Food and Nutrition Sciences, 2013, 4, 233-239
http://dx.doi.org/10.4236/fns.2013.43031 Published Online March 2013 (http://www.scirp.org/journal/fns)
Etiology of Diarrhea among Severely Malnourished
Infants and Young Children: Observation of Urban-Rural
Differences over One Decade in Bangladesh*
Sumon Kumar Das, Mohammod Jobayer Chisti, Sayeeda Huq, Mohammad Abdul Malek,
Mohammed Abdus Salam, Tahmeed Ahmed, Abu Syed Golam Faruque#
International Centre for Diarrheal Disease Research, Dhaka, Bangladesh.
Email: sumon@icddrb.org, chisti@icddrb.org, sayeeda@icddrb.org, mamalek@icddrb.org, masalam@icddrb.org,
tahmeed@icddrb.org, #gfaruque@icddrb.org
Received December 12th, 2012; revised January 12th, 2013; accepted January 20th, 2013
ABSTRACT
There is inadequate information on the etiology of diarrhea in severely malnourished (SM) young children. Thus, the
study aimed to determine the etiology of diarrhea among severely malnourished (z score < 3.00 SD) children in rural
and urban Bangladesh. From the database (2000-2011) of Diarrheal Disease Surveillance Systems (DDSS) at rural
Matlab and urban Dhaka hospitals of icddr,b, 2234 and 3109 under-5 children were found severely malnourished (un-
derweight, stunted or wasted) respectively. Two comparison groups [moderately malnourished (MM) and well-nour-
ished (WN)] were randomly selected in a ratio of 1:1:1. Children with all categories of SM were more likely to be in-
fected with Vibrio cholerae (rural—11%; urban—15%), Shigella (16%; 9%), Salmonella (1%; 2%) and Campylobacter
(3%; 4%); and less likely to have rotavirus (25%; 20%) compared to only one SM category. Isolation rate of Vibrio
cholerae was significantly higher among SM both in rural and urban children (7%; 13%) than those of MM (5%; 10%)
and WN (2%; 8%) and lower for rotavirus (30%; 31%), (34%; 43%), (35%; 47%) respectively (p < 0.01). However, for
Shigella it was only higher among rural SM children (11%) [MM (9%), and WN (8%) (p < 0.01)]. The isolation rate of
Salmonella in SM (2%) was similar to that in MM (2%; p = 0.72) but significantly higher than that in WN (1%; p <
0.01) among urban children. Isolation rates of bacterial enteric pathogens were higher but rotavirus was lower in SM
children in both rural and urban area with geographical heterogeneity.
Keywords: Diarrhea; Under-5 Children; Rural; Severe Malnutrition; Urban
1. Introduction
Despite reductions in global deaths due to diarrhea in
under five children to around 400,000 each year, globally
(range, 200,000 to 500,000) during 2000-2010, the mor-
tality rate is still high [1] and diarrhea remains the second
leading cause of childhood deaths [2]. Malnutrition is
associated with both macro-and micronutrient deficien-
cies [3], and directly or indirectly related to 35% of all
deaths among under-five children [4]. Severe malnutri-
tion is often associated with life-threatening consequences
such as hypoglycaemia, hypothermia, hypernatremia, se-
vere chest infection, sepsis, and severe electrolyte dis-
turbances [5].
Childhood malnutrition remains an important public
health problem in Asian subcontinent; although most of
the countries in this region have experienced rapid eco-
nomic development in the recent years [3]. Each of the
different types of nutritional deficits such as underweight,
stunting and wasting is associated with increased deaths
from diarrhea, respiratory infections and other infectious
diseases such as measles [6]. A 4-year prospective study
among severely acute malnourished children aged 6
months to 12 years, hospitalized with diarrhea experi-
enced higher deaths compared to the children who did
not have diarrhea during their hospital stay [7]. A cohort
study of 430 Zambian children aged 6 - 59 months with
severe acute malnutrition noted 2.5 times higher deaths
in those with diarrhea on admission compared to those
who did not have diarrhea [8].
*There is no potent conflict of interest to declare. All authors confirm
that there is no professional affiliation, financial agreement or other
involvement with any company whose product figures prominently in
the submitted manuscript.
#Corresponding author.
According to Bangladesh Demographic and Health
Survey 2011, the prevalence of childhood stunting, un-
derweight and wasting were 43%, 41% and 17% respec-
tively [9]. Most of the earlier studies have identified as-
Copyright © 2013 SciRes. FNS
Etiology of Diarrhea among Severely Malnourished Infants and Young Children:
Observation of Urban-Rural Differences over One Decade in Bangladesh
234
sociation between malnutrition and diarrhea and exam-
ined association of etiologic agents of diarrhea with mal-
nutrition [10-12]. However, most of the analyses did not
consider geographical diversity. In our analysis, we ex-
amined the distribution of the common etiology of diar-
rhea among severely malnourished under-five children in
two distinct geographical locations.
2. Materials and Methods
2.1. Study Site
The study was conducted among the under-five children
visiting the urban Dhaka Hospital and rural Matlab Hos-
pital of the International Centre for Diarrheal Disease
Research, Bangladesh (icddr,b).
2.1.1. Dh aka Hospital
Established in 1963, the Dhaka Hospital, located in urban
Dhaka, currently provides cost free care and treatment to
around 140,000 diarrheal patients each year. The hospital
maintains a Diarrheal Disease Surveillance System (DDSS)
since 1979, and systematically enrolls (2% since 1996)
patients attending the facility, irrespective of age and sex.
The DDSS provides valuable information to hospital
clinicians in their decision-making processes and enables
to detect the emergence of new pathogens and in early
identification of outbreaks and their locations, thereby
alerts the host government to take appropriate preventive
and control measures. Extensive microbiological assess-
ments of fecal samples (culture, ELISA, and microscopy)
are performed to identify diarrheal pathogens.
2.1.2. M atlab Hospi tal
icddr,b maintains a treatment facility in rural Matlab
(Matlab Hospital), about 55 kilometres from Dhaka,
since 1963. It provides free treatment to 12,000 - 15,000
diarrhea patients annually reporting from Health and
Demographic Surveillance System area and other ad-
joining sub-districts. The Matlab DDSS has been initi-
ated in 2000, which enrolls all patients coming from the
areas of active Health and Demographic Surveillance
System (HDSS) of icddr,b.
2.2. Definition
Diarrhea was defined as passage of three or more abnor-
mally loose or watery stool within last 24 hours. Severe
malnutrition was defined (using z-scores) as: severe stunt-
ing (SS; height-for-age z-score < 3.00); severe under-
weight (SU; weight-for-age z-score < 3.00), and severe
wasting (SW; weight-for-height z-score < 3.00), using
the World Health Organization reference value [12].
Moderate malnutrition was defined as follows: moderate
stunting (height-for-age z-score 3.00 to < 2.00); mod-
erate underweight (weight-for-age z-score 3.00 to <
2.00); and moderate wasting (weight-for-height z-score
3.00 to < 2.00). We considered children as well-nour-
ished if their z-scores for weight-for-age, height-for-age
and weight-for-height z-score were form 2.00 to +1.00.
2.3. Sample Frame
From 2000 to 2011, at the rural Matlab Hospital 10,794
under-five children were enrolled in DDSS; and 27,276
under-five children at the urban Dhaka Hospital. Out of
all under-5 children, 2234 children in Matlab and 3109
children in Dhaka were severely malnourished defined
by any of the above mentioned categories: SU (364 and
518 respectively); SS (449 and 502 respectively); SW
(253 and 242 respectively); SU with SS (530 and 929
respectively); SU with SW (456 and 563 respectively);
and SU with SS with SW (182 and 355 respectively); but
none of them had both SS and SW. For each severely
malnourished child, we randomly selected one child with
moderate malnutrition and one well-nourished child for
comparison from both rural and urban hospitals.
2.4. Data Analysis
Data analyses were done using Statistical Package for
Social Sciences (SPSS) Windows (Version 15.2; Chicago,
IL) and Epi Info (Version 6.0, USD, Stone Mountain,
GA). Descriptive analysis was employed and Chi-square
test was performed for comparing proportions and a
probability of <0.05 was considered as statistically sig-
nificant. Strength of association was determined by esti-
mating odds ratio (OR) and its 95% confidence interval
(CI).
2.5. Ethical Consideration
The DDSS of icddr,b is a regular disease monitoring
system of the hospitals, which had approval of the Re-
search Review Committee (RRC) and Ethical Review
Committee (ERC) of icddr,b.
3. Results
Children under 5 years, who were severely underweight,
wasted and stunted, were more likely to be infected with
Vibrio cholerae, Shigella, Salmonella and Campylobac-
ter; and less likely to be infected with rotavirus in rural
Matlab (Tab le 1). Analogous observation was also found
only for rotavirus in the urban Dhaka; however, distribu-
tion of other pathogens was found almost similar (Table
2).
The isolation rates of Shigella were higher in rural area.
However, Vibrio cholerae and Campylobacter were higher
among urban severely malnourished children compared
Copyright © 2013 SciRes. FNS
Etiology of Diarrhea among Severely Malnourished Infants and Young Children:
Observation of Urban-Rural Differences over One Decade in Bangladesh
Copyright © 2013 SciRes. FNS
235
to their rural counterparts (Table 3).
Severely malnourished children from rural Matlab
were more likely to be infected with Vibrio cholerae than
well-nourished and moderately malnourished children.
So for Shigella; Shigella flexneri and Shigella dysente-
riae were more prevalent among severely malnourished
children compared to well-nourished. Conversely, chil-
dren with severe malnutrition less likely experienced rota-
viral diarrhea compared to well-nourished children, and
the proportion was even lower than moderately malnour-
ished children (Table 4).
On the other hand, in urban Dhaka, similar trend of
isolation pattern for Vibrio cholerae and rotavirus was
observed among under-5 children with severe malnutri-
tion compared to moderately malnourished and well-
nourished. Although, isolation rate of Salmonella was
very low among all the groups, it was higher among se-
verely malnourished children than others (Table 5). The
isolation rates of Campylobacter, Entamoeba histolytica,
and Giardia lamblia were found to be identical in all the
groups (Tables 4 and 5).
4. Discussion
Significant variations in isolation pattern of common
enteropathogens causing diarrhea among severely mal-
nourished under-5 years old children in both rural and
urban areas were observed. However, isolation rates were
also significantly different between urban and rural area.
Vibrio cholerae, Shigella and rotavirus are the major
pathogens that cause diarrhea [13]. Children under 5
years of age have the highest burden of cholera in the
endemic areas [14,15], and also at risk to have dehydrate-
ing diarrhea [16,17]. Study suggested a lack of innate and
cell-mediated immune responses among children against
V. cholerae [18]. Conversely, malnutrition is a risk factor
for shigellosis and children infected with Shigella were
also likely to become malnourished [19]. Malnutrition
Table 1. Distribution of pathogens by nutritional status category of the under-five children at rural Matlab Hospital (2000-201 1) .
Pathogens SU
n = 364 (%) SS
n = 449 (%) SW
n = 253 (%) SU with SS
n = 530 (%) SU with SW
n = 456 (%) SU with SS with SW
n = 182 (%)
Vibrio cholerae 23 (6)* 20 (5)* 5 (2)* 47 (9) 39 (9) 20 (11)
Overall Shigella 34 (9)* 51 (11) 25 (10)* 63 (12) 48 (11) 29 (16)
S. flexneri 26 (7) 37 (8) 18 (7) 46 (9) 38 (8) 20 (11)
S. sonnei 1 (0) 2 (0) 4 (2) 8 (2) 3 (1) 2 (1)
S. dysenteriae 5 (1) 5 (1) 2 (1) 4 (1) 1 (0) 4 (2)
S. boydii 2 (1) 7 (2) 1 (0) 5 (1) 6 (1) 3 (2)
Salmonella 7 (2) 4 (1 ) 4 (2) 7 (1) 8 (2) 1 (1)
Rotavirus 108 (30) 144 (32) 95 (38)* 135 (26) 141 (31) 46 (25)
Campylobacter 7 (2) 5 (1) 8 (3) 14 (3) 12 (3) 5 (3)
E. histolytica 1 (0) 3 (1) 1 (0) 9 (2) 1 (0) 0
Giardia lamblia 9 (3) 3 (1) 2 (1) 14 (3) 5 (1) 2 (1)
SU, severe underweight; SS, severe stunting; SW, severe wasting. *Values were compared with SU with SS with SW and were significant at 5% level.
Table 2. Distribution of pathogens by nutritional status category of the under-five children at urban Dhaka Hospital (2000-2011).
Pathogens SU
n = 518 (%) SS
n = 502 (%) SW
n = 242 (%) SU with SS
n = 929 (%) SU with SW
n = 563 (%) SU with SS with SW
n = 355 (%)
Vibrio cholerae 63 (12) 61 (12) 39 (16) 124 (13) 62 (11) 54 (15)
Overall Shigella 27 (5) 26 (5) 8 (3)* 56 (6) 30 (5) 31 (9)
S. flexneri 15 (3) 16 (3) 2 (1) 31 (3) 15 (3) 21 (6)
S. sonnei 2 (0) 2 (0) 0 (0) 7 (1) 8 (1) 3 (1)
S. dysenteriae 6 (1) 2 (0) 1 (0) 4 (2) 5 (1) 2 (1)
S. boydii 4 (1) 6 (1) 5 (2) 14 (2) 2 (0) 5 (1)
Salmonella 7 (1) 9 (2) 5 (2) 13 (1) 15 (3) 7 (2)
Rotavirus 176 (35)* 208 (42)* 84 (35)* 231 (25)* 177 (32)* 68 (20)
Campylobacter 22 (4) 17 (3) 12 (5) 35 (4) 22 (4) 14 (4)
E. histolytica 0 (0) 3 (1) 0 (0) 2 (0) 6 (1) 1 (0)
Giardia lamblia 2 (0) 4 (1) 0 (0) 6 (1) 3 (1) 1 (0)
SU, severe underweight; SS, severe stunting; SW, severe wasting. *Values were compared with SU with SS with SW and were significant at 5% level.
Etiology of Diarrhea among Severely Malnourished Infants and Young Children:
Observation of Urban-Rural Differences over One Decade in Bangladesh
236
Table 3. Urban-rural differentiation of pathogens among severely malnourished under-5 children (2000-2011).
Pathogens Rural; n = 2234 (%) Urban; n = 3109 (%) OR (95% CI) p value
Vibrio cholerae 154 (7) 403 (13) 0.50 (0.40, 0.61) <0.001
Overall Shigella 250 (11) 178 (6) 2.07 (1.69, 2.55) <0.001
S. flexneri 185 (8) 100 (3) 2.72 (2.10, 3.51) <0.001
S. sonnei 20 (1) 22 (1) 1.27 (0.66, 2.42) 0.542
S. dysenteriae 21 (1) 20 (6) 1.47 (0.76, 2.82) 0.285
S. boydii 24 (1) 36 (1) 0.93 (0.53, 1.60) 0.877
Salmonella 31 (1) 56 (2) 0.77 (0.48, 1.22) 0.285
Rotavirus 669 (30) 944 (31) 0.98 (0.87, 1.11) 0.766
Campylobacter 51 (2) 122 (4) 0.57 (0.41, 0.81) 0.001
E. histolytica 15 (1) 12 (0) 1.74 (0.77, 3.97) 0.209
Giardia lamblia 35 (1) 16 (1) 3.08 (1.64, 5.82) <0.001
Table 4. Distribution of pathogens among severely malnourished, moderately malnourished and well nourished under-5 chil-
dren in rural Matlab Hospital (2000-2011).
Pathogens Severely malnourished
n = 2234 (%) Moderately malnourished
n = 2234 (%) OR (95% CI) p valueaWell nourished
n = 2234 (%) OR (95% CI) p valueb
Vibrio cholerae 154 (7) 107 (5) 1.47 (1.13, 1.91) 0.00341 (2) 3.969 (2.76, 5.71) <0.001
Overall Shigella 250 (11) 202 (9) 1.27 (1.04, 1.55) 0.019176 (8) 1.47 (1.20, 1.81) <0.001
S. flexneri 185 (8) 157 (7) 1.19 (0.95, 1.50) 1.28136 (6) 1.39 (1.10, 1.76) 0.005
S. sonnei 20 (1) 20 (1) 1.00 (0.51, 1.94) 0.87313 (1) 1.54 (0.73, 3.29) 0.294
S. dysenteriae 21 (1) 12 (1) 1.76 (0.82, 3.80) 0.1626 (0) 3.52 (1.35, 9.75) 0.006
S. boydii 24 (1) 13 (1) 1.86 (0.90, 3.86) 0.09821 (1) 1.14 (0.61, 2.14) 0.764
Salmonella 31 (1) 29 (1) 1.07 (0.62, 1.83) 0.89631 (1) 1.00 (0.59, 1.70) 0.898
Rotavirus 669 (30) 755 (34) 0.84 (0.74, 0.95) 0.006771 (35) 0.81 (0.71, 0.92) 0.001
Campylobacter 51 (2) 44 (2) 1.16 (0.76, 1.78) 0.53338 (2) 1.35 (0.87, 2.11) 0.198
E. histolytica 15 (1) 11 (1) 1.37 (0.59, 3.19) 0.5554 (0) 3.77 (1.17, 13.43) 0.021
Giardia lamblia 35 (2) 36 (2) 0.97 (0.59, 1.59) 1.00035 (2) 1.00 (0.61, 1.64) 0.904
aComparison between severely malnourished vs. moderately malnourished; bComparison between severely malnourished vs. well-nourished.
Table 5. Distribution of pathogens among severely malnourished, moderately malnourished and well nourished under-five
children at the urban Dhaka Hospital (2000-2011).
Pathogens Severely malnourished
n = 3109 (%) Moderately malnourished
n = 3109 (%) OR (95% CI) p valueaWell nourished
n = 3109 (%) OR (95% CI) p value b
Vibrio cholerae 403 (13) 317 (10) 1.31 (1.12, 1.54) <0.001248(8) 1.72 (1.45, 2.04) <0.001
Overall Shigella 178 (6) 151 (5) 1.19 (0.95, 1.50) 0.140160 (5) 1.12 (0.89, 1.40) 0.341
S. flexneri 100 (3) 82 (3) 1.23 (0.90, 1.67) 0.20082 (3) 1.23 (0.90, 1.67) 0.200
S. sonnei 22 (1) 23 (1) 0.96 (0.51, 1.78) 1.00029 (1) 0.76 (0.42, 1.36) 0.398
S. dysenteriae 20 (6) 9 (0) 1.06 (0.54, 2.07) 0.9919 (0) 2.23 (0.96, 5.29) 0.062
S. boydii 36 (1) 37 (1) 0.97 (0.60, 1.58) 1.00040 (1) 0.90 (0.56, 1.45) 0.729
Salmonella 56 (2) 38 (1) 1.48 (0.96, 2.29) 0.07730 (1) 1.88 (1.18, 3.01) 0.006
Rotavirus 944 (31) 1328 (43) 0.58 (0.53, 0.65) <0.0011445 (47) 0.50 (0.45, 0.56) <0.001
Campylobacter 122 (4) 143 (5) 0.85 (0.66, 1.09) 0.209124 (4) 0.98 ( 0.76, 1.28) 0.948
E. histolytica 12 (<1) 5 (<1) 2.41 (0.79, 7.82) 0.1453 (<1) 4.01 (1.06, 17.88) 0.038
Giardia lamblia 16 (1) 25 (1) 0.64 (0.32, 1.24) 0.21021 (1) 0.76 (0.38, 1.52) 0.509
aComparison between severely malnourished vs. moderately malnourished; bComparison between severely malnourished vs. well-nourished.
Copyright © 2013 SciRes. FNS
Etiology of Diarrhea among Severely Malnourished Infants and Young Children:
Observation of Urban-Rural Differences over One Decade in Bangladesh
Copyright © 2013 SciRes. FNS
237
causes atrophy and decreased cell proliferation of the
Thymus gland resulting in depletion of CD4+ CD8+
thymocytes [20,21]. Thus, there is impaired peripheral
immune response that favors the pathogens to become
virulent. This might explain the higher rate of isolation of
V. cholerae and Shigella among severely malnourished
children compared to others. Moreover, severe malnutri-
tion leads to atrophy of the gastric mucosa resulting in
less production of hydrochloric acid which favors the
higher rate of infection due to less infective doses of
common bacterial pathogens [22]. On the other hand,
rotavirus causes diarrhea either by malabsorption second-
dary to enterocyte destruction, a virus-encoded toxin,
stimulation of the enteric nervous system (ENS), and
villus ischemia [23,24] in malnutrition. Malnutrition causes
decreased number of intestinal lining epithelial cells and
impair its proliferation [25]. Thus, due to lack of mucosal
cells to adhere for rotavirus causing diarrhea would be
the possible explanation of lower isolation rate among
severely malnourished children.
Distinct geographical variation may explain the diver-
sity in socio-demographic and cultural factors, water-
sanitation practices and also mass rotavirus vaccination
in rural Matlab [26] might explain the diverse isolation
rates between rural-urban areas in addition to household
food security. Recent mass rotaviral vaccination might
trigger the other pathogens to become virulent or survive
better in environment.
Severe malnutrition is a complex phenomenon, in-
volving interactions of the biological, cultural and socio-
economic factors [27]. Parental education, lower socio-
economic status, and poor nutritional characteristics, child-
feeding practices, and birth-order have strong association
with severe malnutrition [10,27]. Conversely, association
with higher family food insecurity, low quality of com-
plementary foods and high burdens of intestinal parasitic
loads and other infections which are persisting despite
improvements in socio-economic conditions over recent
years have also been documented [28,29]. Severely mal-
nourished children are always vulnerable to any infec-
tions including diarrhea due to compromised immune
function [30]. Having all the category of severe malnutri-
tion, a child would be highly susceptible to serious infec-
tions. Severe malnutrition with the co-morbidity of diar-
rhea [31,32] is a life threatening condition with high fa-
tality rate (20%) [7]; however, the present observation
was not aimed to determine the fatal outcome. Other than
that, contaminated weaning foods prepared under unhy-
gienic conditions is a major risk factor for causing diar-
rheal diseases and associated malnutrition [33]. A stan-
dardized protocol for management of severe malnutrition
with diarrhea among under 5 years old children was in-
troduced in the Dhaka hospital of icddr,b that reduced
mortality by at least 47% [34,35]; moreover, early detec-
tion of entero-pathogens helps the clinicians for rational
use of antimicrobials and appropriate management of
these high risk severely malnourished children.
5. Limitations
Although unbiased systematic sampling method was used
to enroll patients into surveillance system irrespective of
age, sex, nutritional status, disease severity or socioeco-
nomic background and the large dataset with standard
laboratory facility were supportive of the strengths of this
analysis; however, hospital data might not be representa-
tive of the general population.
6. Conclusion
Severely malnourished children were more prone to be
infected with common bacterial pathogens compared to
those without severe malnutrition. Integrated manage-
ment with early and appropriate antimicrobial therapy
needs to be introduced in addition to other resuscitative
measures. Furthermore, round the clock monitoring needs
to be continued to observe any changing pattern of isola-
tion rates of the common pathogens and also there are
needs to determine the frequency of isolation of other
pathogens causing diarrhea and fatal outcomes.
7. Acknowledgements
Hospital surveillance was funded by icddr,b and the Gov-
ernment of the People’s Republic of Bangladesh through
IHP-HNPRP. icddr,b acknowledges with gratitude the
commitment of the Government of the People’s Republic
of Bangladesh to the Centre’s research efforts. icddr,b
also gratefully acknowledges the following donors which
provide unrestricted support to the Centre’s research ef-
forts: Australian Agency for International Development
(AusAID), Government of the People’s Republic of Bang-
ladesh, Canadian International Development Agency
(CIDA), Embassy of the Kingdom of the Netherlands
(EKN), Swedish International Development Cooperation
Agency (Sida), Swiss Agency for Development and Co-
operation (SDC), and Department for International De-
velopment, UK (DFID).
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