“If it’s a broad spectrum, it can shoot better”: inappropriate antibiotic prescribing in Cambodia
Om et al. Antimicrobial Resistance and Infection Control
“If it's a broad spectrum, it can shoot better”: inappropriate antibiotic prescribing in Cambodia
Chhorvoin Om 0
Frances Daily 3
Erika Vlieghe 1
James C. McLaughlin 3
Mary-Louise McLaws 0
0 School of Public Health and Community Medicine, UNSW Medicine , UNSW, Level 3 Samuels Building, Sydney, NSW 2052 , Australia
1 Institute of Tropical Medicine , Nationalestraat 155, Antwerp 2000 , Belgium
2 23 (First Floor) , Street 310, BKK 1, Khan Chamcar Morn, Phnom Penh , Cambodia
3 Diagnostic Microbiology Development Program
Background: Cambodia is affected by antibiotic resistance but interventions to reduce the level of resistance require knowledge of the phenomena that lead to inappropriate prescribing. We interviewed physicians working in public hospitals to explore the drivers of inappropriate antibiotic prescribing. Methods: Hospitals participating in a knowledge, attitudes and practices survey prior to this study were purposively selected and physicians were randomly recruited to participate in focus group discussions. Nvivo version 10 was used to inductively code the qualitative transcripts and manage thematic data analysis. Results: Inappropriate antibiotic prescribing was a common practice and driven by seven factors: prescribing habit, limited diagnostic capacity, lack of microbiology evidence, non-evidence-based clinical guidelines, perceived patient demand, poor hygiene and infection control, and perceived bacterial resistance to narrow spectrum antibiotics.
Antibiotic resistance; Infection control; Preventive; Microbiology; Qualitative study; Prescribing habit
Soon after the introduction of penicillin for clinical
treatment in 1940s Alexander Flaming expressed
concern that physicians frequently failed to respect
prescribing rules and warned of bacterial resistance to penicillin
. Nearly three decades ago the Infectious Diseases
Society of America developed guidelines in an effort to
improve antibiotic prescribing  and recently the World
Health Organization (WHO) released a disturbing report
of global inappropriate antibiotic use that is now in
epidemic proportions . In accordance with WHO the
definition of inappropriate antibiotic use includes seven
errors: over prescription, omission of prescription,
incorrect selection, unnecessary expense, inappropriate
dosage, incorrect route and incorrect duration .
Inappropriate antibiotic use is especially high in
resource-poor countries and occurs in both healthcare
and non-healthcare settings with physicians, patients
and the general public accelerating the trend [5–7]. In
resource-poor settings poor prescribing is driven by a
complex combination of socio-behavioural and
economic factors and a weak functioning healthcare system
that is absent of the ability to enforce guidelines [8–10].
Like other resource-poor settings inappropriate
antibiotic use [11, 12] and antibiotic resistance [13–15] in
Cambodia are common place. Effective interventions
require background knowledge of the phenomena that
drive inappropriate antibiotic prescribing. We recently
reported that over half of Cambodian physicians working in
public hospitals surveyed nationally acknowledged that
their antibiotic prescribing was inappropriate .
Following from this prescribing practice survey we used
qualitative interviews to explore their antibiotic prescribing
practices that may drive antibiotic resistance in Cambodia.
Study design and setting
This qualitative study used focus group discussions
(FGDs) to collect data. Cambodia is a low-income
country located in Southeast Asia with over 11 out of 15
million people being poor or near poor . It was reported
in 2011 that the Cambodian healthcare system employed
19,721 healthcare staff including 3,196 physicians
working in 91 hospitals across the country .
Sampling and data collection
Purposive sampling  was used to select hospitals that
participated in a knowledge, attitude and practice (KAP)
survey  of antibiotic prescribing prior to this current
study and physicians were randomly selected from these
facilities to participate in FGDs. Data collection occurred
between September 2013 and February 2014. Participating
physicians were invited to a meeting room in their hospital
where they were given an information sheet and were
consented to participate in FGDs. There were between four
to 10 physicians in each FGD depending on the size of
participating hospitals. A standardized prompting question
guide and probing techniques were used in each FGD.
Enrolment continued until data saturation was achieved when
no new conceptual ideas or themes emerged to warrant
further investigation . All FGDs were digitally recorded.
Each digital record of FGDs was transcribed verbatim
into Khmer. A local physician was employed to check
the accuracy of the transcripts against the audio to
ensure correct transcribing of the medical terminology
used by participating physicians. All edited Khmer texts
were then translated into English and checked by CO.
An inductive approach was used to code patterns or
ideas that emerged from the data. Coding was conducted
by two coders (CO and MM) and any unclear text were
checked (CO) and any discrepancies between the two
codes were discussed. Nvivo version 10 was used for
coding and managing data analysis. Data were analysed using
thematic data analysis techniques and presented as
thematic syntheses and an illustrative visual display [21, 22].
We conducted 17 FGDs with 103 participating
physicians from 11 public hospitals including four hospitals
that had microbiology services. Our findings revealed
that antibiotics prescribing occurred in the absence of
microbiology evidence of infection.
“Every day, doctors are not performing appropriately.
We have made lots of mistakes with our antibiotic
“Nowadays we prescribe antibiotics blindly. We just
think that this is perhaps Gram negative or Gram
positive. So we just give antibiotics to cover Gram
positive or negative. But to make sure which one is
correct or how many days we should give this or that
type to patients, we don’t know.” Ph#2-MBR
This empirical prescribing of antibiotics was common
regardless of accessibility to microbiology services and
facilitated by seven factors as reported below:
Empirical prescribing habit
When a suspected case of bacterial infections was not
responsive to the initial antibiotic treatment the
common and habitual approach was to change to a broader
spectrum antibiotic without microbiology evidence.
Amoxicillin, ampicillin, gentamicin, ciprofloxacin, and
cotrimoxazole were routinely the initial choice but when
the clinical condition was unresponsive physicians would
change to a third generation cephalosporin (usually
ceftriaxone) as this was the currently broadest spectrum
beta-lactam antibiotic supplied in public hospitals. If the
disease remained unresponsive to ceftriaxone, physicians
working in hospitals without microbiology services
would need to send patients to a referral hospital for
further treatment (Fig. 1). When physicians perceived
patients were severely ill or suspected the patients had
received treatment prior to admission they were less
likely to prescribe a narrow spectrum antibiotic.
“When we suspect typhoid fever, we initially prescribe
quinolone for 3 days. If the patients’ body temperature
cools down, then we will continue for 5 days or 1 week
more and then we stop. If the body’s temperature does
not cool down after 3 days we will do another blood
cell count. If we see something strange or the white
blood cell count is getting high, then we will change to
use ceftriaxone. If ceftriaxone is still not effective, then
we will refer the patients to have culture.” Ph#3-KTL
“For me in the medical ward, I often give ceftriaxone
because when I take the clinical history of patients, it
always shows that they have already received
treatment a few days from private clinic but they
didn’t get better. They took antibiotics or we found
antibiotics with them.” Ph#7-KSFH
Limited diagnostic capacity
Diagnostic uncertainty facilitated antibiotic prescribing.
The most challenging was the difficulties in
differentiating bacterial from viral infections and when physicians
were uncertain about diagnosis their first option was an
antibiotic rather than waiting several days to see if the
patient’s condition improved.
“When our diagnosis is not certain we can’t avoid
antibiotics. For example, now we have a patient with
sore throat, we are not sure if it is caused by virus or
bacteria. We don’t know. The problem of uncertainty
forces physicians to give antibiotics because if we don’t,
we are afraid.” Ph# 4-KCH
“For me I think whether the prescription is correct
or not, it relates to the capacity of physicians. For
some physicians their prescriptions look
inappropriate. There are no signs of an infection
but still they prescribe antibiotics, and three types
of antibiotics are prescribed. It relates to the
capacity and knowledge of the physicians. When
physicians think that they are incompetent, they
prescribe antibiotics.” Ph#1-SRP
Physicians focused on the ability to make the correct
diagnosis in the absence of microbiology rather than the
impact of an incorrect choice of antibiotics.
“First make a correct diagnosis and then if the
medicines are not working, that diagnosis is
incorrect causing ineffective antibiotic therapy.”
Absence of microbiology evidence of bacterial infection
Access to microbiology services remained scarce in
Cambodia, especially for physicians working in
provincial and district referral hospitals where empirical
antibiotic prescribing was based solely on clinical
presentation and prescribing experience.
“We don’t have culture that is why we prescribe a trial
of antibiotics for 3 days and if that is ineffective, we
would change to other antibiotics.” Ph#2-KTL
Fig. 1 Habitual Pattern of Empirical Antibiotic Prescribing
“Firstly in severe cases we can’t wait and we have
to fight the infection immediately (with antibiotics).
We can’t wait (just) because we don’t have
microbiology available to us, we can’t delay
Empirical antibiotic prescribing was common even
when microbiology services were available as diagnostic
and antibiotic susceptibility testing were only sought when
the broadest spectrum antibiotics, such as ceftriaxone,
had failed to improve the patient’s condition (Fig. 1).
“Here we have it [microbiology]…they [physicians] are
not likely to request culture until the patient under
treatment has not improved then they order it
[culture]. For first line antibiotics, they rarely do it
[culture]. Most of them practice like this. I think this is
a habit from the previous time when there was no
culture. Now, we have culture service but their habit
does not change. It deeply rooted.” Ph#4-KCH
Some treatment guidelines were up-to-date but only for
some specific diseases such as neonatal sepsis or normal
vaginal delivery. Yet, antibiotic prescribing was based on
habit rather than these guidelines. For instant, antibiotics
were not indicated for normal vaginal delivery but every
patient received a 5-day course of antibiotics and the
treatment of neonatal sepsis was based on the individual
physicians’ experience not the guidelines.
“For women with a cesarean they receive (5 days of )
injections of ampicillin, gentamicin or ceftriaxone.
Depending on physicians, sometimes they give
ceftriaxone, sometimes ampicillin, gentamicin. For
normal delivery, we also use for 5 days.” Ph#6-SFH
“Well, it is heterogeneous…it varies from physician to
physician. One physician does it differently from
another without following the epidemiology, the
disease in that locality, country service, or disease.
They don’t have that basis.” Ph#4-NPH
Physicians’ reasons for not using microbiology services
included prescribing habit, a perception that the time to
results was excessive, culture results were unreliable or
poor meaning results and clinical progression were
discordant, and patient’s financial constraints.
Physicians believed these treatment guidelines were
based on those from developed countries where the
standard of hygiene and infection control was high.
Physicians wanted locally developed guidelines as they
believed these would help them improve their prescribing.
“Of course, I do not know why the lab takes so long;
maybe it is about quality of lab that is not reliable.
Because of that physicians don’t wait. As the baby now
has very high temperature and in a bad condition,
physicians are concerned about sepsis and afraid that
the baby may die, so they stop giving ampicillin and
gentamicin, they only prescribe ceftriaxone and add
“For the culture, what is important is the patients and
money. They don’t have money to continue their stay
in hospital to wait for culture results that take long
time. That’s why we often give the medicines right
away. Generally speaking, the important thing is
people don’t have money to follow our treatment
Perceived non evidence-based clinical guidelines
At the time of the interviews all available clinical
practice guidelines were not current.
“We have [treatment guidelines] but most are old…
there are no newly updated guidelines.” Ph#3-KCH
“No, we don’t have [treatment guidelines] yet in my
[Infectious Diseases] ward…I want them so that the
whole hospital can practice consistently.” Ph#5-NPH
“In public hospitals, we want to change our attitude
to just give prophylactic antibiotics. So we need a
study.…....comparisons between prophylaxis and
treatment and then show results to physicians so
that they can try to prescribe only prophylaxis with
narrow spectrum antibiotics to reduce resistance
and the antibiotic budget; and it’s also easier
because the staff don’t need to give injection every
Physicians described that patients commonly expected
injections not tablets because they believed that
injections were more effective. In private clinics patients
asked physicians for ‘strong’ and ‘quality’ medicine
because they wanted a quick cure to ensure they had a
short clinic admission. Although patients in reality did
not demand antibiotics physicians prescribed them to
meet this perceived demand.
“In private services, we think about what to do to
make patients stay short and cure. This is the
important point. If we spend the first 5 days on
amoxicillin and there’s no improvement and then
we change to cefexime for another 5 days. That’s
too long for them and they still may not be cured.”
“A wealthy family comes to us and asks for a ‘strong’
medication for their kid, and we would give them
something like augmentin (amoxicillin and
clavulanate potassium) from France and so on.”
“Patients want ‘quality’ medicine. They don’t say ‘ceftri
[ceftriaxone]’ they just say that they want ‘quality’
medicine. With stronger medicine, they believe they
recover faster.” Ph#4-NPH
Post-partum patients on discharge commonly asked
for antibiotics in a belief that the antibiotics would heal
their internal wounds and reduced their pain. Physicians
fulfilled this request by prescribing an additional 5 days
of antibiotics. This occurred in both a national speciality
hospital and general hospitals.
“Patients say they want a prescription to buy
additional medicines to take to reduce pain or
something like that. So we just prescribe one antibiotic,
one analgesic, and one vitamin for all kinds of
patients, like those who have normal delivery and so
Perceived poor hygiene and infection control
Patients’ rooms were commonly over-crowded, unclean
and untidy (Fig. 2). Families provided the patients with
bedding material, cooking utensils and food and assisted
with the patient’s general hygiene. In addition, physicians
perceived infection control practices were substandard,
and community sanitation and patient personal hygiene
were poor. Because of these challenges and their
constant concern about infection transmission physicians
prescribed antibiotics for ‘preventive purpose’.
“We often prescribe for prevention. When we prescribe,
we don’t know whether disease is cured by antibiotics or
Fig. 2 Patient room in medical ward of a provincial hospital
there is no infection. We don’t know. I’m always afraid
because everything is not clean and the patients are not
hygienic so we give antibiotics right away.” Ph#4-KSM
“Yes. Normally even though we know that it is viral
[infection], we still prescribe amoxicillin or something
else. Why? We think that the environment outside is
not good as there is a lots of flying dust.” Ph#1-KRV
Physicians were concerned about wound cleaning,
sterilization of surgical instruments and contaminated
hands and prescribed antibiotics to ‘prevent’ complications.
“We think our practice doesn’t comply with infection
control guidelines. Before delivering a baby, we use
gloves but we touch vaginal tears, touch everything. It
is not appropriate. So we haven’t respected the
infection control guidelines. When we know that our
practices are not correct we use antibiotics immediately,
and this continues over and over.” Ph#6-KCH
“We aren’t confident in the way staff clean wounds.
And are we confident that sterilization
is done correctly? Are the materials correctly sterilised?
And the other thing is the responsibility of staff. We
acknowledge they are less responsible. These are
factors that worry us and we always think that we
don’t want to make things more complicated. That’s
why we have to use antibiotics to prevent infection so
we can sleep well [no complication].” Ph#5-SRP
Perceived resistance to narrow spectrum antibiotics
Although physicians described their prescribing for
‘preventive’ purposes they also believed that pathogens were
resistant to narrow spectrum antibiotics as a result of
unrestricted antibiotic access in the community. Prior to
consulting with a physician, patients self-administered a
small dose of antibiotics purchased from a community
pharmacy or drug outlet, or sought treatment from
community-based healthcare providers.
“Patients come through a healthcare provider at a
community center, they also come through the
untrained village healthcare provider who goes from
house to house, and if they don’t get better they would
turn to us [physician]. When they come to us, if we use
ampicillin, it seems useless.” Ph#1-KP
“From day to day problem [antibiotic resistance]
persists and with antibiotics prescribed in private
practice we prescribe cefixime, 3rd generation
cephalosporin, which is now considered to be a very
low level antibiotics, as low as ampicillin.” Ph#9-KCH
The perception of resistance to narrow spectrum
antibiotics encouraged physicians to prescribe broad spectrum
antibiotics so that a multitude of perceived resistant
pathogens could be covered. Physicians then believed that they
could keep their reputation and their private practice
business. This prescribing in private practice included the
latest group of fluoroquinolones and cephalosporins.
“If it’s a broad spectrum, it can shoot better. Therefore,
there are more chances of success.” Ph#2-NPH
“We also think about business because we run a
business. If our treatment is not effective or it’s just
similar to the treatments of the other [physicians] they
[patients] don’t come to us again later.” Ph#1-KRV
“In my private place I always provide injections of
ceftriaxone for patients before cesarean and five more
doses later. For normal delivery I used simple pill. I used
curam [amoxicillin and potassium clavulanate] for five
days. Because I think that in Cambodia now ampicillin
and something like that are all resistant.” Ph#5-NMCH
In our previous national survey on the antibiotic
prescribing practices using case presentations and attitudes
over half of our physicians acknowledged that their
prescribing was inappropriate . In this current study we
can confirm that antibiotic prescribing is inappropriate
and one important factor is the practice of habitual
empirical prescribing. There are several other driving
factors, many of which are similar to other low resource
settings [10, 23, 24]. Habitual prescribing has been
observed elsewhere [24–28] and may be an important
driver of global inappropriate antibiotic prescribing. To
reduce unnecessary prescribing an intervention should
start with changing habitual prescribing practices .
Our physicians’ inability to distinguish between bacterial
and viral infections drives them to inappropriately
prescribe an antibiotic which is also a global phenomenon
[10, 23]. A study in India reported that such diagnostic
uncertainty is a reason physicians prescribed antibiotics
inappropriately . A barrier to evidence-based
prescribing in resource-poor countries is the lack of access
to and inappropriate use of microbiology services .
A study in Bangladesh revealed that over 90% of
antibiotic prescribing was empirical due to lack of access to
and unreliable results of microbiology test . But
habitual prescribing can be so entrenched that even
providing microbiology services may not change a
physician’s prescribing if they choose not to order an
antibiogram . Physicians in India were reported to seldom
request microbiology testing though accessible yet their
prescribing was mainly empirical . Underuse of or lack
of access to microbiology services results in indiscriminate
prescribing of broad spectrum antibiotics . From our
field observations, Cambodian physicians have very little
appreciation about the usefulness of microbiology services
and these are therefore under-utilized. They have little
knowledge about what specimens to collect and the
method of collection that will prevent the specimen from
being contaminated. A Gram stain is a rapid and
inexpensive test that can be utilized to assist prescribing while
waiting for an antibiogram. Yet, our physicians do not
know of this benefit which would reduce habitual and
empiric prescribing. Training physicians about how to use
microbiology may improve the use of microbiology
services and improve antibiotic prescribing .
Poor hygiene and infection control practices
encouraged our physicians to prescribe antibiotics excessively
for preventive purpose although they were never certain
about the outcomes of their prescribing in these
circumstances. It is a common fear in resource-poor settings
that poor infection control and environmental
cleanliness will result in patients acquiring a healthcare
associated infection and this encourages physicians to
prescribe antibiotics [9, 10, 23]. Hygiene and infection
control are not a priority in Cambodian hospitals and
environmental cleaning and waste management are
performed by illiterate staff who are not receive exceptional
Our previous survey reported over half of Cambodian
physicians preferred to prescribe broad-spectrum
antibiotics in their private practices . Our physicians in
this current study described how they preferred
prescribing broad spectrum antibiotics in their private
practice because they perceived that the unrestricted access
to antibiotics in the community resulted in bacterial
resistance to narrower spectrum antibiotics. Several
studies have shown that in reality patients actual
demand antibiotics or physicians just perceive this demand
[10, 24, 29]. Our current study has described a similar
perception with post-partum patients requesting
antibiotics thinking that this will reduce pain and heal internal
wounds. Physicians also described their private practice
patients demanded ‘strong’ and ‘quality’ medicines
resulting in broad spectrum antibiotics being prescribed
to meet this perceived demand.
The practice of prescribing antibiotics by Cambodian
physicians is inappropriate and based on prescribing
habit rather than microbiology evidence. Improving
antibiotic prescribing is unlikely to occur unless education
programs are provided to improve the diagnostic
capacity and the usefulness of microbiology services. In the
meantime antibiotic therapeutic guidelines should be
developed from the limited microbiology services that are
currently available. In parallel, hygiene and infection
control in hospital must be improved, and access to
antibiotics in community must be restricted.
We would like to thank Fondation Mérieux, Cambodia and Institutes of
Tropical Medicine, Antwerp, Belgium, for providing financial supports for
fieldwork and to the Australian government for the Australia Awards
Scholarship to Chhorvoin Om, and the University Research Co., LLC,
Cambodia for providing office space during the fieldwork. Special thanks to
participating physicians for their contribution to this important study. We
thank the Department of Hospital Services, Cambodian Ministry of Health, for
invaluable fieldwork contributions.
The fieldwork was financially supported by Fondation Mérieux, Cambodia
and Institutes of Tropical Medicine, Antwerp, Belgium. Both supporters had
no role in the study design, data collection, analysis, interpretation, writing of
this manuscript, or the decision to submit the manuscript for publication. Dr
Chhorvoin Om was supported by a four-year Australia Awards Scholarship
for his PhD at UNSW and the scholarship had to role in this study.
Availability of data and materials
Data are stored securely at UNSW, Australia according to the university data
storage policy. If requested, the data can be shared.
All authors contributed to this study and gave approval for publishing
this manuscript. CO and MLM designed the study and interview guides,
conducted data coding and analysis and wrote the manuscript. CO
conducted all FGDs with the physicians. FD, JM and EV provided guidance
in the field and feedback on the manuscript.
Ethics approval and consent to participate
This study was approved by the National Ethics Committee for Health
Research of the Cambodian Ministry of Health, UNSW Australia, and the
Institute of Tropical Medicine, Antwerp, Belgium. All physicians signed
consent form to participate in FGDs.
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