Schwarz et al. BMC Infectious Diseases 2010, 10:319http://www.biomedcentral.com/1471-2334/10/319
Systemic bacteraemia in children presenting
with clinical pneumonia and the impact of
non-typhoid salmonella (NTS)Norbert G Schwarz1*, Nimako Sarpong2, Frank Hünger2, Florian Marks3, Samuel EK Acquah2, Alex Agyekum2,Bernard Nkrumah2, Wibke Loag1, Ralf M Hagen1, Jennifer A Evans4, Denise Dekker2, Julius N Fobil1,Christian G Meyer1, Jürgen May1, Yaw Adu-Sarkodie5
Background: The diagnosis and antimicrobial treatment of pneumonia in African children in the absence ofdiagnostic means such as x-ray facilities or microbiological laboratories relies primarily on clinical symptomspresented by the patients. In order to assess the spectrum of bacterial pathogens, blood cultures were performedin children fulfilling the clinical criteria of pneumonia.
Methods: In total, 1032 blood cultures were taken from children between 2 months and 5 years of age who wereadmitted to a rural hospital in Ghana between September 2007 and July 2009. Pneumonia was diagnosed clinicallyand according to WHO criteria classified as “non-severe pneumonia” and “severe pneumonia” ("severe pneumonia”includes the WHO categories “severe pneumonia” and “very severe pneumonia”).
Results: The proportion of bacteriaemia with non-typhoid salmonella (NTS) was similar in children with pneumonia(16/173, 9.2%) compared to children hospitalized for other reasons (112/859, 13%). NTS were the predominantorganisms isolated from children with clinical pneumonia and significantly more frequent than Streptococcuspneumoniae (8/173, 4.6%). Nine percent (9/101) of children presenting with severe pneumonia and 10% (7/72) ofchildren with non-severe pneumonia were infected with NTS. Nineteen out of 123 NTS isolates (15%) weresusceptible to aminopenicillins (amoxycillin/ampicillin), 23/127 (18%) to chlorampenicol, and 23/98 (23%) to co-trimoxazole. All NTS isolates were sensitive to ceftriaxone and ciprofloxacin.
Conclusion: In Sub-saharan Africa, sepsis with NTS should be considered in children with symptoms of pneumoniaand aminopenicillins might often not be the adequate drugs for treatment.
the commonly suspected organisms (e.g. Streptococcus
Pneumonia is one of the most common diagnoses in
pneumoniae and Haemophilus influenzae) . However,
African children presenting at hospitals and peripheral
this treatment scheme does not capture enteric bacteria
health centres and is the most important cause of mor-
and there is some evidence that Gram-negative bacteria
tality in children under five years of age [1,2]. Due to
such as Salmonella spp. occur more frequently among
the lack of bacteriological laboratory facilities, antibiotic
African children with septic pneumonia than expected.
treatment of pneumonia is guided by presumptions
Among 166 Kenyan children with blood cultures posi-
based on clinical symptoms. According to the WHO-
tive for non-typhoidal salmonella (NTS), 46% fulfilled
IMCI (World Health Organisation Integrated Manage-
the clinical criteria of pneumonia according to WHO-
ment of Childhood Illness) amoxicillin is the first line
IMCI. On the other hand, bacteraemia due to NTS was
drug for empirical treatment of pneumonia as it covers
not associated with diarrhoea . In other reports fromEast, West and Central Africa, the impact of NTS insystemic infections was recognized as well [5-16]. More-
* Correspondence: email@example.com
1Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
over, NTS were among the most frequent organisms
Full list of author information is available at the end of the article
2010 Schwarz et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative CommonsAttribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction inany medium, provided the original work is properly cited.
Schwarz et al. BMC Infectious Diseases 2010, 10:319
isolated from children with clinical pneumonia in some
definitions for “very severe pneumonia” and “severe
studies that were carried out before the vaccination
against H. influenzae (Hib-vaccination) was introduced[14,17-19]. In the context of an improving coverage of
Hib and pneumococcal immunisations, the impact of
1-3 ml of venous blood was taken from hospitalized
NTS as a cause of pneumonia will, most likely, increase
children and directly injected into a Becton Dickinson
considerably among African children .
(BD) BACTEC™ PEDS PLUS™/F bottle containing 20 ml
In the present study, blood cultures were performed in
of enriched broth with resin. The bottles were incubated
children admitted to a rural hospital with pneumonia
at 35°C in a BD BACTEC™ 9050 automated Blood Cul-
symptoms according to the WHO-IMCI definition in
ture system (BD Diagnostics, Sparks, Massachussets,
order to quantify the impact of systemic infections with
USA)  for 5 days or until rated positive. Broth from
NTS and to assess antibiotic drug resistance patterns.
positive bottles was directly examined by Gram stainand 20 μl were cultured further on sheep blood-agar,
chocolate-agar and MacConkey agar (prepared in-house
from Oxoid dehydrated media). Agar plates were incu-
The study hospital is located in the village Agogo in the
bated at 37°C for 18-24 h. Microscopical diagnosis after
Asante Akim North District of the Ashanti Region in
Gram staining was immediately reported to the clinical
Ghana, West Africa, and is the principal hospital of the
staff. Identification of S. pneumoniae was based on mor-
district. Its catchment population encompasses approxi-
phology of colonies and the optochin test. Oxacillin
mately 80,000 people with roughly 25,000 citizens of
discs were used to determine sensitivity to penicillin.
Agogo itself. The HIV/AIDS prevalence in the area is
Diphteroids and propionibacteriae were classified as
around 1.9% according to the National AIDS Control
contaminants. If the patient was not known to be HIV
Programme in 2009. Vaccination programmes against
positive, coagulase negative staphylococci, bacillus spe-
H. influenzae have been established in 2001.
cies and non-fermenters were usually also classified ascontaminants. On the same day, antibiotic susceptibility
testing was performed using the disc diffusion method
Between September 2007 and July 2009, 948 children
with the susceptibility breakpoints suggested by the
between 2 months and 5 years of age who were hospita-
Clinical and Laboratory Standards Institute (CLSI). The
lized and from whom a blood culture was taken were
following antibiotics were tested: amoxycillin/ampicillin,
included into the study. In total, 1032 blood cultures
amoxyclav (amoxicillin & clavulanic acid), cefuroxime,
were taken during 1169 hospitalizations. The study
ceftriaxone, co-trimoxazole, ciprofloxacin, gentamicin,
complied with the “Ethical Principles for Medical
tetracycline and chloramphenicol. The microbiological
Research Involving Human Subjects” as laid out in the
laboratory that was involved in the study is enrolled in a
Declaration of Helsinki and was approved by the Com-
quarterly external quality assurance program in bacter-
mittee on Human Research Publications and Ethics
iology from the National Institute for Communicable
(CHRPE) of the School of Medical Sciences, Kumasi,
Diseases (NICD) of South Africa. If blood cultures that
Ghana. Informed consent was sought from the parents
were taken from the same child presenting twice within
or the guardians of the child after detailed explanation
2 weeks yielded identical results, only the first result
of the study and the study procedures.
Pneumonia was classified following established WHO
At admission of children, clinical data were recorded on
guidelines . Children with cough or difficult breath-
standardized forms. Data collection was entirely
ing were classified as “pneumonia cases” if they had an
embedded into the clinical routine. The admission chart
increased respiratory rate of ≥ 50 per minute in children
contained a 4-paged admission sheet to be filled in by
of 2 months up to 11 months of age and ≥ 40 per min-
the admitting doctor. Double data entry was done by
ute in children of 12 months up to 5 years of age. Chil-
data entry clerks using a 4th Dimension Database (4D
dren with symptoms of lower chest wall indrawing,
San Jose, California, United States). Data analysis was
nasal flaring, grunting (in young children) and/or sub-
carried out using the STATA 10 software (College Sta-
costal retraction or additional signs of central cyanosis,
severe respiratory distress, vomiting everything or inabil-
For each pathogen, the number of isolates and their
ity to breastfeed/drink, or other danger signs were clas-
proportion among all blood cultures performed was cal-
sified as “severe pneumonia” (including the WHO
culated separately for children fulfilling the case
Schwarz et al. BMC Infectious Diseases 2010, 10:319
definition for pneumonia, severe pneumonia and for
co-infection was found in 35% of non-cases, 28% of
pneumonia cases and 22% of severe pneumonia cases.
In patients without pneumonia, NTS represented
66.7% (112/168), S. aureus 10.1% (17/168), S. pneumo-
Of the 1032 blood cultures included, 734 (71%) did not
niae 7.1% (12/168) and S. Typhi 6.5% (11/168) of the
yield bacterial growth and 90 (9%) were positive with
pathogen isolates. In non-severe pneumonia cases NTS
non-pathogenic microorganisms (contaminants).
represented 53.8% (7/13), S. aureus 7.7% (1/13), S. pneu-
Pathogens were isolated from the remaining 208 (20%)
moniae 15.4% (2/13) and S. Typhi 7.7% (1/13) of the
blood cultures. Antiobiotic pre-medication was
pathogen isolates. In severe pneumonia cases NTS
reported from 7% of children and was independent of
represented 33.3% (9/27), S. aureus 14.8% (4/27),
the positivity of blood cultures. The frequency of chil-
S. pneumoniae 22.2% (6/27) and S. Typhi 11.1% (3/27)
dren without pneumonia (12.2%), pneumonia cases
of the pathogen isolates. When looking at all pneumonia
(8.9%) and severe pneumonia cases (9.8%), was similar
cases of any severity, 16 of 40 (40%) of all pathogen iso-
in children with available and with missing blood cul-
In total, 173 children fulfilled the case definition of
pneumonia of any severity. Blood cultures were positive
All NTS and S. pneumoniae isolates from children aged
in 18.1% (13/72) of children with non-severe pneumonia
2 months to 5 years were included for sensitivity testing
and in 26.7% (27/101) of children with severe pneumo-
against 9 antibiotics irrespective of their clinical diagno-
nia. The frequency of bacteraemia was similar high in
sis (Table 2). 15% of all NTS isolates were sensitive
the 859 children without pneumonia (168/859, 19.6%).
to aminopenicillins (amoxycillin/ampicillin), 18% to
Ten children with severe pneumonia died: 2 children
chloramphenicol, 23% to co-trimoxazole, and 71% to
with a systemic NTS infection (1 with aminopenicillin
gentamicin. All isolates of NTS were susceptible to cef-
resistant strains), 3 with S. pneumoniae bacteraemia, 1
triaxone and ciprofloxacin. The frequency of multidrug
with S. Typhi, and 4 with negative blood cultures. Fatal-
resistance (MDR, resistance against amoxycillin, chlor-
ities were not observed among the patients with non-
amphenicol, and co-trimoxazole) was 75.5% (74/98).
Among all children with and without bacteraemia,
24% and 34% were positive for malaria parasites, respec-
In the present study, non-typhoid salmonella (NTS)
tively. Children with NTS bacteraemia had more often a
were found in 10% of the blood cultures and were the
co-infection with malaria parasites (24%) compared to
predominant cause of bacteraemia in hospitalized chil-
those with S. pneumoniae bacteraemia (18%). Malaria
dren. This prevalence is, most likely, underestimated
Table 1 Blood culture results in children between 2 months and 5 years of age
* Pneumonia cases according to WHO-IMCI definition. Agogo Presbyterian Hospital 09/2007-07/2009# Severe pneumonia included the WHO definitions for “very severe pneumonia” and “severe pneumonia”
Schwarz et al. BMC Infectious Diseases 2010, 10:319
Table 2 Proportion susceptible to antibiotics among NTS
Republic of Congo , Malawi [8,25], The Gambia
[26,27] and Kenya . A study from Tanzania has
demonstrated strong association of antimicrobial resis-
tance with fatal courses of children with bloodstream
infections . Fifteen years ago, no resistance to chlor-
amphenicol and 57% resistance to ampicillin was
reported in NTS collected from children in Accra,
Ghana . A more recent study from Accra found
MDR in 87% of Salmonella serogroup B isolates . In
Northern Ghana, among 6 isolates of Salmonella spp.
from children with diarrhoea, only one was resistant to
ampicillin and chloramphenicol . This demonstrates
that marked local and temporal differences of antibiotic
resistance patterns of NTS exist .
Ceftriaxone or ciprofloxacin may be appropriate alter-
natives to treat bacterial infections causing pneumonia
*Blood cultures from children aged 2 months to 5 years of age. Agogo
in areas with prevalences of NTS. Notably, 50% of the
pneumococcal isolates were resistant to ciprofloxacin inthe present study compared to only 4% of all pneumo-
due to the small blood volumes that were available in
coccal and NTS isolates in 1997 . However, the use
the paediatric patients and the frequent self-medication
of ceftriaxone in low-resource countries has consider-
with antibiotics prior to blood sampling. It has been
able disadvantages which have to be considered: (i) the
reported that the sensitivity of blood cultures fell by
drug has to be adminstered intravenously or intramus-
almost one third if a blood volume of 1 ml was inocu-
cularly; (ii) well trained staff is necessary; (iii) uncritical
lated to blood culture bottles compared to a volume of
use may promote the development of resistance; (iv) cef-
triaxone is approximately 3 to 10 times more expensive
The frequency of NTS was similar among children
with pneumonia and those without pneumonia and itcannot be determined whether bacteraemia due to NTS
is the exclusive cause of pneumonia or predisposes to
Aminopenicillins may often not be adequate for the
secondary infections with other microorganisms. How-
treatment of children presenting with pneumonia symp-
ever, from a practical point of view this may be irrele-
toms in Sub-saharan Africa and NTS in children with
vant: if NTS occur frequently among children with
pneumonia should strongly be considered as possible
severe respiratory symptoms, empirical treatment of
infectious agent. The development of alternative drugs
pneumonia must include coverage of NTS.
and, best, vaccines against NTS as well as appropriate
In Africa, aminopenicillins or co-trimoxazole are cur-
surveillance of this neglected infectious disease is
rently recommended for empirical treatment of commu-
nity-acquired pneumonia in children, assuming that themost frequent causal infectious organisms are S. pneu-moniae and H. influenzae. The IMCI-WHO guidelines
recommend treating non-severe pneumonia with cotri-
We thank the chirdren and their parents for their participation in this study.
We are also grateful for the continuous endeavours of fieldworkers and
moxazole or amoxicillin given orally, severe pneumonia
interviewers of the Kumasi Centre for Collaborative Research in Tropical
with oral amoxicillin or injectable penicillin and very
Medicine (KCCR), and to the staff of the Public Health Unit of the Agogo
severe pneumonia with injectable ampicillin plus inject-
Presbyterian Hospital for their collaboration. We gratefully acknowledge thefinancial support received from a Swiss Foundation. The findings and
conclusions in this paper are those of the authors and do not necessarily
Empirical treatment of childhood pneumonia with the
represent the views of any of their affiliated Research Institutions.
aforementioned first line drugs may readily fail due to
the high frequency of drug resistance of NTS . In
1Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany. 2Kumasi
the present study, only 15.5%, 23.5% and 70.9% of NTS
Centre for Collaborative Research in Tropical Medicine, Kumasi, Ghana.
isolates were sensitive to aminopenicillins, co-trimoxa-
International Vaccine Institute, Seoul, South Korea. 4University Hospital of
Wales, Cardiff, UK. 5School of Medical Sciences, Kwame Nkrumah University
zole and gentamicin, respectively. Multi-drug resistance
of Science and Technology, Kumasi, Ghana.
against the three standard drugs amoxicillin, chloram-
phenicol and co-trimoxazole was 75.5%. High levels of
Authors contribution: JM, CGM, JAE, and YAS planned and initiated the
MDR have also been reported from the Democratic
study. NS organised the day-to-day work as study coordinator. FH planned
Schwarz et al. BMC Infectious Diseases 2010, 10:319
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Cite this article as: Schwarz et al.: Systemic bacteraemia in children
17. Berkley JA, Maitland K, Mwangi I, Ngetsa C, Mwarumba S, Lowe BS,
presenting with clinical pneumonia and the impact of non-typhoid
Newton CR, Marsh K, Scott JA, English M: Use of clinical syndromes to
salmonella (NTS). BMC Infectious Diseases 2010 10:319.
target antibiotic prescribing in seriously ill children in malaria endemicarea: observational study. BMJ (Clinical research ed 2005, 330(7498):995.
PDM: WS 2.2 (Day 1) Finding Maxima & Minima Values Directions: In 1 – 4 write the solutions in “interval notation”. 1. Using y = -x2 + x + 4 identify the minimum value ______________, maximum value ________________ and range ____________________. 2. What is the maximum value _________________, minimum value ______________ and 3. What is the minimum value _________________
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