Effect of handrubbing using locally-manufactured alcohol-based handrubs in paediatric wards in Harare, Zimbabwe
Gudza-Mugabe et al. Antimicrobial Resistance and Infection Control
Effect of handrubbing using locally- manufactured alcohol-based handrubs in paediatric wards in Harare, Zimbabwe
Muchaneta Gudza-Mugabe 0
Marcelyn T. Magwenzi 2
Hilda A. Mujuru 1
Mutsa Bwakura-Dangarembizi 1 5
Valerie Robertson 2
Alexander M. Aiken 3 4
0 National Microbiology Reference Laboratory, Harare Central Hospital , Harare , Zimbabwe
1 Department of Paediatrics and Child Health, University of Zimbabwe-College of Health Sciences , Harare , Zimbabwe
2 Department of Medical Microbiology, University of Zimbabwe-College of Health Sciences , Harare , Zimbabwe
3 Biomedical Research and Training Institute , Harare , Zimbabwe
4 London School of Hygiene and Tropical Medicine , London , UK
5 Parirenyatwa Hospital , Harare , Zimbabwe
We assessed bacterial contamination of hands of adults present in paediatric wards in two tertiary-care hospitals in Harare, Zimbabwe and the microbiologic efficacy of locally-manufactured alcohol-based hand rub (ABHR). During unannounced visits, samples were collected using hand-print and hand-rinse methods. Samples were collected from 152 individuals (16 nurses, 10 doctors, 28 students, 86 parents/guardians, 12 others). Contamination of hands with Gram-negative bacteria was found in 91% of adults tested with a mean of 14.6 CFU (hand-rinse method; IQR 3-65), representing a high risk for transmission of pathogens potentially leading to nosocomial infections. A single application of ABHR under controlled conditions achieved an average of 82% (or 0.72 log) reduction in detectable counts. Amongst 49 Enterobacteriaceae isolates from hands, 53% were resistant to gentamicin and 63% were resistant to cefpodoxime. Use of ABHR represents an attractive intervention for reducing nosocomial infections in this setting.
Hand hygiene; Contamination; Gram negative bacteria; Nosocomial infection; Paediatric; Alcohol-based hand rub
Health-care workers’ (HCWs) hands have frequently
been found to be colonized with potential pathogens
during routine patient care . These organisms survive
if hand hygiene by HCWs is inadequate or omitted
entirely. Infections are transmitted  when contaminated
hands come in direct contact with another patient or an
object used for patient care [3, 4].
Zimbabwe has been undergoing strenuous economic
challenges for more than a decade. Amongst other
difficulties, this has led to intermittent water supply in many
hospitals. Alcohol-based hand-rub (ABHR) is
recommended as an effective method of hand decontamination
during routine patient care [5, 6] and is locally-produced
in many hospitals in low-income countries .
This study was a cross-sectional evaluation ahead of a
planned trial of an ABHR-based intervention. We focused
on the detection of Gram-negative Enterobacteriaceae on
the hands of adults to determine whether this potentially
represented a major vector for transmission of
antibioticresistant Enterobacteriaceae between paediatric patients in
Study participants were recruited from the paediatrics
wards of two tertiary government-sector hospitals in
Harare, Zimbabwe. These hospitals have established
hospital infection programs, but no routine data on
hand-hygiene performance was being collected at the
time of the study.
After relevant ethics approvals, all adults present in
wards on unannounced study dates were approached for
participation. After informed consent was obtained, one
hand (either left or right) was tested before and after
ABHR use . Four fingers of the selected hand were
lightly pressed to an agar plate to make a print
(handprint method). The same hand was then rinsed in a bag
containing 200 ml of sterile water by inserting the entire
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hand, shaking vigorously and rubbing fingers and
thumb together for 15 s (hand-rinse method). Plastic
bags (Zipwave, Multix, Australia) were sterilized
between uses by immersion in boiling water. From each
hand-rinse sample, 100 ml of liquid was filtered using
paper with 0.45 μm apertures (Millipore, UK). A 0.5
MacFarland suspension of ATCC 25923 E.coli and
sterile water were used as controls.
Alcohol-based hand rub prepared at Parirenyatwa
Hospital Pharmacy following the WHO guidelines 
was used. For quality control in production, the
percentage alcohol content was routinely tested using a
hydrometer . Additionally, a sample of ABHR from
the same production batch as used in this study was
analysed by spectrography in University Hospital
Geneva Pharmacy, Switzerland in June 2015.
Approximately 5 ml of ABHR was dispensed onto both the
hands of the participant and the investigator showed
how to rub the hands together according to standard
WHO method for hand-cleansing . After ABHR
use, samples were immediately collected from the
opposite hand using the same methods as described
Samples from both methods were cultured aerobically
on MacConkey agar at 37 °C for 18–24 h. Plates were
read and the Gram-negative colonies were counted
manually. Fifty oxidase-negative isolates identified to the
level of family/genus and species using API10S strips
(Biomerieux, France). Enterobacteriaceae isolates were
tested for resistance to six antibiotics according to the
British Society of Antimicrobial Chemotherapy standard
method . Analysis of data was performed using a
Microsoft Excel spreadsheet and statistical tests were
performed using STATA v14.1.
Table 1 Gram-negative CFU counts before and after use of ABHR
The study took place over a 2-week period in May
2015. Samples were collected from 152 individuals in
the participating wards (16 nurses, 10 doctors, 86
parents/guardians, 28 students, 12 others). Before the use
of ABHR, Gram-negative bacteria were detected on the
hands of 91% (138/152) of adults tested by either the
hand-print or hand-rinse method. The mean recovery
rate for Gram-negative bacteria was high, with a
geometric mean of 6.8 CFU (IQR 1–21) and 14.6 CFU
(IQR 3–65) detected by the hand-print and hand-rinse
method respectively. Immediately after ABHR use, the
mean recovery rate for Gram-negative bacteria from
the opposite hand was 1.2 CFU (IQR 0–2) and 2.4 CFU
(IQR 0–5 CFU) by hand-print and hand-rinse methods
There was some indication that on the hand tested
before the use of ABHR, the recovery rate for
Gramnegative bacteria was higher on the non-dominant hand
(mean for hand-rinse method = 33.4 CFU; n = 14) than
on the dominant hand (mean = 13.7 CFU; n = 116) but
the difference was not statistically significant (Wilcoxon
rank sum test; p = 0.21).
Amongst sub-groups of people, the recovery of
Gramnegative bacteria before use of ABHR was lowest
amongst doctors (mean for hand-rinse method = 4.8 CFU;
n = 10) and highest amongst parents/guardians
(mean = 18.5 CFU; n = 86), although this difference
did not reach statistical significance (Wilcoxon rank
sum test; p = 0.15).
The reductions in Gram-negative bacteria counts with
use of ABHR were 82% (or 0.75 log) according to the
hand-print method and 84% (or 0.78 log) according to
the hand-rinse method. Spectrographic analysis of
Dominant hand “Before”
Non-dominant hand “Before”
Unknown dominant hand
Other/unknown professional group
Geometric mean Gram-negative CFU (IQR)
BEFORE use of ABHR
AFTER use of ABHR
ABHR used showed the correct alcohol concentration
(83%; acceptable range 75-85%), but hydrogen peroxide
was not detected (expected concentration 0.125%).
Amongst Gram-negative oxidase-negative bacterial
isolates recovered from participants hands in this study,
identification using API10S indicated that 49/50 were
Enterobacteriaceae, with the most likely genus being
Klebsiella (n = 21), Citrobacter (n = 15), Pantoea (n = 8),
Escherichia (n = 4) and Yersinia (n = 1). Susceptibility
testing indicated that antibiotic resistance was
widespread in these isolates, including resistance to
gentamicin (26/49; 53%) and cefpodoxime (34/49; 63%)
In paediatrics wards in government hospitals in Harare,
we found that contamination of the hands of HCWs and
parents with Gram-negative bacteria was extremely
common (91% with detectable bacteria) and with a high
burden of organisms, representing a high risk for
transmission of pathogens which might cause infection.
Interestingly, bacterial loads were found to be lowest
amongst doctors and highest amongst the parents/
guardians of paediatric patients and on non-dominant
hands, though these were based on small numbers. We
did not investigate whether specific ward-based tasks
increased levels of contamination. Community-based work
with mothers in Tanzania found that various activities
including cleaning children’s faeces increased faecal
indicator bacteria levels on hands . The organisms we
isolated were frequently resistant to antibiotics routinely
used for treatment, representing a direct risk to patients
. The frequent resistance to cefpodoxime, an agent
used to screen for the presence of Extended-Spectrum
β-lactamases, and gentamicin suggests that transmission
of this form of resistance might be occurring via the
hands of adults in these wards . A single application
of locally-manufactured ABHR achieved substantial but
not complete reduction in detectable Gram-negative
bacteria counts. Ideally, we should have tested equal
numbers of dominant and non-dominant hands prior to
ABHR use—this may have led to underestimation of the
Antibiotic (disc used) Susceptible (%) Intermediate (%) Resistant (%)
Ampicillin (10 μg) 1 (2%) - 48 (98%)
efficacy of ABHR. We cannot say with certainty whether
the reductions in Gram-negative bacteria on hands
demonstrated in this study would reflect on clinical
outcomes in routine practice.
Repeated use of ABHR could be used as a strategy to
prevent cross-infection between patients via the hands
of staff and visitors in this setting . System changes to
enable this practice must be addressed in Zimbabwean
hospitals where ABHR use has not yet become a
standard of care. In addition to making ABHR more widely
available, there is an important need to instruct parents
and HCWs in hospitals in Zimbabwe on the essential
role of hand hygiene in care of hospitalized children.
ABHR: Alcohol-based hand rub; CFU: Colony-forming units; HCWs: Health-care
workers; IQR: Inter-quartile range; WHO: World Health Organisation
We acknowledge with thanks to all the participating healthcare personnel,
parents/care givers for their participation in this study. We thank Memory
Mucheka from Harare Central Hospital, and the laboratory staff in the
Department of Medical Microbiology, University of Zimbabwe for assistance
with sample collection and processing. We also thank Simbiso Midzi of
Parirenyatwa Hospital Pharmacy for preparation of ABHR and Pascal
Bonnabry for performance of ABHR quality testing in HUG, Switzerland.
This work was funded by an Academy of Medical Sciences Starter Grant for
Clinical Lecturers (AA, grant reference AMS-SGCL11-AikenA). This work
formed part of a pilot study ahead of a cluster-randomised trial of a
hand-hygiene intervention in hospitals in sub-Saharan Africa.
Availability of data and materials
Data from this pilot study will be made available through the London
School of Hygiene and Tropical Medicine Data Compass data repository.
Conceived and designed the experiments: MGM, MM, HAM, MBD, VR, AA.
Performed the experiments: MGM, MM. Analysed the data: MGM AA.
Contributed reagents/materials/analysis tools: VR, AA. Wrote the manuscript:
MGM AA. All authors read and approved the manuscript.
The authors declare that they have no competing interests.
Consent for publication
Not applicable—the manuscript does not include details, images, or videos
relating to individual participants but rather presents analysis of aggregated
data on the study population.
Ethics approval and consent to participate
The study was reviewed and approved by the Harare Central Hospital Ethics
Committee (ref HCHEC 031214/80), Joint Parirenyatwa Hospital and University
of Zimbabwe College of Health Sciences Research Ethics Committee (ref 13/15),
the Medical Research Council of Zimbabwe (ref MRCZ/A/1939) and the London
School of Hygiene and Tropical Medicine (ref 8839). Health care workers,
Parents or guardians gave written informed consent to participate in the study.
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