Contents lists available at ScienceDirect
Environment International
journal homepage: www.elsevier.com/locate/envint
Associations of Salmonella hospitalizations with ambient temperature,
humidity and rainfall in Hong Kong
Pin Wang
a,1
, William B. Goggins
a,
⁎
,1
, Emily Y.Y. Chan
b,1
a
School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong, China
b
Collaborating Centre for Oxford University and CUHK for Disaster and Medical Humanitarian Response, Faculty of Medicine, The Chinese University of Hong Kong, Hong
Kong, China
ARTICLE INFO
Handling Editor: Yong Guan Zhu
Keywords:
Salmonella
Temperature
Humidity
Rainfall
Weather
Meteorology
ABSTRACT
Background: Little is known about the relationship between Salmonella infection and meteorological parameters
other than air temperature. This study aimed to explore associations of Salmonella hospitalizations with tem-
perature, relative humidity (RH) and rainfall.
Methods: With negative binomial distribution assumed, time-series regression model adjusting for season and
time trend were constructed employing distributed lag non-linear models and generalized additive models.
Meteorological variables including mean temperature, RH, and daily total rainfall as well as indicator variables
including day of the week and public holiday were incorporated in the models.
Results: Higher temperature was strongly associated with more hospitalizations over the entire range of tem-
peratures observed. There was a net 6.13 (95%Confidence Interval (CI) 3.52–10.67) relative risk of hospitali-
zation at a temperature of 30.5 °C, relative to 13 °C, lag 0–16 days. Positive associations were found for RH above
60% and rainfall between 0 and 0.14 mm. Extreme high humidity (96%) and trace rainfall (0.02 mm) were
associated with 2.06 (95%CI 1.35–3.14), lag 0–17 day, and 1.30 (95%CI 1.01–1.67), lag 0–26 days, relative risks
of hospitalizations, relative to 60% and no rain, respectively.
Conclusions: High temperatures, high RH and light rainfall are positively associated with Salmonella hospitali-
zations. The very strong association with temperatures implies that hotter days will lead to increases in
Salmonella morbidity in the absence of other changes, and the public health implications of this could be ex-
acerbated by global climate change.
1. Introduction
The earth is warming up, and the world has been alerted to the
mounting threat of climate change (The Lancet, 2014). The impact of
climate change on the distribution and spread of infectious diseases is of
significant public health concern.
Non-typhoidal Salmonella infection, also known as salmonellosis, is
caused by Salmonella species other than Salmonella Typhi and
Salmonella Paratyphi, and is one of the most widespread foodborne
diseases (fecal-oral transmission can also occur) with tens of millions of
cases occurring every year all over the world (World Health
Organization, 2013). It has been estimated that 93.8 million gastro-
enteritis cases and 155,000 associated deaths occur yearly worldwide
(Majowicz et al., 2010). In a nine-year investigation between 2003 and
2011 in Hong Kong, of the 4230 bacteria-caused food poisoning
outbreaks reported to the Centre for Health Protection, 763 were as-
sociated with non-typhoidal Salmonella, and a total of 3250 persons
were affected, ranking it the second most common bacterial agent of
food poisoning outbreaks in Hong Kong during that period (Centre for
Health Protection, 2011). However, the worsening situation from 2011
to 2017 has already made it the most common bacterial causative agent
among confirmed cases of food poisoning (Centre for Health Protection,
2017).
Most prior studies of associations between Salmonella and meteor-
ological variables have focused on temperature (Lake et al., 2009;
Fleury et al., 2006; Zhang et al., 2010; Britton et al., 2010; Uejio, 2017;
Jiang et al., 2015; Akil et al., 2014). Higher temperatures have con-
sistently been found to be associated with higher incidence of Salmo-
nella infection, although association magnitudes and lengths of lagged
effects have varied (Lake et al., 2009; Fleury et al., 2006; Zhang et al.,
https://doi.org/10.1016/j.envint.2018.08.014
Received 10 May 2018; Received in revised form 4 July 2018; Accepted 2 August 2018
⁎
Corresponding author at: 5/F, School of Public Health and Primary Care, Prince of Wales Hospital, Shatin, N.T., Hong Kong, China.
1
Current address: School of Public Health and Primary Care, Prince of Wales Hospital, Shatin, N.T., Hong Kong, China.
E-mail address: wgoggins@cuhk.edu.hk (W.B. Goggins).
Environment International 120 (2018) 223–230
Available online 10 August 2018
0160-4120/ © 2018 Elsevier Ltd. All rights reserved.
T