p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Available online at www.sciencedirect.com
Public Health journal homepage: www.elsevier.com/puhe
Original Research
Daily temperature change in relation to the risk of childhood bacillary dysentery among different age groups and sexes in a temperate city in China K. Li a, K. Zhao b, L. Shi c, L. Wen a, H. Yang a, J. Cheng a, X. Wang a, H. Su a,* a
Department of Epidemiology and Health Statistics, School of Public Health, Anhui Medical University, Hefei, Anhui, China b Hefei Centre for Disease Control and Prevention of Anhui Province, Hefei, Anhui, China c Department of Nutrition and Food Hygiene, School of Public Health, Dalian Medical University, Dalian, Liaoning, China
article info
abstract
Article history:
Background: In recent years, many studies have found that ambient temperature is signif-
Received 23 October 2014
icantly associated with bacillary dysentery (BD). However, there is limited evidence on the
Received in revised form
relationship between temperature and childhood BD in temperate areas.
14 July 2015
Objectives: To investigate the relationship between daily mean temperature (MT) and
Accepted 23 October 2015
childhood BD in China.
Available online 30 November 2015
Methods: Data on daily MT and childhood BD between 2006 and 2012 were collected from the Bureau of Meteorology and the Centre for Disease Control and Prevention in Hefei,
Keywords:
Anhui Province, China. A Poisson generalized linear regression model combined with a
Childhood
distributed lag non-linear model was used to analyse the effects of temperature on
Bacillary dysentery
childhood BD across different age and sex subgroups.
Mean temperature
Results: An increase in temperature was significantly associated with childhood BD, and
Climate
each 1 C increase corresponded to an increase of 1.58% [95% confidence interval (CI) 0.46 e2.71%] in the number of cases of BD. Children aged 0e5 years and girls were particularly sensitive to the effects of temperature. Conclusions: High temperatures may increase the risk of childhood BD in Hefei. Children aged 0e5 years and girls appear to be particularly sensitive to the effects of high temperature. © 2015 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Department of Epidemiology and Health Statistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, Anhui Province 230032, China. Tel./fax: þ86 55163869140. E-mail address: [email protected] (H. Su). http://dx.doi.org/10.1016/j.puhe.2015.10.011 0033-3506/© 2015 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Introduction Bacillary dysentery (BD) is mainly caused by Shigella. Common clinical manifestations include fever, chills, abdominal pain and diarrhoea after an incubation period of one or two days.1 BD is mainly spread through the faecaleoral route and person-toperson contacts. BD epidemics are common among overcrowded populations with poor sanitation. Previous studies have found that trends in BD transmission show significant seasonality, and its incidence peaks in summer and autumn.2e4 In recent decades, although the incidence of BD has declined considerably in developing countries,5 the considerable burden of BD is still a great public health concern in impoverished areas.6e8 Globally, BD remains an important cause of mortality among children aged 14 years),12e14 suggesting that research into childhood BD would be of more practical significance. Many individual, social and environmental factors are associated with the occurrence of BD.15 In northeast China, Huang et al. found that climatic factors (including temperature, evaporation, precipitation and relative humidity) were positively correlated with cases of BD.11 Associations between mean and maximum temperatures and BD have also been observed in Taiwan.16 Available evidence strongly suggests that children are more susceptible to BD, while few studies to date have focused on assessing the impact of temperature on BD among children, and little is known about whether the relationship between temperature and childhood BD varies by age and sex. The incidence of BD in China is high, which can be largely attributable to the extremely high population mobility and high population density. Adverse effects of mean temperature (MT) on BD may exist in different areas with various socioeconomic statuses, population characteristics and weather conditions. As such, an eastern inland city of China (Hefei) was selected as the study site. This study attempted to address the following research issues using a Poisson generalized linear regression model combined with a distributed lag non-linear model (DLNM):17 What is the relationship between daily MT and childhood BD? Which subgroups are more vulnerable to the effects of MT on BD? Is there a delayed effect of MT on childhood BD?
Methods Setting Hefei, the capital city of Anhui Province, is located in the east of China (31 520 N, 117 170 E) (see Fig. 1). The city has an area of 11,408 km2, a population of approximately 7.61 million, and
21
18.1% of the population are aged 0e14 years.18 Hefei has a typical subtropical humid monsoon climate, with hot summers and mild winters.
Data collection Daily data on BD morbidity in children (aged 0e14 years) between 2006 and 2012 were collected from Hefei Centre for Disease Control and Prevention. Age (0e5 years and 6e14 years) and sex (male and female) stratified analyses were conducted. The quality of BD data used in this study is reliable. BD occurs frequently in China, and it is easy for doctors to make a correct diagnosis. In addition, all cases of BD need to be reported to the local infectious disease surveillance system by the surveillance system network in a standardized format. Meteorological data were collected from the Hefei Bureau of Meteorology between 2006 and 2012, including daily MT, maximum temperature, minimum temperature, precipitation and relative humidity (RH). The prevalence of BD in children aged 17 C (vertical dotted line). The doseeresponse relationship for the cumulative effect of MT on childhood BD and range of MT are illustrated in Fig. 3. An almost linear relationship was observed for the different group variables. The relationship between BD and MT in children aged 14 years is shown in Table 2, suggesting that the temperature effects on childhood BD appeared to be acute and greatest on the day of exposure (lag of 0 days). However, the lag time of MT on BD for children aged 0e14 years, children aged 0e5 years, and boys and girls was six days, which differed from that in children aged 6e14 years (three days). The effect of MT on BD in children aged 6e14 years was greater than that in children aged 0e5 years, while the effect of MT on BD in children aged 0e5 years lasted longer. In particular, each 1 C increase in MT corresponded to an increase of 1.58% (95% CI 0.46e2.71%) in cases of BD.
Table 1 e Descriptive statistics for bacillary dysentery (BD) and weather variables among children in Hefei, China, from 2006 to 2012. Variables BD in children aged 0e14 years BD in boys BD in girls BD in children aged 0e5 years BD in children aged 6e14 years Maximum temperature ( C) Mean temperature ( C) Minimum temperature ( C) Relative humidity (%) Precipitation (mm) SD, standard deviation.
Mean
SD
Min
Max
5.1 3.4 1.7 4.3 0.8 21.3 16.7 13.0 73.4 3.0
2.8 1.9 1.2 2.7 0.9 9.8 9.6 9.6 14.6 9.1
0 0 0 0 0 1.8 5.1 11.2 21.0 0
15.0 13.0 8.0 18.0 6.0 38.8 34.0 30.6 100.0 146.0
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Fig. 2 e The daily distribution of mean temperature and the cases of bacillary dysentery in Hefei, 2006e2012.
To evaluate the adequacy of the model, the residuals of the model were checked. The results are shown in Fig. 4.
Discussion The purpose of this study was to investigate the relationship between MT and childhood BD. Several notable findings were observed. First, there was a significant relationship between MT and childhood BD, particularly in children aged 0e5 years, boys and girls. Second, the longest lagged effects of MT on BD differed between age and sex groups (lag of 7, 6, 3, 4 and 7 days for children aged 0e14 years, children aged 0e5 years, children aged 6e14 years, boys and girls, respectively). Third, the lagged effect of MT on childhood BD was greatest on the day of exposure (lag of 0 days) and decreased over time. A significant relationship between childhood BD and MT was detected. Previous studies have found a 12% and 16% increase in BD for every 1 C increase in maximum or minimum temperature in Jinan City and Shenzhen, respectively, in China.2 In Peru, each 1 C increase in temperature corresponded to an 8% increase in the risk of childhood diarrhoea.24 To date, the underlying mechanism of the effect of high temperature on childhood BD remains unclear, but there are some possible explanations for the relationship. Firstly, it has been reported that higher temperatures may indirectly increase bacterial transmission, multiplication and survival rate.25,26 Bacteria will breed rapidly in raw food at high
23
temperatures, which means that the rate of infection will increase.27e29 Secondly, high temperatures may increase the risk of contracting pathogens by increased chance of personto-person contact and increased population density.30 Thirdly, incubation and survival of BD could be affected by weather variability, which could become one of major predictors of a BD outbreak.11 This study found that the greatest effect of MT on childhood BD occurred with a lag of 0 days, which is consistent with a previous study that examined the relationship between diurnal temperature range and childhood diarrhoea caused by BD.21 The result may imply that the effect of MT on childhood BD is acute due to the short incubation period of BD,1 which is consistent with a previous study.31 Some studies have found a linear relationship between MT and BD, which is generally consistent with the present finding (Fig. 3). In previous studies, different lagged effects of temperature on BD have been reported, ranging from a few days to several weeks.25,32 In the present study, the longest lagged effect of MT on BD in children aged 0e5 years was 6 days, which was longer than that in children aged 6e14 years. This means that children aged 5 years appeared to be more vulnerable to the effects of BD, which is consistent with previous studies.33,34 This may be due to the immaturity of the immune systems of younger children.26,29 At the same time, increased susceptibility to BD due to a less effective immune response of younger children will prolong the response time.35 Moreover, previous studies have shown that education levels and self-care ability were correlated with diarrhoeal diseases.25 It seems that older children are more likely to benefit from health education than younger children. A surprising finding was that the longest lagged effect of MT on BD in boys (four days) differed from that in girls (seven days). Currently, it is not clear why the effects of MT lasted longer in girls than in boys. A reasonable speculation may be that boys and girls have different physiological structures, distinct genetic levels and social behaviours, such as routine activity.36,37 In addition, different regions, populations, sanitary concepts and hygienic conditions may contribute to the difference between boys and girls.38,39 The main strengths of this study were as follows. First, this is the first study to examine the relationship between lagged effects of MT and childhood BD in different age and sex subgroups. Furthermore, non-linear and lagged effects of MT on childhood BD were quantified using advanced statistical methods combining non-linear and lagged effects. In addition, previous studies looking at the temperatureeBD relationship mainly focused on monthly or weekly data; the daily data used in the present study could make the estimation more accurate. This study also had several limitations. First, only data from recent years from one city were included, and thus the results of this study may not be generalizable to populations in other regions. Therefore, more studies in other locations are needed to further understand the effect of MT on childhood BD. Second, there may be some exposure bias in this study, as identifiable individual exposure information was not available. Third, other factors (e.g. personal social information) were not controlled for in this study.
24
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Fig. 3 e The overall effects of mean temperature range on bacillary dysentery among children. RR (relative risk), Grey area (95% confidence intervals of overall effects of mean temperature).
Table 2 e Relative risk (95% confidence interval) of bacillary dysentery in children aged ≤14 years associated with 1 unit increase in mean temperature range. Relative risk (95% confidence interval) 0e14 years Lag0 Lag1 Lag2 Lag3 Lag4 Lag5 Lag6 a
1.0158 1.0142 1.0127 1.0112 1.0097 1.0083 1.0070
P < 0.05.
Boys a
(1.0046e1.0271) (1.0045e1.0240)a (1.0040e1.0211)a (1.0039e1.0184)a (1.0034e1.0161)a (1.0025e1.0141)a (1.0015e1.0126)a
1.0133 1.0118 1.0104 1.0091 1.0078 1.0065 1.0054
Girls a
(1.0001e1.0266) (1.0004e1.0234)a (1.0006e1.0203)a (1.0006e1.0176)a (1.0003e1.0152)a (0.9997e1.0134) (0.9989e1.0120)
1.0220 1.0200 1.0181 1.0162 1.0143 1.0125 1.0108
0e5 years a
(1.0041e1.0401) (1.0045e1.0358)a (1.0047e1.0317)a (1.0046e1.0279)a (1.0042e1.0246)a (1.0033e1.0219)a (1.0019e1.0197)a
1.0122 1.0112 1.0102 1.0092 1.0082 1.0073 1.0065
6e14 years a
(1.0005e1.0242) (1.0010e1.0216)a (1.0014e1.0191)a (1.0016e1.0169)a (1.0016e1.0150)a (1.0012e1.0135)a (1.0006e1.0123)a
1.0331 1.0285 1.0239 1.0195 1.0153 1.0114 1.0077
(1.0032e1.0639)a (1.0026e1.0550)a (1.0018e1.0466)a (1.0004e1.0390)a (0.9960e1.0324) (0.9960e1.0270) (0.9929e1.0228)
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Fig. 4 e The scatter plot of residuals from 2006 to 2012.
Conclusions In conclusion, this study found a significant association between MT and childhood BD among children aged 0e14 years and children aged 0e5 years, boys and girls. MT had longerlasting effects on BD in children aged 0e5 years and girls than children aged 0e14 years and boys. The effect of MT on childhood BD was greatest at a lag of 0 days, and then decreased. It is important for both health practitioners and parents to be aware of the adverse effect of MT on childhood BD, and to take preventive measures to protect children (particularly children aged 0e5 years and boys) from the associated risks of high temperature. As climate change continues, unstable weather conditions are likely to become more frequent. Therefore, there is a great need to strengthen health education regarding temperature changes in order to improve people's awareness about childhood BD protection.
Author statements Ethical approval Ethical approval was obtained from the Ethic Review Board of Anhui Medical University.
Funding This research was funded by Anhui Natural Science Fund (NO.1408085MH159).
Competing interests None declared.
references
1. Niyogi SK. Shigellosis. J Microbiol 2005;43:133e43.
25
2. Zhang Y, Bi P, Hiller JE, Sun Y, Ryan P. Climate variations and bacillary dysentery in northern and southern cities of China. J Infect 2007;55:194e200. 3. Guan P, Huang D, Guo J, Wang P, Zhou B. Bacillary dysentery and meteorological factors in northeastern China: a historical review based on classification and regression trees. Jpn J Infect Dis 2008;61:356e60. 4. Joh RI, Hoekstra RM, Barzilay EJ, Bowen A, Mintz ED, Weiss H, Weitz JS. Dynamics of shigellosis epidemics: estimating individual-level transmission and reporting rates from national epidemiologic data sets. Am J Epidemiol 2013;178:1319e26. 5. Parashar UD, Gibson CJ, Bresee JS, Glass RI. Rotavirus and severe childhood diarrhea. Emerg Infect Dis 2006;12:304e6. 6. Iwalokun BA, Gbenle GO, Smith SI, Ogunledun A, Akinsinde KA, Omonigbehin EA. Epidemiology of shigellosis in Lagos, Nigeria: trends in antimicrobial resistance. J Health Popul Nutr 2001;19:183e90. 7. Ram PK, Crump JA, Gupta SK, Miller MA, Mintz ED. Part II. Analysis of data gaps pertaining to Shigella infections in low and medium human development index countries, 1984e2005. Epidemiol Infect 2008;136:577e603. 8. World Health Organization. Shigellosis: disease burden, epidemiology and case management. Wkly Epidemiol Rec 2005;80:94e9. 9. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, Jha P, Campbell H, Walker CF, Cibulskis R, Eisele T, Liu L, Mathers CChild Health Epidemiology Reference Group of WHO and UNICEF. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010;375:1969e87. 10. Sui JL, Zhang J, Sun JL, Chang SR, Zhang WD, Wang ZJ. Surveillance of bacillary dysentery in China, 2009. Dis Surveill 2010;25:947e50. 11. Huang D, Guan P, Guo J, Wang P, Zhou B. Investigating the effects of climate variations on bacillary dysentery incidence in northeast China using ridge regression and hierarchical cluster analysis. BMC Infect Dis 2008;8:130. 12. Zhang Y, Bi P, Sun Y, Hiller JE. Projected years lost due to disabilities (YLDs) for bacillary dysentery related to increased temperature in temperate and subtropical cities of China. J Environ Monit 2012;14:510e6. 13. Lee H, Kotloff K, Chukaserm P, Samosornsuk S, Chompook P, Deen JL, Von Seidlein L, Clemens JD, Wanpen C. Shigellosis remains an important problem in children less than 5 years of age in Thailand. Epidemiol Infect 2005;133:469e74. 14. D'Souza RM, Hall G, Becker NG. Climatic factors associated with hospitalizations for rotavirus diarrhoea in children under 5 years of age. Epidemiol Infect 2008;136:56e64. 15. Kosek M, Bern C, Guerrant RL. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 2003;81:197e204. 16. Chou WC, Wu JL, Wang YC, Huang H, Sung FC, Chuang CY. Modeling the impact of climate variability on diarrheaassociated diseases in Taiwan (1996e2007). Sci Total Environ 2010;409:43e51. 17. Gasparrini A, Armstrong B, Kenward MG. Distributed lag nonlinear models. Stat Med 2010;29:2224e34. 18. Statistics Bureau of Anhui Province. Statistical bulletin of the national economic and social development in Anhui Province, in 2013. Hefei, Anhui Province, China: Anhui Journal of Preventive Medicine. Available at: http://www.ahtjj.gov.cn/ tjj/web/info_view.jsp?strId¼1392799909282214; 2014 (last accessed 12 October 2014).
26
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
19. Wu SY, Hu MX, Zhao KF. Epidemiological analysis on bacterial dysentery from 2009 to 2011 in Hefei City. Anhui J Prev Med 2013;19:126e7. 20. Zhao KF, Hu MX. Epidemiological analysis on bacterial dysentery from 2004 to 2009 in Hefei City. Chin J Dis Control Prev 2011;15:494e6. 21. Xu Z, Huang C, Turner LR, Su H, Qiao Z, Tong S. Is diurnal temperature range a risk factor for childhood diarrhea? PLoS One 2013;8:e64713. 22. Kelly-Hope LA, Alonso WJ, Thiem VD, Canh do G, Anh DD, Lee H, Miller MA. Temporal trends and climatic factors associated with bacterial enteric diseases in Vietnam, 1991e2001. Environ Health Perspect 2008;116:7e12. 23. Gasparrini A. Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 2011;43:1e20. 24. Checkley W, Epstein LD, Gilman RH, Figueroa D, Cama RI, ~ o and ambient temperature Patz JA, Black RE. Effect of El Nin on hospital admissions for diarrhoeal diseases in Peruvian children. Lancet 2000;355:442e50. 25. Zhang Y, Bi P, Hiller JE. Weather and the transmission of bacillary dysentery in Jinan, northern China: a time-series analysis. Public Health Rep 2008;123:61e6. 26. Tirado MC, Clarke R, Jaykus LA, McQuatters-Gollop A, Frank JM. Climate change and food safety: a review. Food Res Int 2010;43:1745e65. 27. Lake IR, Gillespie IA, Bentham G, Nichols GL, Lane C, Adak GK, Threlfall EJ. A re-evaluation of the impact of temperature and climate change on foodborne illness. Epidemiol Infect 2009;137:1538e47. 28. Hall GV, D'Souza RM, Kirk MD. Foodborne disease in the new millennium: out of the frying pan and into the fire? Med J Aust 2002;177:614e8. 29. Lehane L. Ciguatera update. Med J Aust 2000;172:176e9. 30. Ashbolt R, Givney R, Gregory JE, Hall G, Hundy R, Kirk M, McKay I, Meuleners L, Millard G, Raupach J, Roche P, Plaizier NP, Sarna MK, Stafford R, Tomaska N, Unicomb L, Williams COzFoodNet Working Group. Enhancing foodborne disease surveillance across Australia in 2001: the
31.
32.
33.
34.
35.
36.
37.
38.
39.
OzFoodNet Working Group. Commun Dis Intell Q Rep 2002;26:375e406. Li Z, Wang L, Sun W, Hou X, Yang H, Sun L, Xu S, Sun Q, Zhang J, Song H, Lin H. Identifying high-risk areas of bacillary dysentery and associated meteorological factors in Wuhan, China. Sci Rep 2013;3:3239. Singh RB, Hales S, de Wet N, Raj R, Hearnden M, Weinstein P. The influence of climate variation and change on diarrheal disease in the Pacific Islands. Environ Health Perspect 2001;109:155e9. el Saadi OE, Esterman AJ, Cameron S, Roder DM. Murray river water, raised cyanobacterial cell counts, and gastrointestinal and dermatological symptoms. Med J Aust 1995;162:122e5. Wang XY, Tao FB, Xiao DL, Lee H, Deen J, Gong J, Zhao YL, Zhou WZ, Li WM, Shen B, Song Y, Ma JM, Li ZM, Wang ZJ, Su PY, Chang N, Xu JH, Ouyang PY, Seidlein LZ, Xu ZY, Clemens JD. Trend and disease burden of bacillary dysentery in China (1991e2000). Bull World Health Organ 2006;84:561e8. Von SL, Kim DR, Ali M, Lee H, Wang X, Thiem VD, Canh DG, Chaicumpa W, Agtini MD, Hossain A, Bhutta ZA, Mason C, Sethabutr O, Talukder K, Nair GB, Deen JL, Kotloff K, Clemens J. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med 2006;3:e353. Wang XY, Du L, Von Seidlein L, Xu ZY, Zhang YL, Hao ZY, Han OP, Ma JC, Lee HJ, Ali M, Han CQ, Xing ZC, Chen JC, Clemens J. Occurrence of shigellosis in the young and elderly in rural China: results of a 12-month population-based surveillance study. Am J Trop Med Hyg 2005;73:416e22. quier E. Decreased thermal Frascarolo P, Schutz Y, Je conductance during the luteal phase of the menstrual cycle in women. J Appl Physiol 1990;69:2029e33. Grucza R. Efficiency of thermoregulatory system in man under endogenous and exogenous heat loads. Acta Physiol Pol 1990;41:123e45. Basu R. High ambient temperature and mortality: a review of epidemiologic studies from 2001 to 2008. Environ Health 2009;8:40.
Available online at www.sciencedirect.com
Public Health journal homepage: www.elsevier.com/puhe
Original Research
Daily temperature change in relation to the risk of childhood bacillary dysentery among different age groups and sexes in a temperate city in China K. Li a, K. Zhao b, L. Shi c, L. Wen a, H. Yang a, J. Cheng a, X. Wang a, H. Su a,* a
Department of Epidemiology and Health Statistics, School of Public Health, Anhui Medical University, Hefei, Anhui, China b Hefei Centre for Disease Control and Prevention of Anhui Province, Hefei, Anhui, China c Department of Nutrition and Food Hygiene, School of Public Health, Dalian Medical University, Dalian, Liaoning, China
article info
abstract
Article history:
Background: In recent years, many studies have found that ambient temperature is signif-
Received 23 October 2014
icantly associated with bacillary dysentery (BD). However, there is limited evidence on the
Received in revised form
relationship between temperature and childhood BD in temperate areas.
14 July 2015
Objectives: To investigate the relationship between daily mean temperature (MT) and
Accepted 23 October 2015
childhood BD in China.
Available online 30 November 2015
Methods: Data on daily MT and childhood BD between 2006 and 2012 were collected from the Bureau of Meteorology and the Centre for Disease Control and Prevention in Hefei,
Keywords:
Anhui Province, China. A Poisson generalized linear regression model combined with a
Childhood
distributed lag non-linear model was used to analyse the effects of temperature on
Bacillary dysentery
childhood BD across different age and sex subgroups.
Mean temperature
Results: An increase in temperature was significantly associated with childhood BD, and
Climate
each 1 C increase corresponded to an increase of 1.58% [95% confidence interval (CI) 0.46 e2.71%] in the number of cases of BD. Children aged 0e5 years and girls were particularly sensitive to the effects of temperature. Conclusions: High temperatures may increase the risk of childhood BD in Hefei. Children aged 0e5 years and girls appear to be particularly sensitive to the effects of high temperature. © 2015 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Department of Epidemiology and Health Statistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, Anhui Province 230032, China. Tel./fax: þ86 55163869140. E-mail address: [email protected] (H. Su). http://dx.doi.org/10.1016/j.puhe.2015.10.011 0033-3506/© 2015 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Introduction Bacillary dysentery (BD) is mainly caused by Shigella. Common clinical manifestations include fever, chills, abdominal pain and diarrhoea after an incubation period of one or two days.1 BD is mainly spread through the faecaleoral route and person-toperson contacts. BD epidemics are common among overcrowded populations with poor sanitation. Previous studies have found that trends in BD transmission show significant seasonality, and its incidence peaks in summer and autumn.2e4 In recent decades, although the incidence of BD has declined considerably in developing countries,5 the considerable burden of BD is still a great public health concern in impoverished areas.6e8 Globally, BD remains an important cause of mortality among children aged 14 years),12e14 suggesting that research into childhood BD would be of more practical significance. Many individual, social and environmental factors are associated with the occurrence of BD.15 In northeast China, Huang et al. found that climatic factors (including temperature, evaporation, precipitation and relative humidity) were positively correlated with cases of BD.11 Associations between mean and maximum temperatures and BD have also been observed in Taiwan.16 Available evidence strongly suggests that children are more susceptible to BD, while few studies to date have focused on assessing the impact of temperature on BD among children, and little is known about whether the relationship between temperature and childhood BD varies by age and sex. The incidence of BD in China is high, which can be largely attributable to the extremely high population mobility and high population density. Adverse effects of mean temperature (MT) on BD may exist in different areas with various socioeconomic statuses, population characteristics and weather conditions. As such, an eastern inland city of China (Hefei) was selected as the study site. This study attempted to address the following research issues using a Poisson generalized linear regression model combined with a distributed lag non-linear model (DLNM):17 What is the relationship between daily MT and childhood BD? Which subgroups are more vulnerable to the effects of MT on BD? Is there a delayed effect of MT on childhood BD?
Methods Setting Hefei, the capital city of Anhui Province, is located in the east of China (31 520 N, 117 170 E) (see Fig. 1). The city has an area of 11,408 km2, a population of approximately 7.61 million, and
21
18.1% of the population are aged 0e14 years.18 Hefei has a typical subtropical humid monsoon climate, with hot summers and mild winters.
Data collection Daily data on BD morbidity in children (aged 0e14 years) between 2006 and 2012 were collected from Hefei Centre for Disease Control and Prevention. Age (0e5 years and 6e14 years) and sex (male and female) stratified analyses were conducted. The quality of BD data used in this study is reliable. BD occurs frequently in China, and it is easy for doctors to make a correct diagnosis. In addition, all cases of BD need to be reported to the local infectious disease surveillance system by the surveillance system network in a standardized format. Meteorological data were collected from the Hefei Bureau of Meteorology between 2006 and 2012, including daily MT, maximum temperature, minimum temperature, precipitation and relative humidity (RH). The prevalence of BD in children aged 17 C (vertical dotted line). The doseeresponse relationship for the cumulative effect of MT on childhood BD and range of MT are illustrated in Fig. 3. An almost linear relationship was observed for the different group variables. The relationship between BD and MT in children aged 14 years is shown in Table 2, suggesting that the temperature effects on childhood BD appeared to be acute and greatest on the day of exposure (lag of 0 days). However, the lag time of MT on BD for children aged 0e14 years, children aged 0e5 years, and boys and girls was six days, which differed from that in children aged 6e14 years (three days). The effect of MT on BD in children aged 6e14 years was greater than that in children aged 0e5 years, while the effect of MT on BD in children aged 0e5 years lasted longer. In particular, each 1 C increase in MT corresponded to an increase of 1.58% (95% CI 0.46e2.71%) in cases of BD.
Table 1 e Descriptive statistics for bacillary dysentery (BD) and weather variables among children in Hefei, China, from 2006 to 2012. Variables BD in children aged 0e14 years BD in boys BD in girls BD in children aged 0e5 years BD in children aged 6e14 years Maximum temperature ( C) Mean temperature ( C) Minimum temperature ( C) Relative humidity (%) Precipitation (mm) SD, standard deviation.
Mean
SD
Min
Max
5.1 3.4 1.7 4.3 0.8 21.3 16.7 13.0 73.4 3.0
2.8 1.9 1.2 2.7 0.9 9.8 9.6 9.6 14.6 9.1
0 0 0 0 0 1.8 5.1 11.2 21.0 0
15.0 13.0 8.0 18.0 6.0 38.8 34.0 30.6 100.0 146.0
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Fig. 2 e The daily distribution of mean temperature and the cases of bacillary dysentery in Hefei, 2006e2012.
To evaluate the adequacy of the model, the residuals of the model were checked. The results are shown in Fig. 4.
Discussion The purpose of this study was to investigate the relationship between MT and childhood BD. Several notable findings were observed. First, there was a significant relationship between MT and childhood BD, particularly in children aged 0e5 years, boys and girls. Second, the longest lagged effects of MT on BD differed between age and sex groups (lag of 7, 6, 3, 4 and 7 days for children aged 0e14 years, children aged 0e5 years, children aged 6e14 years, boys and girls, respectively). Third, the lagged effect of MT on childhood BD was greatest on the day of exposure (lag of 0 days) and decreased over time. A significant relationship between childhood BD and MT was detected. Previous studies have found a 12% and 16% increase in BD for every 1 C increase in maximum or minimum temperature in Jinan City and Shenzhen, respectively, in China.2 In Peru, each 1 C increase in temperature corresponded to an 8% increase in the risk of childhood diarrhoea.24 To date, the underlying mechanism of the effect of high temperature on childhood BD remains unclear, but there are some possible explanations for the relationship. Firstly, it has been reported that higher temperatures may indirectly increase bacterial transmission, multiplication and survival rate.25,26 Bacteria will breed rapidly in raw food at high
23
temperatures, which means that the rate of infection will increase.27e29 Secondly, high temperatures may increase the risk of contracting pathogens by increased chance of personto-person contact and increased population density.30 Thirdly, incubation and survival of BD could be affected by weather variability, which could become one of major predictors of a BD outbreak.11 This study found that the greatest effect of MT on childhood BD occurred with a lag of 0 days, which is consistent with a previous study that examined the relationship between diurnal temperature range and childhood diarrhoea caused by BD.21 The result may imply that the effect of MT on childhood BD is acute due to the short incubation period of BD,1 which is consistent with a previous study.31 Some studies have found a linear relationship between MT and BD, which is generally consistent with the present finding (Fig. 3). In previous studies, different lagged effects of temperature on BD have been reported, ranging from a few days to several weeks.25,32 In the present study, the longest lagged effect of MT on BD in children aged 0e5 years was 6 days, which was longer than that in children aged 6e14 years. This means that children aged 5 years appeared to be more vulnerable to the effects of BD, which is consistent with previous studies.33,34 This may be due to the immaturity of the immune systems of younger children.26,29 At the same time, increased susceptibility to BD due to a less effective immune response of younger children will prolong the response time.35 Moreover, previous studies have shown that education levels and self-care ability were correlated with diarrhoeal diseases.25 It seems that older children are more likely to benefit from health education than younger children. A surprising finding was that the longest lagged effect of MT on BD in boys (four days) differed from that in girls (seven days). Currently, it is not clear why the effects of MT lasted longer in girls than in boys. A reasonable speculation may be that boys and girls have different physiological structures, distinct genetic levels and social behaviours, such as routine activity.36,37 In addition, different regions, populations, sanitary concepts and hygienic conditions may contribute to the difference between boys and girls.38,39 The main strengths of this study were as follows. First, this is the first study to examine the relationship between lagged effects of MT and childhood BD in different age and sex subgroups. Furthermore, non-linear and lagged effects of MT on childhood BD were quantified using advanced statistical methods combining non-linear and lagged effects. In addition, previous studies looking at the temperatureeBD relationship mainly focused on monthly or weekly data; the daily data used in the present study could make the estimation more accurate. This study also had several limitations. First, only data from recent years from one city were included, and thus the results of this study may not be generalizable to populations in other regions. Therefore, more studies in other locations are needed to further understand the effect of MT on childhood BD. Second, there may be some exposure bias in this study, as identifiable individual exposure information was not available. Third, other factors (e.g. personal social information) were not controlled for in this study.
24
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Fig. 3 e The overall effects of mean temperature range on bacillary dysentery among children. RR (relative risk), Grey area (95% confidence intervals of overall effects of mean temperature).
Table 2 e Relative risk (95% confidence interval) of bacillary dysentery in children aged ≤14 years associated with 1 unit increase in mean temperature range. Relative risk (95% confidence interval) 0e14 years Lag0 Lag1 Lag2 Lag3 Lag4 Lag5 Lag6 a
1.0158 1.0142 1.0127 1.0112 1.0097 1.0083 1.0070
P < 0.05.
Boys a
(1.0046e1.0271) (1.0045e1.0240)a (1.0040e1.0211)a (1.0039e1.0184)a (1.0034e1.0161)a (1.0025e1.0141)a (1.0015e1.0126)a
1.0133 1.0118 1.0104 1.0091 1.0078 1.0065 1.0054
Girls a
(1.0001e1.0266) (1.0004e1.0234)a (1.0006e1.0203)a (1.0006e1.0176)a (1.0003e1.0152)a (0.9997e1.0134) (0.9989e1.0120)
1.0220 1.0200 1.0181 1.0162 1.0143 1.0125 1.0108
0e5 years a
(1.0041e1.0401) (1.0045e1.0358)a (1.0047e1.0317)a (1.0046e1.0279)a (1.0042e1.0246)a (1.0033e1.0219)a (1.0019e1.0197)a
1.0122 1.0112 1.0102 1.0092 1.0082 1.0073 1.0065
6e14 years a
(1.0005e1.0242) (1.0010e1.0216)a (1.0014e1.0191)a (1.0016e1.0169)a (1.0016e1.0150)a (1.0012e1.0135)a (1.0006e1.0123)a
1.0331 1.0285 1.0239 1.0195 1.0153 1.0114 1.0077
(1.0032e1.0639)a (1.0026e1.0550)a (1.0018e1.0466)a (1.0004e1.0390)a (0.9960e1.0324) (0.9960e1.0270) (0.9929e1.0228)
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
Fig. 4 e The scatter plot of residuals from 2006 to 2012.
Conclusions In conclusion, this study found a significant association between MT and childhood BD among children aged 0e14 years and children aged 0e5 years, boys and girls. MT had longerlasting effects on BD in children aged 0e5 years and girls than children aged 0e14 years and boys. The effect of MT on childhood BD was greatest at a lag of 0 days, and then decreased. It is important for both health practitioners and parents to be aware of the adverse effect of MT on childhood BD, and to take preventive measures to protect children (particularly children aged 0e5 years and boys) from the associated risks of high temperature. As climate change continues, unstable weather conditions are likely to become more frequent. Therefore, there is a great need to strengthen health education regarding temperature changes in order to improve people's awareness about childhood BD protection.
Author statements Ethical approval Ethical approval was obtained from the Ethic Review Board of Anhui Medical University.
Funding This research was funded by Anhui Natural Science Fund (NO.1408085MH159).
Competing interests None declared.
references
1. Niyogi SK. Shigellosis. J Microbiol 2005;43:133e43.
25
2. Zhang Y, Bi P, Hiller JE, Sun Y, Ryan P. Climate variations and bacillary dysentery in northern and southern cities of China. J Infect 2007;55:194e200. 3. Guan P, Huang D, Guo J, Wang P, Zhou B. Bacillary dysentery and meteorological factors in northeastern China: a historical review based on classification and regression trees. Jpn J Infect Dis 2008;61:356e60. 4. Joh RI, Hoekstra RM, Barzilay EJ, Bowen A, Mintz ED, Weiss H, Weitz JS. Dynamics of shigellosis epidemics: estimating individual-level transmission and reporting rates from national epidemiologic data sets. Am J Epidemiol 2013;178:1319e26. 5. Parashar UD, Gibson CJ, Bresee JS, Glass RI. Rotavirus and severe childhood diarrhea. Emerg Infect Dis 2006;12:304e6. 6. Iwalokun BA, Gbenle GO, Smith SI, Ogunledun A, Akinsinde KA, Omonigbehin EA. Epidemiology of shigellosis in Lagos, Nigeria: trends in antimicrobial resistance. J Health Popul Nutr 2001;19:183e90. 7. Ram PK, Crump JA, Gupta SK, Miller MA, Mintz ED. Part II. Analysis of data gaps pertaining to Shigella infections in low and medium human development index countries, 1984e2005. Epidemiol Infect 2008;136:577e603. 8. World Health Organization. Shigellosis: disease burden, epidemiology and case management. Wkly Epidemiol Rec 2005;80:94e9. 9. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, Jha P, Campbell H, Walker CF, Cibulskis R, Eisele T, Liu L, Mathers CChild Health Epidemiology Reference Group of WHO and UNICEF. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010;375:1969e87. 10. Sui JL, Zhang J, Sun JL, Chang SR, Zhang WD, Wang ZJ. Surveillance of bacillary dysentery in China, 2009. Dis Surveill 2010;25:947e50. 11. Huang D, Guan P, Guo J, Wang P, Zhou B. Investigating the effects of climate variations on bacillary dysentery incidence in northeast China using ridge regression and hierarchical cluster analysis. BMC Infect Dis 2008;8:130. 12. Zhang Y, Bi P, Sun Y, Hiller JE. Projected years lost due to disabilities (YLDs) for bacillary dysentery related to increased temperature in temperate and subtropical cities of China. J Environ Monit 2012;14:510e6. 13. Lee H, Kotloff K, Chukaserm P, Samosornsuk S, Chompook P, Deen JL, Von Seidlein L, Clemens JD, Wanpen C. Shigellosis remains an important problem in children less than 5 years of age in Thailand. Epidemiol Infect 2005;133:469e74. 14. D'Souza RM, Hall G, Becker NG. Climatic factors associated with hospitalizations for rotavirus diarrhoea in children under 5 years of age. Epidemiol Infect 2008;136:56e64. 15. Kosek M, Bern C, Guerrant RL. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 2003;81:197e204. 16. Chou WC, Wu JL, Wang YC, Huang H, Sung FC, Chuang CY. Modeling the impact of climate variability on diarrheaassociated diseases in Taiwan (1996e2007). Sci Total Environ 2010;409:43e51. 17. Gasparrini A, Armstrong B, Kenward MG. Distributed lag nonlinear models. Stat Med 2010;29:2224e34. 18. Statistics Bureau of Anhui Province. Statistical bulletin of the national economic and social development in Anhui Province, in 2013. Hefei, Anhui Province, China: Anhui Journal of Preventive Medicine. Available at: http://www.ahtjj.gov.cn/ tjj/web/info_view.jsp?strId¼1392799909282214; 2014 (last accessed 12 October 2014).
26
p u b l i c h e a l t h 1 3 1 ( 2 0 1 6 ) 2 0 e2 6
19. Wu SY, Hu MX, Zhao KF. Epidemiological analysis on bacterial dysentery from 2009 to 2011 in Hefei City. Anhui J Prev Med 2013;19:126e7. 20. Zhao KF, Hu MX. Epidemiological analysis on bacterial dysentery from 2004 to 2009 in Hefei City. Chin J Dis Control Prev 2011;15:494e6. 21. Xu Z, Huang C, Turner LR, Su H, Qiao Z, Tong S. Is diurnal temperature range a risk factor for childhood diarrhea? PLoS One 2013;8:e64713. 22. Kelly-Hope LA, Alonso WJ, Thiem VD, Canh do G, Anh DD, Lee H, Miller MA. Temporal trends and climatic factors associated with bacterial enteric diseases in Vietnam, 1991e2001. Environ Health Perspect 2008;116:7e12. 23. Gasparrini A. Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 2011;43:1e20. 24. Checkley W, Epstein LD, Gilman RH, Figueroa D, Cama RI, ~ o and ambient temperature Patz JA, Black RE. Effect of El Nin on hospital admissions for diarrhoeal diseases in Peruvian children. Lancet 2000;355:442e50. 25. Zhang Y, Bi P, Hiller JE. Weather and the transmission of bacillary dysentery in Jinan, northern China: a time-series analysis. Public Health Rep 2008;123:61e6. 26. Tirado MC, Clarke R, Jaykus LA, McQuatters-Gollop A, Frank JM. Climate change and food safety: a review. Food Res Int 2010;43:1745e65. 27. Lake IR, Gillespie IA, Bentham G, Nichols GL, Lane C, Adak GK, Threlfall EJ. A re-evaluation of the impact of temperature and climate change on foodborne illness. Epidemiol Infect 2009;137:1538e47. 28. Hall GV, D'Souza RM, Kirk MD. Foodborne disease in the new millennium: out of the frying pan and into the fire? Med J Aust 2002;177:614e8. 29. Lehane L. Ciguatera update. Med J Aust 2000;172:176e9. 30. Ashbolt R, Givney R, Gregory JE, Hall G, Hundy R, Kirk M, McKay I, Meuleners L, Millard G, Raupach J, Roche P, Plaizier NP, Sarna MK, Stafford R, Tomaska N, Unicomb L, Williams COzFoodNet Working Group. Enhancing foodborne disease surveillance across Australia in 2001: the
31.
32.
33.
34.
35.
36.
37.
38.
39.
OzFoodNet Working Group. Commun Dis Intell Q Rep 2002;26:375e406. Li Z, Wang L, Sun W, Hou X, Yang H, Sun L, Xu S, Sun Q, Zhang J, Song H, Lin H. Identifying high-risk areas of bacillary dysentery and associated meteorological factors in Wuhan, China. Sci Rep 2013;3:3239. Singh RB, Hales S, de Wet N, Raj R, Hearnden M, Weinstein P. The influence of climate variation and change on diarrheal disease in the Pacific Islands. Environ Health Perspect 2001;109:155e9. el Saadi OE, Esterman AJ, Cameron S, Roder DM. Murray river water, raised cyanobacterial cell counts, and gastrointestinal and dermatological symptoms. Med J Aust 1995;162:122e5. Wang XY, Tao FB, Xiao DL, Lee H, Deen J, Gong J, Zhao YL, Zhou WZ, Li WM, Shen B, Song Y, Ma JM, Li ZM, Wang ZJ, Su PY, Chang N, Xu JH, Ouyang PY, Seidlein LZ, Xu ZY, Clemens JD. Trend and disease burden of bacillary dysentery in China (1991e2000). Bull World Health Organ 2006;84:561e8. Von SL, Kim DR, Ali M, Lee H, Wang X, Thiem VD, Canh DG, Chaicumpa W, Agtini MD, Hossain A, Bhutta ZA, Mason C, Sethabutr O, Talukder K, Nair GB, Deen JL, Kotloff K, Clemens J. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med 2006;3:e353. Wang XY, Du L, Von Seidlein L, Xu ZY, Zhang YL, Hao ZY, Han OP, Ma JC, Lee HJ, Ali M, Han CQ, Xing ZC, Chen JC, Clemens J. Occurrence of shigellosis in the young and elderly in rural China: results of a 12-month population-based surveillance study. Am J Trop Med Hyg 2005;73:416e22. quier E. Decreased thermal Frascarolo P, Schutz Y, Je conductance during the luteal phase of the menstrual cycle in women. J Appl Physiol 1990;69:2029e33. Grucza R. Efficiency of thermoregulatory system in man under endogenous and exogenous heat loads. Acta Physiol Pol 1990;41:123e45. Basu R. High ambient temperature and mortality: a review of epidemiologic studies from 2001 to 2008. Environ Health 2009;8:40.
