Campylobacter Infection in Children in Malawi Is
Common and Is Frequently Associated with Enteric Virus
Jenifer Mason1, Miren Iturriza-Gomara1, Sarah J. O’Brien1, Bagrey M. Ngwira2, Winifred Dove1,
Martin C. J. Maiden3, Nigel A. Cunliffe1*
1Institute of Infection and Global Health, University of Liverpool, Liverpool, United Kingdom, 2Department of Community Health, College of Medicine, University of
Malawi, Blantyre, Malawi, 3Department of Zoology, University of Oxford, Oxford, United Kingdom
Background: Campylobacter species are the most common cause of bacterial gastroenteritis in the developed world.
However, comparatively few studies have determined the epidemiological features of campylobacteriosis in resource-poor
Methods: A total of 1,941 faecal specimens collected from symptomatic (diarrhoeic) children and 507 specimens from
asymptomatic (non-diarrhoeic) children hospitalised in Blantyre, Malawi, between 1997 and 2007, and previously tested for
the presence of rotavirus and norovirus, was analysed for C. jejuni and C. coli using a real time PCR assay.
Results: Campylobacter species were detected in 415/1,941 (21%) of diarrhoeic children, with C. jejuni accounting for 85% of
all cases. The median age of children with Campylobacter infection was 11 months (range 0.1–55 months), and was
significantly higher than that for children with rotavirus and norovirus (6 months and 7 months respectively; P,0.001). Co-
infection with either rotavirus or norovirus was noted in 41% of all cases in the diarrhoeic group. In contrast, the detection
rate of Campylobacter in the non-diarrhoeic group was 14%, with viral co-infection identified in 16% of children with
Campylobacter. There was no association between Campylobacter detection rate and season over the 10 year period.
Discussion: Using molecular detection methodology in hospitalised Malawian children, we have demonstrated a high
prevalence of Campylobacter infection, with frequent viral co-infection. The burden of Campylobacter infection in young
African children may be greater than previously recognised.
Citation: Mason J, Iturriza-Gomara M, O’Brien SJ, Ngwira BM, Dove W, et al. (2013) Campylobacter Infection in Children in Malawi Is Common and Is Frequently
Associated with Enteric Virus Co-Infections. PLoS ONE 8(3): e59663. doi:10.1371/journal.pone.0059663
Editor: Georgina L. Hold, University of Aberdeen, United Kingdom
Received November 29, 2012; Accepted February 17, 2013; Published March 26, 2013
Copyright: ? 2013 Mason et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The study was funded by the University of Liverpool. The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: N.A.Cunliffe@liverpool.ac.uk
It is estimated that 3.552 million children under the age of five
years die each year in Africa; diarrhoeal disease accounts for 11%
of these deaths . Diarrhoea also contributes to childhood
morbidity, particularly malnutrition and growth stunting [2,3].
The introduction of intervention strategies, such as provision of
oral rehydration therapy, has had a positive impact on reducing
childhood diarrhoea mortality, with an estimated annual reduction
of diarrhoeal deaths in Africa since 2000 of 3.7% ; however
diarrhoea remains a leading cause of child mortality and morbidity
in this region. The importance of pathogens such as rotavirus and
enterotoxigenic Escherichia coli in the aetiology of severe childhood
diarrhoea in developing countries is well recognised [4,5].
However the role of Campylobacter is less well understood.
Campylobacter is a fastidious gram negative bacterium and C. jejuni
and C. coli are considered the most common cause of bacterial
gastroenteritis in the developed world. The clinical presentation
ranges from mild watery to severe inflammatory diarrhoea which
may be complicated by post infectious sequelae such as Guillain-
Barre ´ Syndrome . Using bacterial culture methodology,
estimates of the prevalence of Campylobacter infection in young
children with diarrhoea in Sub Saharan Africa range from 1.5% to
18% [7,8,9,10,11]. While molecular techniques have been
developed and employed for Campylobacter detection in epidemi-
ological studies in developed countries, such methods have not
been widely adopted in Sub Saharan Africa. Where molecular
detection (notably PCR) was used to examine for Campylobacter
species in adults and children with diarrhoea in South Africa the
prevalence estimates of C. jejuni, C. coli and C. concisus were 12%,
7.5% and 2.7% respectively; however only 34 of the 255 samples
analysed were from children ,5 years of age .
As part of a long-term research programme investigating viral
gastroenteritis in children in Malawi, we have collected stool
samples since 1997 from children ,5 years of age admitted to the
Queen Elizabeth Central Hospital (QECH), Blantyre, Malawi
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with moderate to severe diarrhoea . We have now examined
stored faecal specimens using a real time PCR assay to determine
the prevalence and epidemiological features of Campylobacter
infection in this population.
Written, informed consent was obtained from the child’s parent
or guardian prior to enrolment. Ethical approval was obtained
from the Malawi National Health Sciences Research Committee.
The QECH is a large government run tertiary referral hospital
in the southern Malawian city of Blantyre, which has a population
of approximately 1 million living in urban and peri-urban
Enrolment and data collection procedures have previously been
described in detail . Briefly, children age ,5 years admitted to
the QECH with $3 loose or watery stools within a 24 hour period
for ,14 days, were eligible for inclusion. Children were enrolled
Monday to Friday, 9 am to 5 pm, from 1stJuly 1997 to 30thJune
2007. A second group of children ,5 years of age without
diarrhoea, who were admitted to the QECH with conditions such
as malaria and respiratory infections, were enrolled between 1997
and 1999. A single faecal specimen was obtained from each child.
Clinical data (illness severity, blood in stools etc.) were not
routinely gathered. Following EIA testing for rotavirus ,
remaining samples were shipped to the University of Liverpool
and stored at 280uC until testing for norovirus by real time PCR
 and for Campylobacter (this study).
Of 2,458 faecal specimens collected from hospitalised diarrhoeic
children in the primary study , 1,941 were available for testing
for Campylobacter infection, together with 507 samples from
children admitted to hospital without diarrhoea. DNA was
extracted from all samples using an automated extractor
(Qiasymphony, Qiagen). The presence of a 95 base pair fragment
of the mapA gene of C. jejuni and a 103 base pair fragment of the
ceuE gene of C. coli were detected using a real time PCR method
Data were analysed using ‘‘IBM SPSS Statistics Data Editor’’
version 11. Categorical data were analysed using Chi2test and
continuous data using paired T-tests. A p-value of ,0.05 was
Characteristics of the Study Population
In total 2,448 samples was analysed; 1,941 from diarrhoeic
children and 507 from non-diarrhoeic children. The median age
of children in the diarrhoeic group was 9 months (range 0–55
months) and in the non-diarrhoeic group was 6 months (range 1–
50 months). The diarrhoeic group contained 55% males and the
non-diarrhoeic group 52% males.
Over the 10 year study period (1997–2007) Campylobacter was
detected in 415/1941 (21%) of diarrhoeic specimens. For the two
year period (1997–1999) in which faecal specimens from non-
diarrhoeic children were collected, the detection rate of Campylo-
bacter was significantly higher in the diarrhoeic specimens than the
non-diarrhoeic specimens (28% vs. 14%; p,0.001) (Table 1). Of
the Campylobacter species detected between 1997 and 1999, C. coli
comprised 10% and 4% of all Campylobacter from diarrhoeic and
non-diarrhoeic specimens respectively (p,0.001). There was no
statistical difference in the Campylobacter cycle threshold values
obtained from diarrhoeic vs. non-diarrhoeic specimens (data not
The median age of children with diarrhoea in whom
Campylobacter was detected was 11 months (range 0.1–55 months)
which was higher than the age of children with rotavirus or
norovirus (median age 6 months and 7 months respectively
(p,0.001)). The detection rate of Campylobacter was relatively
constant across all age groups, in contrast to the detection rate of
rotavirus and norovirus which decreased with age (Figure 1). The
median age of non-diarrhoeic children with Campylobacter infection
was 11 months (range 1–34 months); the detection rate increased
from 5% of children in the 0–2 month age group to 20% of
children age .18 months (Table 1).
In the diarrhoeic group 40% of children with Campylobacter had
an enteric virus co-infection. These co-infections occurred
predominantly in children ,1 year of age with 50% of all
Campylobacter cases in this age group also having either rotavirus or
norovirus in the specimen. In the non-diarrhoeic group 16% of
children with Campylobacter in the specimen also had a viral co-
infection (Table 1). Although the overall prevalence of Campylo-
bacter was significantly higher in the diarrhoeic than in the non-
diarrhoeic group, when single infections were considered (i.e. in
the absence of either rotavirus or norovirus) this difference is less
pronounced (Campylobacter detection rate of 16% in the diarrhoeic
vs. 11% in the non-diarrhoeic group, p=0.02).
The detection rate of Campylobacter did not vary consistently by
month or season of specimen collection during the 10 year study
period. In total 49% of Campylobacter positive specimens in the
diarrhoeic group occurred in the dry season (May to October) and
51% in the wet season (November to April). In the non-diarrhoeic
group 41% and 59% of positive specimens occurred in the dry and
wet season respectively (p=0.89; data not shown).
In this large study of Campylobacter infection in Malawian
children, using a sensitive molecular assay we documented
Campylobacter in 21% of specimens obtained from children ,5
years of age hospitalised with diarrhoea. There are no previous
data describing the prevalence of Campylobacter infection in Malawi.
Estimates of the prevalence of Campylobacter infection in hospital-
ised children ,5 years of age with diarrhoea in Sub Saharan
Africa range from 1.5% in Botswana , 1.7% in Mozambique
, 9% in Uganda , 11% in The Central African Republic 
to 18% in Tanzania . In community settings the detection rate
of Campylobacter in diarrhoeal faecal specimens among children ,5
years of age has been estimated at 15.9% in The Central African
Republic , 3.3% in Djibouti  and 0.8% in Guinea-Bissau
. This variation in detection rate across Sub Saharan Africa
may reflect the technical difficulties of isolating Campylobacter
Campylobacter Infection in Malawian Children
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species in resource poor settings because of its fastidious growth
requirements and/or the relative insensitivity of some culture
Comparing culture and PCR in the detection of C. jejuni and C.
coli in diarrhoeal faecal specimens in Ireland suggested that culture
alone detected only 55% of all cases . In the UK, Campylobacter
detection rates in community diarrhoea cases increased from 4.0%
by direct culture, to 5.0% after a faecal enrichment procedure was
added, to 15% by PCR . A study in South Africa of 255 adults
and children with diarrhoea and 67 children without diarrhoea,
demonstrated similar overall rates of Campylobacter using PCR to
those reported in the current Malawi study (19.6% in symptomatic
patients and 11% in asymptomatic patients) ; however the
prevalence in children ,5 years of age with diarrhoea was 11%
compared with 21% in the current study. Thus our data suggest
that the detection rate of C. jejuni and C. coli using a sensitive and
specific PCR assay in faecal specimens of children ,5 years of age
hospitalised with diarrhoea in Sub Saharan Africa may be higher
than previously reported.
Of note, we documented a relative over-representation of C. coli
compared with C. jejuni in the faecal specimens of diarrhoeic
compared with non-diarrhoeic children. A similar pattern was
reported in Tanzania where C. coli was present in 20% of
diarrhoeic and 6% of non-diarrhoeic specimens from adults and
Figure 1. Age distribution of Campylobacter, rotavirus and norovirus infections in Malawian children with acute diarrhoea, 1997–
Table 1. Age Distribution of Campylobacter infection.
Age Group TotalCampylobacter positive Campylobacter+ +virusCampylobacter alone
Diarrhoeic (1997–2007)0–2 months156 31 (20%) 20 (13%) 11 (7%)
3–5 months 41283 (20%)43 (10%) 40 (10%)
6–11 months 673153 (23%) 70 (10%)83 (12%)
12–17 months418 82 (20%)28 (7%) 54 (13%)
.18 months282 66 (23%)7 (2%) 59 (21%)
Total : 1997–1999738 206 (28%) 87 (12%) 119 (16%)
Total: 1997–2007 1941 415 (21%) 168 (9%)247 (13%)
Non-diarrhoeic (1997–1999) 0–2 months140 7 (5%)0 7 (5%)
3–5 months 10414 (13%)0 14 (13%)
6–11 months 81 15 (19%)6 (7%) 9 (11%)
12–17 months 8012 (15%) 2 (3%) 10 (13%)
.18 months102 21(21%)3 (3%) 18 (18%)
Total: 1997–1999507 69 (14%) 11 (2%)58 (11%)
x2(Diarrhoeic vs. non-
35.7 38.3 5.4
Campylobacter Infection in Malawian Children
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children . In the developed world C. coli is particularly
associated with chicken  and the over-representation of C. coli
in children with diarrhoea raises the possibility that poultry may be
a particularly important source of infection in this group.
Campylobacter spp. other than C. jejuni and C. coli, which require
either non-selective culture or specific molecular techniques for
their optimal detection, are reported to be common in some
studies. For example in South Africa C. concisus and C. upsaliensis
accounted for 23%, and C. coli for 3%, of all Campylobacter and
related species isolated  and in Ireland using PCR C. ureolyticus
accounted for 22.3% of all Campylobacter species detected .
Although both C. jejuni and C. coli were commonly detected among
hospitalised Malawian children with diarrhoea, the contribution of
other Campylobacter species has not yet been determined.
The prevalence of Campylobacter remained relatively constant in
children up to 5 years of age in the current study suggesting that
unlike viral infections, Campylobacter may make a relatively greater
contribution to diarrhoeal disease in children aged .12 months. It
is possible that repeated exposure to Campylobacter species from
environmental sources throughout childhood may explain the
relatively high prevalence in children .1 year of age; however
further clinical, epidemiological, and immunological studies are
required to confirm the sources of transmission, environmental
reservoirs and the role of Campylobacter infection in diarrhoeal
disease in this setting. Where detailed age related prevalence rates
have been determined in children in Sub Saharan Africa similar
patterns have been observed, for example a large cohort study in
The Central African Republic reported an average Campylobacter
detection rate of 9.5% across all age groups . Although deaths
in children secondary to diarrhoea are decreasing worldwide,
diarrhoea morbidity remains constant, particularly in older
children . Given the association of childhood diarrhoea with
growth stunting in this population  the contribution of
Campylobacter to the burden of diarrhoeal disease children .1 year
of age requires further elucidation.
A significant proportion of diarrhoeal specimens in which
Campylobacter was detected also contained norovirus or rotavirus,
particularly in children ,12 months of age. Given the high
prevalence of Campylobacter in non-diarrhoeic specimens, its
detection in diarrhoeic specimens may represent ‘‘flushing out’’
of organisms in diarrhoeal episodes caused by a viral pathogen.
We do not have data on the presence of other bacterial or parasitic
organisms. We are therefore unable to ascertain which, if any,
pathogen is the causative agent of the diarrhoeal episode, although
we speculate that Campylobacter when detected alone in older
children may be more likely to be the causative agent of disease.
Furthermore, although there was a significant difference in the
rate of detection of Campylobacter in isolation between the
diarrhoeic and non-diarrhoeic groups (16% vs. 11% respectively),
further case control studies are required to confirm this finding.
Mixed infections involving Campylobacter have been described
previously; one large (n=3,038) surveillance study of diarrhoea in
hospitalised children ,5 years of age in Bangladesh reported that
59% of all Campylobacter infections were associated with at least one
other bacterial or protozoan pathogen . Few studies have
reported mixed infections of Campylobacter and viral pathogens; a
cohort study in India demonstrated that rotavirus was associated
with 11/18 Campylobacter infections in children ,5 years of age
. Since data from in-vitro cell culture systems suggest that viral
co-infection increases the adhesion and invasion of pathogenic
Campylobacter species , further work should explore the clinical
consequences of co-infection with viral enteric pathogens on the
pathogenesis of Campylobacter infection.
Campylobacter was detected in 14% of non-diarrhoeic children
who were recruited over a two-year period. Since no preceding
clinical or microbiological data are available for these children, we
are unable to determine whether this finding represents asymp-
tomatic colonisation or extended excretion after resolution of a
Campylobacter diarrhoeal episode. Asymptomatic colonisation ap-
pears to occur frequently in children in Sub Saharan Africa; one
longitudinal study reported that 41.7% of all children in a
community birth cohort were asymptomatically colonised with
Campylobacter within the first 6 months of life . This
phenomenon does not appear to occur in the developed world
with the exception of workers occupationally exposed to Campylo-
bacter . It is thought that regular exposure to Campylobacter
within an abattoir or farm environment results in immune
tolerance towards Campylobacter species and hence facilitates
colonisation . It is feasible that a similar response occurs in
children in Sub Saharan Africa explaining the observed high rates
of asymptomatic infection. Given the high sensitivity and
specificity of the assay used in this study it is also possible that
the detection rates seen in the control cohort could represent post
excretion following a diarrhoeal episode as Campylobacter is known
to be excreted for up to 12 weeks post infection .
This study highlights specific differences in the epidemiology of
Campylobacter in developed compared to developing countries.
Firstly, in the UK, the detection rate of Campylobacter in children
with and without diarrhoea is less than that seen in children in Sub
Saharan Africa (6.8% and 2% in diarrhoeal and non-diarrhoeal
children in the UK respectively) ; secondly, there are age
specific differences in detection rates in children in the UK with
prevalence increasing throughout childhood ; and lastly there
is a strong seasonal association in temperate climates with a peak
in incidence occurring during the warmer months whereas no
seasonal association was seen in Malawi . These differences
may be explained by a number of factors including differences in
the routes of transmission between the two settings; in the
developed world the majority of Campylobacter strains causing
human infections can be epidemiologically linked to strains that
colonise poultry, with the main route of transmission of the
pathogen thought to be through the handling and consumption of
contaminated meat . Although there are no comparative
epidemiological studies linking poultry and human strains in Sub
Saharan Africa, up to 40% of commercial chickens in Senegal and
60% in South Africa are colonised with Campylobacter [33,34].
Furthermore, strains colonising chickens in Senegal are genetically
similar to strains colonising chickens in the UK, The Netherlands
and United States suggesting that the host association of
Campylobacter genotypes transcends geographical boundaries .
Chicken is a widely consumed meat in Malawi and many families
keep chicken flocks which are routinely housed within the human
dwelling including in food preparation areas . Thus in contrast
to the developed world, there is increased potential for acquisition
and spread of zoonotic and foodborne disease such as Campylobacter
which may account for the higher prevalence rates reported in this
and other studies.
In conclusion, this large study of children hospitalised with
diarrhoea in Malawi suggests that the burden of Campylobacter is
higher than previously appreciated, and is frequently identified in
association with concomitant rotavirus and/or norovirus infection.
Given the recent introduction of rotavirus vaccines into childhood
immunisation programmes in Malawi and other parts of Sub
Saharan Africa it is predicted that bacterial pathogens including
Campylobacter could play a more prominent role in the aetiology of
diarrhoeal disease in young children in this region in the future.
An improved understanding of the clinical features, epidemiology,
Campylobacter Infection in Malawian Children
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and pathogenesis of Campylobacter infection in Sub Saharan Africa Download full-text
will inform future prevention strategies against this foodborne
Dr. Jenifer Mason is a National Institute for Health Research (NIHR)
Academic Clinical Fellow in Medical Microbiology.
Conceived and designed the experiments: NC MIG BN JM. Performed the
experiments: WD JM. Analyzed the data: JM MIG WD NC SOB.
Contributed reagents/materials/analysis tools: BN NC MIG. Wrote the
paper: JM MIG SOB MM NC.
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