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Int J Clin Pract. 2017;71:e13042. wileyonlinelibrary.com/journal/ijcp
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https://doi.org/10.1111/ijcp.13042
© 2017 John Wiley & Sons Ltd
Received:26May2017
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Accepted:31October2017
DOI:10.1111/ijcp.13042
ORIGINAL PAPER
Assessment of prescribing practices at the primary healthcare
facilities in Botswana with an emphasis on antibiotics: Findings
and implications
Yohana Mashalla1 | Vincent Setlhare2 | Amos Massele1 | Enoch Sepako1 |
Celda Tiroyakgosi3 | Joyce Kgatlwane4 | Mpo Chuma5 | Brian Godman6,7,8
1Department of Biomedical Sciences, Faculty
of Medicine, University of Botswana,
Gaborone, Botswana
2Department of Family Medicine and Public
Health, Faculty of Medicine, University of
Botswana, Gaborone, Botswana
3Ministry of Health, Gaborone, Botswana
4SchoolofAlliedHealthProfessions,
University of Botswana, Gaborone, Botswana
5School of Public Health, Faculty of Health
Sciences, University of Botswana, Gaborone,
Botswana
6Department of Clinical Pharmacology,
KarolinskaInstitute,Stockholm,Sweden
7StrathclydeInstituteofPharmacyand
Biomedical Sciences, Strathclyde University,
Glasgow, UK
8Health Economics Centre, University of
Liverpool Management School, Liverpool, UK
Correspondence
Brian Godman, Division of Clinical
Pharmacology,KarolinskaInstitute,Karolinska
University Hospital, Stockholm, Sweden.
Emails: brian.godman@ki.se;
brian.godman@strath.ac.uk
Funding information
UniversityofBotswanaOfficeofResearch
and Development
Summary
Background and Aims: Inappropriatedrugprescribing hasincreasedespecially inde-
veloping countries where systems for monitoring medicine use are not well devel-
oped. This increases the rate of antimicrobial resistance. The study aim was to assess
the prescribing patterns among urban primary health facilities in Botswana to provide
future guidance including developing future quality indicators.
Methods: Retrospective data from patients’ records between January and December
2013in19clinicswerecollectedinacross-sectionalstudy.TheWHO/International
Network for Rational Use of Drugs indicators were used to assess prescribing patterns
in the study clinics.
Results:Averagenumberofdrugs perprescriptionwas2.8;78.6%oftheprescribed
antibioticswerebyInternationalNon-proprietaryNameand96.1%compliedwiththe
BotswanaEssentialDrugsList.Overallrateofantibioticprescribingwashigh(42.7%)
with14.7%,5.9%and1.3%of prescriptions having two, three and four antibiotics,
respectively.Systemicantibiotics(JO1C)accountedfor45.4%ofprescribedantibiot-
icsofwhichamoxicillinaccountedfor28.4%andmetronidazole14.4%ofallantibiotic
prescriptions.Therewaslowuseofco-amoxiclav(0.3%ofallantibioticprescriptions).
Third generation cephalosporins and macrolides accounted for 9.8% and 6.2% of
antibiotic prescriptions respectively, with no prescribing of fluoroquinolones. The
majority of indications (87%) for antibiotic prescriptions were according to ICD
classification.
Conclusions: While most indications for antibiotic prescriptions were based on signs
andsymptomsaccordingtoICD,antibioticprescribingrateswerehighwithsomecon-
ditions not requiring antibiotics because they are viral infections. There is a need to
further improve prescribing practices through induction and training of in- service pre-
scribers.Aneffectivemanagementtoolformonitoringantibioticprescribingpractices
at Primary Health Care facilities should be designed and implemented, including devel-
oping robust quality indicators.
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1 | INTRODUCTION
TheWorldHealthOrganization(WHO)definestherationaluseofmedi-
cines as “patients receive medications appropriate to their clinical needs,
in doses that meet their own individual requirements for an adequate
period of time, at the lowest cost to them and their community”.1 To ad-
dress the irrational use of medicines, including inappropriate use of anti-
bioticsleadingtoincreasingratesofantimicrobialresistance(AMR)with
its associated impact on morbidity, mortality and costs,2-8the WHOin
collaborationwiththe InternationalNetworkforRationalUseofDrugs
(INRUD)hasdevelopedcoreindicatorsforprescribingpractices,patient
care and facility- specific factors.2,9,10 These include the number of anti-
biotics per prescription without looking at issues of necessity or whether
prescribing adheres to current guidelines.11ThecurrentWHOreference
value for the average number of medicines per encounter is <2,10,12,13
with a comprehensive review between 1990 and 2009 reporting the
averagenumber among 104countries was 2.6for the Africaregion.14
Morerecentreports indicatea45.8%increasefrom2.4between 1995
and 2005 to 3.5 between 2006 and 2015.10 The percentage of medi-
cines prescribed by the generic (International Non-proprietary Name;
INN)nameshould be 100% (acceptable >80%).2,9,13 However, studies
havereported lower ratesforthe Africanregionat between60%and
68%.5,12
Currently, there is a scarcity of data regarding the quality of antibi-
oticprescribingindevelopingcountries.Inthesesettings,itiscommon
for antibiotics to be prescribed for typically self- limiting conditions
suchas acuteupper respiratorytractinfections (URTIs)thatare pre-
dominantly viral in origin and for other infections which do not require
antibiotics.4,15-19ThissituationisworseinAfricancountries.Thecom-
parativereportofantibioticprescribingratesin theAfricaregionbe-
tween 1995- 2005 and 2006- 2015 shows during the later period high
antibiotic prescribingrates (22%, 58% and 22%) in Ghana, Tanzania
and Nigeria, respectively,20-22 with most of the increase because of
prescribing in URTIs,which are typically viral in origin. Overall, ap-
proximately 50% of current antibiotic prescribing in outpatient de-
partments is seen as inappropriate.23 In Malaysia, as in Botswana,
antibiotics are commonly and inappropriately prescribed by primary
healthcare (PHC) providers at PHC facilities.24-27 Most of these re-
ports though are based on small- scale studies, which could be under-
estimation of the extent of antibiotic use in developing countries.
Following the Alma Ata Declaration in 1978,28 Botswana de-
veloped a successful and comprehensive PHC system with treat-
ment provided in accordance with the standards set out in the
Ministry of Health guidelines.29 However to date, few studies have
been undertaken to assess prescribing practices in PHC facilities
in Botswana.30-32 We have previously reported that 52 different
documents/guidelines existed at 18 PHC facilities in the Greater
Gaborone areaof Botswana, of which 50% focused on treatment
andmanagementofdiseases,the remaining50% weregeneral in-
formation and policy related.33 Except for the guidelines for treating
STIs found at 86% ofthe facilities, the majority of PHC facilities
(56%)didnot have currentguidelines available andtheBotswana
TreatmentGuidewasonlyfoundat50%oftheclinics.33
1.1 | Aims
The aim of this study was to assess current drug prescribing
practices in PHC facilities in Gaborone and surrounding areas
with a specific emphasis on antibiotic prescribing. The study
results would be used to guide future corrective interventions.
The interventions may include suggestions to develop new qual-
ity indicators, especially for antibiotic prescribing, in ambula-
torycaregiventherathercrudenatureofcurrentWHO/INRUD
indicators.9,10
2 | METHODOLOGY
This was a non- experimental cross- sectional descriptive study initially
usingtheWHO/INRUDindicators9 before looking more specifically at
antibiotic prescribing. The study was carried out between November
and December 2015, collecting retrospective data from patient re-
cords for the period between January and December 2013. The PHC
facilitieswerefromGaboroneDistrict,Tlokweng(SouthEastDistrict)
andMogoditshane(Kweneng District). The facilitiesarerepresenta-
tive of urban settings in Botswana where the majority of patients seek
their treatment from.
What’s known
• There is considerable overuse of common antibiotics
across countries particularly in primary healthcare cen-
tres, leading to increasing resistance rate.
• There are ongoing developments to improve the use of
antibioticsacrosscountriesincludingWHO/International
NetworkforRationalUseofDrugs(INRUD)indicatorsas
well as guidelines.
• However, there are concerns with the specificity of
WHO/INRUDindicatorstofullyassessthequalityofan-
tibiotic prescribing in ambulatory care as well as adher-
encetoICDcodeswhenprescribing.
What’s new
• There were high rates of International Non-proprietary
Name prescribing in Botswana as well as high rates of
prescribing of medicines contained in the Botswana EDL.
• However, there were high rates of antibiotic prescribing
as well as high rates of prescribing two or more antibiot-
ics on the first encounter. This may be because of a high
prevalence of gynaecological and sexually transmitted
infections in presenting patients in Botswana.
• The majority of indications for antibiotic prescribing
(87%)werein accordance with ICD-10 codes;however
rates could be improved to enhance future quality of
prescribing
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2.1 | Sample size and sampling procedures
TheWHO9 recommends that there should be a minimum of 600 pre-
scribing episodes included in a cross- sectional indicators survey, and
where there are fewer than 20 facilities in a geographical or admin-
istrative region to be studied, all facilities should be included in the
sample. The selected districts have a total of 20 PHC facilities; all were
included in the study.
Data were collected by trained research assistants under the
supervision of the principal researchers (YM and ES). Using pa-
tient’s records, we estimated to collect at least 30 prescriptions
from each PHC. To achieve this, patient prescription records were
listed according to the month in which they were prescribed and
assigned random numbers. Records were then randomly selected
untilasamplesizeof30patientrecordswasrealised.Wewanted
to assess initial prescriptions only in this study. Consequently, all
records that showed re- attendances were excluded from the study.
The diagnoses on the patient’s records were used to determine
the indication for antibiotic prescription without contact with the
prescriber.
2.2 | Quality of antibiotic prescribing
The quality of antibiotic prescribing practices was assessed as fol-
lows:(i) prescribingagainstWHO/INRUD criteria9,10,13;(ii)antibiotic
prescribing against indicators developed and proposed by European
organisations and (iii) antibiotic prescribing against the Botswana
Essential Drug List.34
The following indicators have been proposed and used by
European organisations to assess the quality of systemic antibiotic
(J01)prescribing35-37:
• Utilisationofpenicillin(J01C)asa%oftotalantibioticuse.
• Utilisation of combination penicillin (eg, co-amoxiclav)as a % of
total amoxicillin use.
• Utilisation of third- and fourth-generation cephalosporins vs first-
and second- generation cephalosporins.
• Utilisationoffluoroquinolones(J01MA)asa%oftotalantibioticuse.
Prescribing rates at PHC facilities in Botswana were assessed against
published rates among low and middle income European countries, in-
cluding former Soviet Union Republics, as no baseline data currently
exist for these facilities in Botswana.37,38
The utilisation metric used is a prescription rather than interna-
tionally recognised metrics such as defined daily doses (DDDs) or
DDDs per 1000 inhabitants perday (DIDs).37-39 This is because we
wanted to assess antibiotic prescribing for the first indication, and we
were evaluating antibiotic prescribing among providers at PHC facili-
ties rather than the population as a whole.
2.3 | Data processing and analysis
For the purpose of improving the quality of data and the rigour of
research results, data management procedures and processes were
in accordance with the methodology proposed by Vittinghoff et al40
This included data preparation, cleaning, editing and creation of vari-
ables and identification of missing data. Since we were not testing any
outcome variables against exposure interventions, and we were not
assessing associations between the prescribers and prescribed drugs,
only descriptive and inferential analysis frameworks were used to ana-
lyse prescribing information. Percentages, averages and frequencies
were also used to describe the data.
2.4 | Ethical considerations
The study received ethical clearance from the University of Botswana,
InstitutionalReviewBoard(Ref.URB/IRB/1506)andapermittocarry
out the study in the PHC facilities was obtained from the Ministry
of Health and Wellness (Ref. PME.13/18/87). The District Health
Management Team Coordinator granted access to the facilities vide
letter Ref: GGDHMT/14/2/i dated 28 November 2014. The identity
of the clinics was protected by keeping them anonymous and assigned
coded numbers.
3 | RESULTS
3.1 | General
Data from 19 PHC facilities only were analysed. Data from one clinic
were not collected because during data collection, the clinic staff were
on vacation. Out of an estimated 570 prescriptions that were col-
lected, 20 prescriptions were excluded from the final analysis because
seven patients had come to the clinics for routine Antenatal Clinic,
six were patients who had visited the clinics for counselling services
andanothersevenvisitedthe facilitiesforHIV testing.Thisreportis
therefore based on 550 prescriptions.
3.2 | Prescribing practices against
documented indicators
The total number of prescriptions analysed were 550 and the total
number of medicines prescribed for all conditions were 1551, giving
anaverageof2.8drugsperprescription.Ofthetotalmedicinespre-
scribed,1219(78.6%)wereprescribedusingINN and235(42.7%)
encounters contained at least one antibiotic prescription. 1490
(96.1%)wereprescribedfrom the Botswana Essential Drug (EDL)
(Table1).
3.3 | Prescriptions with antibiotics
Table 2 shows that 306 antibiotics were prescribed during 235 patient
encounters,ofwhich17weretopicalapplications(13Chloramphenicol
ointments, 3 Tetracycline ointments and one gentamicin ointment
prescription). Systemic antibiotics (J01) were the most commonly
prescribed.Thebeta-lactamantibiotics (J01C)accountedfor 45.4%
ofprescriptions,risingto48.1%whenonlysystemicantibioticswere
considered.Amoxicillinwasthemostcommonlyprescribedantibiotic
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MASHALLA et AL.
(28.4%)followedbymetronidazole(14.4%).Co-amoxiclavaccounted
foronly0.3%ofallantibioticprescriptions,whilecotrimoxazole(sul-
phamethoxazole+tromethropim) accounted for 9.2% of all antibi-
otic prescriptions. Third generation cephalosporin (ceftriaxone) and
macrolides(erythromycin)accountedfor9.8%and6.2%ofantibiotic
prescriptions,respectively.Thisincreasedto10.4%and6.6%,respec-
tively when only J01 systemic antibiotics were considered. No fluoro-
quinolones(J01MA)wereprescribed.
3.4 | Indications for antibiotic prescriptions
Table 3 shows 69 diagnoses for which antibiotic prescriptions were
written. Most diagnoses were based on signs and symptoms whilst
some were specific disease conditions including asthma, diabetes,
bronchitis, tonsillitis, conjunctivitis and chicken pox.
Themajorityoftheantibioticprescriptions(60)werecompliantwith
theInternationalClassification ofDiseases (2017ICD)while ninewere
not. The nine prescriptions were non- specific, unconventional and lacked
crucial information such as sputum information on the amount, colour,
odour and the presence of blood; “enlarged stomach” did not specify
whether the enlargement was because of gas, solid mass, shifting or fluc-
tuating; “local sepsis” did not contain information on location and nature
ofsepsisandforbacterialexudatethenatureoftheexudate(clearfluid,
puss,odour)wasnot provided.Painfularmpitlackedinformationon the
natureofpain(throbbing,piercing,dull)andwithorwithoutinduration.
Cough, vaginal discharge and sexually transmitted infections were
most commonly indicated for antibiotic prescriptions in that order. For
symptoms and signs involving the gastrointestinal system, diarrhoea
was the commonest indication for antibiotic.
3.5 | Indications for more than one antibiotic per
prescription
Outofthe235encounterswithantibioticprescriptions,45(19.1%),
18(7.7%)and4(1.7%)hadtwo,threeandfourantibioticsperpre-
scription, respectively. Doxycycline was the most common antibi-
oticcombinedasasecondlinedrugfollowedbymetronidazoleand
ceftriaxone,respectively(Table4).Theindicationsforcombination
of antibiotics were mostly sexually transmitted conditions includ-
ing vaginal and urethral discharge and pelvic inflammatory diseases.
Antibiotic ATC classification Frequency (N) Per cent
Beta-lactams (J01C)
Amoxicillin J01CA04 87 28.4
Ampicillin J01CA01 3 1.0
Benzathinepenicillin(Retarpen) J01CE08 13 4.2
Cloxacillin J01CF02 21 6.9
Co- amoxiclav J01CR02 1 0.3
Crystalline penicillin J01CE01 1 0.3
Penicillin V J01CE02 13 4.2
Total Beta- lactams 139 45.4
Cotrimoxazole J01EE01 28 9.2
Ceftriaxone J01DD54 30 9.8
Chloramphenicol capsules S01A01 3 1.0
Chloramphenicol ointment S01AA01 13 4.2
Doxycycline J01AA02 23 7.5
Erythromycin J01FA01 19 6.2
Gentamicin J01GB03 2 0.7
Metronidazole J01XD01 44 14.4
Nitrofurantoin(nitrofuran
derivative)
J01XE 1 0.3
Tetracycline ointment S01AA 3 1.0
Gentamicin ointment SO1AA 1 0.3
Total 306 100
TABLE2 Commonly prescribed
antibiotics at PHC facilities in Botswana
TABLE1 Prescribing practices against documented indicators
Prescription practices N %
Total number of prescriptions analysed 550
Total number of drugs prescribed 1551
Averagedrugs/prescription 2.8
Totalprescriptionswithgeneric(INN)names 1219 78.6
Total antibiotic encounters 235 42.7
Medicines from EDL 1490 96.1
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TABLE3 Classification of the diseases, symptoms and signs
indicated for antibiotics prescription at PHC facilities in Botswana by
2017ICD10-CM/code
Condition ICD- 10- CM/code Frequency
General symptoms and signs
Fever R50 10
Headache R51 8
Dehydration E86.0 1
Symptoms and signs involving the circulatory and respiratory systems
Cough R05 37
Acutetonsillitis J03 18
Nasalcongestion(common
cold)
J00 7
Pharyngitis J02 4
Sputum(unspecified) R09.3 3
Swollenpalate(acute
laryngitisandtracheitis)
J04 2
Asthma J45.909 2
Pleural thickening L85.9 2
Upper respiratory
infections
J06 2
Aspirationpneumonia J69.0 1
Bronchitis J20.0 1
Symptoms and signs involving the digestive system and abdomen
Diarrhoea R19 15
Abdominalandpelvicpain R10 11
Loss of appetite R63 6
Nausea and vomiting R11 4
Constipation K59.0 1
Enteritis K52.9 1
Heartburn(epigastricpain) R12 1
Symptoms and signs involving the skin and subcutaneous tissues
Wound/sores T81.30 12
Rash CM/21 9
Boils and abscesses CM/22 8
Skin condition unspecified R23 7
Herpeszoster B02 2
Chickenpox B01 2
Burn T30.0 2
Allergicdermatitis
(unspecified)
L23.89 2
Acne CM/706 1
Fibrobullar M72 1
Viralwarts(genital) B07 1
Implantation(sub-dermal
contraceptive)
V25.5 1
Skin fungal infection
(unspecified)
L08.9 1
(Continues)
Condition ICD- 10- CM/code Frequency
Endocrine, nutritional and metabolic disease
Diabetes mellitus E08 1
Symptoms and signs involving genitourinary system
Vaginal discharge
(unspecified)
N89.8 34
Sexually transmitted
infections(unspecified)
A64 25
Dysuria(unspecified) R30.0 6
Penile discharge
(unspecified)
R36.9 5
Pelvic inflammatory
disease
N73.9 4
Vagina itching
(unspecified)
N89.4 3
Menstrual disorder
syndrome
N92.6 3
Ovariancyst N83.2 3
Pregnancy masses CM/09A 3
Orchitis N45.2 2
Postsafe male circumcision
(SMC)
Z41.2 2
Painful urinary bladder
(unspecified)
N32.9 1
Diseases of the ear and mastoid process
Otitismedia H60 7
Painful jaw 2
Disorders of soft tissues and chest
Chestpain(unspecified) R07.9 10
Backache M54.9 2
Joint pain M79.609 1
Diseases of the eye and adnexa
Conjunctivitis H10.0 5
Dacryocystitis
(unspecified)
H04.309 1
Symptoms and signs involving breast
Swollenbreast(engorged) N64.59 1
Dental and oral diseases
Dentalcaries(unspecified) K02.9 3
Chronic periodontitis K05.3 2
Toothache(Unspecified) K08.8 1
Traumatic disorders
Injury(unspecified) CM/929.9 14
Fractured index finger
(unspecified)
S62.600A 1
Other unspecified symptoms and signs
Altereddiscomfort 1
Swollen foreskin 1
TABLE3 (Continued)
(Continues)
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4 | DISCUSSION
WhentreatmentswereassessedagainstcrudeWHO/INRUDindicators,
there was evidence of good prescribing practices in Botswana. This is
shownbythefactthat96%ofmedicinesprescribedwereinaccordance
withtheBotswanaEDLand79%ofprescribingwasbyINNname(Table2).
The high rate of prescribing in accordance with the Botswana EDL34 com-
paresfavourablywithWHOrecommendationsof100%10,12,13,41 as well
asratesof55%-80%reportedfortheAfrica,Europe,AmericasandSouth
EastAsiaregions.2,10,42 The high prescribing rate from the EDL could be
attributed to easy accessibility of the Botswana Treatment Guidelines at
PHC facilities,33 the routine availability of medicines incorporated into the
Botswana EDL in PHCs, and the limited influence of pharmaceutical com-
panies unlike other countries.2,21,43-46
ThehighrateofINNprescribinginthisstudyiscomparableto78%
intheWesternPacificregionbuthigherthanratesof27.7%and48.9%
reportedin theEasternMediterraneanandSoutheastAsianregions41
aswell as 68%forAfricaas awhole.10 Possible explanations for high
INN prescribing in this studycould be a result of frequent in-service
training workshops for health workers in Botswana sponsored by the
government, benchmarking with colleagues in the region, the establish-
ment of a medical school whose trainees are exposed to patient care
earlyintheirtrainingwhereprescribingistypicallyINN,andeasyaccess
to digital information. This mirrors successful campaigns in other coun-
triessuchastheUKwithitshighrateofINNprescribing.47,48Inorderto
attainWHO recommendation,9,10we believeINNprescribing training
should be intensified through regular training of in- service practitioners.
In this study, 42.7% of the encounters contained an antibiotic
prescription,higherthan<30%recommendedbyWHO.10,12,13 This is
marginallyhigherthan 39%and 34%fortheAmericasandEuropean
regions,but lowerthan 53%for theEastern Mediterraneanregion41
and Africaas a whole (47%).10 This rate is also higher than 27% in
a previous study in Botswana,31 and higher than 30% for Acute
Respiratory Infections in children under 5 years old previously re-
ported in Botswana.32 The high use of antibiotics could be because
of a high burden of gynaecological and sexually transmitted infec-
tions (Table3). There is also high prevalence (pandemic) of HIV in
Botswana.49 However, these patients are normally treated in spe-
cialist clinics, although in some cases, opportunistic infections may
be treated in PHCs. The extent of multiple antibiotic prescribing is a
concern, but again may reflect the high prevalence of gynaecological
and sexually transmitted infections in our study with up to three an-
tibiotics recommended in the Botswana guidelines for these patients
(Table4).Thiswillbeafutureareaofresearch.
Regarding the quality of antibiotic prescribing, it is generally ac-
cepted as good clinical practice that antibiotics should be prescribed for
specific diagnosis. We found that most of the indications for antibiotic
prescriptions were based on signs and symptoms, rather than specific
diagnoses,andwerecompliantwithICD(Table3).However,ninecondi-
tionsdidnotmatchtheICDwhichcouldeitherresultfromfailureofpa-
tients to express themselves during history taking, poor history taking or
theinabilityofprescriberstoapplyICDcodeswhenarrivingatdifferen-
tialanddefinitivediagnoses.AdoptionofICD10codesforprimarycare
diagnoses would go a long way towards creating a common language
for classifying undifferentiated conditions that are seen in PHC settings.
There are concerns that some diagnoses such as a common cold,
diarrhoea, painful legs, constipation and unclassified muscular pains,
donotwarrantantibiotics(Table3).Inaddition,fourprescriptionseach
containing antibiotics had no established diagnosis. The situation in this
studyishoweverbetterthanreportedinNigeriawhereover50%ofthe
patient’s folders reviewed had no established diagnosis.50 The factors
that contribute to over prescribing of antibiotics include inadequate
in- service training, socio- cultural factors and patient demand.16,18,27,51
Most health facilities in Botswana and elsewhere are characterised
by inadequate skilled human resources. These lower level healthcare
workers are overwhelmed by the large number of patients seeking care
and some pressurising on prescribers to prescribe injections and anti-
biotics.52-54 The establishment of the Medical School in 2009 is a ded-
icated effort by the Government of Botswana to improve the number
andqualityofhealthcareprovidersinthe country.Assessmentoffac-
tors influencing antibiotic prescribing practices was outside the scope
of this study but will be explored further in future research.
The high use of beta- lactamase antibiotics compares favourably
withformerSovietUnionRepublics andTurkeywith ratesof37.5%-
65.6%oftotalJ01 antibiotics.37 The low use of co- amoxiclav is also
encouraging as there are concerns that high utilisation increases side
effects and resistance as well as costs.55-57 With rising concerns on
the development of Clostridium difficile resistance,58,59 the low utilisa-
tionof cephalosporinsin thisstudy (Table2)is alsoencouragingand
comparesfavourablywithrates of0.5%-12.2%among formerSoviet
Union Republics and Turkey.37 Similarly, the lack of fluoroquinolone
prescribing is encouraging attributed to the non-inclusion of these
medicines in the Botswana EDL.34
Inourfutureresearch,wewillaimtoexploreadherencetotreat-
ment guidelines alongside establishing quality indicators for antibiotic
prescribing among providers in both urban and rural PHC facilities in
Botswana, which will assist prescribers with improving their quality
of care.60Adherenceisacomplexphenomenonandtypicallyfarfrom
optimal across countries.19,61-63For instance,46% of antibioticpre-
scriptions in a recent study were not indicated by the guidelines.64
However, higher adherence rates were recently seen in Namibia
(62%),althoughbelow nationaltarget ratesof95%.11 Guideline ad-
herence is influenced by several factors including the level of training
Condition ICD- 10- CM/code Frequency
Enlarged stomach 1
Swellings(unspecified) 4
Local sepsis 2
Bacterial exudate 1
Itchyeyes 8
Painful armpit 1
Musclepain(unspecified) 1
TABLE3 (Continued)
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MASHALLA et AL.
of PHC personnel, available resources at healthcare facilities, work-
load, staff motivation, staff experience and the availability of mana-
gerial tools for monitoring prescribing patterns. Physicians may also
misinterpret patient expectations, influencing adherence rates.65
Effective monitoring can enhance adherence rates.66 Care though
must be taken in communicating appropriate guidelines, especially
if there are differences between different policies and guidelines as
recently seen in Namibia.67
TABLE4 The pattern of antibiotic combinations and the indications at PHC facilities in Gaborone, South East and Kweneng districts,
Botswana
Antibiotics Diagnoses
Amoxicillin Metronidazole Cough Chest pain
Amoxicillin Gentamicin ear drops Ear sores
Amoxicillin Metronidazole Agsoris Headache
Amoxicillin Metronidazole Retarpen Pharyngitis Swollen jaw
Amoxicillin Cotrimoxazole Post SMC
Amoxicillin Cotrimoxazole Cough Eye watering
Amoxicillin Metronidazole Abscess
Amoxicillin Ceftriaxone PV discharge
Amoxicillin Metronidazole Dental caries
Augmentin Doxycycline Pelvic pain Pleural thickening
BenzathinePenicillin Doxycycline Metronidazone Ceftriaxone PV discharge
BenzathinePenicillin Ceftriaxone Gonococcal infection
BenzathinePenicillin Penicillin V Tonsillitis
BenzathinePenicillin Amoxicillin Sputum
BenzathinePenicillin Amoxicillin NIL
BenzathinePenicillin Amoxicillin Bacterial exudate
Ceftriaxone Metronidazole Doxycycline PV discharge
Ceftriaxone Doxycycline Metronidazole PV discharge
Ceftriaxone Doxycycline Metronidazole PV discharge
Ceftriaxone Doxycycline Metronidazole Penile rash
Ceftriaxone Metronidazole Abdominalpain
Ceftriaxone Doxycycline Urethral discharge
Ceftriaxone Doxycycline Metronidazole Pelvic pain PV discharge
Ceftriaxone Doxycycline Metronidazole PV discharge
Ceftriaxone Doxycycline Metronidazole STIdischarge
Ceftriaxone Erythromycin PV discharge Gynaecological pelvis
Ceftriaxone Doxycycline Metronidazole PV discharge VRT
Ceftriaxone Cotrimoxazole Metronidazole Doxycycline PV discharge
Ceftriaxone Metronidazole Erythromycin Pregnant masses
Ceftriaxone Erythromycin Metronidazole Cotrimoxazole PV discharge Dysuria
Ceftriaxone Doxycycline Urethral discharge
Cloxacillin Bactrim Abscess
Cotrimoxazole Ceftriaxone Doxycycline Metronidazole PID
Doxycycline Ceftriaxone Orchitis
Doxycycline Metronidazole STIcontact
Doxycycline Metronidazole STIcontact
Doxycycline Ceftriaxone Metronidazole PV discharge
Gentamicin Chloramphenicol Dacryocystitis Chest pain
Metronidazole Ceftriaxone Erythromycin PV discharge
Metronidazole Ceftriaxone Doxycycline PV discharge
Continues
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MASHALLA et AL.
Based on our findings, we recommended that in order to improve
prescribing at PHC facilities in Botswana, it is essential that prescrib-
ers be provided with in- service training on the use of current national
treatment guidelines, classification of diseases, INN prescribing, as
wellas properhistorytaking andrecordingofdiagnoses.Inaddition,
BotswanashouldconsideradoptingICD10forprimarycaretoaideas-
ier classification of undifferentiated conditions that present in PHC
facilities. Pharmacists should also play a key role in promoting rational
prescribing practices by conducting drug utilisation reviews and using
the findings to stimulate dialogue among practitioners to enhance the
future rational use of medicines at PHC facilities.
The Ministry of Health and Wellness, as the major stakeholder re-
sponsible for policy formulation and guidance, should seek to design a
harmonised managerial tool that will contain pertinent quality indica-
tors for monitoring antibiotic prescribing practices at all PHC facilities.
This includes targets for adherence to National Treatment Guidelines
as well as classes of antibiotics prescribed, building on European and
otherguidance.Anyqualityindicatorsdevelopedmustreflectcurrent
conditions in ambulatory care as seen by the high prevalence of gy-
naecological and sexually transmitted infections in Botswana, which
is not universal especially among European populations. This will help
addressconcernswithcurrentWHO/INRUDcriteria.Similarly,multi-
sector antimicrobial initiatives and programmes should be developed
and implemented across all locations to improve future antibiotic
prescribing through monitoring antimicrobial usage as well as devel-
oping and implementing strategic interventions aimed at optimising
antimicrobialuse andreducingAMR.This mayhelp toimprove anti-
biotic prescribing in the futurein Botswana and reduce AMR rates.
Hopefully any quality indicators developed will also be of interest to
otherAfricancountriesandwiderwithsimilarpopulations.
5 | LIMITATIONS
The study was carried out in an urban area of Botswana and did
not include rural areas. However, as mentioned, this is where the
majority of patients are currently treated in Botswana, although we
recognise there could be differences in the characteristics of the re-
spectivepatientpopulations.Inaddition,theresultsarefromaret-
rospective collection of data, and information on the characteristics
of practitioners was not collected. However, we believe our findings
will already give guidance to key stakeholders on ways to improve
antibiotic prescribing in Botswana. We also believe our ongoing re-
search to develop pertinent quality indicators across all locations,
including both urban and rural PHCs, will be of interest to other
Africancountriesandwider.
ACKNOWLEDGEMENTS
This study was funded by the University of Botswana Office of
Research and Development and the authors wish to acknowledge the
Ministry of Health, Botswana for granting permission to carry out the
study and to the staff and patients in the PHC facilities. We would also
liketothankDrAmanjBakerKurdiforhishelpfulcommentsregarding
potential statistical analyses.
DISCLOSURE
The authors declare no competing interests with this study.
AUTHOR CONTRIBUTIONS
YM, VS, AM, ES and MC designed the study and were involved in
thecollectionandanalysis.YH,AMandBGproducedtheinitialdraft
manuscript.Allauthorscritiquedsuccessive draftsofthemanuscript
before submission and re- submission.
ORCID
Brian Godman http://orcid.org/0000-0001-6539-6972
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How to cite this article:MashallaY,SetlhareV,MasseleA,
etal.Assessmentofprescribingpracticesattheprimary
healthcare facilities in Botswana with an emphasis on
antibiotics: Findings and implications. Int J Clin Pract.
2017;71:e13042. https://doi.org/10.1111/ijcp.13042