Trans R Soc Trop Med Hyg 2023; 0: 1–7

https://doi.org/10.1093/trstmh/trad083 Advance Access publication 0 2023

National health insurance scheme improves access and optimization of

ORIGINAL ARTICLE
antimicrobial use in the Obafemi Awolowo University Teaching
Hospitals Complex, Ile-Ife, Nigeria

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a,∗
Temitope O. Obadare , Taiwo O. Ogundipeb , Adeyemi T. Adeyemo a , Caleb M. Aboderinc , Doyin R. Abiolaa ,
Naheemot O. Suled , and Aaron O. Aboderin a ,e

a
Department of Medical Microbiology and Parasitology, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Osun State,
P.M.B. 5538 220222, Nigeria; b Pharmacy Department, Obafemi Awolowo University Teaching Hospitals Complex. Ile-Ife, Osun State,
P.M.B. 5538 220222, Nigeria; c Faculty of Clinical Sciences, Obafemi Awolowo University, Ile-Ife, Osun state, P.M.B. 13 220282, Nigeria;
d
Department of Epidemiology, Biostatistics and Occupational Statistics, McGill University, Montreal, Quebec, 845 Sherbrooke, H3A 0GA,
Canada; e Department of Medical Microbiology and Parasitology, Obafemi Awolowo University, Ile-Ife, Osun State, P.M.B. 220282,
Nigeria
∗ Corresponding author: Tel: +234 80 6416 7371; E-mail: [email protected]

Received 28 April 2023; revised 27 September 2023; editorial decision 29 October 2023

Background: Nigeria instituted the National Health Insurance Scheme (NHIS) for universal health coverage. This
study compared the NHIS and out-of-pocket (OOP) antibiotic prescribing with the World Health Organization
(WHO) optimal values.
Methods: A total of 2190 prescription forms from the NHIS and OOP were included in this study conducted at
Obafemi Awolowo University Teaching Hospitals Complex, Nigeria from January 2021 to December 2022 and
analysed using WHO drug prescribing guidelines.
Results: The average number of drugs per encounter was higher in the NHIS prescribing (χ 2 =58.956, p=0.00)
than in OOP prescribing. The percentage of encounters with an antibiotic prescribed is higher in NHIS prescribing
(χ 2 =46.034, p=0.000) than in OOP prescribing. The percentage of parenteral antibiotic prescribing is higher in
OOP prescribing (χ 2 =25.413, p=0.000) than in NHIS prescribing. The percentage of antibiotic prescribed from
the National Essential Medicine List is higher in NHIS prescribing (χ 2 =8.227, p=0.000) as well as the antibiotics
prescribed from the Access category of the WHO Access, Watch and Reserve (AWaRe) Classification of antibiotics
(χ 2 =23.946, p=0.000) when compared with OOP prescribing.
Conclusions: Prescribing indicators show better performances with NHIS antibiotic prescribing and are closer to
the WHO-recommended optimal values than in OPP prescribing. Hence NHIS prescribing can be an easy target
for hospital antibiotic stewardship intervention for optimal antibiotic prescribing.

Keywords: antibiotic stewardship, AWaRe categories, NHIS, Nigeria, prescribing pattern

Introduction OOP health expenditures are decreasing globally, in Nigeria they

are increasing (74.68%), making it one of the highest in the
Health inequality exists globally, however, its effect is more pro- world.3
nounced in low- and middle-income countries (LMICs) because Furthermore, the emergence of antimicrobial resistance (AMR)
of meagre government investments in health infrastructure; poor has complicated the management of infections generally, erod-
water, sanitation and hygiene; absent or low health insurance ing the possibilities of modern medicine and derailing the Sustain-
coverage; poor accessibility or availability of essential medicines able Development Goals (SDGs) and economic advancement.4
and high household out-of-pocket (OOP) health expenditures.1 , 2 While AMR is an evolutionary process, it is hastened by misuse
In the World Health Organization (WHO) African Region, about and overuse of antimicrobials, manifesting as inept, excessive
10% of the population reports that their health expenditures prescribing, especially in situations where antibiotics are used as
exceed one-tenth of their total household expenditures. While

© The Author(s) 2023. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene.
All rights reserved. For permissions, please e-mail: [email protected]

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T. O. Obadare et al.

a ‘quick fix’ for a dilapidated healthcare system, as well as equi- (OAUTHC), Ile-Ife, Southwest, Nigeria. The NHIS was instituted
table healthcare delivery which is pervasive in LMICs.5 at the OAUTHC in 2011 with an average number of 1500 NHIS-
In an effort to achieve universal health coverage (UHC) as rec- covered prescriptions monthly. The OAUTHC has a capacity of 600
ommended by the WHO to ensure health equity, Nigeria insti- beds with an average of 21 000 patients per month. It has 10
tuted the National Health Insurance Scheme (NHIS) in 2009 with pharmacy outlets and the bulk of the NHIS operations take place
a mandate to enrol 30% of Nigerians by 2015. The scheme at the main pharmacy unit. The main pharmacy unit is managed
became an act of law (National Health Insurance Authority Act by six resident pharmacists, three intern pharmacists and three

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[NHIA]) in 2022 to eliminate the inherent limitations of the NHIS health attendants.
and make health insurance enrolment compulsory irrespective
of employment status, with the aim of improving health cover-
age as well as the Gini index (a direct measure of income and Study design and study population
wealth inequality) of the country.6–8 This is in tandem with the This cross-sectional study surveyed all the NHIS and OOP pre-
recommendation of the Lancet Nigeria Commission that aimed scriptions over a 24-month period (January 2021–December
to shape future health policy in Nigeria to achieve UHC for all and 2022). Illegible and/or torn prescription forms where critical
eliminate OOP expenditures, which is implicated as a major driver details were missing were excluded from the study.
of antibiotic overprescribing in LMICs.9
Core drug use indicators to objectively measure drug use were
introduced by the WHO about 3 decades ago to determine the Sampling
drug use situation in a county, region or healthcare facility.10 , 11
A systematic sampling method was used for this study. The dis-
In 2017, the WHO updated the Model List of Essential Medicines
pensary record book (where the details of the patients as well
(EML) and incorporated AWaRe (Access, Watch, Reserve; Not rec-
as the drugs dispensed are recorded) was obtained from the
ommended was added in 2019) classification of antibiotics as an
pharmacy through the permission of the pharmacy head. Ballot-
antimicrobial stewardship tool to help physicians, pharmacists,
ing was used to select the first name on the dispensary record
hospital administrators and relevant ministries and government
among the list of the first 10 names on the record for each month.
departments to work towards a common goal to optimize
Subsequently, other names were systematically selected at a
appropriate prescribing of antimicrobial drugs, thereby tackling
fixed interval of 10 names for both OOP and NHIS prescriptions.
antimicrobial resistance.12 One of the major achievements of
The corresponding names on the dispensary record were then
the NHIS is the prompt, affordable accessibility to anti-infective
matched with the prescription sheets selected for the study.
drugs.13 , 14 However, this should be situated in the context of the
sustainable effectiveness of antimicrobials, which is principally
hinged on robust and well-structured antibiotic stewardship
Data collection
programs to prevent excessive or irrational use.15 Healthcare
insurance has been reported to increase the prescribing of A total of 10 500 (5575 OOP, 4925 NHIS) prescription sheets were
antibiotics and other drugs, especially so in resource-constrained recorded in the dispensary record book over the period of investi-
settings with intrinsic problems of poverty and ignorance, which gation and 2190 (1095 OOP, 1095 NHIS) prescription sheets were
make patients perceive the scheme as one that can provide systematically sampled for this study. The prescriptions were all
them more drugs than needed at minimal or no cost.16 , 17 Access paper-based and the sampling of the prescription sheets was
to UHC accompanied by appropriate antibiotic stewardship done manually by the three scientific officers and a research
intervention, could potentially contribute to curbing AMR by assistant who were trained in data collection and confidential-
optimizing antibiotic use.18 However, there is a dearth of data on ity (by a consultant clinical microbiologist) before the sampling
the pattern of antibiotic prescribing in the NHIS in Nigeria despite in this study. The prescription sheet selection and data collection
increasing enrolment in tertiary hospitals. There have been were all done under the supervision of a consultant clinical micro-
national and facility efforts at developing an antibiotic steward- biologist. All the data were stored on a password-protected com-
ship program (ASP) in Nigeria, but the possibility of integrating it puter for confidentiality. Prescription sheets that were torn or had
into the NHIS in a context-specific manner has not been explored. unreadable handwriting were excluded from the study. The data
There is also no information on the alignment of NHIS antibiotic entry was done using Excel 2022 (Microsoft, Redmond, WA, USA).
prescribing with the WHO AWaRe classification in Nigeria as well
as its role in antibiotic use optimization. This study investigated
the pattern of antibiotic prescribing in the NHIS and compared Data collection tool
it with OOP prescribing in a tertiary hospital and determined Section 1 of the form recorded socio-demographic information.
its compliance with the optimal value for rational prescribing Section 2 of the form recorded the indicators for drug use
indicators and WHO AWaRe classification for antibiotics. (what WHO classifies as core indicators only). Prescribing
core indicators included the number of medicines per encounter,
number of antibiotics per encounter, prescription for a generic
Methods form of the antibiotic, antibiotic prescriptions from the NHIS
essential formularies, route of drug administration and
Study location duration.10–12 , 19
This study was conducted in the pharmacy department of Section 3 of the form recorded AWaRe categories, Anatomical
the Obafemi Awolowo University Teaching Hospitals Complex Therapeutic Chemical (ATC) classification of the antibiotics as well

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as their inclusion in the National Essential Drug List of Nigeria (7th encountered per prescription 0.59±0.78), which accounted for
edition).12 , 20 19.6% (1291/6597) of the total drug encounters. Oral antibi-
otics were the most prescribed route of antibiotic administra-
tion (67.4% [870/1291]). Overall, 66% (852/1291) of antibiotics
Data analysis were prescribed by the generic name, while 96.6% (1247/1291)
Statistical analysis was done using Statistical Package for Social were prescribed from the national EML (Table 1). The overall
Sciences version 23 software (IBM, Armonk, NY, USA). Descrip- antibiotics prescribed in the Access category of the WHO AWaRe

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tive analysis of data was done and presented as frequencies, classification was 47.4% (612/1291) (Table 1). Antibiotics were
means, proportions and percentages. The categorical variables prescribed more for paediatric patients (Pearson’s χ 2 =4.446,
were compared by χ 2 and p-values <0.05 were considered p=0.035), while polypharmacy (number of drugs/encounter ≥5)
significant.21 The average number of drugs per encounter, was more significantly associated with antibiotics prescribing in
percentage of encounters with an antibiotic prescription, per- NHIS prescribing (χ 2 =12.744, p=0.000).
centage of parenteral antibiotics prescribed, percentage of The most prescribed specific antibiotic in NHIS prescribing
antibiotics prescribed from the national EML and percentage was metronidazole (J01XD01/P01AB01; 25.91% [206/795]),
of antibiotics prescribed from the Access category of the WHO followed by cefuroxime (J01DC02; 21.01% [167/795]),
AWaRe classification of antibiotics were calculated. The cut-off ciprofloxacin (J01MA02; 15.60% [124/795]), amoxicillin–
for the optimal values for rational prescribing was adapted from clavulanate (J01CR02; 12.08% [96/795]) and amoxicillin
the WHO documents ‘Guide to Drug Financing Mechanisms’ and (J01CA04; 11.70% [93/795]). In the OOP, the most common
‘Adopt AWaRe: Handle Antibiotics with Care’.11 , 22 For example, prescribed antibiotic was metronidazole (J01XD01/P01AB01;
the optimal value of the average number of drugs per encounter 24.40% [121/496], followed by ciprofloxacin (J01MA02; 17.54%
is <2 and the optimal value of the percentage of encounters [87/496]), cefuroxime (J01DC02; 13.51% [67/496]), ceftriax-
with an antibiotic prescription is <30%.11 , 22 one (J01DD04; 11.49% [57/496]) and amoxicillin–clavulanate
(J01CR02; 10.08% [50/496]) (Table 2). Penicillin (J01C; χ 2 =9.052,
p=0.0030) and macrolides (J01F; χ 2 =13.311, p=0.000) were
prescribed significantly more in NHIS prescribing compared with
Results OOP prescribing (Table 2).
Appraisal of documentation on NHIS and OPP
prescription forms Comparison of NHIS and OOP antibiotic prescribing
The demographic characteristics of the patients were docu- indicators with WHO optimal values
mented on the prescription sheets. The patients’ names, iden- The average number of drugs per encounter was significantly
tification numbers, dates and names of the prescribing doctors higher in NHIS prescribing (3.21±4.6/2.81±1.43; WHO optimal
(as well as the signatures) were present on all the prescrip- value <2; χ 2 =58.956, p=0.00) than in OOP prescribing. The per-
tions; for confidentiality, personal identifiers were excluded in the centage of encounters with an antibiotic prescribed was sig-
data capturing. However, weights and heights were not included nificantly more in NHIS prescribing (22.6%/15.2%; WHO opti-
in both the OPP and NHIS prescription sheets. A total of 41% mal value <30%; χ 2 =46.034, p=0.000) than in OOP prescribing
(456/1095) of OOP and 62.6% (685/1095) of NHIS prescription (Table 1). The percentage of encounters with an oral antibiotic
sheets had the exact age documented (the remaining had age was significantly greater in NHIS prescribing (72.7%/15.2%; WHO
categories: paediatric [≤14 y] or adult [>14 y]). Drug-related optimal value <30%; χ 2 =26.597, p=0.000), while parenteral
information such as the name of the prescribed drug, dosage, antibiotic prescribing was significantly greater in OOP prescribing
duration of use and formulation was stated for all the prescrip- (40.5%/27.0%; WHO optimal value <20%; χ 2 =25.413, p=0.000).
tions reviewed, but there was no diagnosis or indication for the Moreover, the percentage of antibiotics prescribed from the
prescriptions documented (Supplementary File 1). national EML was significantly greater in NHIS prescriptions
(97.7%/94.8%; WHO optimal value 100%; χ 2 =8.227, p=0.000),
as well as the antibiotics prescribed from the Access category of
Demographic distribution of prescriptions
the WHO AWaRe classification of antibiotics (52.7%/38.9%; WHO
A total of 2190 prescriptions were analysed in this study, 1095 optimal value >60%; χ 2 =23.946, p=0.000) when compared with
each for NHIS and OOP. The distribution of the prescription across OOP prescriptions.
sexes was a female:male ratio of 2.1:1 (1472/718) and most
of the prescriptions (91.2% [1998/2190]) belonged to the adult
(≥15 y) unit of the hospital (Table 1). Discussion
The average number of drugs per encounter in the NHIS in
this study (3.21) conforms with earlier documented patterns in
Pattern of antibiotic prescribing Nigeria.13 , 16 , 23 Likewise, antibiotics are prescribed significantly
A total of 6597 drug encounters were included in 2190 pre- more in the NHIS than in OPP (22.6%/15.2%), which is in keep-
scriptions. The average number of drugs encountered per pre- ing with the Fadare et al.16 study in Nigeria (49.4% vs 33.6%).
scription was 3.01±1.82, with 3519 from NHIS and 3078 However, the percentage of antibiotics prescribed in the NHIS
from OOP prescriptions. A total of 1291 antibiotic encounters in our setting is lower compared with what was reported in the
were obtained in this study (average number of antibiotics Fadare et al.16 (49.4%) and Okoro et al.13 (46.9%) studies, which

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Table 1. Sociodemographic and prescription characteristics, medicine, and antibiotic prescribing indicators at the OAUTHC from January 2021
to December 2022

Sociodemographic and prescription characteristics

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Test statistics
WHO-
NHIS (n=1095), OOP (n=1095), recommended
Variables n (%) n (%) standard Pearson’s χ 2 p-Value

Sex
Female 723 (66.0) 749 (68.4)
Male 372 (34.0) 346 (31.6)
Unit of the hospital
Paediatric (≤14 y) 146 (13.3) 66 (6.0) 33.424 0.000
Adult (≥15 y) 949 (86.7) 1029 (94.0) 33.424 0.000
Number of drugs/encounter
1–2 381 (34.8) 511 (46.7) 16.362 0.000
3–4 500 (45.7) 440 (40.2)
≥5 214 (19.5) 144 (13.2)
Drug prescribing indicators (N=6597)
NHIS (n=3519) OOP (n=3078)
Average number of drugs per encounter, 3.21±4.6 2.81±1.43 <2 58.956 0.00
mean±SD
Encounters with an antibiotic 795 (22.6) 469 (15.2) <30 46.034 0.000
prescribed, n (%)
Antibiotic prescribing indicators (N=1291)
NHIS (n=795) OOP (n=496)
Encounter an antibiotic injection prescribed, n (%)
Parenteral 215 (27.0) 201 (40.5) <20 25.413 0.000
Oral 578 (72.7) 292 (58.9) 26.597 0.000
Guttate 2 (0.3) 3 (0.6)
Antibiotic prescribed from national EML, 777 (97.7) 470 (94.8) 100% 8.227 0.004
n (%)
Antibiotic prescribed by generic name, 795 (22.6) 496 (15.2) 100% 46.034 0.000
n (%)
AWaRe categories, n (%)
Access 419 (52.7) 193 (38.9) >60% 23.946 0.000
Watch 366 (43.0) 296 (59.7)
Reserve 0 (0.0) 0.0 (0.0)
Not recommended 10 (1.3) 7 (1.4)
Encounter with antibiotic (N=925)
NHIS (n=576) OPP (n=349)
Unit of the hospital, n (%)
Paediatric (≤14 y) 69 (12.0) 28 (8.0) 3.624 0.057
Adult (≥15 y) 507 (88.0) 321 (92.0)
Number of drugs/encounter, n (%)
1–2 159 (27.6) 132 (37.8) 5.311 0.025
3–4 272 (47.2) 152 (43.6)
≥5 145 (25.2) 65 (18.6)

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Transactions of the Royal Society of Tropical Medicine and Hygiene

Table 2. The pattern of antibiotic prescription by ATC classification at the OAUTHC from January 2021 to December 2022

NHIS (n=795), OOP (n=496),

Classes of antibiotics Antibiotic ATC classification n (%) n (%) Pearson’s χ 2 p-Value

Penicillins J01C 9.052 0.003

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Amoxicillin J01CA04 93 (11.7) 40 (8.06)
Amoxicillin-Clavulanate J01CR02 96 (12.1) 50 (10.1)
Ampicillin J01CA01 15 (1.9) 0 (0.0)
Ampicillin-Cloxacillin 10 (1.3) 7 (1.4)
Macrolides J01F 13.311 0.000
Azithromycin J01FA10 9 (1.1) 10 (2.0)
Clarithromycin J01FA09 6 (0.8) 15 (3.0)
Erythromycin J01FA01 2 (0.3) 5 (1.0)
Lincosamides J01FA01 J01F 1.604 0.205
Clindamycin J01FF01 0 (0.0) 1 (0.2)
Cephalosporins J01D 0.022 0.882
2nd generation Cefuroxime J01DC02 167 (21.0) 67 (13.5)
3rd generation Ceftriaxone J01DD04 32 (4.0) 57 (11.5)
Cefixime J01DD08 4 (0.5) 0 (0.0)
Cefpodoxime J01DD13 3 (0.4) 6 (1.2)
Ceftazidime J01DD02 1 (0.1) 1 (0.2)
Quinolones J01M 2.248 0.134
Ciprofloxacin J01MA02 124 (15.6) 87 (17.5)
Levofloxacin J01MA12 7 (0.9) 11 (2.2)
Ofloxacin J01MA01 6 (0.8) 4 (0.8)
Tetracyclines J01A 5.140 0.023
Doxycycline J01AA02 1 (0.1) 5 (1.0)
Aminoglycosides J01G 0.456 0.499
Gentamicin J01GB03 4 (0.5) 4 (0.8)
Carbapenem J01D 0.005 0.942
Meropenem J01DH02 3 (0.38) 2 (0.40)
Imidazole J01X/P01A 0.372 0.542
Metronidazole J01XD01/P01AB01 206 (25.9) 121 (24.4)
Nitrofurantoin J01XE01 0.059 0.809
Nitrofurantoin J01XE01 4 (0.5)
Glycopeptides J01X 1.250 0.264
Vancomycin J01XA01 2 (0.3) 0 (0.0)

are comparable with another study in Africa (Tanzania; 46.4%).17 While there is a dearth of data on the pattern of antibiotic
This change could be due to prescription modification among prescribing in outpatient settings in Nigeria, in a study from a
prescribers at our facility due to previous prescription audits and tertiary hospital in Ethiopia, 69.7% of outpatients had antibiotics
upgraded medical microbiology laboratory support by the Flem- prescribed. Thus NHIS prescribing can be targeted towards imple-
ing Fund for improved diagnostic capacity.24 The NHIS facilitates menting outpatient ASPs, as most antibiotics were inappropri-
the affordability of drugs, including antibiotics, in hospital set- ately prescribed.27 For example, the registry of the prescribers
tings and subsequently improves the availability of appropriate in the NHIS could be leveraged to provide targeted ASP inter-
antimicrobials of assured quality in resource-constrained settings ventions for antibiotic prescribers, as these data can be anal-
where substandard and falsified antibiotics provide selective ysed to identify ‘high-volume’ antibiotic prescribers in health-
pressure for the emergence of antibiotic-resistant pathogens.25 care facilities that could be targeted for antibiotic stewardship
There were more oral antibiotics prescribed in the NHIS than interventions.28 However, this should be in the context of possi-
in the OPP (72.7% vs 58.9%) and this reflects that the majority ble interventions such as prescribers’ education, peer comparison
of prescribing in the NHIS is on an outpatient basis. While most audits and feedback. Restrictive interventions such as formulary
of the ASPs are focused on patients admitted to the hospital, restrictions and compulsory order forms might not be available
outpatients, who accounted for the most prescribed antibi- in many African countries because of the nascent development
otics, were grossly untargeted for ASP interventions generally.26 of national antimicrobial stewardship interventions.29

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T. O. Obadare et al.

The use of penicillins and macrolides is usually driven by out- percentage of antibiotics by generic name, encounters with
patients for the treatment of respiratory tract infections (RTIs), antibiotic prescribing, oral antibiotic prescribing, compliance with
which is the most common indication for antibiotic prescrip- the EML and the proportion of the Access antibiotic category)
tion in general practice.30 In our setting, penicillins (J01C) and show better performance with NHIS prescribing compared with
macrolides (J01F) were prescribed significantly more in NHIS pre- OOP prescribing. While the antibiotic prescribing indicators were
scribing than OOP prescribing, and this could be explained by generally suboptimal in our settings, antibiotic prescribing in
high use of antibiotics among patients from the paediatric unit the NHIS was closer to the WHO-recommended optimal values

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in the NHIS as well as the availability of both drugs in oral formu- than in OOP prescribing. This should encourage further studies
lations. Penicillins and macrolides prescribing, especially in RTIs, to investigate antibiotic prescribing in the NHIS and how this can
is usually precautionary due to the tendency for bacterial infec- be incorporated into the hospital-based antibiotic stewardship
tion complications in paediatric patients because of their naïve program to optimize antibiotic use in our settings, especially in
immunity. This, coupled with parental anxiety and perceived outpatient care.
antibiotic expectations, puts pressure on prescribers to prescribe
antibiotics.30 However, prescribing of penicillins and macrolides
in the NHIS could be reduced by providing parental education on Supplementary data
the need for no antibiotics in uncomplicated RTIs and utilization Supplementary data are available at Transactions online.
of medical microbiology laboratory investigations of the present-
ing complaints before antibiotics use.30 , 31
In this study, the antibiotic prescribing indicators such as the
Authors’ contributions: TOObadare, ATA and AOA conceived and con-
percentage of encounters with an antibiotic injection prescribed, ceptualized the study. TOObadare, AOA, ATA, TOOgundipe designed the
the percentage of antibiotics prescribed from the national EML, study protocol. TOObadare and ATA assessed the prescription patterns.
the percentage of antibiotics prescribed by generic name and the TOObadare, ATA, CMA, DRA and NOS performed, analysed and interpreted
percentage of antibiotics in the Access category of the AWaRe prescription data. TOObadare and ATA drafted the manuscript. AOA crit-
classification prescribed, were less than the WHO-recommended ically reviewed the manuscript for intellectual content. All authors read,
optimal values. However, the study revealed that prescribing indi- revised, edited and approved the final version of the manuscript and had
cators were significantly closer to the WHO optimal values in NHIS the final responsibility for the decision to submit for publication.
prescribing than in OPP prescribing. This shows that the NHIS has
a unique inherent capability to optimize antibiotic prescribing in Acknowledgments: We thank the staff and leadership of the pharmacy
department of the OAUTHC for their cooperation during and after this
our settings and therefore it can be a potential target for antibi-
survey.
otic stewardship programs in hospital settings for interventions
by further reinforcement of prescribing from the national EML.28
Funding: None.
In this study, more than half of the total prescriptions did
not have the exact age of the patient included the prescrip- Competing interests: None declared.
tion sheets. This omission might be due to the fatigue of the
high volume of patients that the prescribers have to attend to, Ethical approval: Ethical approval for this study was obtained
which might reduce attention to details. Moreover, the indi- from the Ethics and Research Committee of the OAUTHC (protocol
cation or diagnosis was not documented on the prescription ERC/2021/03/01).
sheets because of a design limitation of the prescription sheets
(Supplementary File 1). These omissions limited the scope of Data availability: Data are available from the authors upon reasonable
this study, as analyses could not be done across age groups request and with the permission of the OAUTHC data management and
and diagnoses. Moreover, the paper-based prescriptions in use ethical committee.
in our settings limited easy matching of high-volume antibiotic
prescribers by looking at the prescription sheets alone. This might
complicate the prescription audit necessary to generate data References
that are required to implement antibiotic stewardship interven- 1 Tackling drug-resistant infections globally: final report and recom-
tions and also limited this study. However, the findings of this mendation. 2016. Available from: https://apo.org.au/sites/default/
study are valid as this study employed a unique methodological files/resource- files/2016- 05/apo- nid63983.pdf
approach, the first of its kind in Nigeria (to our best knowledge) 2 World Health Organization. WHO report on surveillance of antibiotic
to investigate antibiotic prescribing patterns in the NHIS, their consumption. Geneva: World Health Organization; 2018. Avail-
compliance with the WHO AWaRe classification and WHO- able from: https://iris.who.int/bitstream/handle/10665/277359/
recommended rational prescribing values compared with OOP 9789241514880-eng.pdf?sequence=1
prescribing. This study explored the role of antibiotics prescribing 3 World Health Organization. Global health expenditure database. Avail-
in the NHIS for possible leverage for antibiotic stewardship to able from: https://apps.who.int/nha/database/country_profile/Index/
address the dearth of data on this subject. en
4 Jamrozik E, Selgelid M, editors. Ethics and drug resistance: collec-
tive responsibility for global public health. Volume 5. Melbourne, VIC,
Conclusions Australia: Monash University.
There is improved antibiotic use with NHIS prescribing because 5 Denyer Willis L, Chandler C. Quick fix for care, productivity, hygiene and
all the quality indicators (average number of drug encounters, inequality: reframing the entrenched problem of antibiotic overuse.

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Transactions of the Royal Society of Tropical Medicine and Hygiene

BMJ Glob Health. 2019;4(4):e001590. https://doi.org/10.1136/ 19 Asenso RO. A closer look at the World Health Organization’s prescrib-
bmjgh- 2019- 001590 ing indicators. J Pharmacol Pharmacother. 2016;7(1):51–4.
6 Adebisi SA, Odiachi JM, Chikere NA. The National Health Insurance 20 Federal Ministry of Health and Social Welfare. Nigeria Essen-
Scheme (NHIS) in Nigeria: has the policy achieved its intended objec- tial Medicines List 2020 7th Edition. Abuja: Federal Ministry of
tives? Acad J Econ Stud. 2019;5(3):97–104. Health and Social Welfare; 2020:1–65. https://www.health.gov.ng/
7 Christina C, Latifat T, Collins N, et al. National health insurance scheme: doc/Nigeria- Essential- Medicine- List- 2020.pdf
how receptive are the private healthcare practitioners in a local gov- 21 Vetter TR. Descriptive statistics: reporting the answers to the 5 basic

Downloaded from https://academic.oup.com/trstmh/advance-article/doi/10.1093/trstmh/trad083/7453513 by guest on 29 November 2023

ernment area of Lagos state. Niger Med J. 2014;55(6):512–6. questions of who, what, why, when, where, and a sixth, so what?
8 Ipinnimo TM, Durowade KA, Afolayan CA, et al. The Nigeria national Anesth Analg. 2017;125(5):1797–802.
health insurance authority act and its implications towards achieving 22 World Health Organization. The 2019 WHO AWaRe classification of
universal health coverage. Niger Postgr Med J. 2022;29(4):19–26. antibiotics for evaluation and monitoring of use. 2019. Geneva: World
9 Abubakar I, Dalglish SL, Angell B, et al. The Lancet Nigeria Com- Health Organization.
mission: investing in health and the future of the nation. Lancet. 23 Adebayo ET, Hussain NA. Pattern of prescription drug use in Nigerian
2022;399(10330):1155–200. army hospitals. Ann Afr Med. 2010;9(3):152–8.
10 World Health Organization. How to investigate drug use in health facil- 24 Aboderin AO, Adeyemo AT, Olayinka AA, et al. Antimicrobial use
ities: selected drug use indicators. Geneva: World Health Organization; among hospitalized patients : a multi-center, point prevalence sur-
1993. vey across public healthcare facilities, Osun State, Nigeria. Germs.
11 Dumoulin J, Miloud Kaddar GV. Guide to drug financing mechanisms. 2021;11(4):523–35.
Geneva: World Health Organization; 1998. 25 Mendelson M, Røttingen J-A, Gopinathan U, et al. Maximising access
12 World Health Organization. The 2019 WHO AWaRe classification of to achieve appropriate human antimicrobial use in low-income and
antibiotics for evaluation and monitoring of use. Geneva: World Health middle-income countries. Lancet. 2016;387(10014):188–98.
Organization; 2019. 26 Dijck CV, Vlieghe E, Arnoldine JC. Antibiotic stewardship interventions
13 Okoro RN, Nmeka C, Erah PO. Antibiotics prescription pattern and in hospitals in low-and middle-income countries: a systematic review.
determinants of utilization in the national health insurance scheme Bull World Health Org. 2018;96(4):266–80.
at a tertiary hospital in Nigeria. Afr Health Sci. 2019;19(3):2356–64. 27 Yimenu DK, Emam A, Elemineh E, et al. Assessment of antibiotic
14 Tangcharoensathien V, Chanvatik S, Sommanustweechai A. Complex prescribing patterns at outpatient pharmacy using World Health
determinants of inappropriate use of antibiotics. Bull World Health Organization prescribing indicators. J Prim Care Community Health.
Org. 2018;96(2):141–4. 2019;10:2150132719886942.
15 Karanika S, Paudel S, Grigoras C, et al. Systematic review and meta- 28 World Health Organization. Antimicrobial stewardship programmes in
analysis of clinical and economic outcomes from the implementa- health-care facilities in low- and middle-income countries: a WHO
tion of hospital-based antimicrobial stewardship programs. Antimi- practical toolkit. Geneva: World Health Organization; 2019.
crob Agents Chemother. 2016;60(8):4840–52. 29 Fuller WL, Aboderin AO, Yahaya A, et al. Gaps in the implementation of
16 Fadare J, Adeoti A, Aina F, et al. The influence of health insurance national core elements for sustainable antimicrobial use in the WHO-
scheme on the drug prescribing pattern in a Nigerian tertiary health- African region. Front Antibiot. 2022;23:1047565.
care facility. Niger Med J. 2015;56(5):344. 30 Bou-Antoun S, Costelloe C, Honeyford K, et al. Age-related decline in
17 Khalfan MA, Sasi PG, Mugusi SF. The prevalence and pattern of antibi- antibiotic prescribing for uncomplicated respiratory tract infections
otic prescription among insured patients in Dar es Salaam Tanzania. in primary care in England following the introduction of a national
Pan Afr Med J. 2021;40:140. financial incentive (the Quality Premium) for health commissioners
to reduce use of antibiotic. J Antimicrob Chemother. 2018;73(10):
18 Singn PK. A universal good: how increased health coverage can help
2883–92.
beat back antimicrobial resistance. Geneva: World Health Orga-
nization; 2017. https://www.who.int/southeastasia/news/opinion- 31 Muraki Y, Kusama Y, Tanabe M, et al. Impact of antimicrobial stew-
editorials/detail/a- universal- good- how- increased- health- coverage- ardship fee on prescribing for Japanese pediatric patients with upper
can- help- beat- back- antimicrobial- resistance respiratory infections. BMC Health Serv Res. 2020;20(1):399.

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