Int. J. Environ. Res. Public Health 2015, 12, 1054-1068; doi:10.

3390/ijerph120201054
OPEN ACCESS

International Journal of
Environmental Research and
Public Health
ISSN 1660-4601
www.mdpi.com/journal/ijerph
Article

Impacts of Tropical Cyclones and Accompanying Precipitation

on Infectious Diarrhea in Cyclone Landing Areas of Zhejiang
Province, China
Zhengyi Deng 1,†, Huanmiao Xun 1,2,†, Maigeng Zhou 3, Baofa Jiang 1,2, Songwang Wang 4,
Qing Guo 4, Wei Wang 1, Ruihua Kang 1, Xin Wang 1, Gifty Marley 1 and Wei Ma 1,2,*

1
Department of Epidemiology and Health Statistics, School of Public Health, Shandong University,
44 West Wenhua Road, Jinan 250012, China; E-Mails: deng.zhengyi@hotmail.com (Z.D.);
xun1huan2miao3@yeah.net (H.X.); bjiang@sdu.edu.cn (B.J.); shandawangwei@163.com (W.W.);
kangrh@yahoo.com (R.K.); wangxin0730@yeah.net (X.W.); giftatluck@yahoo.com (G.M.)
2
Shandong University Climate Change and Health Center, 44 West Wenhua Road,
Jinan 250012, China
3
National Center for Chronic and Noncommunicable Disease Control and Prevention,
Chinese Center for Disease Control and Prevention, 155 Changbai Road, Changping District,
Beijing 102206, China; E-Mail: maigengzhou@126.com
4
National Center for Public Health Surveillance and Information Services, Chinese Center for
Disease Control and Prevention, 155 Changbai Road, Changping District, Beijing 102206, China;
E-Mails: wsw002@126.com (S.W.); guoqing@chinacdc.cn (Q.G.)

†
These authors contributed equally to this work and should be regarded as co-first author.

* Author to whom correspondence should be addressed; E-Mail: weima@sdu.edu.cn;

Tel.: +86-531-8838-2141.

Academic Editors: Kristie L. Ebi and Jeremy Hess

Received: 1 November 2014 / Accepted: 16 January 2015 / Published: 22 January 2015

Abstract: Background: Zhejiang Province, located in southeastern China, is frequently hit

by tropical cyclones. This study quantified the associations between infectious diarrhea and
the seven tropical cyclones that landed in Zhejiang from 2005–2011 to assess the impacts of
the accompanying precipitation on the studied diseases. Method: A unidirectional
case-crossover study design was used to evaluate the impacts of tropical storms and typhoons
on infectious diarrhea. Principal component analysis (PCA) was applied to eliminate
Int. J. Environ. Res. Public Health 2015, 12 1055

multicollinearity. A multivariate logistic regression model was used to estimate the odds
ratios (ORs) and the 95% confidence intervals (CIs). Results: For all typhoons studied,
the greatest impacts on bacillary dysentery and other infectious diarrhea were identified on
lag 6 days (OR = 2.30, 95% CI: 1.81–2.93) and lag 5 days (OR = 3.56, 95% CI: 2.98–4.25),
respectively. For all tropical storms, impacts on these diseases were highest on lag 2 days
(OR = 2.47, 95% CI: 1.41–4.33) and lag 6 days (OR = 2.46, 95% CI: 1.69–3.56),
respectively. The tropical cyclone precipitation was a risk factor for both bacillary dysentery
and other infectious diarrhea when daily precipitation reached 25 mm and 50 mm with the
largest OR = 3.25 (95% CI: 1.45–7.27) and OR = 3.05 (95% CI: 2.20–4.23), respectively.
Conclusions: Both typhoons and tropical storms could contribute to an increase in risk of
bacillary dysentery and other infectious diarrhea in Zhejiang. Tropical cyclone precipitation
may also be a risk factor for these diseases when it reaches or is above 25 mm and 50 mm,
respectively. Public health preventive and intervention measures should consider the adverse
health impacts from tropical cyclones.

Keywords: tropical cyclone; precipitation; infectious diarrhea; bacillary dysentery; risk factor

1. Introduction

Tropical cyclones, also called typhoons, hurricanes or cyclones depending on the geographical area,
are periodically associated with disasters [1]. According to the Chinese national standard, tropical
cyclones are categorized as tropical depressions when the maximum average wind velocity near the
bottom of the tropical cyclone center reaches 10.8 m/s–17.1 m/s; tropical storms at 17.2 m/s–24.4 m/s;
severe tropical storms at 24.5 m/s–32.6 m/s; typhoons at 32.7 m/s–41.4 m/s, severe typhoons at
41.5 m/s–50.9 m/s, and super typhoons at 51.0 m/s [2]. Around the world, the annual average number of
meteorological disasters including tropical cyclones during the 2002–2011 period was 102. In 2012 they
represented 25% of all disasters [3]. Zhejiang Province is one of the most developed provinces in China.
It is located at the southeastern coast and hence vulnerable to the tropical cyclones which land on
Zhejiang every year, often from July to September, leading to severe injury and large economic losses.
Tropical cyclones can cause severe public health consequences, such as death, injuries, psychosocial
problems, and increases in infectious diseases [1]. For instance, the super typhoon Saomai in 2006
affected an estimated disaster area of 103,000 hectares, nearly 3.5 million citizens were affected with
1 million forced to evacuate, 204 people died, and 50 thousand buildings were damaged in Zhejiang.
The total estimated economic damage in Zhejiang was higher than 12 billion Yuan [4].
Previous studies have analyzed the relationship between tropical cyclones and infectious diseases
such as leptospirosis, dengue, cholera, and other infectious diarrhea [5–8]. For example, typhoon
Morakot brought unusual epidemics of leptospirosis to Taiwan in 2009 [9]. Hsieh’s study illustrated that
Hurricane Michelle potentially facilitated the spread of the dengue serotype DENV-3 in Havana [8].
Research on infectious diarrhea indicates that tropical cyclones may increase the risk of infectious
diarrheal diseases in affected areas. For example, after Cyclone Aila in 2009, there was an increase in
infectious diarrheal patients in Bengal, India [10]. An outbreak of norovirus gastroenteritis was detected
Int. J. Environ. Res. Public Health 2015, 12 1056

among evacuees after the landfall of Hurricane Katrina in America in 2005 [11]. In South Korea, there
was a significant increase in infectious diarrhea hospitalization cases after a typhoon [7]. However,
analyses of these studies were not comprehensive with respect to classification of tropical cyclone and
some were not quantitative. In addition, there are few systematical studies conducted in China, which
may be quite different from other countries due to variance in local environmental and socio-economic
situations.
Infectious diarrhea is a severe infectious disease and an important public health issue in China, leading
to more than 7 million people affected each year. In 2009 and 2010, 655,658 and 746,551 cases of
infectious diarrhea were reported, respectively [12]. Therefore, there is a need to examine the influence
of tropical cyclones on this group of infectious diseases.
Water quality and sanitation coverage are the most important intermediate factors determining the
association between tropical cyclones and infectious diarrhea [13]. Tropical cyclones can bring strong
precipitation, increasing the turbidity levels of drinking water [14]. Floodwaters caused by extreme
precipitation aids in the dispersion of diarrheal-causing pathogens (bacteria, protozoa and viruses) and
human infection [15]. Sewage overflow and damage of sewage system due to cyclone precipitation can
contaminate clean drinking water sources [16]. Because infectious diarrhea is spread through fecal-oral
pathways, contaminated water plays a crucial role in transmission. Therefore, precipitation can be a
major influential factor on infectious diarrhea.
Climate extremes including tropical cyclones are projected to increase in China [17]. Precipitation
and wind velocity are the typical meteorological characteristics used to describe tropical cyclones.
Studying the health effects of these factors can further understand the influence of tropical cyclones on
population health. Because tropical cyclones are categorized by wind velocity, analyzing the impact of
cyclone categories on infectious diarrhea may reflect the effect of wind velocity. There are few studies
on the association between other potentially hazardous factors, such as the typhoon-accompanied
precipitation, and infectious diarrhea.
The aim of this study was to quantitatively assess the impact of different classifications of tropical
cyclones landing on Zhejiang Province and the varied grades of accompanied precipitation on infectious
diarrhea from 2005–2011. Results provide scientific information for establishing a disease alerting
system during tropical cyclones. On the basis of the tropical cyclone category and the grade of
precipitation, the government can evaluate the risk of infectious diarrhea, and thus, take effective and
timely preventive measures.

2. Materials and Methods

2.1. Study Areas and Demographical Information

From 2005 to 2011, tropical cyclones affected Zhejiang Province, landing primarily in Wenzhou,
Taizhou and Lishui. These cities are located in the southeast of Zhejiang Province (Figure 1). The total
estimated area of these three cities was 38,495 square kilometers, accounting for 36.97% of Zhejiang
Province, with a total population in 2011 of approximately 16,464,800, including 8,508,000 men and
7,956,800 women [18].
Int. J. Environ. Res. Public Health 2015, 12 1057

Figure 1. Landing areas of tropical cyclones in Zhejiang Province, China (2005–2011).

2.2. Disease Data

Report forms of notified cases of infectious diarrhea in the study areas in Zhejiang Province from
2005 to 2011 were obtained from the National Notifiable Disease Surveillance System (NDSS). The
NDSS defines infectious diarrhea as a group of human diseases mainly caused by microbes (including
bacteria, parasites, and viruses) that have diarrhea as the typical symptom. Diarrheal diseases include
cholera, typhoid, paratyphoid, dysentery (bacillary dysentery and amebic dysentery) and other infectious
diarrhea. The category of other infectious diarrhea includes all kinds of infectious diarrhea except
cholera, dysentery, typhoid and paratyphoid; examples are salmonella enteritis and rotavirus enteritis.
Among these, vibrio para-haemolyticus and salmonella accounted for 65.26% and 20.70% of pathogens
in reported bacterial diarrhea. In 2008, the percentage of rotavirus and adenovirus in all reported viral
diarrhea was 92.75% and 4.34%, respectively [19]. There were no or few cases of cholera, amebic
dysentery, typhoid, and paratyphoid during the study period, thus the analyses focused on bacillary
dysentery and other infectious diarrhea. For each case, information on age, gender, date of onset,
classification of disease, and location of disease occurrence were obtained from the NDSS records. Cases
of bacillary dysentery were diagnosed by physicians, based on the history of exposure, clinical
manifestation, and laboratory testing. Symptoms often include abdominal pain, diarrhea, tenesmus, etc.
Increase in white blood cell counts (WBC ≥ 15/HPF 400 times) and isolation of Shigella from patients’
feces help make a definite diagnosis [20]. All other infectious diarrhea cases were diagnosed by
physicians based on the joint evidence from the history of exposure, clinical symptoms, and laboratory
test results [21]. The National Communicable Disease Control Act requires physicians in hospitals to
report cases of infectious diarrhea to the local center for disease control and prevention within 24 h.
Int. J. Environ. Res. Public Health 2015, 12 1058

2.3. Meteorological Data

Our study included all tropical cyclones that landed on Zhejiang Province from 2005 to 2011.
For analytic stability, severe typhoons and super typhoon were combined into one typhoon category.
We didn’t include tropical depressions, severe tropical storms, and typhoons due to a lack of tropical
cyclone events. Daily meteorological data from 2005 to 2011 of Zhejiang Province were obtained from
the China Meteorological Data Sharing Service System (http://cdc.cma.gov.cn/). The meteorological
variables included daily average temperature (AT), daily minimum temperature (MiT), daily maximum
temperature (MaT), daily average relative humidity (ARH), daily minimum relative humidity (MiRH),
daily average air pressure (AAP), daily minimum air pressure (MiAP), daily maximum air pressure
(MaAP), daily average wind velocity (AWV), daily maximum wind velocity (MaWV), daily extreme
wind velocity (EWV), daily precipitation (DP), daily average vapor pressure (AVP), and daily sunshine
duration (SD). We used meteorological data from the meteorological station in the landing city or the
nearest station if there was no station in the city of landfall. Based on the classification of precipitation
by the China Meteorological Administration and data during the studied tropical cyclones, daily
precipitation was categorized as grade 0 (less than 10 mm), grade 1 (10–24.9 mm), grade 2 (25–49.9
mm), grade 3 (50–99.9 mm) and grade 4 (more than 100 mm) [22].

2.4. Epidemiological Method and Statistical Analysis

In this study, a unidirectional 1:1 case-crossover design combined with conditional logistic regression
models were used to analyze the exposure odds for the case period compared with the control period.
Case-crossover design is an effective method to measure the influence of transient exposure to acute
diseases [23]. As in a matched case-control study, this design compares each case’s exposure before a
case-defining event with that case’s exposure during other period. Because this design is similar to a
crossover study, in which each case serves as their own control, characteristics that did not change
between case and control periods, such as age, sex, geographic region and so on could not confound the
association between tropical cyclones and infectious diarrhea [24]. The case period in this study includes
the exposure period to the typhoon and the following maximum incubation period (7 days for bacillary
dysentery and 14 days for other infectious diarrheal disease). Control periods were one week for bacillary
dysentery and two weeks for other infectious diarrhea before the first onset of case reports. If the
estimated date of control day overlapped with a case period, another period one or two prior weeks would
be chosen until all control days were not in the case period. Thus, each case day was equally matched
with one control day. All of the cases occurring on a given day shared the same exposures in the case
and control periods.
Principal component analysis (PCA) was used to reduce the dimensionality of interrelated variables,
while retaining the maximum variability in the data [25]. In order to eliminate multicollinearity between
meteorological factors, variables except tropical cyclone, DP, MaWV, and EWV were processed using
PCA [26]. Principal components (PCs) were calculated and used to represent all other meteorological
factors; no multicollinearity between PCs, DP, MaWV and EWV was observed. Based on daily disease
cases records, we estimated the odds ratio (OR) and 95% confidence interval (CI) of bacillary dysentery
and other infectious diarrhea for different categories of tropical cyclones using the multivariate logistic
Int. J. Environ. Res. Public Health 2015, 12 1059

regression model. In this model, DP, MaWV, EWV and PCs were adjusted. When OR and 95%CI due
to exposure to precipitation were calculated, we used grade 0 (0–9.9 mm) as the reference group and
adjusted MaWV, EWV, and PCs in the same model. In addition, we calculated the impacts of different
precipitation levels on bacillary dysentery and other infectious diarrhea in the two strata: tropical storms
and typhoons. The equation of the model is:
 P 
ln  = β 0 + β1TC + β 2 DP + β 3 EWV + β 4 MaWV + β 5 PC1 + β 6 PC 2 + ... + β m PC n (1)
1− P 

where P is the probability of suffering disease, β0 is the intercept, β1, β2,... βm are partial regression
coefficients, TC is the category of tropical cyclone, PC1, PC2,... PCn are principal components.
Taking into account the incubation period of infectious diarrhea and disease management, we
considered lagged effects of lag 0–7 days (e.g., lag 7 means the lagged effect of exposure on the disease
at the seventh day after the case period) [27]. All statistical analyses were conducted using SPSS 21.0.

3. Results

3.1. Basic Information on Tropical Cyclones, Daily Precipitation, and Cases of Infectious Diarrhea
during the Study Period

From 2005 to 2011, seven tropical cyclones landed on Zhejiang province, including three tropical
storms, three severe typhoons, and one super typhoon. Details of each event are presented in Table 1.

Table 1. Basic information of tropical cyclones landing in the study areas from 2005–2011.
Name Grade (Period) Landing City Exposure Duration (d)
Matsa Severe typhoon (5–6 Aug 2005) Taizhou 2
Khanun Severe typhoon (11 Sep 2005) Taizhou 1
Saomai Super typhoon (10–11 Aug 2006) Wenzhou 2
Wipha Severe typhoon (18–19 Sep 2007) Wenzhou 2
Kalmaegi Tropical storm (19 Jul 2008) Wenzhou 1
Morakot Tropical storm (8–10 Aug 2009) Wenzhou 3
Meranti Tropical storm (11 Sep 2010) Lishui 1

Daily precipitation during the study period in the landing city is described in Figure 2. The number
of cases of bacillary dysentery and other infectious diarrhea in the landing city are also listed in Figure 2.
Description and analyses of the impacts on cholera, amebic dysentery, typhoid, and paratyphoid during
the study period were not included due to limited numbers of cases.
Int. J. Environ. Res. Public Health 2015, 12 1060

Figure 2. Daily precipitation and infectious diarrhea cases in study period of each tropical
cyclone landing on Zhejiang Province during 2005–2011.

3.2. Effects of Tropical Cyclones on Infectious Diarrhea (Figure 3)

The results indicate that typhoons and tropical storms increased the risk of bacillary dysentery and
other infectious diarrhea. The largest impacts of tropical storms and typhoons on bacillary dysentery
were on lag 2 days (OR = 2.47, 95% CI: 1.41–4.33) and lag 6 days (OR = 2.30, 95% CI: 1.81–2.93),
Int. J. Environ. Res. Public Health 2015, 12 1061

respectively. The impacts of typhoons on other infectious diarrhea was higher than the effects of tropical
storms, with OR = 3.56 (95% CI: 2.98–4.25) on lag 5 days and OR = 2.46 (95% CI: 1.69–3.56) on lag 6
days. More details are shown in Figure 3.

Figure 3. ORs and 95% CIs of tropical cyclones on the risk of bacillary dysentery and other
infectious diarrhea on different lagged days. OR: odds ratio; CI: confidence interval; A:
impact of typhoon on bacillary dysentery; B: impact of tropical storm on bacillary dysentery;
C: impact of typhoon on other infectious diarrhea; D: impact of tropical storm on other
infectious diarrhea.

3.3. Effects of Precipitation on Infectious Diarrhea

The ORs of different grades of tropical cyclone precipitation on bacillary dysentery are detailed in
Figure 4. Tropical cyclone precipitation within 10–24.9 mm (grade 1) was protective with an OR = 0.13
(95% CI: 0.03–0.53) on lag 0 day. However, the tropical cyclone precipitation was a risk factor when
daily precipitation reached 25mm and more with the largest OR = 2.17 (95% CI: 1.10–4.27) for grade 2
on lag 1 days, OR = 2.60 (95% CI: 1.43–4.74) for grade 3 on lag 0 day, and OR = 3.25 (95% CI:
1.45–7.27) for grade 4 on lag 0 day. Precipitation grades from 2 to 4 had the largest impacts on bacillary
dysentery. Precipitation on lag 5 days was not statistically significant and therefore excluded from the
model. Compared with bacillary dysentery, grade 1 and grade 2 precipitation had longer lags with other
infectious diarrhea (Figure 5). Tropical cyclone precipitation less than 50 mm was protective of other
infectious diarrhea, with OR = 0.28 (95% CI: 0.19–0.41) and OR = 0.31 (95% CI: 0.20–0.47) on lag 5
and lag 6 days, respectively. Precipitation more than 50 mm was a risk factor for other infectious
diarrhea. The largest impacts (OR = 3.05, 95%CI: 2.20–4.23 in grade 3; OR = 5.40, 95%CI: 3.47–8.38
in grade 4) were on the days when tropical cyclones landed (lag 0 day). The impact of tropical cyclone
precipitation at grade 4 was larger than that of grade 3.
Int. J. Environ. Res. Public Health 2015, 12 1062

Figure 4. ORs and 95% CIs of tropical cyclone precipitation on the risk of bacillary
dysentery on different lagged days. OR: odds ratio; CI: confidence interval; A: impact of
grade 1 (10–24.9 mm) precipitation on bacillary dysentery; B: impact of grade 2 (25–49.9 mm)
precipitation on bacillary dysentery; C: impact of grade 3 (50–99.9 mm) precipitation
on bacillary dysentery; D: impact of grade 4 (more than 100 mm) precipitation on
bacillary dysentery.

Figure 5. ORs and 95% CIs of tropical cyclone precipitation as the risk for other infectious
diarrhea on different lagged days. OR: odds ratio; CI: confidence interval; A: impact of grade
1 (10–24.9 mm) precipitation on other infectious diarrhea; B: impact of grade 2
(25–49.9 mm) precipitation on other infectious diarrhea; C: impact of grade 3 (50–99.9 mm)
precipitation on other infectious diarrhea; D: impact of grade 4 (more than 100 mm)
precipitation on other infectious diarrhea.
Int. J. Environ. Res. Public Health 2015, 12 1063

4. Discussion

This study quantified the relationships between tropical cyclones from 2005–2011 and infectious
diarrhea in Zhejiang Province, China. Our results suggest that typhoon and tropical storm could
contribute to an increased risk of bacillary dysentery and other infectious diarrhea.
Increases in diarrheal diseases following tropical cyclone have been reported in developed and
developing countries. For instance, a significant increased incidence of diarrhea after typhoon AILA was
reported in two Indian subdivisions: Haldia and Egra in 2009 [28]. A Burmese study also observed an
obvious increase in the incidence rate for acute diarrhea in the post-Nargis months of 2008 [29].
In South Korea, risk of infectious diarrhea increased more than sixteen percent during typhoon periods [7].
The U.S. Centers for Disease Control and Prevention (CDC) reported that gastrointestinal diseases were
the most commonly recorded acute disease among evacuees from Memphis and Tennessee after
hurricane Katrina in 2005 [30]. Results from these studies are consistent with our findings in that there
is a relationship between tropical cyclones and increase in diarrhea in Zhejiang.
Our study also identified that tropical storms and typhoons differentially influenced different groups
of infectious diarrhea. Both tropical storms and typhoons had lagged effects, ranging from 2 to 6 days.
For the group of other infectious diarrhea, the impact of typhoons was apparently higher than that of
tropical storms. Whereas for bacillary dysentery, risks of typhoons were slightly lower than that of
tropical storms. However, there were merely minimal differences between the ORs of these types of
cyclones, thus we cannot draw a definitive conclusion that storms and typhoons influence bacillary
dysentery to different extents. This may be due to the limited number of tropical cyclone related events
analyzed. In addition, because the group of other infectious diarrhea includes several kinds of infectious
diarrhea, the different causal mechanisms for each disease category may have influenced the result.
Because the categorization of tropical cyclones is defined by wind velocity, the impact of a particular
category of tropical cyclone can represent the influence of wind speed associated with it. Our study
suggests that stronger wind might increase the risk for the group of other infectious diarrhea. Results
from previous research were inconsistent in how wind speed could impact infectious diarrhea. A study
suggested increased wind speed could result in a lower prevalence of bacillary dysentery [31]. However,
studies in Shanghai, Wuhan and northeastern China found no significant relationships between wind
speed and infectious diarrhea [32–34].
We also identified that cyclone precipitation could be either a protective or a risk factor for the
occurrence of infectious diarrheal diseases, depending on the amount of precipitation. Twenty-five
millimeter and 50 mm could be turning points of the impacts of tropical cyclone precipitation on
bacillary dysentery and other infectious diarrhea, respectively. When the daily precipitation was higher
than 25 mm or 50 mm, i.e., the greater the tropical cyclone precipitation, the higher the risk of suffering
bacillary dysentery or other infectious diarrhea. We found that ORs of precipitation between 10–25 mm
were significantly lower than one, which indicated that tropical cyclone precipitation between 10–25
mm was probably beneficial to human health. The mechanism of this protective effect needs further
study. One possible reason is that tropical cyclones are characterized by strong wind and precipitation;
thus, tropical cyclones with relatively little precipitation and strong wind result in dry weather, which
may be adverse to human health. In addition, a very short or no lagged effect was observed for tropical
cyclone precipitation. These results suggest that more attention should be focused on prevention and
Int. J. Environ. Res. Public Health 2015, 12 1064

control of infectious diarrhea diseases when precipitation reaches 25 mm or above following tropical
cyclones. Previous studies documented that heavy precipitation was associated
with gastrointestinal illness. Positive association between extreme precipitation and gastrointestinal
illness-related hospital admission also was reported from 2004 to 2007 in Chennai, India [35]. Our
findings indicate that risks of bacillary dysentery increased significantly after exposure to heavy rain
(25.0–49.9 mm), torrential rain (50–99.9 mm), and extreme torrential rain (≥100 mm) caused by tropical
cyclones, which is similar to the Taiwanese study, which found that risks of bacillary dysentery increased
nearly twofold after exposure to torrential rain and seven times after exposure to extreme torrential
rain [27]. Also in northeast China, a positive correlation between precipitation and bacillary dysentery
was noted [36].
However, the association between precipitation and diarrhea was far from clear. In a study in Wuhan,
China, researchers obtained results confirming an inverse association between precipitation and
infectious diarrhea [32]. Another study in Ecuador found that heavy precipitation events were associated
with increased diarrheal disease incidence following dry periods and decreased diarrhea incidence
following wet periods [37]. Another two studies did not detect any significant effects of precipitation on
infectious diarrhea in cities at the northern and southern parts of China [38,39]. This observed
discrepancy may have resulted from socioeconomic factors such as individual perceptions and
behaviors, socio-economic status, and access to health services. For instance, citizens’ low awareness of
health issues and unhealthy drinking habits may make them more susceptible to infectious diarrhea.
Economic status determines the level of health service and the drinking water sanitation to some extent,
and thus, may influence the risk of suffering infectious diarrhea. In addition, different intensities of
precipitation in different studies might be another reason for varying results.
For example, the Taiwanese study investigated the impact of extreme torrential precipitation
(>350 mm/day) on bacillary dysentery [27], while the impact of a quite lower daily precipitation
(3.1 mm) was studied in Wuhan [32].
Due to limited number of tropical cyclone events in Zhejiang province during 2005–2011, the impacts
of other categories of tropical cyclones, such as tropical depression and severe tropical storm, on
infectious diarrhea with longer lags could not be assessed in our study. In addition, there might be other
factors that could influence transmission of infectious diarrhea.
Irrespective of these limitations, there are some advantages of this study. First, the case-crossover
study design, similar to a matched case–control study, is advantageous in controlling confounders.
Confounders, such as geographical characteristics, behaviors and economic status, would remain
constant across the study period. Second, we considered the day of week effect in the selection of the
control period for controlling any possible time trend. Third, we had a relatively long study period with
quality data collected from patients’ case records. In particular, we calculated the impacts of seven
different tropical cyclones on bacillary dysentery and other infectious diarrhea, producing robust results.

5. Conclusions

Our study shows that both tropical storm and typhoon could increase the risk of bacillary dysentery
and other infectious diarrhea in the study areas in China. Tropical cyclone precipitation is a risk factor
for bacillary dysentery and other infectious diarrhea when it reaches 25 mm and 50 mm or above. These
Int. J. Environ. Res. Public Health 2015, 12 1065

findings may assist in public health preparation to reduce the adverse health impacts from tropical
cyclones.

Acknowledgements

The study was supported by the National Basic Research Program of China (973 Program) (Grant
No. 2012CB955500-955502). We appreciate National Notifiable Disease Surveillance System as well
as China Meteorological Data Sharing Service System for providing data for our research.

Author Contributions

Zhengyi Deng, Huanmiao Xun and Wei Ma conceived and designed the study; Zhengyi Deng,
Huanmiao Xun, Songwang Wang and Qing Guo performed the study; Zhengyi Deng, Huanmiao Xun,
Maigeng Zhou and Baofa Jiang analyzed the data; Wei Wang, Xin Wang, Ruihua Kang and Gifty Marley
contributed reagents/materials/analysis tools; Zhengyi Deng and Huanmiao Xun wrote the paper.

Conflicts of Interest

The authors declare no conflict of interest. The founding sponsors had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the
decision to publish the results.

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