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Research
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Temporal Trends and Climatic Factors
Associated with Bacterial
Enteric Diseases in Vietnam,
1991–2001 Louise A. Kelly-Hope,1 Wladimir J.
Alonso,1 Vu Dinh Thiem,2 Do Gia Canh,2 Dang Duc Anh,2 Hyejon Lee,3 and Mark A. Miller1 1Division
of International Epidemiology and Population Studies, Fogarty
International Center, National Institutes of Health, Department
of Health and Human Services, Bethesda, Maryland, USA; 2National
Institute of Hygiene and Epidemiology, Hanoi, Vietnam; 3International
Vaccine Institute, SNU Research Park, Seoul, Korea Abstract Objective: In Vietnam, shigellosis/dysentery, typhoid fever, and cholera are important enteric diseases. To better understand their epidemiology, we determined temporal trends, seasonal patterns, and climatic factors associated with high risk periods in eight regions across Vietnam. Methods: We quantified monthly cases and incidence rates (IR) for each region from national surveillance data (1991–2001) . High- and low-disease periods were defined from the highest and lowest IRs (1 SD above and below the mean) and from outbreaks from positive outliers (4 SDs higher in 1 month or 2 SDs higher in ≥ 2 consecutive months) . We used general linear models to compare precipitation, temperature, and humidity between high- and low-risk periods. Results: Shigellosis/dysentery was widespread and increased 2.5 times during the study period, with the highest average IRs found between June and August (2.1/100,000–26.2/100,000) . Typhoid fever was endemic in the Mekong River DeltaDelta ; and emerged in the Northwest in the mid-1990s, with peaks between April and August (0.38–8.6) . Cholera was mostly epidemic along the central coast between May and November (0.07–2.7) , and then decreased dramatically nationwide from 1997 onward. Significant climate differences were found only between high- and low-disease periods. We were able to define 4 shigellosis/dysentery, 14 typhoid fever, and 8 cholera outbreaks, with minimal geotemporal overlap and no significant climatic associations. Conclusions: In Vietnam, bacterial enteric diseases have distinct temporal trends and seasonal patterns. Climate plays a role in defining high- and low-disease periods, but it does not appear to be an important factor influencing outbreaks. Key words: cholera, climate, dysentery, enteric disease, epidemiology, outbreaks, seasonality, shigellosis, typhoid fever, Vietnam. Environ Health Perspect 116: 7–12 (2008) . doi:10.1289/ehp.9658 available via http://dx.doi.org/ [Online 16 October 2007] Address correspondence to L.A. Kelly-Hope, Division of International Epidemiology and Population Studies, Fogarty International Center, 16 Center Dr., National Institutes of Health, Bethesda, MD 20892 USA. Telephone: (301) 496-3110. Fax: (301) 496-8496. E-mail: kellyhopel@mail.nih.gov We thank the International Vaccine Institute (Korea) for providing disease data. We also thank C. Schuck Paim (University of São Paulo, Brazil) for assistance with statistical methods. This study was funded by the Fogarty International Center and the Bill and Melinda Gates Foundation. The authors declare they have no competing financial interests. Received 28 August 2006 ; accepted 15 October 2007. |
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In Vietnam, shigellosis (bacillary
dysentery), typhoid fever, and cholera are enteric diseases of
significant public health concern (DeRoeck et al. 2005). They
are primarily caused by the bacterial pathogens Shigella spp., Salmonella typhi,
and Vibrio cholerae, respectively, and transmission occurs through
fecal contamination of food or water or by person-to-person
contact (Bhan et al. 2005; Crump et al. 2004; Kindhauser 2003;
Kotloff et al. 1999; Lanata et al. 2002). Infection rates and
outbreaks are highest where the standards of living, water
supply, and human behaviors related to personal hygiene and
food preparation are poor. The distribution and ecologic
determinants of shigellosis/dysentery, typhoid fever, and
cholera have recently been described from surveillance data in
Vietnam (Kelly-Hope et al. 2007). The data show that each
disease varies in magnitude and has a distinct spatial pattern,
which appears to be driven by a combination of human and
environmental factors, including poverty, water sources, and
climate.
Many infectious diseases, including
shigellosis/dysentery, typhoid fever, and cholera, are
influenced by climate. Specifically, climate plays an important
role in the transmission process and can influence spatial
and
seasonal distributions, as well as interannual variability and
long-term trends [Burke et al. 2001; Kovats et al. 2003; World
Health Organization (WHO) 2004]. Although climate is one aspect
of the complex epidemiology of these enteric diseases, it can
help to define high-risk periods. Few studies conducted in
Asia
have described the temporal patterns and outbreaks of
shigellosis/dysentery and typhoid fever, and no study has
specifically examined the impact of climate on these diseases.
In general, cholera has been studied more widely, and formal
and informal listings of outbreaks and putative risk factors
are available from various sources (Griffith et al. 2006; Kelly-Hope
et al. 2007; WHO 2003, 2005, 2006). Studies have shown
associations of V. cholerae with climate, including rainfall,
flooding, water temperature and depth, sea surface temperatures,
and the
El Niño Southern Oscillation (ENSO) (Huq et al. 2005;
Koelle et al. 2005b; Lipp et al. 2002; Lobitz et al. 2000;
Pascual et al. 2000; Rodo et al. 2002).
In Vietnam, monthly shigellosis/dysentery,
typhoid fever, and cholera surveillance data have been collated
for 1991–2001. We used these national data to determine
the long-term temporal trends and seasonal patterns of shigellosis/dysentery,
typhoid fever, and cholera in eight geographic regions of
Vietnam, and to examine climatic factors associated with
high-risk periods.
Study location. Vietnam is a narrow, densely populated country in
southeastern Asia bordering China, Laos, and Cambodia (General
Statistics Office of Vietnam 2005). It has approximately 85 million
people living in an area of 330,000 km2,
with > 3,000
km of coastline. In the south the climate is tropical, whereas
in the north, the two main seasons are a warm, wet summer and
a
cool, humid winter. The terrain is diverse with low, flat
deltaDelta;s in the south and north; highlands in the center; and
hilly mountains in the northwestern region. Vietnam experiences
occasional typhoons with extensive flooding, especially in the
southern Mekong River DeltaDelta;. Vietnam currently is divided into
64 provinces and eight agro-ecologic regions (Figure 1):
Northeast, Northwest, Red River DeltaDelta;, North Central Coast,
South Central Coast, Central Highlands, Southeast, and Mekong
River DeltaDelta;. We used the eight geographic regions as the basis
of our temporal and climatic analyses.
Disease data. We
obtained data on shigellosis/dysentery, typhoid fever, and
cholera for each province in Vietnam from 1991 to 2001 from the
Epidemiology Department, National Institute of Hygiene and
Epidemiology (Hanoi), and from a central database collated by
the International Vaccine Institute (Korea). Data were
primarily (> 90%) based on treated episodes, which are
routinely collected by district health centers as part of the
surveillance system of the Vietnam Ministry of Health; these
episodes were supplemented with cases reported in the published
scientific literature and unpublished national health reports.
Thus, the database comprised a combination of cases that were
diagnosed clinically and confirmed by serology and stool
culture. Provincial data were pooled to provide estimates for
each of the eight study regions.
Temporal trends and seasonal patterns. To
determine long-term temporal trends and seasonal patterns of shigellosis/dysentery,
typhoid fever, and
cholera, we quantified the monthly number of cases and average
incidence rates (IRs) per 100,000 population for each region.
Population data for 1995–2001 were obtained from the
General Statistics Office of Vietnam (2005), and population
estimates for 1991–1994 were extrapolated from the fitted
cubic spline of the known years (Eubank 1999) in order to
obtain regional population estimates and crude IRs for each
study year.
Figure 1. Vietnam
and its eight regions: Northeast [NE; 8,524,800 (average
population for 1996)], Northwest (NW; 2,112,900), Red River
DeltaDelta; (RRD; 16,331,800), North Central Coast (NCC; 9,696,100),
South Central Coast (SCC; 6,287,300), Southeast (SE;
10,947,300), Central Highlands (CH; 3,563,000), and Mekong
River DeltaDelta; (MRD; 15,693,500).
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Figure 2. The
monthly number of shigellosis/dysentery, typhoid fever, and
cholera cases reported in Vietnam during 1991–2001.
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Figure 3. Monthly incidence rates per 100,000 population
and outbreaks of shigellosis/dysentery, typhoid fever, and cholera
in eight
regions of Vietnam. (A) Incidence rates. (B) Outbreaks. Dotted
vertical lines define years, and individual bands indicate values
for months; geographic
regions are sorted by latitude.Outbreaks are displayed as SD
above the modeled Fourier function.
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Figure 4. Average
monthly shigellosis/dysentery, typhoid fever, and cholera
incidence rates per 100,000 population in eight regions of
Vietnam. Note the different scale for shigellosis in the
Central Highlands.
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Table 1.
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Table 2.
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To identify distinct
seasonal variations, we detrended (with a fourth-degree polynomial)
and
log-transformed monthly IRs in each region for each disease,
and defined "high" and "low" disease
periods based on the months with the highest and lowest rates
(months with values at least 1 SD above and below the mean,
respectively). Outbreak periods were detected similarly, but
we defined them empirically as the positive outliers that were
4 SDs
higher in 1 month or 2 SDs higher in ≥ 2 consecutive
months from the modeled Fourier function of the time series
(Bloomfield 2000; Pollock 1999), which was performed on each
time series, accounting for disease seasonality.
Climate data and analysis. Monthly
climatic data were obtained from worldwide climate maps generated
by the interpolation of data
from ground-based meteorologic stations with a monthly temporal
resolution and 0.5° (latitude) by 0.5° (longitude)
spatial resolution (Mitchell and Jones 2005). The climatic
variables used were precipitation; average daily minimum,
maximum, and mean temperatures; vapor pressure; and number of
wet days. Monthly climate data during 1991–2001 were
extracted from the pixels containing the centroid of each
province and clustered according to the eight regional
divisions of Vietnam. To calculate climatic averages for the
eight regions, we used the climatic values for each province
weighted by its respective population (to account for the
proportional relevance of the diseases of each province within
the regions, so the climatology of places where few people live
would, in fact, account proportionally less in the regional
analyses than places with a large demographic concentration).
To explore climatic factors associated
with high-risk times, we examined differences between high- and
low-disease periods and outbreak and non-outbreak periods.
First, we used a general linear model to test significant
differences between high- and low-disease periods with time
lags from 0 to 2 months. Because multiple tests were conducted
(four climatic variables tested at three time lags of 0, 1,
and
2 months, thus yielding 12 tests for each disease at each
region), significance levels were adjusted with the Bonferroni
correction (Sokol and Rohlf 1995); we considered p-values < 0.05/12
significant.
Second, we compared climate data
corresponding to the outbreak period in each region with
climate data for the same months in previous years when
outbreaks did not occur (i.e., the non-outbreak period), with
time lags from 0 to 2 months. We used general linear models
with the climate variables as dependent variables, outbreak
presence as a fixed factor, and region as a random factor.
All analyses were performed using
Microsoft Excel (Microsoft Corporation, Redmond, WA, USA),
ArcGIS 9.1 (ESRI, Redlands, CA, USA), and MATLAB software (The
MathWorks, Inc., Natick, MA, USA).
Temporal trends and seasonal patterns. The
monthly numbers of shigellosis/dysentery, typhoid fever, and cholera
cases reported in Vietnam during
1991–2001 are shown in Figure 2. Shigellosis/dysentery
was the most prevalent disease and increased approximately 2.5 times
during the study period, with 16,976 cases (annual IR of 25.3
per 100,000) reported in 1991 compared with 46,292 cases (IR,
58.8) in 2001. The annual number of typhoid fever cases was
similar at the beginning (7,592 cases; IR, 11.3) and end (9,614
cases; IR, 12.2) of the study period; however, there was a 3-fold
increase during 1994 to 1997, with an average of 24,553 cases
(IR, 33.8) reported annually. Overall, there were fewer cholera
cases, which appeared episodically during 1991–1996, with
four main peaks in May 1992 (1,851 cases; IR, 2.7),
August–September 1993 (943–1,054 cases; IR,
1.4–1.5), May 1994 (1,127 cases; IR, 1.6), and
June–July 1995 (1,097–1,492 cases; IR,
1.5–2.1). From January 1997 onward, the number of cholera
cases reported nationwide decreased significantly, with only
two minor peaks reported in January–February 1999 (188
cases; IR, 0.25) and September–October 2000 (166 cases;
IR, 0.21).
Figure 3A shows the monthly
IRs of shigellosis/dysentery, typhoid fever, and cholera for
each
region during 1991–2001. This figure highlights the
widespread incidence of shigellosis/dysentery and its increase
in the Central Highlands and the South Central Coast, the
endemicity of typhoid fever in the Mekong River DeltaDelta; and its
emergence in the Northwest region, and the significant decline
of cholera nationwide.
Overall, we found distinct
seasonal variations in each region, as shown by the average monthly
IRs
in Figure 4. Shigellosis/dysentery rates peaked in the northern
regions of the country (Northeast, Northwest, Red River DeltaDelta;,
North Central Coast) between June and August (IR range,
2.1–7.8), and in the southern regions (South Central
Coast, Central Highlands, Southeast, Mekong River DeltaDelta;) between
May and July (IR range, 8.2–26.2); the highest monthly IR
occurred in the Central Highlands in June (IR, 26.2). Typhoid
fever rates peaked in the northern regions between May and
September (IR range, 0.38–5.2) and in the southern
regions between April and July (IR range, 0.43–8.6); the
highest monthly IRs occurred in the Northwest in July (IR, 5.2)
and the Mekong River DeltaDelta; in April (IR, 8.6). Cholera rates
peaked in the northern regions between May and November (IR
range, 0.07–2.7) and in the southern regions between May
and July (IR range, 0.51–2.6). No cholera cases were
reported in the Northwest, whereas the highest monthly IRs
occurred in the North Central Coast in May (IR, 2.7) and in the
South Central Coast in July (IR, 2.6).
In total, 26 enteric outbreaks
were identified—4 shigellosis/dysentery, 14 typhoid fever, and
8 cholera—during 1991–2001 (Figure 3B). Apart from
typhoid and cholera in the Mekong River DeltaDelta; in June 1995, no
disease outbreak coincided temporally with any other disease
outbreak in any region. However, typhoid outbreaks in the
Northeast, Red River DeltaDelta;, North Central Coast, South Central
Coast, and Southeast regions in 1996 overlapped temporally,
with outbreak months ranging from March to July. Overall,
outbreaks occurred most commonly in the months of May, June,
and July, followed by April, August, and September. No
outbreaks occurred in December, and only one to three outbreaks
occurred in October–March.
Climate associations. The climatic measures during high- and low-disease
periods at 0-month lag are shown in Table 1. The data highlight
that, in most regions, conditions were warmer, wetter, and more
humid in high-disease periods than in low-disease periods.
Overall, we found significant differences in precipitation and
the number of wet days between the high and low periods. For
shigellosis/dysentery and cholera, precipitation was
significantly different (F1,11 =
14.7, p
= 0.002, r2adj = 47.7%; and F1,10 =
15.7, p
= 0.002, r2adj = 53.1%, respectively), as was the number of
wet days (F1,11 = 18, p = 0.001, r2adj =
53.2%; and F1,10 = 14.4, p = 0.003, r2adj =
50.7%, respectively) at the 0-month time lag. Similarly, for
typhoid fever, precipitation was significantly different at the
0-month time lag (F1,11 =
40.1, p < 0.001, r2adj = 72.3%), as was the number of wet days at the
0- and 1-month time lags (F1,11 =
24.8, p < 0.001, r2adj = 61.4%; and F1,11 =
28.1, p < 0.001, r2adj = 64.3%, respectively). No significant climatic
differences were found at the 2-month time lag for any of the
diseases, even when tests were not Bonferroni adjusted.
In our climate analyses
we found no significant differences in the climatic conditions
between the
months during or preceding each outbreak period compared with
non-outbreak periods in previous years. The data in Table 2
highlight the range of climate conditions under which enteric
outbreaks occurred. Overall, precipitation ranged from 37 to
311 mm; for the majority (> 80%) of the outbreaks, > 100 mm
was recorded. All mean temperatures were > 21.9°C
(majority > 25°C); the number of wet days ranged from
4.9 to 20.3 (majority > 11); and most outbreaks occurred in
months with an average vapor pressure > 26 hPa.
This is the first time
that temporal patterns of endemic and epidemic shigellosis/dysentery,
typhoid
fever, and cholera have been defined concurrently on such a
large scale. In the present study we used surveillance data to
highlight the different magnitudes and epidemiologic patterns
of each disease in Vietnam during 1991–2001, and we offer
some insight into the role of climate. Notwithstanding the
inherent limitations associated with surveillance data, this
large data set is probably the most comprehensive available
in
any developing country, and provides the basis for more
specific and well-defined hypotheses in relation to climate and
disease.
Overall, we found that the incidence of
shigellosis/dysentery was widespread and increased
significantly during the study period, especially in the
Central Highlands and South Central Coast. The reported
dysentery could have been caused by other pathogens such as Campylobacter or Escherichia coli
(Isenbarger et al. 2001, 2002; Ngan et al. 1992); however, Shigella spp. are
the most common cause of dysentery, with four distinct species
able to exist in a range of ecologic niches (Kotloff et al.
1999). Also, new variants have potentially emerged in Vietnam
(Isenbarger et al. 2001). In addition, the increase in
shigellosis/dysentery may be related to widespread antibiotic
resistance (Anh et al. 2001; Isenbarger et al. 2001, 2002;
Nguyen et al. 2005; Vinh et al. 2000) and the fact that no
vaccines or alternative treatments are available. Thus,
shigellosis is potentially one of the most important enteric
pathogens in Vietnam.
We found typhoid
fever concentrated in three regions of the country, each with
differing temporal
patterns. In the Mekong River DeltaDelta; the disease was endemic and
rates were among the highest in the country, which supports
previous studies (Lin et al. 2000; Luxemburger et al. 2001;
Nguyen et al. 1993). In the central region of Vietnam,
especially the North Central Coast, South Central Coast, and
Southeast, a substantial increase occurred between 1995 and
1998, which may account for the high number of cases reported
nationwide and the series of outbreaks we identified during
this period. In the Northwestern region, typhoid fever first
appeared in 1996–1997 and remained endemic thereafter
(Tran et al. 2005). The reason for its emergence and
persistence in this remote rural region is unclear. It is
possible that ENSO, which resulted in extremely hot conditions
across the country in 1997–1998, somehow enhanced the
transmission of Salmonella typhi in this region or endemicity is related to new
border openings.
In contrast, cholera decreased
dramatically from 1997 onward, and many regions reported no
further cases after years of epidemic and endemic activity
(Dalsgaard et al. 1999). This sudden widespread reduction in
cholera may be attributable to several factors, including
interannual variability, immunity, economic development, and
improvements and interventions in hygiene and sanitation.
The
initial decline probably reflects the episodic nature of
cholera. Other studies have also shown that interannual
variability is common and is affected by climate and events
such as the ENSO, as well as by levels of immunity within
populations (Koelle et al. 2005a, 2005b; Lipp et al. 2002;
Lobitz et al. 2000; Pascual et al. 2000; Rodo et al. 2002).
However, the fact
that cholera numbers remained low from 1997 to 2001 may be related
to the
introduction of a new locally produced vaccine in 1997 (Trach
et al. 1997; Vu et al. 2003) instead of ENSO influence, given
that in 1996 there were already virtually no reported cases of
cholera (with the exception of the outbreak in the Northeast
region). Public health campaigns and > 5 million doses of
the cholera vaccine targeting both V.
cholerae 01 and 0139 pathogens have
since been distributed primarily to epidemic-prone regions via
the national vaccine program, thus influencing the epidemiology
of cholera (Thiem et al. 2006). It is impossible to know which
factor is most responsible for this decline and almost
disappearance of cholera in Vietnam, but this success is
undoubtedly due to a combination of public health
interventions, including water and sanitation improvements,
vaccine delivery to high-risk populations, and changes in
public awareness, as well as cyclical population immunity.
Identifying peak periods of disease helps
to focus local interventions. We were able to better define the
seasonality of each disease and found that, on average, the
highest IRs of shigellosis/dysentery occurred between May and
August; of typhoid fever between April and September; and of
cholera between May and November. For all diseases, the highest
monthly IRs occurred earlier (April/May to July) in the
southern regions than in the northern regions (May/June to
November) of the country, which may be indicative of the
different climatic patterns of the north and south. In
particular, the tropical conditions of the south may help local
health authorities implement timely interventions because peak
periods of disease coincided with the onset of the wet season.
Distinct climatic differences were evident
between the high- and low-disease periods, with hotter, wetter,
and more humid conditions associated with an increased
incidence of disease. Climatic associations, however, were not
strong, and we found significant differences mainly when we
compared the high- and low-disease periods (0-month lags) and
not the months leading up to (2-month lag) each specific
period. This may be because high and low periods occurred
during more extreme climate conditions (i.e., wet and dry
seasons) and because climate conditions outside these
parameters are more variable and not specific enough to
dramatically increase or decrease disease transmission.
The overall weak association with climate
could also be related to the quality of surveillance data,
which are inevitably flawed because of underreporting,
misdiagnosis, and misclassification. In Vietnam, adequate
diagnostic facilities are not universally available, and
detection can be difficult and may be biased to those
individuals with severe symptoms or better access to health
centers (Dalsgaard et al. 1999; Hong et al. 2003). Further,
other factors such as poor socioeconomic conditions play a role
(Fewtrell et al. 2005: Kelly-Hope et al. 2007) and are also
likely to be as important, if not more important, than climate.
This theory is supported by our analysis of outbreaks, which
found no significant climatic differences in the same months
between years with outbreaks and years without outbreaks.
Using a robust method, we were able to
define statistically 4 outbreaks of shigellosis/dysentery, 14
of typhoid fever, and 8 of cholera. We found little or no
overlap between outbreaks of the three diseases within each
region, which suggests that a combination of different factors
triggered each event in each region, and that competition may
have occurred between these enteric microbes for available
hosts (Rabbani and Greenough 1999). Comparisons of climatic
factors between outbreak and non-outbreak periods indicated
that no specific or unusual climate conditions preceded any
outbreak. However, most outbreaks occurred within certain
periods and climatic parameters, with May, June, and July being
the most common outbreak months, followed by April, August,
and
September.
We acknowledge that climate is only one
aspect of a multitude of complex interactions that cause
disease. Although the role of climate is limited, we believe
that climate factors help define high- and low-risk periods
and
potentially provide some clues into the ecology and
epidemiology of these enteric diseases. It is reasonable to
expect that the different pathogens, as well as humans, respond
to seasonal changes in the environment and that some conditions
are more favorable than others for disease transmission.
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