www.thelancet.com/infection Vol 9 February 2009
Staphylococcus aureus disease and drug resistance in
resource-limited countries in south and east Asia
Emma K Nickerson, T Eoin West, Nicholas P Day, Sharon J Peacock
By contrast with high-income countries, Staphylococcus aureus disease ranks low on the public-health agenda in low-
income countries. We undertook a literature review of S aureus disease in resource-limited countries in south and
east Asia, and found that its neglected status as a developing world pathogen does not equate with low rates of
disease. The incidence of the disease seems to be highest in neonates, its range of clinical manifestations is as broad
as that seen in other settings, and the mortality rate associated with serious S aureus infection, such as bacteraemia,
is as high as 50%. The prevalence of meticillin-resistant S aureus (MRSA) infection across much of resource-limited
Asia is largely unknown. Antibiotic drugs are readily and widely available from pharmacists in most parts of Asia,
where ease of purchase and frequent self-medication are likely to be major drivers in the emergence of drug resistance.
In our global culture, the epidemiology of important drug-resistant pathogens in resource-limited countries is
inextricably linked with the health of both developing and developed communities. An initiative is needed to raise the
profi le of S aureus disease in developing countries, and to defi ne a programme of research to fi nd practical solutions
to the health-care challenges posed by this important global pathogen.
S aureus disease in low-income countries is perceived as
trivial in terms of morbidity and mortality compared with
other infectious diseases such as malaria, tuberculosis,
and HIV infection. On closer inspection, however, the
neglected status of S aureus as a developing world
pathogen does not equate with low rates of disease. This
view is based on an assessment of the growing body of
literature on S aureus disease that originates from low-
income and lower-middle income countries in south and
east Asia, consisting in large part of retrospective studies
or case reports but also including several recent
The dissemination of meticillin-resistant S aureus
(MRSA) across low-income regions would have major
implications for the antibiotic treatment and outcome of
serious S aureus disease. MRSA infection is likely to go
unnoticed in these regions because of the widespread
lack of diagnostic microbiology facilities; thus, the
probability of ineff ective antibiotic prescribing and poor
outcome will inevitably increase. As elsewhere in the
world, serious MRSA infection in Asia requires treatment
with glycopeptides, but these expensive antibiotics are of
limited availability across low-income settings and
require administration by
Furthermore, optimum glycopeptide dosing requires
monitoring of serum drug concentrations, a capability
that is usually absent. Despite its perceived importance
and the large volume of research devoted to its study
across the developed world, almost nothing is known
about the emergence and transmission of MRSA in
resource-poor regions of the world.
We describe the features of S aureus disease and drug
resistance in resource-limited countries in south and east
Asia, and compare and contrast these features with those
in developed countries,
knowledge gaps for future research. Asia is the world’s
largest and most populated continent, consisting of a
patchwork of developed and developing countries in
close proximity. The study of this region, therefore, serves
as a useful proxy for understanding staphylococcal
disease worldwide. The resource-limited countries
included in this Review are those classifi ed by the World
Bank as being low-income or lower-middle income on
the basis of gross national income (GNI) per head.1 The
countries included are Afghanistan, Bangladesh, Bhutan,
Burma, Cambodia, China, India, Indonesia, Laos,
Maldives, Mongolia, Nepal, North Korea, Pakistan,
Philippines, Sri Lanka, Thailand, Timor-Leste, and
Vietnam. Together, the 3·37 billion inhabitants of these
countries comprise more than half the world’s population
and account for over 70% of the 4·73 billion people
worldwide who live in resource-limited areas.2 The
relative lack of published S aureus research from our
target resource-limited countries compared with
resource-rich countries around the world is highlighted
in the fi gure.
Epidemiology and risk factors for S aureus
Several recent studies have identifi ed S aureus as a major
bacterial pathogen in resource-limited regions of Asia. A
study at a provincial 1000-bed hospital in northeast
Thailand showed that S aureus was the third most
common cause of bacteraemia (after Escherichia coli and
Burkholderia pseudomallei), and was associated with a
mortality rate of 48%.3 Unselected patients of all ages
were included in this study, and a striking feature was
that S aureus disease was most common in neonates
(25% of all cases).3 This trend was also seen in the fi rst
reported blood culture study from Laos, in which S aureus
was the most common cause of bacteraemia in children
under 1 year of age.4 From an examination of additional
research of S aureus disease that included patients of all
ages,5–16 three studies confi rmed this observation.5,6,11
These fi ndings contrast with age-specifi c rates of invasive
Lancet Infect Dis 2009;
Medicine Research Unit,
Faculty of Tropical Medicine,
Mahidol University, Bangkok,
Thailand (E K Nickerson MRCP,
Prof N P Day DM,
S J Peacock PhD); Centre for
Clinical Vaccinology and
Tropical Medicine, Nuffi eld
Department of Clinical
Medicine, University of Oxford,
Churchill Hospital, Oxford, UK
(E K Nickerson, N P Day,
S J Peacock); and Department of
Medicine, Harborview Medical
Center, University of
Washington, Seattle, WA, USA
(T E West MD)
Dr Emma Nickerson,
Medicine Research Unit,
3rd Floor, 60th Anniversary
420/6 Rajvithi Road, Bangkok,
www.thelancet.com/infection Vol 9 February 2009 131
S aureus disease in high-income countries, where the
disease has been reported to either increase with age17,18
or to reach a maximum incidence at the extremes of
age.19–21 However, S aureus infection might also occur at a
higher frequency than that reported in elderly people in
resource-poor regions of Asia; it is possible that a
reporting bias or age-related diff erences in the pattern of
hospital referral or admission has resulted in under-
representation of disease in this group. Alternatively,
there might be increased availability or use of
microbiology facilities in hospitals with neonatal care
units, resulting in over-representation of neonates.
Accurately defi ning the epidemiology of staphylococcal
infection in many developing countries is hampered by
substantial variability in medical care, inadequate
diagnostic microbiology facilities, and lack of published
Risk factors for S aureus disease in resource-rich
countries include nasal carriage, presence of invasive
devices, surgical procedures, and for MRSA, hospital
admission and antibiotic exposure.17,22–25 In resource-
limited countries in Asia, medical devices or procedures
and previous antibiotic exposure have been identifi ed as
risk factors for the development of nosocomial S aureus
infection,26–33 but hospital admission as a risk factor for
MRSA colonisation and infection has been the subject of
very few published studies.7,29 Available data, including
some limited molecular typing of MRSA strains, link
MRSA with the hospital setting in these regions. Risk
factors for S aureus infection in neonates in resource-
poor countries in Asia have not been defi ned, but might
include absence of infection control procedures and
associated nosocomial infection, or practices related to
umbilical stump care and vaccination.
Clinical manifestations and outcome
The range of clinical manifestations of S aureus infection
reported from resource-limited countries in Asia is as
broad as that seen in other settings. These include
bacteraemia, endocarditis, meningitis and brain abscess,
pneumonia, empyema, septic arthritis and osteomyelitis,
abscesses of solid organs, pyomyositis, and soft tissue
infections.34–42 Most published studies that involve
S aureus in neonates report bacteraemia, including both
early and late onset sepsis. Bacteraemia is also the most
common presentation of serious infection reported in
older children, although lower respiratory tract infections
(including empyema) and endocarditis are often
described. Despite the textbook focus on pyomyositis as
the “tropical” form of S aureus disease, only ten studies
from our target countries describe pyomyositis.41,43–51
Thus, S aureus infection in resource-limited regions of
Asia is not only common but frequently presents as
The overall mortality from S aureus bacteraemia in a
large study of 157 patients at a provincial hospital in
northeast Thailand was 48%,3 which is over double that
reported in a similarly designed study in the USA
(157 deaths [22%] in 724 cases).52 It is diffi cult to calculate
the death rate for serious S aureus infection with data
provided by other studies from resource-limited countries
in Asia because most studies report all-cause bacterial
sepsis in which S aureus disease represents a small subset
and organism-specifi c outcomes are not identifi ed.
However, several studies did comment that infection
with S aureus had an increased risk of death compared
with other bacterial pathogens.53–55
The proportion of S aureus blood culture isolates that are
meticillin-resistant currently reaches 70% in high-income
Asian countries such as Japan56 and South Korea,57 but
rates of MRSA infection in less affl uent Asian countries
are generally poorly defi ned. Large-scale surveillance
systems in Asia such as the SENTRY Antimicrobial
Surveillance Program and ANSORP (Asian Network for
Surveillance of Resistant Pathogens) focus for the large
part on more affl uent countries,58–60 and strain collections
are inevitably biased towards areas that contain diagnostic
microbiology facilities. Most studies that describe MRSA
rates involve subgroups of patients, especially high-risk
patients such as those with burns, from which meaningful
conclusions on MRSA prevalence cannot be drawn.
However, multicentre MRSA surveillance data from
China and India suggest that MRSA accounts for a
substantial burden of disease in these countries.61–63
Additionally, data published by the National Staphylococcal
Phage Typing Centre in India shows that MRSA rates
GNI per head (US$)
Number of papers
20003000 4000 50006000 7000800030 000 50 000
Figure: Number of published papers on S aureus from resource-limited countries in south and east Asia
compared with Japan, UK, and USA
Each square represents one country. The cluster of countries includes Bangladesh, Bhutan, Cambodia, Indonesia,
Laos, Maldives, Mongolia, Nepal, Pakistan, Philippines, Sri Lanka, Timor-Leste, and Vietnam. Since Afghanistan,
Burma, and North Korea do not have gross national income (GNI) per head data available on the World Bank
website, they are not included on the graph; however, they all have fi ve or fewer papers published on S aureus
disease. Data from reference 1.
www.thelancet.com/infection Vol 9 February 2009
rose yearly during the 1990s.64 Inappropriate antibiotic
prescribing and limited hospital infection control might
have been important contributing factors for this
There are very few studies from resource-limited regions
of Asia that describe MRSA infection in the absence of
contact with health-care facilities.7,39,65 In these reports,
putative community-associated (CA-MRSA) strains (as
defi ned by absence of hospital contact) accounted for
3–11% of S aureus infections. These studies did not apply
the molecular tools often used to characterise MRSA
strains, such as staphylococcal chromosome cassette mec
(SCCmec) typing (which is usually type IV or V for
CA-MRSA strains), pulsed-fi eld gel electrophoresis or
multilocus sequence typing.
Over-the-counter antibiotics (penicillins [including
cloxacillin], cephalosporins, tetracyclines, quinolones,
and co-trimoxazole) are available across much of Asia
and these drugs are frequently self-administered for
inappropriate indications, and taken for irregular
durations.66–68 The cost of ten tablets of cloxacillin
purchased over-the-counter from a pharmacy in rural
Thailand in 2007 was around £1 (US$1·8), and the cost of
ten tablets of amoxicillin, doxycycline, or ciprofl oxacin
was around £0·85 ($1·5). This uncontrolled antimicrobial
use is likely to fuel the emergence of CA-MRSA as well as
drug resistance in a broad range of other human
pathogens. Substandard antibiotics are commonly
reported in resource-limited regions of Asia,69 the
presence of which could further drive resistance.
Reduced susceptibility to vancomycin
738 clinical S aureus isolates collected in India from
August, 2002, to July, 2005, were tested for vancomycin
resistance.70 Two isolates were vancomycin resistant
(mimimum inhibitory concentrations [MICs] of
32 μg/mL and MIC 64 μg/mL) and six isolates had
intermediate resistance (MIC 16 μg/mL for two isolates
and 8 μg/mL for four isolates) as defi ned by agar
dilution. None of the isolates was positive for vanA by
PCR. The gene vanA encodes resistance to the drug in
vancomycin-resistant S aureus (VRSA) and is likely to
be acquired from vancomycin-resistant enterococci
(VRE). However, the reduced susceptibility seen in
vancomycin-intermediate S aureus (VISA) is not
mediated by the van genes, but is associated with a
marked thickening of the cell wall.71 A further VRSA
strain (MIC ≥64 μg/mL) was isolated from the pus
specimen of an outpatient in Kolkata, India, in 2005,
which was positive for the vanA gene.72
Heterogeneous VISA refers to an isolate with a
subpopulation of colonies showing intermediate
resistance to vancomycin. A study of strains collected by
ANSORP reported the isolation of heterogeneous VISA
in India (fi ve isolates, 6.3% of all Indian MRSA strains
tested), Thailand (two isolates, 2.1%), Vietnam (one
isolate, 2.4%), and the Philippines (one isolate, 3.6%).60 A
further four heterogeneous VISA strains have been
reported in Thailand.73,74 Most other studies that we
reviewed used a disc diff usion method for detection of
vancomycin susceptibility, which is an inaccurate method
for the assessment of intermediate resistance.75 Although
strains with reduced susceptibility to vancomycin have
been identifi ed in our target countries, they remain
infrequent at present.
Bacterial genotype and SCCmec typing
S aureus epidemiology has relied extensively in recent
years on multilocus sequence typing to defi ne bacterial
population genetic structure. Studies from our target
countries that assessed MRSA strains have shown a
predominance of sequence type (ST) 239 (SCCmec type
III or IIIA) and ST 5 (SCCmec type II or IV).76,77 A study
of 74 MRSA isolates from 12 Asian countries (fi ve or six
isolates from most countries) collected between 1998 to
2003 found that most isolates from South Korea and
Japan were ST 5, whereas ST 239 predominated in
China, Indonesia, India, Philippines, Sri Lanka,
Thailand, and Vietnam.76 A subsequent study from South
Korea suggested that ST 239 had recently emerged
there.78 Further studies have confi rmed the predominance
of ST 239 in China, India, Mongolia, and Thailand.79–83 A
study in China of a selected group of MRSA strains
(selected on the basis of positivity for genes encoding
Panton-Valentine leukocidin [PVL]) reported equal
numbers of ST 88, ST 239, and ST 398.84
The usefulness of typing in resource-limited countries
in Asia has been shown by a report of an outbreak of
MRSA infection in Vietnam associated with vaccination.85
The same MRSA strain was isolated from injection site
abscesses from four children and from nasal and
throat swabs from their vaccinator. SCCmec typing of
the isolates showed that they were SCCmec type V (or
type 5C) and ST 59, the endemic CA-MRSA clone in
Overseas volunteer health-care staff who come from
settings where MRSA carriage occurs can put non-
governmental organisations and hospitals at risk of
MRSA. This potential problem was highlighted by a
study from Laos that reported the fi rst isolation of MRSA
in this country. Molecular typing showed that the SCCmec
type of the strain in question matched the type carried by
CA-MRSA strains in Japan.87 The hospital from which it
was isolated received many Japanese exchange staff ,
suggesting international spread by medical staff . This
example underlines the importance of several approaches
in resource-poor settings for identifying the emergence
of MRSA and for understanding routes of MRSA
transmission, including the screening of health-care
workers before arrival, ongoing vigilance, and the
judicious use of molecular techniques. It is also possible
that overseas staff could become colonised with MRSA
www.thelancet.com/infection Vol 9 February 2009 133
while working in low-income countries and then return
to hospitals in developed countries carrying these
PVL is a bicomponent cytotoxin and putative virulence
factor associated with skin and soft tissue infections and
also more serious infections, such as severe necrotising
pneumonia, in developing countries.88–90 pvl-positive
S aureus strains in our target countries have been
associated with skin and soft tissue infections,85,91 and
there has been one reported case of fatal necrotising
pneumonia.92 Data on the proportion of S aureus isolates
positive for pvl in resource-limited countries in Asia are
sparse and only available for a few countries. pvl has been
detected in 7.2–13.3% of disease-associated S aureus
isolates in China,84,93–95 and in 10·6% of meticillin-sensitive
S aureus carriage strains in Indonesia.96
Prevention of nosocomial MRSA transmission
and S aureus infection
Eff orts to prevent nosocomial MRSA transmission and
infection in developed world settings receive major
research funding as well as attention from the medical
profession, the media, and the public. This is generally
not the case, however, in resource-limited countries in
south and east Asia. The absence of data on rates of
MRSA colonisation or infection contributes to the
inadequate recognition given by health-care workers and
the public to the threat of nosocomial infection. Attempts
to combat nosocomial infection might be hampered by a
lack of infection control teams or policies, inadequate
infrastructure (eg, handwash basins), and the cost of
alcohol handrubs. This situation is further exacerbated by
the absence of literature on implementation and effi cacy
of infection control measures in resource-poor regions of
Asia. It is crucial to address these issues to curb the trend
of rising MRSA infections in these regions.
The burden of S aureus disease in developing regions is
inadequately appreciated or understood. An initiative is
needed to raise the profi le of S aureus disease in
developing countries, and to fund studies to better defi ne
the health-care challenges and potential practical
solutions relating to this important global pathogen.
Additionally, research questions should be focused on
areas that are most likely to eff ect quality of patient care.
These include the prevalence of and risk factors for
S aureus infection across south and east Asia, the
presence and rate of MRSA infection, appropriate
empirical prescribing regimens in these settings, and
mechanisms to disseminate and instigate cheap but
eff ective infection control strategies based on hand
hygiene. Additional research is essential to characterise
further the rate and causes of S aureus-related mortality
in resource-poor regions of Asia.
Confl icts of interest
We declare that we have no confl icts of interest.
EKN, NPD, and SJP are funded by the Wellcome Trust. TEW is funded
by National Institutes of Health award U54 AI057141 and by a Parker B
Francis Fellowship in Pulmonary Research.
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Search strategy and selection criteria
Data for this Review were identifi ed by searches of PubMed,
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