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\begin{document}

\title{Gaps between antibiotic prescribing practices and international
guidelines for women undergoing caesarean deliveries in rural Rwanda: A
retrospective cohort study}



\author[1]{Fredrick Kateera}%
\author[2]{Kara Faktor}%
\author[3]{Theoneste Nkurunziza}%
\author[2]{Teena Cherian}%
\author[2]{Bethany Hedt-Gauthier}%
\author[3]{Laban Bikorimana}%
\author[3]{Jonathan Nkurunziza}%
\author[2]{Rachel  Koch}%
\author[4]{Patient Ngamije}%
\author[2]{Robert  Riviello}%
\affil[1]{Partners In Health / Inshuti Mu Buzima}%
\affil[2]{Harvard Medical School}%
\affil[3]{Partners in Health / Inshuti Mu Buzima}%
\affil[4]{Republic of Rwanda Ministry of Health}%


\vspace{-1em}



  
  \date{May 05, 2024}


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\selectlanguage{english}
\begin{abstract}
Objective: Antibiotic stewardship remains a significant challenge in
sub-Saharan Africa, with paucity of systematic data on antimicrobial use
in surgical care. We characterise antibiotic prescribing practices for
women who delivered via caesarean section (c-section) in rural Rwanda.
Design: Nested retrospective cohort study. Setting: Kirehe District,
rural Eastern Rwanda. Population: All women aged \textgreater{} 18 years
who delivered by c-section between November 2017 and February 2018.
Methods: Data on antibiotic use, including name, indication,
dose/frequency/route, time, and duration of administration were
extracted from patient charts. Prescribing practices statistics were
summarised by the timing and type. Main Outcome Measures: Pre-operative
and post-operative antibiotic prescriptions, by time, name and dose.
Results: A total of 506 patients were enrolled. 80.8\% received a
pre-operative antibiotic, with 67.4\% receiving an antibiotic within one
hour of incision. The most prevalent pre-operative antibiotics
prescribed were Ceftriaxone (83.3\%) and Ampicillin (15.0\%).
Post-operatively during hospitalisation, 95.7\% of patients received two
antibiotics, most commonly Ampicillin (99.2\%) in combination with
Gentamicin (98.5\%). For all but one, antibiotics were prescribed
without indication of infection. At discharge, while 27.8\% of patients
were not prescribed any additional antibiotics, 72.2\% were prescribed
at least one antibiotic. Conclusions: Large deviations in antibiotic
prescribing practices as compared to international prophylaxis
guidelines were observed. Further studies to understand the rationale
for these deviations and the effects of over-prescription on infection
prevention and antibiotic resistance are needed to support
context-appropriate guidelines in Rwanda and in comparable settings.
Funding: NIH R21EB022369 Keywords: Antimicrobial use, sub-Saharan
Africa, global surgery%
\end{abstract}%



\sloppy


\emph{Introduction}

Globally, approximately 5 million cases of pregnancy-related infection
occur annually, of which 75,000 result in death.\textsuperscript{1} Risk
of developing a post-partum infection is much higher in low- and
middle-income countries (LMICs) due to poor hygiene conditions coupled
with limited resources.\textsuperscript{1,2} While access to caesarean
sections (c-sections) in sub-Saharan Africa (SSA) has improved,
associated surgical site infections (SSIs) present a new challenge. SSIs
are one of the most common healthcare-associated infections
worldwide.\textsuperscript{3} Given that c-sections comprise a large
portion of surgical care in SSA, they account for a large portion of
SSIs in this setting.\textsuperscript{4--6}

Pre-operative antibiotic prophylaxis reduces post-caesarean infection
rates,\textsuperscript{7} with one systematic review reporting a 39\%
decrease in SSI incidence among those receiving antibiotic
prophylaxis.\textsuperscript{8} Several studies, including randomized
control trials (RCTs), conducted in resource-limited settings suggest
non-inferiority of single dose pre-surgical prophylaxis compared to
prolonged antibiotic administration.\textsuperscript{9--11} Yet,
rational antibiotic use remains a significant challenge in SSA where
there are limited antimicrobial stewardship-related trainings,
compliance processes, and on-site access to data-informed prescribing
protocols that collectively support effective, context-specific
antibiotic use practices.\textsuperscript{12}

According to the World Health Organization (WHO) global guidelines for
the prevention of SSIs, antibiotic prophylaxis should be administered
within 120 minutes before the first incision without prolongation after
completion of the operation.\textsuperscript{13} Locally, the Rwandan
Ministry of Health (RMOH) protocol published in 2012 recommends use of
Ampicillin for c-section pre-operative prophylaxis, but doesn't specify
timing.\textsuperscript{14} At the hospital where the study was
conducted, anecdotal reports indicate general practitioners (GPs) follow
Society for Healthcare Epidemiology of America (SHEA)/Infectious Disease
Society of America (IDSA) guidelines, which recommend administration of
intravenous antibiotics within 1 hour of incision to maximize tissue
concentration.\textsuperscript{15} Inconsistences in guidance may partly
account for variation in antibiotic prescribing.

In SSA, SSI incidence among women undergoing a c-section ranges from
7.1-12\%.\textsuperscript{7,16} Our group recently reported a
post-caesarean SSI rate of 10.9\% at the district hospital involved in
this study.\textsuperscript{17} While there is limited information on
pathogens and antibiotic sensitivity within
SSA,\textsuperscript{18--22}especially with respect to post-caesarean
wound infections,\textsuperscript{23--26} existing data suggest emerging
antimicrobial resistance. However, to our knowledge, no study has
focused on rural district hospitals. Moreover, there is a paucity of
systematic data on antibiotic prescribing practices aimed at SSI
prevention.\textsuperscript{22,27,28} Here, we characterize
perioperative antibiotic prescriptions for women who underwent a
c-section at a rural Rwandan district hospital to better understand
prescribing practices as they relate to international protocols.

\emph{Methods}

Study data were collected as part of an ongoing prospective study to
evaluate the impact of a mobile health technology (mHealth)-community
health worker (CHW) intervention on detection of women with suspected
post-caesarean SSIs and their subsequent return to a health centre or
hospital for management.\textsuperscript{29} The prospective mHealth-CHW
study was funded by the National Institute of Health (NIH R21EB022369)
and included external peer review for scientific quality. Patients were
not involved in study design.

\textbf{Study Site}

The study was conducted in rural Eastern Rwanda at Kirehe District
Hospital (KDH), which provides maternal and child health services to a
catchment area of approximately 370,000 people. In 2017, 1,465 women
delivered by c-section at KDH. The vast majority of c-sections are
performed by the 14 GPs, with a few performed by a resident obstetrician
at KDH. In the absence of complications, a mother is routinely
discharged on post-operative day three and instructed to attend a
follow-up visit at her local health centre for wound care. We analysed
use of antibiotics pre-operatively relative to the hospital
leadership-reported protocol of administering antibiotic prophylaxis
within 1-hour prior to incision, similar to the United States SHEA/IDSA
recommendations.\textsuperscript{15}

\textbf{Data Collection and Analysis}

All women aged [?]18 years, who are residents in Kirehe district and
underwent a c-section at KDH between November 2017 and February 2018
were eligible for inclusion. In the parent study, women living in the
Mahama refugee camp who delivered by c-section at KDH were excluded from
study enrolment because camp care protocols would not allow the women to
comply with our study protocols. For all eligible patients, a signed
written informed consent was obtained before patient enrolment. At
enrolment, study-trained data collectors administered a sociodemographic
survey and subsequently, at discharge, performed clinical chart review
where data on antibiotic(s) administered, indication,
dose/frequency/route, timing and duration of administration were
extracted. Descriptive statistics are used to summarize
socio-demographic and clinical data. Data on prescribing practices are
presented as frequencies and percentages, and stratified by time of
antibiotic prescription (pre-operative, post-operative during admission,
and at discharge).

\textbf{Ethics}

All eligible women were read and provided with a copy of a written
informed consent document in the local language (Kinyarwanda), and
invited to provide a signed written consent prior to study enrolment.
Data were collected using encrypted study tablets and entered directly
into Research Electronic Data Capture (REDCap), a secure
password-protected database.\textsuperscript{30}

\emph{Results}

Of the 506 women enrolled, 357 (70.6\%) were aged between 18 and 30
years (Table 1). Most were either married (n=228, 45.1\%) or living with
a partner (n=228, 45.1\%), had at least a primary education (n=443,
87.5\%) and reported farming (n=356, 70.4\%) as their principle
occupation. For 453 (89.5\%) women, the reported monthly household
income was less than 30,000 RWF (approximately 33.30 USD).

Nearly all women underwent a c-section for either emergent indications
(n=140, 27.7\%)--- requiring an immediate intervention---or urgent
indications (n=355, 70.2\%), for which the patient could wait for
intervention until she was medically stable. The indications for a
c-section included foetal distress (n=174, 34.4\%) and a previous
c-section scar (n=160, 31.6\%) as most prevalent, followed by
cephalopelvic disproportion (n=82, 16.2\%), prolonged or obstructed
labour (n=60, 11.9\%) and malpresentation (n=54, 10.7\%).

A majority (n=409, 80.8\%) of the 506 enrolled patients received a
pre-operative antibiotic (Table 2). Of these, 239 (58.4\%) had data on
timing of the pre-operative dose, with 161 (67.4\%) receiving the
antibiotic within an hour prior to incision. The median time between
antibiotic prophylaxis and the surgical incision was 40 minutes
(interquartile range (IQR): 25, 74 minutes). For the 409 women who
received pre-operative prophylaxis, the antibiotics most frequently
prescribed were Ceftriaxone (n=343, 83.9\%) and Ampicillin (n=62,
15.2\%)---almost exclusively as a single dose (n=405, 99.3\%).

After surgery and before hospital discharge, 485 (98.6\%) of the 492
patients with post-operative prescription data, were given at least one
antibiotic (Figure 1). Apart from one patient who received therapeutic
antibiotics for a surgical site infection, all antibiotics (n=484,
99.8\%) were prescribed for prophylaxis \emph{only} . The median time
between surgery completion and the first post-operative dose was 15.6
hours (IQR: 10.9, 21.7 hours). Of the 485 patients who received
post-operative antibiotics, most were prescribed two antibiotics (n=464,
95.7\%). Ampicillin was the most commonly prescribed (n=481, 99.2\%),
and almost always in combination with Gentamicin (n=468, 98.5\%). Ten
patients (2.1\%) received only one antibiotic and another ten (2.1\%)
patients received three antibiotics. Among those who received a third
antibiotic, four received Metronidazole, five received Gentamicin and
one received Cloxacillin.

At discharge, 134 (27.8\%) of the 482 patients with discharge antibiotic
prescription data were not prescribed any antibiotics (Figure 2). Among
patients who received antibiotics at discharge, 332 (96.2\%) patients
were prescribed only one antibiotic, while 13 (3.8\%) patients were
prescribed two antibiotics. The most prevalent monotherapies prescribed
upon discharge were Amoxicillin (n=265, 76.1\%) and Cloxacillin (n=74,
21.3\%). Among the 13 patients who were prescribed two antibiotics at
discharge, 11 (84.6\%) were prescribed Metronidazole as one of the two
antibiotics.

\emph{Discussion}

\emph{Main Findings}

In our study, antibiotic prescribing at KDH showed noteworthy divergence
from the SHEA/IDSA recommendations for the prevention of SSIs in acute
care hospitals.\textsuperscript{15} This divergence is consistent with
the 29-country WHO Multicountry Survey on Maternal and Newborn Health
which found that 34.3\% of included facilities in Africa, Asia, Latin
America and the Middle East reported less than 90\% pre-surgical
prophylaxis coverage.\textsuperscript{31} A recent systematic review on
c-sections in SSA, which summarized 17 studies that reported on
antibiotic prescribing practices, similarly noted divergence from the
WHO's SSI prevention guidelines.\textsuperscript{32} Deviations noted in
our study included under-use of pre-operative antibiotics, with only
67.4\% of our study participants having a pre-operative antibiotic
prescribed within an hour prior to the first incision. Of concern,
nearly all patients received \emph{two} antibiotics after surgery and
before discharge, while the WHO guidelines indicate none should be
prescribed in the absence of indications of infection.

One challenge for pre-operative antibiotics is that neither KDH nor RMOH
obstetrics and gynaecology guidelines specify the timing of these
antibiotics during c-section care.\textsuperscript{14} While this study
did not explore reasons for failure to administer pre-operative
antibiotics, or for the timing deviations, lack of local guidelines and
inconsistencies in guidelines released by entities like the WHO, CDC and
SHEA/IDSA may contribute to the observed variations. In fact, in the
multicountry survey conducted by the WHO, coverage of pre-surgical
prophylaxis was greater in facilities using local and WHO guidelines, as
well those reporting clinical audits of antibiotic prescribing
practices.\textsuperscript{31}

Our observation of over-prescription of antibiotics post-operatively has
been noted elsewhere in SSA,\textsuperscript{33,34} and
internationally,\textsuperscript{35} showing high rates of poorly-timed
pre-surgical antibiotic doses with prophylaxis often extending beyond
the operative period. In a study at a Sudanese hospital where an overall
SSI rate of 7.8\% was reported, a lack of evidence-based guidelines and
fear of the patient developing SSI complications were suggested as
possible contributors to extended post-operative prescribing by
healthcare providers.\textsuperscript{33} A follow-up study in this
setting is currently underway.

Beyond the timing and duration of the antibiotics prescribed, selection
of an antibiotic with appropriate coverage and half-life is also
important in achieving adequate pre-operative prophylaxis. At KDH,
Ceftriaxone (83.9\%) was overwhelmingly the most frequently prescribed
pre-operative antibiotic, followed by Ampicillin (15.2\%), the
antibiotic recommended in Rwanda's national obstetrics and gynaecology
guidelines.\textsuperscript{14} Reasons for the predominate use of
Ceftriaxone were not elucidated in this study. Such discrepancies may
partly be explained by a GP's training-based prescribing habits, a
consequence of antibiotic availability, a preference for oral rather
than invasively provided medications or differential pharma-driven
marketing influences. A further exploration of influencers of antibiotic
prescribing habits is needed.

When compared to international guidelines, antibiotics were over-used in
this study with respect to prolonged duration, too broad a spectrum of
antimicrobial coverage or use of multiple antimicrobial agents, as
reported elsewhere.\textsuperscript{33,35} What is not clear is whether
international guidelines---based predominantly on data from high-income
countries---are optimized for settings such as rural district hospitals
in SSA. In support of international guidelines, a recent RCT in rural
Tanzania demonstrated non-inferiority of single-dose antibiotic
prophylaxis when compared to extended antibiotic administration for
patients undergoing a c-section.\textsuperscript{9} Furthermore, despite
the high prevalence of post-operative prescribing seen in this study,
the 10.9\% SSI rate found during the RCT is comparable to rates seen
throughout the region, possibly suggesting no benefit to prolonged
antibiotic duration for SSI prevention.\textsuperscript{17} However, a
recent study at KDH showed that women delivering via c-section who were
hospitalized on a day without running water were significantly more
likely to develop a SSI (manuscript in draft), suggesting that infection
risk, and therefore effective prophylaxis, may need to extend beyond the
first incision in this setting.

\emph{Strengths and Limitations}

This study is one of few studies characterizing antibiotic use in the
context of c-section care in rural Africa. The study team prospectively
enrolled patients, worked closely with the hospital teams and collected
high-quality data. However, while interpreting study findings, a number
of limitations should be considered. Collection of antibiotic-related
data was by chart review at the time of discharge, rather than direct
recording at the time of administration, which may affect accuracy of
timing and proper charting of antibiotics prescribed and administered.
Since the data collection occurred as part of a larger prospective
study, providers may have been somewhat aware that the study team was
looking at SSI rates in their patients, potentially causing an
artificial increase in antibiotic prescribing in an effort to keep SSI
rates low. Lastly, some of the patient exposures, including the
peri-operative antibiotics received, may reflect prescribing practices
specific to providers at the district hospital, limiting
generalizability.

\emph{Interpretation}

There are several considerations for interpreting these results. The
first is that the providers deviated from international prescribing
protocols due to a failure to have and/or understand such protocols. The
second is that providers do not believe these protocols take into
consideration the potentially high risk of infection and low likelihood
of mothers returning for consultation within these contexts.
Understanding these contextual factors is key to informing improvements
in prescription practices and compliance to protocols.

\emph{Conclusion}

Compared to the SHEA/IDSA international guidelines for women who
delivered by c-section, our data show large deviations in antibiotic
prescribing practices both pre and post-operatively, as well as among
different prescribers. Our findings raise questions on whether insisting
on a single pre-operative antibiotic dosing regimen, established based
on research in developed settings, oversimplifies the challenges of
providing optimal care for women undergoing a c-section in this
environment. More data is needed to guide development of area-specific
guidelines that are both effective and feasible. Furthermore, studies
exploring the rationale of antibiotic prescribing decisions, those
assessing the effect of over-prescription on infection prevention, and
those tracking evolving antibiotic sensitivity are recommended to guide
evidence-based antibiotic prescription practices.

\textbf{Disclosure of interests}

The authors have no relevant interests to disclose.

\textbf{Contribution to authorship}

FK, BHG, and RR are the three principal investigators for this study,
instigated the original idea for the study, developed the funding
proposal, applied for funding, and led study design, implementation,
data analysis, and the dissemination of results. KF led the
implementation of the antimicrobial resistance work specifically. TN,
TC, and RK led the implementation of the larger study in which this
study is nested. LB, JN, and TN collected data for use in this analysis.
PN provided hospital oversight and assisted in study design and data
collection. All authors read and commented on manuscript drafts and
approved the final version.

\textbf{Details of ethics approval}

The study protocol was approved by the Partners in Health (PIH)/Inshuti
Mu Buzima (IMB) Research Committee and Rwanda National Health Research
Committee, with ethics approvals from Rwanda National Ethics Committee
in Kigali, Rwanda (1 November 2016; No. 848/RNEC/2016) and Partners
Human Research Committee in Boston, USA (9 September 2017; No.
2016P001943/MGH). The study was also approved by the Rwanda Ministry of
Health prior to implementation.

\textbf{Funding}

This study was funded by the National Institutes of Health (NIH
R21EB022369) and supported by Partners In Health (PIH) / Inshuti Mu
Buzima (IMB).

\textbf{Acknowledgements}

We are grateful for the support of Kirehe District Hospital leadership
and staff during data collection. \emph{}

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\emph{Tables \& Figures}

\textbf{Table 1.} Demographic and clinical characteristics of study
participants (N=506)

\textbf{Table 2.} Antibiotic prescriptions (N=506)

\textbf{Figure 1.} Post-operative antibiotic prescriptions during
hospitalisation

\textbf{Figure 2.} Discharge antibiotic prescriptions

\textbf{Hosted file}

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\textbf{Hosted file}

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