Enteric fever burden in North Jakarta, Indonesia: A prospective, community-based study

Abstract

We undertook a prospective community-based study in North Jakarta, Indonesia, to determine the incidence, clinical characteristics, seasonality, etiologic agent, and antimicrobial susceptibility pattern of enteric fever.
Following a census, treatment centre-based surveillance for febrile illness was conducted for two-years. Clinical data and a blood culture were obtained from each patient.
In a population of 160,261, we detected 296 laboratory-confirmed enteric fever cases during the surveillance period, of which 221 (75%) were typhoid fever and 75 (25%) were paratyphoid fever. The overall incidence of typhoid and paratyphoid cases was 1.4, and 0.5 per thousand populations per year, respectively. Although the incidence of febrile episodes evaluated was highest among children under 5 years of age at 92.6 per thousand persons per year, we found that the burden of typhoid fever was greatest among children between 5 and 20 years of age. Paratyphoid fever occurred most commonly in children and was infrequent in adults.
Enteric fever is a public health problem in North Jakarta with a substantial proportion due to paratyphoid fever. The results highlight the need for control strategies against enteric fever.

Full text

Original Article
Enteric fever burden in North Jakarta, Indonesia: a prospective, community-
based study
Narain H Punjabi1, Magdarina D Agtini2, R Leon Ochiai3, Cyrus H Simanjuntak1,2, Murad Lesmana1,6,
Decy Subekti1, Buhari A Oyofo1, Lorenz von Seidlein3, Jacqueline Deen3, Seonghye Shin3, Camilo
Acosta3, Ferry Wangsasaputra2, Sri P Pulungsih4, Santoso Saroso4, Suyeti Suyeti3, Suharno R2, Pratiwi
Sudarmono5, Agus Syarurachman5, Agus Suwandono2, Sumarjati Arjoso2, H. James Beecham III1,
Andrew L. Corwin1, John D. Clemens3
1U.S. Naval Medical Research Unit No. 2, Jakarta, Indonesia
2National Institute of Health Research and Development R.I, Jakarta, Indonesia
3International Vaccine Institute, Seoul, Korea
4Infectious Diseases Hospital Prof. Dr. Sulianti Saroso, Jakarta, Indonesia
5Microbiology Department, University of Indonesia, Jakarta, Indonesia
6Medical Faculty, Trisakti University, Jakarta, Indonesia
Abstract
Introduction: We undertook a prospective community-based study in North Jakarta, Indonesia, to determine the incidence, clinical
characteristics, seasonality, etiologic agent, and antimicrobial susceptibility pattern of enteric fever.
Methodology: Following a census, treatment centre-based surveillance for febrile illness was conducted for two-years. Clinical data and a
blood culture were obtained from each patient.
Results: In a population of 160,261, we detected 296 laboratory-confirmed enteric fever cases during the surveillance period, of which 221
(75%) were typhoid fever and 75 (25%) were paratyphoid fever. The overall incidence of typhoid and paratyphoid cases was 1.4, and 0.5
per thousand populations per year, respectively. Although the incidence of febrile episodes evaluated was highest among children under 5
years of age at 92.6 per thousand persons per year, we found that the burden of typhoid fever was greatest among children between 5 and 20
years of age. Paratyphoid fever occurred most commonly in children and was infrequent in adults.
Conclusion: Enteric fever is a public health problem in North Jakarta with a substantial proportion due to paratyphoid fever. The results
highlight the need for control strategies against enteric fever.
Key words: enteric fever; typhoid fever; paratyphoid fever; incidence
J Infect Dev Ctries 2013; 7(11):781-787. doi:10.3855/jidc.2629
(Received 15 March 2012 – Accepted 03 October 2012)
Copyright © 2013 Punjabi et al. This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
Introduction
We undertook a prospective study of enteric fever
in all age groups in North Jakarta, Indonesia. Previous
reports from Indonesia [1,2,3,4,5,6], including partial
results from this surveillance study [7,8], indicate that
enteric fever is an important public health problem in
the country. In this paper, we present the data from
two years of surveillance in North Jakarta on the
incidence and characteristics of enteric fever by
etiologic agent and by age group, as well as the
seasonality and antimicrobial susceptibility patterns of
the isolates. Such detailed information on burden of
disease is important to inform policy decisions
regarding disease control strategies.
Methodology
Study area and population
The study was conducted in an impoverished,
congested area of North Jakarta, where the average
annual income per person was US$ 689 in 2000 [9].
Water supply and sanitation is inadequate with only
57% to 65% of the population having access to tap
water [10]. Many residents use water from either a
communal tap or a local river for washing and buy
water from vendors for consumption. Many of the

Punjabi et al. – Enteric fever burden in North Jakarta J Infect Dev Ctries 2013; 7(11):781-787.
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houses are temporary structures with no toilets. There
is no separate sewage system for human waste
disposal in the area.
North Jakarta is divided into seven sub-districts
(kecamatans). The sub-districts of Tanjung Priok and
Koja were targeted for this surveillance study based on
the expected high incidence of enteric disease,
accessibility, and previous research experience in the
area [11]. The study also incorporated cholera and
shigellosis surveillance, the results of which have been
previously reported [12]. The total population
enumerated by a study census in 2001 was 160,261
individuals of whom 15,741 (10%) were younger than
60 months of age [13].
Health care system
The first-level health-care facility in Indonesia is a
primary health center or Puskesmas. There are 54
primary health centers in North Jakarta, 22 of which
are located in Tanjung Priok and Koja, equipped to
conduct preventive measures and treat mild diseases.
More severe conditions are referred to hospitals. The
Infectious Disease Hospital and Koja Hospital are the
main government referral hospitals in North Jakarta.
In 2001, there were 314 private practitioners, 36
polyclinics, 32 maternal clinics, and 29 small private
hospitals in the study area.
Surveillance procedures
The surveillance was conducted from August 2001
to July 2003. We invited patients of all age groups
residing in the study area and presenting to a
participating health-care provider (primary health
centers in the study area, the Infectious Disease
Hospital, and Koja Hospital) with fever for three days
or diarrhoea to join the surveillance. A blood culture
examination for Salmonella species was offered free
of charge. A blood sample (8-10 ml) blood was
collected from each adult participant with fever lasting
three days or longer and used to immediately inoculate
a culture bottle with 10% ox-gall media during the
initial phase of the study or Bactec plus F/Aerobic
bottle (BD Bactec system, Franklin Lakes, USA)
starting on the seventh month of the surveillance.
From children younger than 12 years of age with fever
of longer than three days, 3-5 ml ml of blood were
collected and immediately inoculated in a culture
bottle with 10% ox-gall solution during the initial
phase of the study or a Bactec Peds Plus bottle (BD
Bactec system, Franklin Lakes, USA) starting the
seventh month of the surveillance.
Treatment was provided in accordance with
national guidelines. The participants paid the regular
nominal visiting fee of about US$ 0.20 at the health
centers and US$ 0.30 at the hospitals. Periodic
meetings were held with representatives of all the
health centers and hospitals.
Laboratory procedures
The inoculated bottles were transported twice daily
to the U.S. Naval Medical Research Unit No. 2
laboratory and processed according to standard
procedures for the isolation and identification of
Salmonellae [6,14]. The bottles with 10% ox-gall
media were incubated at 37°C and sub-cultured onto
MacConkey and SS agar plates on days 1, 4, and 7.
The Bactec bottles were incubated in a Bactec
machine and when bacterial growth was detected, a
small aliquot of media was sub-cultured onto
MacConkey and Salmonella-Shigella (SS) agar plates
on days 1, 4 and 7. The MacConkey and SS agar
plates were incubated at 37°C for 18 to 24 hours. On
MacConkey agar, Salmonellae were identified as non-
lactose-fermenting smooth colonies. On SS agar,
Salmonellae were identified as non-lactose-producing,
non-fermenting colonies with a black center.
Suspected colonies were screened using Kligler’s iron
agar, motility indole ornithine, and citrate utilization
tests. Colonies giving biochemical reactions
suggestive of Salmonellae were confirmed
serologically by slide agglutination test with
polyvalent O Salmonella, specific O and Vi antisera
(Difco Laboratories, Franklin Lakes, USA).
The bacterial isolate was then tested by slide
agglutination test for H antigen factor d, a, b and c for
S. Typhi, S. Paratyphi A, S. Paratyphi B and S.
Paratyphi C, respectively. Unusual isolates were
confirmed by biochemical reactions in an API 20E
strip.
Antimicrobial susceptibility testing of S. Typhi and
S. Paratyphi against ampicillin,
trimethoprim/sulfamethoxazole, chloramphenicol,
tetracycline, ceftriaxone, cephalothin, ciprofloxacin
and nalidixic acid was conducted using standard
antimicrobial discs (Becton, Dickinson and Co.,
Sparks, USA) using the Kirby Bauer disc diffusion
method on Muller-Hinton agar [15]. Salmonella
isolates were verified at a reference laboratory,
Balitvet (Veterinarian Research Laboratory), Bogor,
Indonesia, and the University of Oxford, Wellcome
Trust Clinical Research Unit, Ho Chi Minh City,
Vietnam.

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Data management, definitions, and analysis
The case report forms were double-entered into a
custom-made data entry program using FoxPro
software (Microsoft, Seattle, USA). The data
management program included error, range, and
consistency check programs.
A fever episode was defined as a reported history
of fever. The onset was taken as the day on which
fever was reported to have begun. All fever episodes
regardless of duration with a positive culture for
Salmonellae were included in the analysis. Multiple
visits for fever within seven days by the same
individual was considered a single fever episode. A
typhoid and paratyphoid fever case was defined as
fever with isolation by blood culture of S. Typhi or S.
Paratyphi, respectively.
We estimated the annual incidence of fever
episodes, typhoid and paratyphoid fever cases using
the 2001 study census as the denominator, assuming
that each individual in the census contributed 24
months to the denominator and assuming a balance
between in- and out-migration during the surveillance
period. We used the age-specific number of fever
episodes, typhoid and paratyphoid fever cases among
the residents of the study area as the numerator. The
95% confidence intervals of the incidence were
calculated using an exact method based on the
binomial distribution [16]. Odds ratios were
calculated to compare individual characteristics
between typhoid and paratyphoid fever cases. All p-
values and 95% confidence intervals were interpreted
in a two-tailed fashion. Statistical significance was
designated as a p-value less than 0.05. Statistical
analyses were performed using Stata 7 (Stata
Corporation, College Station, USA) software.
Ethics
After the project’s purpose was explained,
patients, or in the case of minors, their parents or
guardians, gave verbal consent prior to participation in
the study. The study was approved by the Ethics
Committee of the Ministry of Health, Indonesia; the
Institutional Review Board, National Institute of
Health Research and Development, Ministry of
Health, Jakarta, Indonesia; the Institutional Review
Board, United States Naval Medical Research Unit No
2, Jakarta, Indonesia; and the Secretariat Committee
on Research Involving Human Subjects, World Health
Organization, Geneva, Switzerland
Results
During the surveillance period, there were 6,708
visits for fever at the participating treatment centers by
residents of the study area (Figure 1). After excluding
933 (14%) visits with no blood culture obtained, 5,775
(86%) fever episodes were included in the analysis.
Figure 1. Flow of patients visiting the participating treatment centers for fever in the North
Jakarta study site, 1 August 2001 to 31 July 2003

Punjabi et al. – Enteric fever burden in North Jakarta J Infect Dev Ctries 2013; 7(11):781-787.
784
Among the fever episodes, we detected 296 enteric
fever cases, of which 221 (74.66%) were typhoid fever
and 75 (25.34%) were paratyphoid fever. Of the latter
cases, 41 (54.67%) were due to S. Paratyphi A, 21
(28.00%) to S. Paratyphi B, and 13 (17.33%) to S.
Paratyphi C. Over the course of the two-year
surveillance period, typhoid or paratyphoid cases
occurred nearly all year round with no seasonal pattern
(Figure 2).
The overall incidence of detected fever episodes,
typhoid, and paratyphoid cases was 41.9, 1.4, and 0.5
per thousand populations per year, respectively (Table
1). The incidence of febrile episodes was highest
among young children. The burden of typhoid fever
was greatest among those 5 to 20 years old with 128
(58%) cases diagnosed in this age group. In children
under 2 years of age the incidence of paratyphoid
fever (2.4 per thousand per year; 95% CI 1.4 - 3.9)
was significantly higher than the incidence of typhoid
fever (0.1 per thousand per year; 95% CI 0.0 to 0.08).
We compared other characteristics between
typhoid and paratyphoid cases (Table 2). There was no
significant difference in clinical presentation except
for diarrhea, which was less frequently reported
among typhoid fever cases (8.6%) compared to
paratyphoid fever cases. Four cases required
hospitalization, all of which were typhoid fever cases.
In general, the S. Paratyphi isolates displayed
greater antimicrobial resistance than S. Typhi (Figure
3). The S. Typhi isolates showed emerging resistance
to ceftriaxone but remained susceptible to other
antimicrobial agents. Multi-resistant S. Typhi was not
isolated from the study site during the surveillance
period.
Discussion
Utilizing a passive surveillance program, we
detected an enteric fever annual incidence of about one
case per thousand populations per year, of which 25%
were paratyphoid. There has been an increasing trend,
or perhaps increasing recognition, of paratyphoid fever
in Indonesia [4,5,7,8], as well as in other parts of Asia
[7,8,17,18,19,20]. This emergence of paratyphoid
fever has been attributed to improved microbiologic
isolation methods, changes in the virulence of the
organism, shifts in herd immunity, and widespread
typhoid vaccination, but the true reason remains
unknown. In addition, our results are notable for the
detection of other S. Paratyphi B and C, since studies
in other sites have mainly detected S. Paratyphi A
[7,8,17,18,19,20].
Our reported incidence of typhoid and paratyphoid
fever probably underestimates the true burden of
disease. We used passive case detection and some of
the enteric fever patients in the study area may not
have used the treatment centers participating in the
surveillance and thus remained undetected. A study in
a Delhi slum utilizing active surveillance by visiting
homes twice weekly found typhoid fever incidence
among children under 5 years and those between 5 to
less than 20 years of age at 27 and 12 per thousand
populations per year, respectively [21]. Differences in
study methodology as well as the epidemiology of the
Figure 2. Number of culture-confirmed typhoid and paratyphoid
fever by month in the North Jakarta study site, 1 August 2001 to
31 July 2003
Figure 3. Antimicrobial resistance patterns of Salmonella
enterica serotype Typhi isolates (n = 221) and Salmonella
enterica serotype Paratyphi A isolates (n =41) in the North
Jakarta study site

Punjabi et al. – Enteric fever burden in North Jakarta J Infect Dev Ctries 2013; 7(11):781-787.
Table 1: Age-specific incidence (per 1,000 persons per year) of fever episodes and culture-confirmed typhoid fever and paratyphoid fever in the North Jakarta study site, 1 August
2001 to 31 July 2003
Age at illness
Population
Fever
episodes
Incidence of fever (95%
CI)
Typhoid
fever cases
Typhoid fever incidence
(95% CI)
Paratyphoid
fever cases
Paratyphoid fever
incidence (95% CI)
Under 5 years
15994
1926
120.4
(115.4, 125.6)
23
1.4
(0.9, 2.2)
20
1.3
(0.8, 1.9)
under 2 years
6959
1243
178.6
(169.7, 187.8)
1
0.1
(0, 0.8)
17
2.4
(1.4, 3.9)
2 to 4.9 years
9035
683
75.6
(70.2, 81.2)
22
2.4
(1.5, 3.7)
3
0.3
(0.1, 1)
5 to under 20 years
47378
2010
42.4
(40.6, 44.3)
128
2.7
(2.3, 3.2)
24
0.5
(0.3, 0.8)
5 to 9.9 years
14674
689
47.0
(43.5, 50.5)
36
2.5
(1.7, 3.4)
2
0.1
(0, 0.5)
10 to 19.9 years
32704
1321
40.4
(38.3, 42.6)
92
2.8
(2.3, 3.5)
22
0.7
(0.4, 1.0)
20 to under 40 years
63785
2059
32.3
(30.9, 33.7)
63
1.0
(0.8, 1.3)
24
0.4
(0.2, 0.6)
20 to 29.9 years
37182
1425
38.3
(36.4, 40.3)
54
1.5
(1.1, 1.9)
14
0.4
(0.2, 0.6)
30 to 39.9 years
26603
634
23.8
(22.0, 25.7)
9
0.3
(0.2, 0.6)
10
0.4
(0.2, 0.7)
40 years and older
33104
713
21.5
(20.0, 23.2)
7
0.2
(0.1, 0.4)
7
0.2
(0.1, 0.4)
40 to under 60 years
26905
540
20.1
(18.4, 21.8)
5
0.2
(0.1, 0.4)
6
0.2
(0.1, 0.5)
60 years and older
6199
173
27.9
(23.9, 32.3)
2
0.3
(0.1, 1.2)
1
0.2
(0, 0.9)
All ages (total)
160261
6708
41.9
(40.9, 42.9)
221
1.4
(1.2, 1.6)
75
0.5
(0.4, 0.6)
Table 2: Comparison of characteristics between the culture-confirmed typhoid and paratyphoid cases in the North Jakarta study site
Typhoid fever
n = 221
Paratyphoid fever
n = 75
P-value
OR
(95% CI) p-value
Mean (median; SD) age
16.5 ( 14.5 ; 10.1)
18.5 (16.4 ; 14.9)
0.3
1.0 ( 0.9,1.0)
No (%) female
107 (48.4)
37 (49.3)
0.9
1.0 ( 0.6,1.8)
No (%) with nausea
153 (69.2)
50 (66.7)
0.7
1.1( 0.6,2.0)
No (%) with vomiting
104 (47.1)
30 (40.0)
0.3
1.3 (0.8, 2.3)
No (%) with abdominal pain
12 (5.4)
5 (6.7)
0.7
0.8 (0.3, 2.4)
No (%) with constipation
18 (8.1)
5 (6.7)
0.7
1.2 ( 0.4, 3.5)
No (%) with diarrhea
19 (8.6)
38 (50.7)
<.0001
0.1 ( 0.1, 0.2)
No (%) with abdominal distention
29 (13.1)
8 (10.7)
0.6
1.3 (0.6, 2.9)
No (%) with abdominal tenderness
29 (13.1)
8 (10.7)
0.6
1.3 (0.6, 3.0)
No (%) referred for hospitalization
4 (1.8)
0
0.6
1.0 (0.9, 1.0)

Punjabi et al. – Enteric fever burden in North Jakarta J Infect Dev Ctries 2013; 7(11):781-787.
786
disease between the study sites probably account for
the lower incidence observed in Jakarta than in Delhi.
A study from Vietnam utilizing passive
surveillance showed a culture-confirmed typhoid fever
incidence similar to our findings: 3.6, 5.3, and 4.3 per
thousand populations per year among those 2 to under
5 years, between 5 to 9 years, and between 10 to 19
years, respectively [22].
A previously published study from Jakarta [4]
suggested that paratyphoid fever is predominantly
transmitted outside the household, in contrast to the in-
household transmission of typhoid fever. However,
we found that 18 enteric fever episodes in children
under 2 years of age were caused by paratyphoid
fever. This finding suggests possible transmission
within the household.
Four episodes of enteric fever required
hospitalization, all of which were typhoid cases. This
difference was not statistically significant and may
have been due to chance. Paratyphoid cases presented
significantly more frequently with diarrhea than
typhoid fever episodes. In general, however, the
clinical appearance of typhoid and paratyphoid cases
in our study was similar, indicating that the infections
could not be differentiated based on presenting signs
and symptoms. Surprisingly, the majority of isolates
from our study remain susceptible to antimicrobial
agents despite the ubiquitous availability of antibiotics
without prescription.
The age distribution of typhoid fever patients
suggests that children and young adults are at highest
risk for typhoid fever and should be targeted for
control strategies such as vaccination. None of the
licensed typhoid vaccines protect against paratyphoid
fever. However, a candidate paratyphoid vaccine
consisting of a modified O-specific polysaccharide of
its lipopolysaccharide conjugated to tetanus toxoid has
been developed and undergone Phase I and II trials in
Vietnamese adults and children [23]. This North
Jakarta study site could be a potential area for the
evaluation of paratyphoid vaccines.
In summary, enteric fever, both typhoid and
paratyphoid, is a problem in Jakarta. Our findings
highlight the need for control strategies against the
disease.
Acknowledgements
We are grateful to the residents of the North Jakarta study
site who made this work possible. We thank all technical
staff and research assistants associated with the study. We
acknowledge Jeremy Farrar, Camilo Acosta, and Claudia
Galindo for their respective contributions. Financial support
was provided by the Bill and Melinda Gates Foundation
through the Diseases of Most Impoverished Program
administered by the International Vaccine Institute, Seoul,
Korea.
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Corresponding author
Dr. Narain H. Punjabi
SOS Medika
Jakarta, Indonesia
Telephone: (62-21) 7506001, Fax (62-21) 7506002
Email: narainhp@yahoo.com
narainh@internationalsos.com
Conflict of interests: No conflict of interests is declared.