with chronic diseases [4]. Hemorrhagic fever with renal syndrome (HFRS) is a natural focal disease, and a large number of studies have shown that its incidence is influenced by climate change [5]. In the context of global warming, temperature, rainfall, and relative humidity are the main meteorological factors that pose a serious threat to human health [6]. Previous studies on the impact of meteorological factors on diseases have identified certain hysteresis effects, which vary in form and by region [7, 8].

Meteorological factors, such as temperature, precipitation, and humidity, might affect human travel, thereby directly affecting the likelihood of rodent-human contact [9]. They can also affect the spread of diseases by affecting crop yields, rodent reproduction, and vector density [10]. For example, temperature and rainfall were associated with the host ecosystem, affecting the HFTS transmission speed and the potential risk of outbreaks [11, 12]. These factors had a lagging effect on HFRS incidence, but lag time ranged 3–5 months in different areas [13,14,15,16]. Moreover, El Niño extreme weather events were also associated with the occurrence of HFRS [17].

The first documented case of HFRS in Zhejiang Province was reported in Jiaxing City in 1963. Since then, the size of the endemic area has gradually increased. In recent years, the number of cases has decreased with vaccination, rodent control strategies, and environmental sanitation improvements [18]. However, the affected areas of Zhejiang Province is gradually expanding, and the incidence rates in some areas remain high [19]. Up to date, cases have been reported in all 11 prefecture-level cities in the province [19]. However, few studies have concentrated on the influence of meteorological factors on HFRS incidence in the area. In this study, distributed lag nonlinearity (DLNM) and generalized additive model (GAM) were used to evaluate the impact of HFRS incidence in Taizhou City, Zhejiang Province, and to determine the key influencing factors.

Material and methods

Study area

Taizhou City, a coastal city in the central part of Zhejiang Province, belongs to the mid-subtropical monsoon area and experiences four distinct seasons (Supplementary Figure S1). The territory experiences mild summers, cold winters, abundant rain, and a mild, humid climate due to the meteorological effects of nearby ocean waters and mountains in the northwest.

Data collection

According to the Law on Prevention and Treatment of Infectious Diseases, HFRS is classified as a Class B infectious disease in China, and cases must be reported within 24 h of diagnosis [19]. Data on HFRS from 2008 to 2020 in Taizhou City were collected from the Chinese Notifiable Disease Reporting System.

We collected daily meteorological data from the China Meteorological Data Sharing Service System (http://data.cma.cn/). These data, including daily average temperature, (Avetemp), minimum temperature (Mintemp), maximum temperature (Maxtemp), relative humidity, and total precipitation, were used to calculate the weekly average for each value.

Statistical methods

Normality test and descriptive analysis were conducted to summarize characteristics of all variables. Spearman correlation was used to assess the relationship between HFRS incidence and meteorological factors. This study developed a time series model based on the GAM and used the cross-basis process to describe the distribution of changes in the independent variable dimension and the lag dimension simultaneously [8]. Further, DLNM was used to fit the non-linear and lag effects of weekly Avetemp, Maxtemp, Mintemp, average relative humidity, and cumulative rainfall on the risk of HFRS [20]. The incubation period for HFRS is affected by the host animal, vector density, and meteorological factors, and lasts for several weeks. In our study, the maximum lag period was set to 16 weeks [13, 20, 21]. Since HFRS cases in Taizhou City were relatively rare, Quasi-Poisson regression was used in this model to control for overdispersion. We used a two-stage analysis method. First, we used the DLNM to estimate the association of weekly Avetemp, Maxtemp, Mintemp, relative humidity, and weekly total precipitation (WTP) with the number of HFRS case [22]. The general algebraical definition of the model are as follows:

$$Log[E(Yt)] = \beta + cb(Kt,16,\beta 1) + S1(x) + S2(z)+S3(m)+S4(n)+ S5(week)$$

Among them, t is the observation week; [E(Yt)] is HFRS cases observed in month Yt, βis the intercept of the entire model; cb (Kt, 16, and β1) is the cross-basis function of K, and K is one of the meteorological elements. S1–4 are factors such as Avtemp, Maxtemp, Mintemp, RH, and WTP; β1 is the estimated value of the effect of K in a specific lag week t; the maximum lag week is set to 16; Week is the ordinal variable of the week in the year; s() is the penalty spline function. This study uses cubic spline functions, s1–4, to adjust the confounding factors in the model, and s5(week) to adjust the weekly confounding factors.

Second, we analyzed the interaction between weekly Avetemp, Maxtemp, Mintemp, relative humidity, and accumulated rainfall with GAMs, and then analyzed the different effects of high and low values of the meteorological factors on the cases. The basic model as follows:

$$Log[\mathrm{E}(\mathrm{Yt})] =\upbeta 2 +\mathrm{ S}1(\mathrm{k},\mathrm{x}) +\mathrm{ S}2(\mathrm{z}) +\mathrm{ S}3(\mathrm{m}) +\mathrm{ S}4(\mathrm{n}) +\mathrm{ S}5(\mathrm{week})$$

β2 is the intercept; K is one of the meteorological factors (Avtemp, Maxtemp, Mintemp, RH, and WTP), and X, Z, M, and N denote the other factors. s() means the penalty spline function. s1 (K and X) is the spline function of the interaction between variables K and X.

In the model, the number of cases was used as the dependent variable, and a cross-basis function was established for the number of cases and temperature. Spline interpolation was used to control the influence of confounding factors such as relative humidity, rainfall, and long-term trends. The best degree of freedom (df) was selected based on the spline function results through sensitivity testing and generalized cross-validation criteria [23].

DLNM can describe the complex nonlinearity and hysteresis correlation of temperature-HFRS through the cross basis function. It is necessary to scientifically define the reasonable lag time of the model [21]. We chose one ns (natural cubic B-spline, df = 6) as the exposure–response. Two nodes are located at the 2.5th and 97.5th percentiles of the meteorological factor distribution, and the other is for the exposure–response relationship, based on high temperature [13, 15]. The assumption that Maxtemp and Mintemp may affect the incidence of HFRS is fixed (df = 6) and the maximum lag time was set at 16 weeks to capture the delayed effects of extreme temperatures. In this study, the degrees of freedom and maximum lag times for mean temperature, relative humidity, accumulated rainfall, mean maximum temperature and mean minimum temperature were set in order: (df = 6, lag = 16; df = 4, lag = 16; df = 3, lag = 10; df = 6, lag = 21; df = 4, lag = 20).

We performed sensitivity analysis by changing the df of the weather variables and time points. All analyses were performed using ArcGIS 10.2 (ESRI, Redlands, CA, USA) and R software (packages "dlnm" and "mgcv") (R Foundation for Statistical Computing, Vienna, Austria).

Results

During the study period, a total of 1196 HFRS cases were reported in Taizhou City. Descriptive statistics collected over the past 13 years indicated that the highest weekly case distribution in Taizhou reached 12 cases (Table 1). The Avetemp, Maxtemp, and Mintemp in Taizhou City from 2008 to 2020 all show a normal distribution and showed obvious periodicity and seasonality (Fig. 1). The average weekly temperature was 18.04 °C; Mintemp, 2.33 °C, and Maxtemp, 30.33 °C. The weekly average Maxtemp and weekly average Mintemp were 19.3 °C and 11.13 °C, respectively. The average weekly humidity was 77.88% and the average weekly rainfall was 38.54 mm (Fig. 2). HFRS incidence was negatively correlated with the Avetemp and the highest Avetemp, while it didn’t significantly related to the weekly average relative humidity, weekly total precipitation, and the lowest Avetemp (Table 2).

Table 1 Descriptive statistics of weekly HFRS cases and meteorological factors in Taizhou City, China from 2008 to 2020
Full size table
Fig. 1
figure 1

Time series of weekly Avetemp,Tmax, Tmin, RH and WTP, and number of HFRS from 2008 to 2020 in Taizhou City, China

Full size image
Fig. 2
figure 2

Boxplot of Avetemp, Mintemp, Max temp, RH and WTP

Full size image
Table 2 Correlation analysis of meteorological factors and HFRS in Taizhou city,China from 2008 to 2020
Full size table

In the DLNM, we used the median of each meteorological factor as a reference and then calculated the relative risk of each variable. The impact of Avetemp on HFRS rapidly decreased and then slowly increased. In Lag 3, weekly Avetemp is most significant at 13 °C (RR = 1.28, 95% CI = 1.04–1.57). In Lag 4, weekly Avetemp was most significant at 12 °C (RR = 1.41, 95% CI = 1.09–1.82) (Fig. 3A, B). In lag 3, Maxtemp is most significant at 18 °C (RR = 1.32, 95% CI = 1.05–1.66) (Fig. 3C). In lag 4, Maxtemp is most significant at 20 °C (RR = 1.12, 95% CI = 1.02–1.24) (Fig. 3D). There was no statistical difference between the high and low values of the Mintemp; the Mintemp of 1 °C had the same RR value in lag1 and lag2 (RR = 1.59, 95% CI = 1.02–2.47) (Fig. 3E, F).

Fig. 3
figure 3

The lag-specific effect of meteorological factors on HFRS in Taizhou City

Full size image

The RR of the highest value of relative humidity in the 97.5th percentile in lag2 and lg16 were 0.97, and 0.61, respectively (Supplementary Fig. S2G, H). A relative humidity of 31% was the most significant in lag 2 and a maximum relative humidity of 40% was the most significant in lag 15 (Fig. 3G, H).

The highest WTP value of the 97.5th percentile had the largest RR in lag13 (RR = 1.35, 95% CI = 1.01–1.79) (Supplementary Fig. S2I, J); a cumulative rainfall of 240 mm in lag3 was the most significant (RR = 1.91, 95% CI = 1.16–2.73) (Fig. 3I). A cumulative rainfall of 120 mm in lag10 was the most significant (RR = 1.27, 95% CI = 1.08–1.49) (Fig. 3J).

We calculated the corresponding RR for the minimum to the maximum lag of each meteorological factor (Fig. 4), and the Avetemp was between lag3–5 (RR = 1.4, 95% CI = 1.09–1.81). The time effect of the Maxtemp was significant, and the risk of infection was the highest in the lag1–2 weeks. Regarding cumulative rainfall, the effect of lag was most significant during lag3–4 weeks. The maximum effect of relative humidity was the most significant at lag3–4 and lag12–15 weeks, respectively.

Fig. 4
figure 4

RRs of meteorological factors on HFRS at different lags in Taizhou city from 2008 to 2020

Full size image

GAMs was used to explore the interaction between Avetemp, WTP, and RH, and the results are shown in Fig. 5. The left side of Fig. 5 showed the interaction between Avetemp and WTP. Obviously, the infection risk of HFRS was inversely proportional to Avetemp and directly proportional to the WTP. As showed in the middle of Fig. 5, the infection risk of HFRS is inversely proportional to Avetemp and directly proportional to RH. Figure 5 showed that as the WTP increased, the RH decreased and the risk of infection increased. The risk of HFRS infection increased with the decrease of Avetemp and the increase of WTP. These indicated that HFRS in Taizhou City increased when Avetemp decreased and WTP increased.

Fig. 5
figure 5

The coefficients of meteorological factors on HFRS in Taizhou City

Full size image

Discussion

In this study, we investigated the relationship between Avetemp, Maxtemp, Mintemp, WTP, relative humidity and HFRS in Taizhou City from 2008 to 2020 using DLNM and GAMs. Our study found that weekly Avetemp and weekly maximum temperature were negatively associated with HFRS incidence, which is consistent with results from Shandong Province [24].

The lagged effects of WTP and relative humidity were also most pronounced in Taizhou City, with a lag of 3–4 weeks. Rather than concentrating rodent control efforts only twice, in winter and spring [7, 19], the high incidence period identified in this study. Several studies have confirmed that extreme weather has a significant impact on many diseases [18, 19]. We found that the effects of Maxtemp and Mintemp on HFRS were most pronounced at a lag of 1 week. Several models have been used to study the effect of later factors on dengue fever, and similarly confirmed the existence of a lag period for climatic factors on local dengue incidence [25].

We found that the risk of infection increased with the increase of precipitation, which was similar with previous findings [26]. The effect of WTP on the risk of disease in Taizhou City was most pronounced at a lag of 1 month, and this effect persisted until a lag of 12 weeks. This study confirmed that infectious diseases in coastal areas such as Zhejiang Province were more affected by tropical cyclones [27]. For example, rainfall and relative humidity had a significant effect on severe fever with thrombocytopenia syndrome [28].

Conclusion

Meteorological factors had non-line relationship with HFRS and lag effects exist. HFRS mostly occurred when temperature and relative humidity were low and WTP was high. Our study results are indicative of the association of environmental factors with the HFRS incidence, probable recommendation could be use of environmental factors as early warning signals for initiating the control measure and response.

Limitations

HFRS incidence was directly associated with density and infection rate of rodents, but these data were not available in this study. More over, other factors including social factors and environmental factors might also influence HFRS. Further research should be conducted to explore the contribution rate of different factors on HFRS.

Availability of data and materials

All data analyzed during this research period are included in the body of this article and supplementary materials.

References

  1. Ma YX, Yang SX, Yu ZA, Jiao HR, Zhang YF, Ma BJ, et al. Effect of diurnal temperature range on outpatient visits for common cold in Shanghai, China. Environ Sci Pollut Res. 2020;27(2):1436–48. https://doi.org/10.1007/s11356-019-06805-4.

    Article  Google Scholar 

  2. Shi P, Dong YQ, Yan HC, Zhao CK, Li XY, Liu W, et al. Impact of temperature on the dynamics of the COVID-19 outbreak in China. Sci Total Environ. 2020;728(1): 138890. https://doi.org/10.1016/j.scitotenv.2020.138890.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ma YX, Zhou JD, Yang SX, Yu ZA, Wang F, Zhou J. Effects of extreme temperatures on hospital emergency room visits for respiratory diseases in Beijing, China. Environ Sci Pollut Res. 2019;26(3):3055–64. https://doi.org/10.1007/s11356-018-3855-4.

    Article  Google Scholar 

  4. Ma YX, Zhao YX, Zhou JD, Jiang YY, Yang SX, Yu ZA. The relationship between diurnal temperature range and COPD hospital admissions in Changchun, China. Environ Sci Pollut Res. 2018;25(18):17942–9. https://doi.org/10.1007/s11356-018-2013-3.

    Article  Google Scholar 

  5. Jiang F, Wang L, Wang S, Zhu L, Dong L, Zhang Z. Meteorological factors affect the epidemiology of hemorrhagic fever with renal syndrome via altering the breeding and hantavirus-carrying states of rodents and mites: a 9 years’ longitudinal study. Emerg Microbes Infect. 2017;11(6):e104. https://doi.org/10.1038/emi.2017.92.

    Article  Google Scholar 

  6. McMichael AJ, Wilkinson P, Kovats RS, Pattenden S, Hajat S, Armstrong B, et al. International study of temperature, heat and urban mortality: the “ISOTHURM” project. Int J Epidemiol. 2008;37(5):1121–31. https://doi.org/10.1093/ije/dyn086.

    Article  PubMed  Google Scholar 

  7. Li YD, Cazelles B, Yang GQ, Laine M, Huang ZXY, Cai J, et al. Intrinsic and extrinsic drivers of transmission dynamics of hemorrhagic fever with renal syndrome caused by Seoul hantavirus. PLoS Negl Trop Dis. 2019;13(9):e7757. https://doi.org/10.1371/journal.pntd.0007757.

    Article  Google Scholar 

  8. Gasparrini A, Armstrong B, Kenward MG. Distributed lag non-linear models. Stat Med. 2010;29(21):2224–34. https://doi.org/10.1002/sim.3940.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wei YH, Wang Y, Li XN, Qin PZ, Lu Y, Xu JM, et al. Meteorological factors and risk of hemorrhagic fever with renal syndrome in Guangzhou, southern China, 2006–2015. PLOS Negl Trop Dis. 2018;12(6):e6604. https://doi.org/10.1371/journal.pntd.0006604.

    Article  Google Scholar 

  10. Hansen A, Cameron S, Liu QY, Sun YH, Weinstein P, Williams C, et al. Transmission of haemorrhagic fever with renal syndrome in china and the role of climate factors: a review. Int J Infect Dis. 2015;33:212–8. https://doi.org/10.1016/j.ijid.2015.02.010.

    Article  PubMed  Google Scholar 

  11. Bi P, Tong SL, Donald K, Parton K, Ni JF. Climatic, reservoir and occupational variables and the transmission of haemorrhagic fever with renal syndrome in China. Int J Epidemiol. 2002;31(1):189–93. https://doi.org/10.1093/ije/31.1.189.

    Article  PubMed  Google Scholar 

  12. Tian HY, Yu PB, Cazelles B, Xu L, Tan H, Yang J, et al. Interannual cycles of Hantaan virus outbreaks at the human–animal interface in Central China are controlled by temperature and rainfall. Proc Natl Acad Sci. 2017;114(30):8041–6. https://doi.org/10.1073/pnas.1701777114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sun WW, Liu XB, Li W, Mao ZY, Sun JM, Lu L. Effects and interaction of meteorological factors on hemorrhagic fever with renal syndrome incidence in Huludao City, northeastern China, 2007–2018. PLoS Negl Trop Dis. 2021;3(15):e9217. https://doi.org/10.1371/journal.pntd.0009217.

    Article  Google Scholar 

  14. Wu HC, Wu C, Lu QB, Ding ZY, Xue M, Lin JF. Spatial-temporal characteristics of severe fever with thrombocytopenia syndrome and the relationship with meteorological factors from 2011 to 2018 in Zhejiang Province, China. PLoS Negl Trop Dis. 2020;14(4):e8186. https://doi.org/10.1371/journal.pntd.0008186.

    Article  CAS  Google Scholar 

  15. Xu QQ, Li RZ, Rutherford S, Luo C, Liu YF, Li XJ. Using a distributed lag non-linear model to identify impact of temperature variables on haemorrhagic fever with renal syndrome in Shandong Province. Epidemiol Infect. 2018;146(13):1671–9. https://doi.org/10.1017/S095026881800184X.

    Article  PubMed  Google Scholar 

  16. Zhang WY, Guo WD, Fang LQ, Li CP, Bi P, Glass GE, et al. Climate variability and hemorrhagic fever with renal syndrome transmission in Northeastern China. Environ Health Perspect. 2010;118(7):915–20. https://doi.org/10.1289/ehp.0901504.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bi P, Parton KA. El Niño and incidence of hemorrhagic fever with renal syndrome in China. JAMA. 2003;289(2):176–7. https://doi.org/10.1001/jama.289.2.176-d.

    Article  PubMed  Google Scholar 

  18. Tian H, Tie WF, Li HB, Hu XQ, Xie GC, Du LY, et al. Orthohantaviruses infections in humans and rodents in Baoji, China. PLoS Negl Trop Dis. 2020;14(10):e8778. https://doi.org/10.1371/journal.pntd.0008778.

    Article  Google Scholar 

  19. Zhang R, Mao ZY, Yang J, Liu SL, Liu Y, Qin SW, et al. The changing epidemiology of hemorrhagic fever with renal syndrome in Southeastern China during 1963–2020: A retrospective analysis of surveillance data. PLoS Negl Trop Dis. 2021;15(8):e9673. https://doi.org/10.1371/journal.pntd.000967320.

    Article  Google Scholar 

  20. Cao LN, Huo XY, Xiang JJ, Lu L, Liu X, Song XP, et al. Interactions and marginal effects of meteorological factors on haemorrhagic fever with renal syndrome in different climate zones: Evidence from 254 cities of China. Sci Total Environ. 2020;721:137564. https://doi.org/10.1016/j.scitotenv.2020.137564.

    Article  CAS  PubMed  Google Scholar 

  21. Wang P, Zhang X, Hashizume M, Goggins WB, Luo C. A systematic review on lagged associations in climate-health studies. Int J Epidemiol. 2021;50(4):1199–212. https://doi.org/10.1093/ije/dyaa286.

    Article  PubMed  Google Scholar 

  22. Ma YX, Jiao HR, Zhang YF, Feng FL, Cheng BW, Ma BJ, et al. Short-term effect of extreme air temperature on hospital emergency room visits for cardiovascular diseases from 2009 to 2012 in Beijing, China. Environ Sci Pollut Res. 2020;27(30):38029–37. https://doi.org/10.1007/s11356-020-09814-w.

    Article  Google Scholar 

  23. Bai X, Peng C, Jiang T, Hu ZM, Huang DS, Guan PG. Distribution of geographical scale, data aggregation unit and period in the correlation analysis between temperature and incidence of HFRS in mainland China: a systematic review of 27 ecological studies. PLOS Negl Trop Dis. 2019;13(8):e7688. https://doi.org/10.1371/journal.pntd.0007688.

    Article  Google Scholar 

  24. Fang LQ, Wang XJ, Liang S, Li YL, Song SX, Zhang WY, et al. Spatiotemporal trends and climatic factors of hemorrhagic fever with renal syndrome epidemic in Shandong Province, China. PLoS Negl Trop Dis. 2010;4(8):e789. https://doi.org/10.1371/journal.pntd.0000789.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Guo P, Liu T, Zhang Q, Wang L, Xiao J, Zhang Q, et al. Developing a dengue forecast model using machine learning: a case study in China. Plos Neglect Trop D. 2017;10(11):e5973. https://doi.org/10.1371/journal.pntd.0005973.

    Article  Google Scholar 

  26. Xiang JJ, Hansen A, Liu QY, Tong MX, Liu XB, Sun YH, et al. Impact of meteorological factors on hemorrhagic fever with renal syndrome in 19 cities in China, 2005–2014. Sci Total Environ. 2018;636:1249–56. https://doi.org/10.1016/j.scitotenv.2018.04.407.

    Article  CAS  PubMed  Google Scholar 

  27. Zheng J, Han W, Jiang B, Ma W, Zhang Y. Infectious Diseases and Tropical Cyclones in Southeast China. Int J Environ Res Public Health. 2017;14(5):494. https://doi.org/10.3390/ijerph14050494.

    Article  PubMed Central  Google Scholar 

  28. Sun JM, Lu L, Liu KK, Yang J, Wu HX, Liu QY. Forecast of severe fever with thrombocytopenia syndrome incidence with meteorological factors. Sci Total Environ. 2018;626:1188–92. https://doi.org/10.1016/j.scitotenv.2018.01.196.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the Taizhou Municipal Health Organization, the Center for Disease Control and Prevention, and the China National Meteorological Information Center for providing data for our research.

Funding

This study was supported by the medical research program of Zhejiang Province (2019KY358).

Author information

Author notes

  1. Rong Zhang, Ning Zhang, Wanwan Sun and Haijiang Lin contribute equally to this work.

Authors and Affiliations

  1. Key Laboratory of Vaccine, Prevention and Control of Infectious Disease of Zhejiang Province, Zhejiang Provincial Center for Disease Control and Prevention, Zhejiang Province, Hangzhou, 310051, China

    Rong Zhang, Wanwan Sun, Ying Liu, Tao Zhang, Jimin Sun, Feng Ling & Zhen Wang

  2. Puyan Street Community Health Service Center of Binjiang District, Zhejiang Province, Hangzhou, 310013, China

    Ning Zhang

  3. Taizhou City Center for Disease Control and Prevention, Zhejiang Province, Taizhou, 318000, China

    Haijiang Lin

  4. Ningbo University School of Medicine, Zhejiang Province, Ningbo, 315000, China

    Mingyong Tao

Authors
  1. Rong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ning Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wanwan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haijiang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mingyong Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jimin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Feng Ling
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Rong Zhang:Conceptual,Methodology, Writing original draft preparation and funding acquisition. Ning Zhang and Wanwan Sun: Analysis and modeling. Haijiang Lin: Resources. Mingyong Tao and Tao Zhang: Visualization.Ying Liu: Software. Jimin Sun: Project administration, writing and editing. Feng Ling and Zhen Wang: writing review, Supervision. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jimin Sun, Feng Ling or Zhen Wang.

Ethics declarations

Ethics approval and consent to participate

All methods were carried out in accordance with relevant guidelines and regulations. This study was reviewed and approved by the Ethics Committee of the Zhejiang Provincial Center for Disease Control and Prevention (No.2020–021). All the data of the individuals were kept confidential as requested and ethical approve.

Consent for publication

Not applicable.

Competing interests

The authors have declared that no competing interest exist.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Figure S1.

Study areas of Taizhou City in China. The map was created by ArcGIS 10.2 (Software, ESRI Inc., Redlands, CA, USA). The base layer of the map of Zhejiang Province was supported from National Earth System Science Data Center, National Science & Technology Infrastructure of China (http://www.geodata.cn). Figure S2. With the median as the reference, the lag effect between Avetemp, Maxtemp, Mintemp, RH and WTP and HFRS infection. Abbreviations: Avetemp, average temperature; CI, confidence interval; df, degree of freedom; DLNM, distributed lag non-linear model; GAM, generalized additive model; HFRS, Hemorrhagic fever with renal syndrome; Maxtemp, maximum temperature; Mintemp, minimum temperature; RH,relative humidity;WTP,weekly total precipitation; RR, relative risk.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, R., Zhang, N., Sun, W. et al. Analysis of the effect of meteorological factors on hemorrhagic fever with renal syndrome in Taizhou City, China, 2008–2020. BMC Public Health 22, 1097 (2022). https://doi.org/10.1186/s12889-022-13423-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12889-022-13423-2

Keywords

  • Hemorrhagic fever with renal syndrome
  • Distributed lag non-linear
  • Generalized additive models
  • Lag effect
  • Interactive effect

BMC Public Health

ISSN: 1471-2458

Contact us