Am. J. Trop. Med. Hyg., 80(5), 2009, pp. 812–818
Copyright © 2009 by The American Society of Tropical Medicine and Hygiene
Population-Based Study of a Widespread Outbreak of Diarrhea Associated with
Increased Mortality and Malnutrition in Botswana, January–March, 2006
Ondrej Mach,* Lydia Lu, Tracy Creek, Anna Bowen, Wences Arvelo, Molly Smit,
Japhter Masunge, Muireann Brennan, and Thomas Handzel
Centers for Disease Control and Prevention, Atlanta, Georgia; BOTUSA Project, Gaborone, Botswana;
Botswana Ministry of Health, Gaborone, Botswana
Abstract. In early 2006, coinciding with heavy rains, Botswana health facilities reported increases in diarrhea, mortality, and acute malnutrition among young children. Data on diarrhea, human immunodeficiency virus, feeding, mortality,
and water/sanitation were collected by random cluster survey. Anthropometric data were measured and drinking water
samples were tested. Of 537 surveyed children less than five years of age, one-third experienced ³ 1 episode of diarrhea.
Prevalence of acute malnutrition was 7.9%, and the mortality rate for children less than five years of age was 2.6/10,000/
day during the outbreak. Significant risk factors for diarrhea included an age less than two years; breastfeeding was protective. Diarrhea lasting for more than 14 days and failure to thrive were risk factors for acute malnutrition. Prevalence
of acute malnutrition was higher than previously documented and the mortality rate in children less than five years of
age during the outbreak was above the international threshold for emergency action with an estimated 547 excess deaths.
This survey highlights the need for safe infant feeding and effective treatment of malnutrition and diarrhea in young
children.
This outbreak occurred in a country with one of the world’s
highest prevalence of human immunodeficiency virus (HIV):
approximately 33% of pregnant women are infected with
HIV.5 A national program to prevent mother-to-child transmission (PMTCT) of HIV recommends that HIV-positive
mothers feed infants with formula instead of breast milk. The
PMTCT program distributes free formula to HIV-exposed
infants less than 12 months of age.
We conducted a population-based, cross-sectional survey to
estimate the burden of illness at the community level and to
quantify age-specific attack rates of diarrhea, mortality, and
prevalence of acute malnutrition among children less than five
years of age during this outbreak, and to better understand
risk factors associated with these outcomes. This survey was
conducted as an outbreak response measure and the findings
were immediately used for action.
BACKGROUND
In early 2006, a four-fold increase in the number of diarrhea
cases among young children was reported to the Ministry of
Health through routine surveillance in Botswana, a country in
southern Africa with a population of approximately 1.76 million.1 At the same time, cases of severe acute malnutrition, a
rare condition in Botswana,2–4 were reported by health personnel providing care to patients with diarrhea. The number
of reported deaths caused by diarrhea among young children
was more than 25 times higher than in the previous two years.
On the basis of Ministry of Health surveillance data, the area
most heavily impacted by the outbreak appeared to be in the
eastern and most densely populated part of the country.
Consultations for diarrhea at the emergency department at
Nyangabgwe Hospital in Francistown, the country’s second
largest referral hospital at the center of this outbreak, began
to increase early in January 2006, peaked in late February, and
returned to normal in April (Figure 1) (Creek T and others,
unpublished data). Additionally, cases of severe acute malnutrition were first seen in the hospital in late January, peaked
in March, and were still occurring when our investigation
ended in mid-April (Arvelo W and others, unpublished data).
The total number of visits for diarrhea during this period was
1,276, and 83 cases of severe acute malnutrition were identified in the emergency department among children less than
five years of age. Almost all the children admitted for acute
malnutrition had experienced diarrhea earlier in 2006 (Creek
T and others, unpublished data).
Laboratory testing of in-patient stool specimens from
Nyangabgwe Hospital performed at The Centers for Disease
Control and Prevention in Atlanta showed a multipathogenic etiology of diarrhea. Cryptosporidium parvum, Cryptosporidium hominis, and enteropathogenic Escherichia coli
were the most common organisms identified. Norovirus and
rotavirus were relatively uncommon (Arvelo W and others,
unpublished data).
METHODS
A two-stage, 30-cluster survey was conducted in three health
districts of Botswana: Francistown, Tutume (also known as
Central), and North-East during the first two weeks of April
2006. The districts were selected based on Botswana surveillance data and on logistical feasibility. The combined population of these districts was estimated to be 256,000, with
approximately 32,000 children less than five years of age (2001
census data). We defined a cluster as a village or section of
town listed in the 2001 census and a household as a group of
persons sharing food from the same cooking pot. In the first
stage, 30 clusters were randomly selected from census lists. The
selection was proportional to population size, ensuring that all
households in the sampling universe had an equal chance of
being selected. For the purposes of this survey, we treated the
population of these three districts as one entity. Of the 30 clusters randomly selected for the survey, 20 were rural villages
and 10 were urban or peri-urban communities. The population
of the clusters ranged from 300 to 18,000 persons.
In the second stage, households with children less than five
years of age were randomly selected in each cluster using the
Expanded Program on Immunization method6,7 until 23 children were identified in each cluster. All children less than
* Address correspondence to Ondrej Mach, Global Immunization
Division, Centers for Disease Control and Prevention, Mailstop E05,
1600 Clifton Road, Atlanta, GA 30333. E-mail: [email protected]
812
POPULATION-BASED STUDY OF A WIDESPREAD OUTBREAK OF DIARRHEA
813
Figure 1. Emergency department visits classified as diarrhea and acute malnutrition at Nyangabgwe Hospital, Francistown, Botswana,
November 15, 2005–April 7, 2006 in children less than five years of age (Creek T and others, unpublished data).
five years of age in a selected household were included in
the survey. Households without a child less than five years of
age were not included unless household members reported a
death of a child less than five years of age during the previous
three months. If household members in a selected household
were absent on two separate visits, the household was skipped
and not replaced.
On the basis of 2001 census data, we estimated an average of one child less than five years of age per household in
Botswana. Assuming an overestimated prevalence of acute
malnutrition at 20%, 367 children less than five years of age
would be needed to estimate prevalence with a precision of
± 5%, taking into account an anticipated design effect of 1.5.
To accommodate for possible loss of data caused by refusal to
participate and absent families, and to use available resources
adequately, we aimed to survey 23 children in each of 30 clusters, resulting in a projected sample size of 690 children less
than five years of age.
Each survey team consisted of one interviewer, one person tasked with taking anthropometric measurements and
collecting water samples, and a driver. Once a household was
selected, the survey team identified the female head of household, obtained informed consent, and administered a questionnaire in the local language. We collected information about the
history of diarrhea among children less than five years of age
between January 1, 2006 and the interview date in April 2006,
nutrition practices, drinking water sources and storage practices, and HIV status of child and mother. The HIV status was
self-reported or based on data from the child health card. The
interviewee was also asked to report any deaths among children less than five years of age occurring between January 1,
2006 and the date of interview. Diarrhea was defined as three
or more loose or watery stools in 24 hours. Data on number of
episodes was not collected, only presence or absence of diarrhea during the recall period was collected. Long-lasting diarrhea was defined as diarrhea lasting for more than 14 days.8
Available child health cards were reviewed to assess child
growth history. In Botswana, children less than five years of
age are weighed monthly in health centers, and their weight is
plotted against their age in a health card. We defined failure to
thrive as having no reported weight gain during the three most
recent health center visits.
Children between 6 months and 5 years of age, whose parents consented, were weighed with digital Seca (Hanover, MD)
scales (with precision of ± 0.1 kg) and height was measured
using Shorr (Olney, MD) height boards (with precision of ±
0.5 cm). The child was classified as having nutritional edema
(kwashiorkor) if pitting edema was present on both feet at the
time of anthropometric measurements.
Acute malnutrition was categorized according to World
Health Organization (WHO) guidelines.9 Moderate acute
malnutrition was defined as a weight-for-height Z-score more
than 2 SD below the median (1978 WHO reference standards). Severe acute malnutrition (SAM) was defined as a
weight-for-height Z-score more than 3 SD below the median,
or the presence of nutritional edema (kwashiorkor). Global
acute malnutrition (GAM), also referred to as acute malnutrition, included children who were either severely or moderately malnourished.
The mortality rate of children less than five years of age
was calculated as the number of deaths among children less
than five years of age per 10,000 person-days. Cause of death
was reported by the primary caregiver and divided into basic
categories: diarrhea and/or vomiting, breathing problems or
cough, HIV, insufficient food, injury, other, or unknown.
Drinking water samples were collected from approximately
every fourth surveyed household. Samples were collected
from the water source and from the vessel used for storage of
drinking water at the household.10 Tap fixtures were sterilized
and flushed to clear the service line before sampling. Water
samples were collected in Whirl-paks (Nasco International,
Inc., Fort Atkinson, WI) or in sterilized bottles containing
814
MACH AND OTHERS
sodium thiosulfate. Water samples were transported to the
laboratory in a cooler with ice for duplicate testing within
six hours of collection. Water was tested for total coliform
bacteria and for E. coli by using either membrane filtration
(Millipore Corporation, Billerica, MA) or Colilert® (IDEXX,
Westbrooke, MA) systems.11
Water contamination was categorized by concentration of
E. coli per 100-mL sample. Categories included no contamination (0 E. coli per 100 mL); low (0–9 E. coli per 100 mL); moderate (10–99 E. coli per 100 mL); and high (> 100 E. coli per
100 mL). Arithmetic mean was used for duplicate testing.
Survey data were analyzed with Epi Info version 3.3.2
Centers for Disease Control and Prevention), SAS version 9.1
(SAS Inc., Cary, NC), and Sudaan version 9 (RTI International,
Research Triangle Park, NC), accounting for cluster design
of the study. Univariate associations are reported by use of
crude risk ratios (RRs) with 95% confidence intervals (CIs)
or by use of adjusted risk ratios when significant confounders
were found. Multivariate associations based on logistic regression models are reported by use of adjusted ORs with 95%
CIs. All risk factors included in the univariate analysis were
included in the initial multivariate regression model. The final
model included only factors that were found to be significant
at P < 0.05.
The survey protocol was reviewed and approved by the
Centers for Disease Control and Prevention and determined
to be non-research; it was approved by the Botswana Health
Research Development Committee.
RESULTS
The study included 537 children less than five years of
age in 339 households, of which 271 (50.5%) were male and
259 (48.2%) were less than two years of age. The household
response rate was 79%. Non-responders included those households that did not consent to participate in the study (< 10%
of non-responders) and those households where residents
were absent on two attempts during the data collection phase
(> 90% of non-responders).
During the first three months of 2006, 170 (32.0%) children
were reported to have had at least one episode of diarrhea
(Table 1). Children 1–2 years of age had the highest attack rate,
and children in the oldest age group (4–5 years) had the lowest
attack rate. The median duration of diarrhea was 7 days, and
long-lasting diarrhea was reported among 23.2% of diarrhea
cases. A high proportion of children with diarrhea received
treatment (152 of 168, 90.5%). Of these children, 144 (94.8%)
consulted a physician or a nurse and 4 (2.6%) visited a traditional healer. Most caregivers reported offering less food and
drink to their children during diarrhea episodes.
The prevalence of GAM among 407 children with complete
anthropometric data between six months and five years of age
was 7.9%, the prevalence of SAM was 2.7%; and the prevalence
of kwashiorkor was 0.2% (Table 1). There were no significant
differences in prevalence between sexes or between age groups.
On the basis of data from 414 (81.7%) children with available health cards, an estimated 16.3% (95% CI = 7.9–24.8%)
were failing to thrive at the time of the survey. The proportion
of children less than two years of age with failure to thrive was
18.1%; among children 2–5 years of age it was 15.0%. This difference was not statistically significant. A total of 13 children
less than five years of age was reported to have died during
the first three months of 2006, providing an estimated mortality rate of children less than five years of age of 2.6/10,000/
day (95% CI = 0.6–4.5). Parents of 11 (84.6%) of the deceased
children reported diarrhea as the cause of death.
Table 1
Diarrhea and acute malnutrition among children less than five years of age in three health districts in Botswana, 2006*
Diarrhea attack rate
Children with episode of diarrhea
between 1/1/06 and 3/31/06)
Diarrhea by age groups, years
<1
1–< 2
2–< 3
3–< 4
4–< 5
Characteristics of diarrhea
Median duration
Duration £ 14 days
Long lasting (> 14 days)
Received treatment
Hospitalized
Received intravenous fluids
Offered less food
Offered less to drink
Prevalence of global acute malnutrition
children 6–59 months of age†
Global acute malnutrition
Male
Female
6–23 months of age
24–59 months of age
Severe acute malnutrition
Kwashiorkor
* CI = confidence interval; IQR = interquartile range.
† With valid anthropometric data.
No.
No. positive
Attack rate, %
95% CI
531
170
32.0
28.1–36.2
128
106
89
99
89
44
61
28
21
11
34.4
57.5
31.5
21.2
12.4
26.2–43.3
47.6–67.1
22.0–42.2
13.6–30.6
6.3–21.0
No.
No. positive
Days or %
95% CI/IQR
170
164
164
168
154
149
169
169
126
38
152
8
13
127
139
7
76.8%
23.2%
90.5%
5.2%
8.7%
75.1%
82.2%
IQR = 3–14
69.6–83.1
16.9–30.4
85.0–94.5
2.3–10.0
4.7–14.5
67.9–81.5
75.6–87.7
No.
No. positive
%
95% CI
407
199
208
159
248
407
407
32
16
16
14
18
11
1
7.9
8.0
7.7
8.8
7.3
2.7
0.2
4.7–11.0
4.7–12.7
4.5–12.2
4.9–14.3
2.9–11.6
0.5–4.8
0.0–0.7
POPULATION-BASED STUDY OF A WIDESPREAD OUTBREAK OF DIARRHEA
Among the households sampled, 205 (65.7%) mothers had
been tested and knew their HIV status. Of those mothers with
known HIV status, 70 (34.1%) were HIV positive and 135
(65.9%) were HIV negative. Among children of HIV positive mothers, 48 (41.9%) had been tested for HIV. Among
these children, 4 (8.3%) were infected with HIV. One additional child was found to be infected with HIV according to
the child’s health card. However, the child’s mother was not
aware of her own HIV status.
At the time of the survey, 73 (30.8%) children less than two
years of age and 41 (67.2%) of children less than one year of
age were being breastfed. Breastfeeding varied significantly
by mother’s HIV status. Breastfeeding at the time of survey
was reported among 51 (47.4%) children less than two years
of age born to HIV-negative mothers compared with 1 (1.7%)
born to HIV-positive mothers. There were 384 (74.0%) children who consumed any type of porridge in the 24 hours preceding the survey, which reflected porridge consumption by
8.2% of children less than 6 months of age and 82.3% of children 6 months to 5 years of age.
Approximately one-third of 339 surveyed households had
a water tap in the house, one-third had a standpipe in their
compound, and one-third used water from a shared standpipe.
A small proportion of households (< 1%) drank water from
a river or an open well. Samples of source water tested from
approximately every fourth household (84) showed contamination with E. coli in 22 (26.2%). In 58 (69%) households,
the drinking water was stored in various containers, mostly
in buckets without lids. Stored water was contaminated in 22
(38%) of households. However, levels of contamination in
stored water were not found to be significantly different from
those of source water.
In our sample of 339 households, 240 (71.4%) used a pit
latrine as their main toilet, 70 (20.8%) had flush toilets, and 26
(7.7%) did not have any toilet facilities and used open space
and bushes to urinate and defecate. In 67 (21.7%) households,
the interviewers observed that soap was available at the place
where household members washed their hands.
Significant risk factors for diarrhea included child’s age
less than 24 months and a child being HIV positive. Current
breastfeeding was found to be significantly protective against
diarrhea (Table 2).
Consumption of any type of porridge, the primary weaning
food of Botswana, during the 24 hours preceding the survey
was significantly associated with history of diarrhea among
children less than two years of age (Table 2) No other factors,
including other foods consumed, were associated with diarrheal disease.
Having a flush toilet was considered to be a possible proxy
for household socioeconomic status. However, we did not
observe any association either between owning a flush toilet
(or a pit latrine) or having soap available for hand-washing
and self-report of any diarrhea during a three-month recall
period. We did not observe a significant association between
contamination of drinking water with E. coli, measured at the
time of survey, and history of diarrhea. Prevalence of diarrhea
was not associated with type of water source (in house versus
yard or public tap) or with water storage practice.
When analyzing risk factors for development of acute malnutrition, long-lasting diarrhea and failure to thrive during the
prior three months were significant risk factors. HIV status,
feeding practices, owning a flush toilet, or formal education
815
of the caretaker were not significantly associated with acute
malnutrition (Table 2).
DISCUSSION
The results of this cross-sectional survey in three heavily
affected areas of Botswana suggest that the outbreak of diarrhea affected a large proportion of the children less than five
years of age and led to increased levels of acute malnutrition
and mortality among children.
Approximately one-third of children less than five years of
age were reported to have experienced at least one episode of
diarrheal illness between January and March 2006. Although
research suggests that 24–72-hour recall periods for pediatric
diarrhea are optimal and that longer recall periods are likely
to be unreliable, we were unable to capture diarrhea incidence in this manner and instead used a three-month recall
period.12,13 The overall attack rate is not unusual for this recall
period.14 However, the dramatic increase in hospitalizations
for diarrhea (Figure 1), the high proportion of long-lasting
diarrheas, and increased levels of acute malnutrition and pediatric deaths provide evidence that this was an outbreak with
unusually severe consequences.
Relevant results from related studies conducted prior to
this survey contribute to a picture of the possible etiology
behind the outbreak. Laboratory findings from hospitalized
children suggested probable sewage contamination of the
environment during heavy rains in late 2005 and early 2006.
Cryptosporidium species are typically indicative of exposure
to sewage contamination of water or the environment.15,16 The
rain was unusually heavy when compared with available meteorologic data from previous years, and it caused flooding and
overflowing of latrines (Arvelo W and others, unpublished
data).17–20 It is likely that the environmental contamination
occurred early in the outbreak and that poor personal hygiene
and sanitary conditions placed food and drinking water stored
within homes at risk of contamination and permitted personto-person transmission. A high proportion of non-breastfed
children created a pool of persons who were more likely to be
severely ill or to die because they lacked protective maternal
antibodies.21 Additionally, most HIV-positive women receiving free infant formula from the PMTCT program reported
having been short of formula at some point because of supply
or distribution problems.
In light of our finding that porridge is an important weaning
food and that it was associated with diarrhea, additional investigation is needed to describe whether the risk is caused by the
properties of the different types of porridge, their preparation,
or whether this finding is an indicator of introduction of solid
foods in general.
Although none of the environmental factors were associated with diarrhea in this analysis, they are well-known risk
factors for diarrhea. Efforts to improve water quality, sanitation, and personal hygiene would likely reduce diarrhea incidence in these communities. Most parents reported offering
less food and drink than usual to their children while they
had diarrhea, which suggests poor awareness of WHO protocols for oral rehydration and nutrition during episodes of
diarrhea.
The prevalence of global acute malnutrition in this survey was higher than that reported in the 2000 Botswana
National Multiple Indicator Cluster Survey (4.9%).22
816
MACH AND OTHERS
Table 2
Risk factors for diarrhea and global acute malnutrition, Botswana, 2006*
Risk factor for diarrhea
No.
No. (%) with diarrhea
Sex
Female
269
79 (29.4)
Male
260
90 (34.6)
Age, months†
³ 24
279
60 (21.5)
< 24
217
104 (47.9)
Child currently breastfed (< 12 months of age)†‡
No
70
27 (38.6)
Yes
56
15 (26.8)
Child currently fed infant formula (< 12 months of age)
No
18
6 (33.3)
Yes
53
18 (33.9)
Consumption of any type of porridge during 24 hours preceding survey (< 24 months)†
No
99
27 (27.3)
Yes
121
70 (57.9)
Failure to thrive§
No
343
110 (32.1)
Yes
68
25 (36.8)
Contamination (Escherichia coli) of source water at the time of survey
None
94
31 (33.0)
1–10/100 mL
29
7 (24.2)
11–100/100 mL
7
3 (42.9)
> 100/100 mL
3
1 (33.3)
Child’s mother HIV positive§¶
No
222
73 (32.9)
Yes
109
34 (31.2)
Child HIV positive†§#
No
273
92 (33.7)
Yes
5
4 (80.0)
Owning flush toilet§
No
438
146 (33.3)
Yes
93
24 (25.8)
Risk factor for global acute malnutrition
Sex
Female
Male
Age, months
³ 24
6–24
Diarrhea
None
£ 14 days duration
> 14 days (long-lasting)†
Failure to thrive†
No
Yes
Child currently breastfed (< 12 months of age)
No
Yes
Child’s mother HIV positive¶
No
Yes
Child HIV positive#
No
Yes
Education of caregiver
Elementary or less
More than elementary
Owning flush toilet
No
Yes
RR
95% CI
Reference
1.2
0.9–1.6
Reference
2.2
1.7–3.0
Reference
0.5
0.3–0.9
Reference
1
0.4–2.7
Reference
2.1
1.5–3.0
Reference
0.9
0.7–1.2
Reference
0.7
1.3
1
0.4–1.5
0.6–2.7
0.7–1.4
Reference
1
0.7–1.4
Reference
3
1.4–6.6
Reference
0.7
0.5–1.1
No.
No. (%) with acute malnutrition
RR
95% CI
208
199
16 (7.7)
16 (8.0)
Reference
1
0.6–1.9
248
159
18 (7.3)
14 (8.8)
Reference
1.2
0.5–2.8
263
103
33
17 (6.5)
9 (8.7)
6 (18.2)
Reference
1.4
2.8
0.5–3.8
1.1–7.5
283
62
18 (6.4)
9 (14.5)
Reference
2.3
1.2–4.3
36
28
4 (10.7)
3 (11.1)
Reference
1
0.1–6.7
178
79
12 (6.7)
7 (8.9)
Reference
1.3
0.5–3.6
215
4
15 (7.0)
1 (25.0)
Reference
3.6
0.6–22.2
51
344
7 (13.7)
24 (7.0)
Reference
0.5
0.2–1.4
338
69
28 (8.3)
4 (5.8)
Reference
0.7
0.3–1.9
* RR = relative risk; CI = confidence interval; HIV = human immunodeficiency virus.
† Significant association (P < 0.05).
‡ Adjusted for mother’s HIV status.
§ Adjusted for child’s age.
¶ Among children of mothers with known HIV status.
# If mother was HIV negative, then child assumed to be HIV negative.
POPULATION-BASED STUDY OF A WIDESPREAD OUTBREAK OF DIARRHEA
However, because of the limited size of the survey, this difference did not reach statistical significance. Our finding of
a significant association between long-lasting diarrhea and
acute malnutrition supported a hypothesis, generated while
observing hospitalized patients, that repeated and prolonged
diarrhea led to acute malnutrition.23 The observed association between failure to thrive, documented at clinic visits,
and acute malnutrition, measured during the survey, points
to a missed opportunity to intervene when growth faltering
is observed by health workers.
We estimated the excess mortality rate in children less than
five years of age during January–March 2006 to be 1.9/10,000/
day by subtracting a baseline mortality rate of 0.7/10,000/day
(converted child mortality rate from the 2005 annual report
of The United Nations Children’s Fund) from our estimate
of 2.6/10,000/day. By extrapolating to the total population of
children less than five years of age in the three health districts, we estimated that approximately 547 (95% CI = 115–
950) children less than five years of age died as a result of
this outbreak, a figure greater than the number of deaths
reported to the Ministry of Health for the same period of time
for the entire country. Furthermore, the mortality rate in children less than five years of age likely exceeded the Sphere
Project threshold for emergency action in sub-Saharan Africa
(2.3/10,000/day).24
This study had several limitations. First, according to hospital data, the outbreak of diarrhea began in mid-December
2005, peaked in February 2006, and had subsided by the end
of March. Thus, our survey conducted in April had the potential to be influenced by a recall bias. This relatively long recall
period, coupled with the publicity surrounding the outbreak,
may also have influenced parents to incorrectly identify the
occurrence, duration, and date of diarrhea in their children.
The study design could not account for repeated episodes
of diarrhea in children and parents may not have paid sufficient attention to loose stools in their children. However,
the fact that more than 90% of children with reported diarrhea received treatment supports the validity of the parental report. It is also possible that parents did not correctly
remember what they fed their children. Additionally, 21%
of households in our sampling frame were considered nonrespondents because of households being found empty
on two or more occasions or consent for interview being
denied. Finally, water contamination was measured at the
time of survey while environmental contamination during
the diarrhea outbreak would have occurred several months
prior. This fact may explain the lack of observed association
between contamination of drinking water and recalled diarrhea morbidity.
Having a high proportion of non-breastfed young children
in a setting where poor environmental and hygiene conditions exist is a potential hazard that can contribute to and
exacerbate diarrhea outbreaks. The role of infant feeding
recommendations for HIV-positive mothers regarding cessation and non-initiation of breastfeeding should be explored.
Furthermore, suboptimal feeding during diarrheal disease
may have resulted in increased rates of acute malnutrition
and high mortality among young children. Failure to respond
to growth faltering and to implement proper treatment measures for long-lasting and severe diarrhea and acute malnutrition likely contributed to the high levels of mortality after
this outbreak.
817
Received August 13, 2008. Accepted for publication January 13, 2009.
Acknowledgments: We thank L. Zaks, A. Kim, T. Finkbeiner, B.
Woodruff, E. Mintz, N. Shaffer, C. Bern, M. Davis and others in
Botswana and Atlanta for their participation in this study.
Financial support: This study was supported by the Centers for Disease
Control and Prevention. However, there was no special grant or fund
made available specifically for this investigation; operational funds for
outbreak response were used.
Authors’ addresses: Ondrej Mach, Lydia Lu, Tracy Creek, Anna
Bowen, Wences Arvelo, Muireann Brennan, and Thomas Handzel,
Global Immunization Division, Centers for Disease Control and
Prevention, Mailstop E05, 1600 Clifton Road, Atlanta, GA 30333,
E-mail: [email protected]. Molly Smit, BOTUSA Project, Gaborone,
Botswana. Japhter Masunge, Botswana Ministry of Health, Gaborone,
Botswana.
REFERENCES
1. UNDP, 2005. Human Development Index. Geneva: World Health
Organization.
2. Boonstra E, Lindbaek M, Fidzani B, Bruusgaard D, 2001. Cattle
eradication and malnutrition in under five’s: a natural experiment in Botswana. Public Health Nutr 4: 877–882.
3. Ismail S, 1991. Nutritional surveillance: experience from developing countries. Proc Nutr Soc 50: 673–679.
4. Grivetti LE, 1978. Nutritional success in a semi-arid land: examination of Tswana agro-pastoralists of the eastern Kalahari,
Botswana. Am J Clin Nutr 31: 1204–1220.
5. UNDP, 2003. Human Development Report 2003. New York:
Oxford University Press.
6. Lemeshow S, Robinson D, 1985. Surveys to measure programme
coverage and impact: a review of the methodology used by the
expanded programme on immunization. World Health Stat Q
38: 65–75.
7. Hoshaw-Woodard S, 2001. Description and Comparison of the
Methods of Cluster Sampling and Lot Quality Assurance
Sampling to Assess Immunization Coverage. Geneva: World
Health Organization.
8. World Health Organization, 2005. The Treatment of Diarrhoea: A
Manual for Physicians and Other Senior Health Workers. Fourth
edition. Geneva: World Health Organization.
9. World Health Organization, 1995. Physical Status: The Use and
Interpretation of Anthropometry. Geneva: World Health
Organization.
10. American Public Health Association, American Water Works
Association, Water Pollution Control Federation, 1980.
Standard Methods for the Examination of Water and Wastewater.
15th edition. Washington, DC: American Public Health
Association.
11. Olson B, Clark D, Milner B, Stewart M, Wolfe R, 1991. Total coliform detection in drinking water: comparison of membrane filtration with Colilert and Coliquick. Appl Environ Microbiol 57:
1535–1539.
12. Alam NHF, Rahaman MM, 1989. Reporting errors in one-week
diarrhoea recall surveys: experience from a prospective study
in rural Bangladesh. Int J Epidemiol 18: 697–700.
13. Ramakrishnan RVT, Koya PK, Kamaraj P, 1999. Influence of recall
period on estimates of diarrhoea morbidity in infants in rural
Tamilnadu. Indian J Public Health 43: 136–139.
14. Genser B, Strina A, Teles CA, Prado MS, Barreto ML, 2006. Risk
factors for childhood diarrhea incidence: dynamic analysis of a
longitudinal study. Epidemiology 17: 658–667.
15. Molbak K, Aaby P, Hojlyng N, da Silva AP, 1994. Risk factors for
Cryptosporidium diarrhea in early childhood: a case-control
study from Guinea-Bissau, West Africa. Am J Epidemiol 139:
734–740.
16. Rose JB, 1997. Environmental ecology of Cryptosporidium and
public health implications. Annu Rev Public Health 18:
135–161.
17. Thomson MC, Mason SJ, Phindela T, Connor SJ, 2005. Use of
rainfall and sea surface temperature monitoring for malaria
early warning in Botswana. Am J Trop Med Hyg 73: 214–221.
818
MACH AND OTHERS
18. Schmitt CV, 2006. Africa Weather Hazards Assessment February
2–8, 2006. Famine Early Warning System Network.
19. Leshomo K, 2006. Diarrhea Epidemic Leads to Threat of Severe
Malnutrition in Botswana. New Yok: UNICEF.
20. Southern African Development Community Food Agricultural
and Natural Resources Directorate, 2006. Agromet-Update:
2005/2006 Agricultural Season. Food Security Early Warning
System.
21. Dop MC, 2002. Breastfeeding in Africa: will positive trends be
challenged by the AIDS epidemic? [in French]. Sante 12: 64–72.
22. UNICEF, 2000. Botswana Multiple Indicator Survey. New York:
The United Nations Children’s Fund.
23. Gracey M, 1996. Diarrhea and malnutrition: a challenge for pediatricians. J Pediatr Gastroenterol Nutr 22: 6–16.
24. The Sphere Project, 2004. Humanitarian Charter and Minimum
Standards in Disaster Response. Geneva: Oxfam Publishing.