Abstract
Introduction
Antimicrobial resistance (AMR) is a global public health crisis. This study assessed the general public’s consumption of antibiotics and associated factors in the Lusaka district of Zambia.
Methods
This cross-sectional study was conducted among 2038 participants between December 2022 and January 2023. Data were analysed using Stata 13.0. Multivariable regression techniques were used to determine the factors that influenced antibiotic consumption.
Results
Of the 2038 participants, 53.4% were female, and 51.5% had attended at least secondary school. Antibiotic use was 99.2%, of which 40.9% were appropriately used. Overall, 79.1% of antibiotics were prescribed in hospitals, while 20.9% were used from leftovers and accessed without prescriptions. This study found that the appropriate use of antibiotics was associated with being female, being aged 35 years and above, attaining secondary school or tertiary education, having a monthly expenditure of 195 USD and above, being aware that antibiotics were not the same as painkillers, and being confident that when someone was hospitalized, they would get well.
Conclusions
This study found that the appropriate use of antibiotics was low, and this is an urgent public health issue requiring community engagement in tackling AMR and adherence to treatment guidelines in healthcare facilities. Additionally, there is a need to implement and strengthen antimicrobial stewardship programmes in healthcare facilities to promote the rational use of antibiotics in Zambia. There is also a need to heighten community awareness campaigns and educational activities on the appropriate use of antibiotics.
Introduction
Antibiotics are medicines used to prevent and treat bacterial infections in humans, animals and plants.1,2 Unfortunately, their inappropriate use is among the major contributing factors to developing antimicrobial resistance (AMR).3–8 AMR is a common public health issue worldwide and is currently referred to as a silent pandemic.5,9–14 It poses a serious threat to all advances in modern medicine, the success of which depends on antimicrobials, causing increased mortality, longer hospital stays and higher medical expenses.5,10,15–17 Consequently, if AMR is not addressed, it is projected that approximately 10 million people more will die annually and an estimated 24 million more will live in extreme poverty by the year 2050.18–20
AMR is an inevitable natural phenomenon but accelerated by the high consumption and misuse of antimicrobials.21,22 This may happen through antimicrobial overprescribing or underprescribing by prescribers, empirical treatment, self-medication and purchasing drugs without a legal prescription.10,23–27 Some determinants affect the choice and attitude towards antimicrobial use (AMU).28–31 Some factors influence individuals’ choices and attitudes toward AMU, including readily accessible retail pharmacies, which have emerged as the predominant source of outpatient care in Africa.28,32 Other determinants of AMU include gender, as well as the individual’s level of knowledge and attitude.33 Other factors contributing to AMR’s emergence include a lack of diagnostic tools in hospitals, a lack of patient education on AMU and AMR, inadequate antibiotic regulatory mechanisms, and the unauthorized sale of antimicrobials.21 Further, the overuse and misuse of antimicrobials in the animal sector also contribute to the emergence and spread of antimicrobial-resistant infections.34–36 This has been demonstrated by an increased number of pathogens that have developed resistance to antimicrobials, some of which are of human priority.37–41
The selling of antimicrobials, especially antibiotics, is recognized as one of the more profitable businesses, especially in the private health sector.42–44 This sector is well developed in low-and middle-income countries (LMICs),45 but it is not well regulated and is frequently neglected by governments, even though private pharmacies are perceived as the community’s first source of healthcare.21,46 This situation constitutes the main reason for the high consumption of antibiotics and, consequently, may contribute to the extensive selection of resistant bacteria in the community.47–49 This is because there is a link between antibiotic consumption and AMR.50–53 Despite this understanding, the misuse and overuse of antibiotics persist globally in both healthcare facilities and the community because of the complex interplay between profitability, regulation and the public health challenges associated with antibiotic use.23,54,55
The inappropriate prescription of antimicrobials is tied to the prescribers’ lack of knowledge and attitudes towards the rational use of antimicrobials, and physicians can be forced to prescribe antibiotics for conditions like upper respiratory tract infections (URTIs) due to the perceived effectiveness of these drugs, even when the evidence indicates that antibiotics may not be necessary.56–60 This pressure is noted to be significant in the context of South Africa, among other African countries.23,56,61,62 Additionally, the inappropriate use of antibiotics has been reported to be due to a lack of: diagnostic tests; poor infection, prevention and control (IPC) practices; insufficient funding; poor vaccine coverage and uptake; illegal drug stores; substandard antibiotics; irresponsible use of laboratory services by clinicians; and a lack of political will.31,63–65 The most inappropriate use of antibiotics is observed in cases of: URTIs; generally self-limited viral infections; acute diarrhoea; and urinary tract infections.21,66,67 The inappropriate prescription of antimicrobials leads to increased AMR and mortality, morbidity and healthcare costs.68 Moreover, inappropriate antibiotic use has economic repercussions, particularly concerning URTIs in the African context.66,69 The escalated costs imply that the inappropriate use of antibiotics not only adds to health-related challenges but also carries economic implications.69
The lack of surveillance on antimicrobial use implies that the breadth of AMR issues in Africa needs to be better documented.70 Currently, there are inadequate updated data on AMR in African countries, with only 42.6% of the countries reported to have documented some data.71 Ample data on the burden of infections caused by antibiotic-resistant bacteria in developed countries, such as the EU, reveal approximately 33 110 (28 480–38 430) deaths and 874 541 (768 837–989 068) disability-adjusted life years (DALYs) are attributed to the resistant microbes,72 whilst the insufficient data on AMR in Zambia reveal that a significant number of pathogens resistant to the most commonly prescribed antibiotics may be circulating in the communities.71,73
Addressing the factors that lead to AMR requires developing and implementing antimicrobial stewardship (AMS) programmes.74–83 AMS programmes are effective in promoting the rational use of antibiotics among community members.77–79,84 Therefore, community engagement through antibiotic awareness campaigns is critical in addressing some factors contributing to the overuse and misuse of antibiotics in communities.85–88 Additionally, community-based educational programmes must also focus on behavioural change in the use of antibiotics.74,89–92 Furthermore, the gravity of this issue is underscored by a recent report from the Organisation for Economic Co-operation and Development (OECD).93 The report predicts that over the next 30 years, 2.4 million individuals in Europe, North America and Australia could die from infections caused by resistant microorganisms, incurring an annual cost of up to 3.5 billion USD.93 Additionally, many LMICs, including Zambia, already grapple with elevated resistance rates, projected to escalate disproportionately. Consequently, the anticipated cost of AMR in these nations might surpass that projected for the developed countries mentioned earlier, given that there is still a high percentage of surveyed pharmacists who still dispense antibiotics without a prescription.94,95
Zambia is a country in sub-Saharan Africa with a high burden of infectious diseases.73,96–103 Additionally, there is evidence of misuse and overuse of antibiotics among Zambian communities.94,104–108 Consequently, there is evidence of antimicrobial-resistant pathogens across the human and animal sectors.37,38,41,99,109–115 A study by Masich et al.116 revealed that about 67% of antimicrobials were inappropriately prescribed to non-critically ill adult patients admitted to the University Teaching Hospital in Lusaka, Zambia. Intriguingly, the Zambian government has put in measures to promote the appropriate use of antibiotics by developing and implementing the National Action Plan (NAP) on AMR.117,118 The Antimicrobial Resistance Coordinating Committee (AMRCC) has been coordinating activities to educate the general public on the appropriate use of antibiotics and AMR. However, there is a paucity of information concerning the appropriate consumption of antibiotics among the general public in Zambian communities. Therefore, this study assessed antibiotic consumption and associated factors among residents in selected communities of Lusaka district, Zambia.
Materials and methods
Study design, setting and population
This cross-sectional study was conducted between December 2022 and January 2023 among residents of Lusaka district in Zambia. A cross-sectional study design was chosen because this was a population-based survey and it allowed for collection of data from the participants during the same period to avoid discrepancies in the findings. Lusaka district was selected because it is the most developed and well-represented population of different ethnicities and communities of different socioeconomic backgrounds and constitutes an excellent attraction factor for any commercial activity. Furthermore, many pharmacies in Lusaka provide healthcare services to the communities.105 The national population of Zambia is agglomerated essentially around Lusaka Province in the south and Copperbelt Province in the North, the two core economic hubs of the country.119 With a total area of 21 896 km2, Lusaka Province is Zambia’s smallest province but the most densely populated and urbanized province. Lusaka Province has a population of about 3 million people and a density of 140.1 people/km2 (Census of Zambia, 2022).120 The province is divided into six districts: Lusaka (population: 2 204 059), Chilanga (population: 225 276), Chongwe (population: 313 389), Kafue (population: 219 574), Luangwa (population: 35 933) and Rufunsa (population: 81 733).120 Based on existing geopolitical structure, population size and covered health services, Lusaka district was divided into 11 study areas: Mtendere, Kaunda Square, Chelstone, Kalingalinga, Chainda, Chipata, Ng’ombe, Matero, George, Kanyama and Chawama. Lusaka Province is located in the south-central part of the country.
Study population and sample size estimation
The sampling sites represented 11 communities with approximately 10 000 people in each area. We used Cochrane’s formula to estimate the sample size.121 Given a 33% expected appropriate use of antibiotics, as reported earlier,116 and a margin of error of 5%, we estimated a minimum sample size of 340 participants. All the participants were selected using stratified and simple random sampling methods. Each area contained at least one health centre and health posts serving approximately 10 000 residents. To be eligible, a participant was an adult resident of the selected communities in the Lusaka district and provided consent to participate in the study. Therefore, this study excluded all respondents under 18 years old and those who had not resided in Lusaka for at least a year. Individuals who did not use antibiotics in the last 12 months during the data collection period were also excluded from the study. All participants were first grouped into their respective community areas. This was followed by sampling each participant from randomly selected households.
Data collection
Data collection was done using a structured questionnaire (Supplementary data S1, available as Supplementary data at JAC-AMR Online). The questionnaire was reviewed for content and face validity by experts from the University of Zambia. Before the main study, a pilot study was undertaken in October 2022, and a sample of 482 participants was collected only from shopping malls, churches, streets, markets, parking areas and healthcare facilities within the selected study areas, which allowed the researchers to understand important variations among the population of the Lusaka district and validated the data collection tool. The findings of the pilot study were excluded from the main study findings. In the main study, from the randomly selected households, a simple random sampling method was used to select participants who were interviewed face to face using a structured questionnaire with Epicollect5 software (https://five.epicollect.net/). The questionnaire was designed in English with three sections: site; sociodemographic information of the participants; access to antibiotics and pattern of antibiotic use. The maximum time for the interview was approximately 20 to 30 min.
Data management and analysis
The data collected from Epicollect5 were imported into a Microsoft Excel spreadsheet version 2013 for data cleaning. The cleaned data were transferred to STATA version 17.0 for descriptive and statistical analysis. The outcome variable was appropriate antibiotic use by the study participants. In this study, appropriate antibiotic use was defined as obtaining antibiotics through a prescription written by a qualified prescriber and completing the course of antibiotic therapy as recommended. Univariable analysis was used to determine the relationship between residents’ antibiotic consumption and explanatory variables, gender, age, level of education, marital status, monthly income, being aware that antibiotics were not the same as painkillers, and confidence that an admitted patient would get well. In the first step, analysis was performed to identify important covariates; we fitted one predictor variable at a time, using the chi-squared test or, where necessary, the Fisher’s exact test, to establish potential determinants of appropriate antibiotic consumption. After that, the candidate variables were selected based on the P value cut-off point of 0.25, which is a purposeful selection of the algorithm as proposed by Hosmer and Lemeshow,122 whereas those risk factors with P > 0.25 were left out as having no significant effect on the outcome. The logistic regression model was built with variables selected in step 1 through a backward selection strategy, using a P value of <0.05 of the likelihood ratio test as inclusion criteria.
Ethics
Ethical approval for this study was sought from ERES CONVERGE IRB, approval Ref. No. 2022-Mar-020. Regulatory approval was obtained from the National Health Research Authority (NHRA) with an approval number of NHRA0000016/31/102022. Participation in the study was voluntary after providing informed and written consent.
Results
Demographic information of the participants
A total of 2038 Lusaka residents were enrolled in this study, of which 53.4% were female and the majority (27.6%) aged between 31 and 35 years. The number of respondents interviewed from each area varied between 146 and 221. Most of the population (57.8%) were married, 72.1% had attended at least secondary school, and 91.9% spent below 195 USD per month (Table 1).
Table 1.
Variable | Variable level/group | Frequency | (%) |
---|---|---|---|
Residential area | Mtendere | 159 | 7.80 |
Kaunda square | 208 | 10.20 | |
Chelstone | 166 | 8.10 | |
Kalingalinga | 177 | 8.70 | |
Chainda | 221 | 10.80 | |
Chipata | 187 | 9.20 | |
Ng’ombe | 179 | 8.80 | |
Matero | 201 | 9.90 | |
George | 195 | 9.60 | |
Kanyama | 199 | 9.80 | |
Chawama | 146 | 7.10 | |
Gender | Male | 950 | 46.60 |
Female | 1088 | 53.40 | |
Age group (years) | 18–25 | 476 | 23.40 |
26–30 | 461 | 22.60 | |
31–35 | 563 | 27.60 | |
Above 35 | 538 | 26.40 | |
Marital status | Unmarried | 860 | 42.20 |
Married | 1178 | 57.80 | |
Level of education | Up to primary level | 568 | 27.90 |
Secondary and above | 1470 | 72.10 | |
Monthly expenditure | Below 195 USD | 1874 | 91.90 |
195 USD and above | 164 | 8.10 |
Antibiotic acquisition information
Most residents (73.2%) obtained their antibiotics from healthcare facilities (hospitals and clinics), and 79.1% of these participants purchased antibiotics at the pharmacy using a medical prescription (Table 2). Few (17/2038) residents claimed never to have used antibiotics in the last 12 months.
Table 2.
Variable | Group | Frequency (n) (N = 2038) | (%) |
---|---|---|---|
Where did you obtain your last antibiotic? | NA (neither suffered nor use of antibiotic) | 17 | 0.8 |
Health facility | 1495 | 73.2 | |
Leftover antibiotics from the previous treatment | 169 | 8.3 | |
Pharmacy | 338 | 16.5 | |
Do not know or do not remember | 24 | 1.2 | |
How did you obtain your last antibiotic used? | Prescribed by a doctor or a clinical officer and dispensed by a pharmacist | 1598 | 79.1 |
Recommended and supplied by a pharmacist or drug retailer without a prescription | 310 | 15.3 | |
Self-medicated (you indicate to the pharmacist what drug you want) | 113 | 5.6 |
Pattern of antibiotic consumption among residents of Lusaka district
Out of the 2021 participants who used antibiotics, 921 (45.6%) used antibiotics correctly, although 95 (4.7%) did not obtain their antibiotics properly. Thus, the proportion of appropriate use of antibiotics is estimated at 40.9% (those who obtained antibiotics using prescriptions and used them as guided), while 59.1% accounted for inappropriate use of antibiotics (Table 3).
Table 3.
When did you stop taking the last antibiotics you purchased? (N = 2021) | How did you obtain the last antibiotics you took? | Total | |
---|---|---|---|
Prescribed by a doctor/clinical officer and dispensed by a pharmacy professional, n (%) | Not prescribed by a doctor or a clinical officer, n (%) | ||
When my illness was better | 741 (36.7) | 323 (16.0) | 1064 |
When I got a full course as prescribed by a doctor or clinical officer | 826 (40.9) | 95 (4.7) | 921 |
I do not remember | 31 (1.5) | 5 (0.3) | 36 |
Total | 1598 | 423 | 2021 |
Antibiotic consumption among residents of Lusaka district with associated factors
The univariable analysis (cross-tabulation between predictor and outcome variable) of the sociodemographic characteristics versus antibiotic consumption among residents of the Lusaka district showed that all the independent variables examined were significantly associated with the study outcome (Table 4).
Table 4.
Characteristic | Total | Taken as prescribed and recommended by the prescriber | Not prescribed nor taken as recommended by the prescriber | P value | ||
---|---|---|---|---|---|---|
N | n | % | n | % | ||
Total | 2038 | 829 | 40.7 | 1209 | 59.3 | |
Gender | <0.001 | |||||
Male | 950 | 343 | 16.8 | 607 | 29.8 | |
Female | 1088 | 486 | 23.9 | 602 | 29.5 | |
Age group (years) | <0.001 | |||||
18–25 | 476 | 163 | 8.0 | 313 | 15.4 | |
26–30 | 461 | 158 | 7.8 | 303 | 14.9 | |
31–35 | 563 | 219 | 10.8 | 344 | 16.9 | |
Above 35 | 538 | 289 | 14.2 | 249 | 12.2 | |
Marital status | <0.037 | |||||
Unmarried | 860 | 327 | 16.1 | 533 | 26.1 | |
Married | 1178 | 502 | 24.6 | 676 | 33.2 | |
Level of education | <0.001 | |||||
Up to primary level | 568 | 108 | 5.3 | 460 | 22.6 | |
Secondary and above | 1470 | 721 | 35.4 | 749 | 36.7 | |
Monthly expenditure | <0.001 | |||||
Below 195 USD | 1874 | 736 | 31.1 | 1138 | 60.8 | |
195 USD and above | 164 | 93 | 4.6 | 71 | 3.5 | |
Antibiotics are the same as Dolaren, Paracetamol, Diclofenac | 0.001 | |||||
True | 182 | 59 | 2.9 | 123 | 6.0 | |
False | 1366 | 540 | 26.5 | 826 | 40.5 | |
I do not know | 490 | 230 | 11.3 | 260 | 12.8 | |
When a patient is admitted to a hospital | <0.001 | |||||
I am confident they will get well | 694 | 256 | 12.6 | 438 | 21.5 | |
Not confident | 1173 | 526 | 25.8 | 647 | 31.7 | |
It depends on the sickness | 124 | 22 | 1.1 | 102 | 5.0 | |
I do not know | 47 | 25 | 1.2 | 22 | 1.1 |
Factors affecting appropriate consumption of antibiotics among study participants
The multivariable logistic regression model results showed that the appropriate use of antibiotics was related to gender. The appropriate use of antibiotics was associated with being female, age above 35 years, attaining secondary school or tertiary education, having a monthly expenditure of 195 USD and above, being aware that antibiotics were not the same as painkillers like paracetamol and diclofenac, and being aware of the disease that a patient suffered made Lusaka residents confident that someone will get well after being admitted to hospital (Table 5). Females were more likely (OR = 1.4) to use antibiotics appropriately than males. Additionally, participants who were aged above 35 years of age were more likely (OR = 2.1) to use antibiotics compared with those who were aged between 18 and 25 years. Further, participants who attained secondary school or tertiary education were more likely (OR = 4.6) to use antibiotics appropriately compared with those who had only reached primary school level. Furthermore, participants who had a monthly expenditure of 195 USD and above were more likely to use antibiotics appropriately than those who spent less than 195 USD per month. Our study also revealed that those who were aware that antibiotics were not the same as painkillers were more likely (OR = 1.5) to use antibiotics appropriately than those who thought antibiotics were the same as painkillers.
Table 5.
Variable | Characteristics | Adjusted OR | 95% CI | P value |
---|---|---|---|---|
Gender | Male | 1 | ||
Female | 1.4 | 1.17–1.73 | <0.001 | |
Age (years) | 18–25 | 1 | ||
26–30 | 0.8 | 0.61–1.08 | 0.155 | |
31–35 | 1.1 | 0.84–1.46 | 0.454 | |
Above 35 | 2.1 | 1.58–2.74 | <0.001 | |
Level of education | Up to primary level | 1 | ||
Secondary and above | 4.6 | 3.53–5.86 | <0.001 | |
Monthly expenditure | Below 195 USD | 1 | ||
195 USD and above | 1.9 | 1.34–2.76 | <0.001 | |
Antibiotics are like painkillers | True | 1 | ||
False | 1.5 | 1.02–2.24 | 0.041 | |
I do not know | 1.1 | 0.79–1.61 | <0.501 | |
A patient is admitted | I am confident they will get well | 1 | ||
Not confident | 0.9 | 0.75–1.18 | 0.582 | |
It depends on the sickness | 0.4 | 0.21–0.59 | <0.001 | |
I do not know | 1.3 | 0.66–2.43 | 0.483 |
Discussion
This study assessed the public consumption of antibiotics and the associated sociodemographic factors among residents of selected communities in the Lusaka district of Zambia. Of the 2038 participants, 2021 (99.2%) had used antibiotics in the last 12 months during data collection. The rate of appropriate use of antibiotics was 40.9% and associated with being female, being aged above 35 years, attaining secondary school or tertiary education, having a monthly expenditure of 195 USD and above, being aware that antibiotics were not the same as painkillers, and being confident that when someone was hospitalized, they would get well. A total of 59.1% of the participants used antibiotics inappropriately.
Our study found a high use of antibiotics (99.2%) among the residents of the Lusaka district. The high use of antibiotics in our study is evidenced by the high use of antibiotics (79.1%) in healthcare facilities and access to antibiotics without prescription (20.9%). These findings corroborated reports from a study that was conducted among communities of Ilala, Kilosa and Kibaha districts of Tanzania, where 99% of residents were reported to have used antibiotics.123 These results could be partially attributed to the easy antibiotic access, as reported by earlier studies.31,94,124–126 Additionally, the high use of antibiotics could be attributed to increased prescribing of antibiotics in healthcare facilities.127,128 The high use of antibiotics in healthcare facilities continues to be reported across the world.129–132
The high use of antibiotics reported in our study could also be attributed to self-medication (SM) practices among the residents of the sampled communities. SM practices were also reported to be 55.2% in Vietnam, 45.7% in Bangladesh, and 36.1% in Ghana.133 However, lower SM practices were reported in Mozambique (8%), Thailand (3.9%) and South Africa (1.2%).133 Community members tend to practise SM because it is more convenient than going to healthcare facilities, cheaper, and less time-consuming than going to the hospital.133 The use of antibiotics reported in our study was higher than the 64.2% reported in Bosnia and Herzegovina134 and 38.4% in Nepal.45 It is evident that the high consumption of antibiotics predisposes individuals to AMR infections.124 Hence, there is a need to reduce these practices to avoid the emergence of AMR and its consequences.
The present study found that the proportion of appropriate use of antibiotics among the study participants was 40.9%, translating into 59.1% of inappropriate use of antibiotics in the sampled communities. The appropriate use of antibiotics in our study is slightly higher than the 33% reported at the University Teaching Hospitals in Lusaka, Zambia.116 The low appropriate use of antibiotics in our study could be due to increased access to antibiotics without prescriptions, non-completion of antibiotic courses by community members, and the taking of leftover antibiotics. A recent study conducted in Southwest China on antibiotic prescribing patterns at children’s outpatient departments of primary care institutions concluded that for over 37 284 visits, only 18.3% of antibiotic prescriptions were appropriate.135 A study in Kuwait reported that 36% of the sampled population had not finished the course of treatment, and 27.5% practised SM with antibiotics to treat mainly common cold, sore throat and cough.136 A survey among residents of sub-Saharan African countries reported high SM practices and access to antibiotics without a prescription.24 However, the level is noticeably lower compared with a previous study done in Zambia where there was 100% access to antibiotics without a prescription.94 Consequently, the population that access antibiotics through community pharmacies tends to be lower than the one that does so through public healthcare facilities.
A study in Ethiopia reported 62.1% appropriate use of antibiotics among community members of Yirgalem town, Sidama regional state, with 37.9% of the residents having used antibiotics inappropriately due to long delays in obtaining services at healthcare facilities, busy day programmes, and cutting costs of medication.137 These practices of accessing antibiotics without a prescription, non-adherence to completion of antibiotic courses, and taking leftover antibiotics have been reported in other studies.138,139 A study in Ghana reported 86.6% inappropriate use of antibiotics, which was due to the community members buying antibiotics using their out-of-pocket money, seeking healthcare services outside hospitals/clinics, seeking medical help in pharmacies, and buying antibiotics in instalments.140 A multinational study involving Cambodia, Madagascar and Senegal found that 76.5% of antibiotics for outpatients were inappropriately prescribed.141 There is also a notable and higher prevalence of SM with antibiotics without a prescription among community pharmacies in South Africa.142 Consequently, the inappropriate use of antibiotics is a driver of AMR and requires urgent community education and engagement.51,137,143–145
Our multivariable logistic regression found that the appropriate use of antibiotics was associated with being female, being aged above 35 years, attaining secondary school or tertiary education, having a monthly expenditure of 195 USD and above, being aware that antibiotics were not the same as painkillers like paracetamol and diclofenac, and being confident that when someone was hospitalized, they would get well. Based on our findings, females tend to use antibiotics more appropriately than males, indicating better compliance with instructions on the medication and avoidance of SM practices. These findings corroborate those reported in another study.137 This is because females tend to have better health-seeking behaviour compared with males.146 Similar to our findings, other studies have demonstrated that older age was associated with the appropriate use of antibiotics,147 while younger populations tend to use antibiotics inappropriately.137,148 This also could indicate poor health-seeking behaviour among the young population and reduced income to access medical services. Evidence has shown that individuals with a low education level tend to misuse antibiotics more compared with those with a high education level.147,149 However, attaining higher education must be accompanied by a change in behaviour for individuals to appropriately utilize antibiotics.150
Consequently, income may affect access to antibiotics as those from low-income settings tend to buy short courses of antibiotics and are unable to access medical services from hospital facilities, thereby resorting to SM and contributing to inappropriate use of antibiotics.27,140,149 Intriguingly, community members with adequate finances can seek medical help and purchase the required courses of antibiotics when prescribed.27 Our findings demonstrate the impact of sociodemographics on the appropriate use of antibiotics among community members.
We are aware that our study had limitations. First, our study was conducted in one district of Lusaka province; hence, the results may not be generalizable for the entire province and the country. Second, this study used a cross-sectional study design that is prone to recall bias. Additionally, a question concerning the use of antibiotics in the last 12 years may also lead to recall bias. Finally, we did not collect information on the actual conditions that led to the use of antibiotics. However, the study provided critical information on the consumption of antibiotics and associated predisposing factors among community members, and this can form the basis for developing and implementing interventional strategies.74,77–79,151 Additionally, educational activities may be used to promote the awareness and knowledge of community members of AMR. Intriguingly, the findings of this study may be used to promote community engagement in the fight against AMR.
Conclusions
This study found high consumption of antibiotics among the community members of the Lusaka district of Zambia, with most antibiotics accessed through the hospitals and clinics. The appropriate use of antibiotics was low among the study participants. Our study found that appropriate use of antibiotics was associated with being female, an age of 35 years and above, attaining secondary school or tertiary education, having a monthly expenditure of 195 USD and above, being aware that antibiotics were not the same as painkillers, and being confident that when someone was hospitalized, they would get well. To address the low appropriate consumption of antibiotics found in this study, there is a need to promote educational campaigns on the appropriate use of antibiotics, improved antibiotic prescribing practices, and heightened regulations on access to antibiotics without a prescription. Additionally, AMS programmes should be strengthened in hospitals and clinics to ensure rational prescribing and use of antibiotics. Finally, there is a need to enhance community engagement in the fight against AMR.
Supplementary Material
Acknowledgements
We acknowledge the participants who took part in this study. We are also grateful to the University of Zambia for providing all the references in this publication.
Contributor Information
Maty Tsumbu Ngoma, Department of Disease Control, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia.
Doreen Sitali, Department of Health Promotion, School of Public Health, University of Zambia, Lusaka, Zambia.
Steward Mudenda, Department of Pharmacy, School of Health Sciences, University of Zambia, Lusaka, Zambia.
Mercy Mukuma, Department of Food Science, School of Agricultural Sciences and Nutrition, University of Zambia, Lusaka, Zambia.
Flavien Nsoni Bumbangi, Department of Medicine and Clinical Sciences, School of Medicine, Eden University, Lusaka, Zambia.
Emmanuel Bunuma, Department of Biomedical Sciences, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia.
Eystein Skjerve, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Ås, Norway.
John Bwalya Muma, Department of Disease Control, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia.
Funding
The Masters' degree programme for the student was supported by the Africa Centre of Excellence for Infectious Disease of Humans and Animals (ACEIDHA) project (grant number P151847) funded by the World Bank and the project NORPART-2018/10213 funded by the Norwegian Agency for International Cooperation and Quality Enhancement in Higher Education.
Transparency declarations
All authors declare no conflict of interest. All the authors do not have any financial interests or connections that may directly or indirectly raise concerns of bias in the work reported or the conclusions, implications or opinions made in this publication.
Supplementary data
Supplementary Data S1 is available as Supplementary data at JAC-AMR Online.
References
- 1. Tacconelli E, Carrara E, Savoldi A et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18: 318–27. 10.1016/S1473-3099(17)30753-3 [DOI] [PubMed] [Google Scholar]
- 2. Cook MA, Wright GD. The past, present, and future of antibiotics. Sci Transl Med 2022; 14: eabo7793. 10.1126/scitranslmed.abo7793 [DOI] [PubMed] [Google Scholar]
- 3. WHO . Antimicrobial Resistance and the United Nations Sustainable Development Cooperation Framework. 2021. https://www.who.int/publications/i/item/9789240036024.
- 4. Martino PA. Antibiotic Resistance: A One-Health Approach. MDPI, 2023. https://mdpi-res.com/bookfiles/book/6603/Antibiotic_Resistance.pdf?v=1708499066.
- 5. Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health 2015; 109: 309. 10.1179/2047773215Y.0000000030 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Chang Y, Chusri S, Sangthong R et al. Clinical pattern of antibiotic overuse and misuse in primary healthcare hospitals in the southwest of China. PLoS One 2018; 14: e0214779. 10.1371/journal.pone.0214779 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Sweileh WM. Global research publications on irrational use of antimicrobials: call for more research to contain antimicrobial resistance. Global Health 2021; 17: 94. 10.1186/s12992-021-00754-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Zanichelli V, Tebano G, Gyssens IC et al. Patient-related determinants of antibiotic use: a systematic review. Clin Microbiol Infect 2019; 25: 48–53. 10.1016/j.cmi.2018.04.031 [DOI] [PubMed] [Google Scholar]
- 9. Jindal BAK, Pandya MK, Khan MID. Antimicrobial resistance: a public health challenge. Med J Armed Forces India 2015; 71: 178–81. 10.1016/j.mjafi.2014.04.011 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Ikuta KS, Swetschinski LR, Robles Aguilar G et al. Global mortality associated with 33 bacterial pathogens in 2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 2022; 400: 2221–48. 10.1016/S0140-6736(22)02185-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Gautam A. Antimicrobial resistance: the next probable pandemic. J Nepal Med Assoc 2022; 60: 225–8. 10.31729/jnma.7174 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Paneri M, Sevta P, Paneri M et al. Overview of antimicrobial resistance: an emerging silent pandemic. Glob J Med Pharm Biomed Updat 2023; 18: 11. 10.25259/GJMPBU_153_2022 [DOI] [Google Scholar]
- 13. Mendelson M, Sharland M, Mpundu M. Antibiotic resistance: calling time on the ‘silent pandemic’. JAC Antimicrobial Resist 2022; 4: dlac016. 10.1093/jacamr/dlac016 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Mahoney AR, Safaee MM, Wuest WM et al. The silent pandemic: emergent antibiotic resistances following the global response to SARS-CoV-2. iScience 2021; 24: 102304. 10.1016/j.isci.2021.102304 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Murray CJ, Ikuta KS, Sharara F et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 2022; 399: 629–55. 10.1016/S0140-6736(21)02724-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Nwobodo DC, Ugwu M, Anie CO et al. Antibiotic resistance: the challenges and some emerging strategies for tackling a global menace. J Clin Lab Anal 2022; 36: e24655. 10.1002/jcla.24655 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Ait Ouakrim D, Cassini A, Cecchini M et al. The health and economic burden of antimicrobial resistance. Eur J Public Health 2020; 30 Suppl 5: 23–44. 10.1093/eurpub/ckaa165.120131270547 [DOI] [Google Scholar]
- 18. de Kraker MEA, Stewardson AJ, Harbarth S. Will 10 million people die a year due to antimicrobial resistance by 2050? PLoS Med 2016; 13: e1002184. 10.1371/journal.pmed.1002184 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Jonas OB, Irwin A, Berthe FCJ et al. Drug-Resistant Infections: A Threat To Our Economic Future. 2017. https://documents.worldbank.org/en/publication/documents-reports/documentdetail/323311493396993758/final-report. [Google Scholar]
- 20. Meerza SIA, Brooks KR, Gustafson CR et al. Information avoidance behavior: does ignorance keep us uninformed about antimicrobial resistance? Food Policy 2021; 102: 102067. 10.1016/j.foodpol.2021.102067 [DOI] [Google Scholar]
- 21. Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: causes and control strategies. Antimicrob Resist Infect Control 2017; 6: 47. 10.1186/s13756-017-0208-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Mir S, Brett D, Adam de la B et al. Antibiotics overuse and bacterial resistance. Ann Microbiol Res 2019; 3: 93–9. 10.36959/958/573 [DOI] [Google Scholar]
- 23. Allabi AC, Agbo AG, Boya B et al. Antimicrobial stewardship: knowledge and attitudes of pharmacy staff on antibiotic dispensing patterns, use and resistance in Benin. Pharmacol Pharm 2023; 14: 189–214. 10.4236/pp.2023.146014 [DOI] [Google Scholar]
- 24. Sono TM, Yeika E, Cook A et al. Current rates of purchasing of antibiotics without a prescription across sub-Saharan Africa; rationale and potential programmes to reduce inappropriate dispensing and resistance. Expert Rev Anti Infect Ther 2023; 21: 1025–55. 10.1080/14787210.2023.2259106 [DOI] [PubMed] [Google Scholar]
- 25. Cambaco O, Alonso Menendez Y, Kinsman J et al. Community knowledge and practices regarding antibiotic use in rural Mozambique: where is the starting point for prevention of antibiotic resistance? BMC Public Health 2020; 20: 1183. 10.1186/s12889-020-09243-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Barker AK, Brown K, Ahsan M et al. What drives inappropriate antibiotic dispensing? A mixed-methods study of pharmacy employee perspectives in Haryana, India. BMJ Open 2017; 7: e013190. 10.1136/bmjopen-2016-013190 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Barker AK, Brown K, Ahsan M et al. Social determinants of antibiotic misuse: a qualitative study of community members in Haryana, India. BMC Public Health 2017; 17: 333. 10.1186/s12889-017-4261-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Goodluck M, Basiliana E, Mgabo MR et al. Community knowledge and attitudes on antibiotic use in Moshi Urban, northern Tanzania: findings from a cross-sectional study. African J Microbiol Res 2017; 11: 1018–26. 10.5897/AJMR2017.8583 [DOI] [Google Scholar]
- 29. Alhomoud F, Almahasnah R, Alhomoud FK. “You could lose when you misuse”—factors affecting over-the-counter sale of antibiotics in community pharmacies in Saudi Arabia: a qualitative study. BMC Health Serv Res 2018; 18: 915. 10.1186/s12913-018-3753-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Harvey EJ, De Brún C, Casale E et al. Influence of factors commonly known to be associated with health inequalities on antibiotic use in high-income countries: a systematic scoping review. J Antimicrob Chemother 2023; 78: 861–70. 10.1093/jac/dkad034 [DOI] [PubMed] [Google Scholar]
- 31. Byrne MK, Miellet S, McGlinn A et al. The drivers of antibiotic use and misuse: the development and investigation of a theory-driven community measure. BMC Public Health 2019; 19: 1425. 10.1186/s12889-019-7796-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32. Dejene H, Birhanu R, Tarekegn ZS. Knowledge, attitude and practices of residents toward antimicrobial usage and resistance in Gondar, Northwest Ethiopia. One Health Outlook 2022; 4: 10. 10.1186/s42522-022-00066-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33. Machowska A, Lundborg CS. Drivers of irrational use of antibiotics in Europe. Int J Environ Res Public Health 2018; 16: 27. 10.3390/ijerph16010027 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34. Mudenda S, Bumbangi FN, Yamba K et al. Drivers of antimicrobial resistance in layer poultry farming: evidence from high prevalence of multidrug-resistant Escherichia coli and enterococci in Zambia. Vet World 2023; 16: 1803–14. 10.14202/vetworld.2023.1803-1814 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35. Lekagul A, Tangcharoensathien V, Yeung S. The use of antimicrobials in global pig production: a systematic review of methods for quantification. Prev Vet Med 2018; 160: 85–98. 10.1016/j.prevetmed.2018.09.016 [DOI] [PubMed] [Google Scholar]
- 36. Van TTH, Yidana Z, Smooker PM et al. Antibiotic use in food animals worldwide, with a focus on Africa: pluses and minuses. J Glob Antimicrob Resist 2020; 20: 170–7. 10.1016/j.jgar.2019.07.031 [DOI] [PubMed] [Google Scholar]
- 37. Mudenda S, Malama S, Munyeme M et al. Antimicrobial resistance profiles of Escherichia coli isolated from laying hens in Zambia: implications and significance on one health. JAC Antimicrob Resist 2023; 5: dlad060. 10.1093/jacamr/dlad060 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38. Mudenda S, Matafwali SK, Malama S et al. Prevalence and antimicrobial resistance patterns of Enterococcus species isolated from laying hens in Lusaka and Copperbelt provinces of Zambia: a call for AMR surveillance in the poultry sector. JAC Antimicrob Resist 2022; 4: dlac126. 10.1093/jacamr/dlac126 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39. Ribeiro J, Silva V, Monteiro A et al. Antibiotic resistance among gastrointestinal bacteria in broilers: a review focused on Enterococcus spp. and Escherichia coli. Animals (Basel) 2023; 13: 1362. 10.3390/ani13081362 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40. Collis RM, Burgess SA, Biggs PJ et al. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in dairy farm environments: a New Zealand perspective. Foodborne Pathog Dis 2019; 16: 5–22. 10.1089/fpd.2018.2524 [DOI] [PubMed] [Google Scholar]
- 41. Mwikuma G, Kainga H, Kallu SA et al. Determination of the prevalence and antimicrobial resistance of Enterococcus faecalis and Enterococcus faecium associated with poultry in four districts in Zambia. Antibiotics 2023; 12: 657. 10.3390/antibiotics12040657 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42. Valimba R, Liana J, Joshi MP et al. Engaging the private sector to improve antimicrobial use in the community: experience from accredited drug dispensing outlets in Tanzania. J Pharm Policy Pract 2014; 7: 11. 10.1186/2052-3211-7-11 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43. Liverani M, Oliveira Hashiguchi L, Khan M et al. Antimicrobial resistance and the private sector in Southeast Asia. In: Ethics and Drug Resistance: Collective Responsibility for Global Public Health. Springer, 2020; 75–87. [Google Scholar]
- 44. Nguyen HH, Ho DP, Vu TLH et al. “I can make more from selling medicine when breaking the rules”—understanding the antibiotic supply network in a rural community in Viet Nam. BMC Public Health 2019; 19: 1560. 10.1186/s12889-019-7812-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45. Nepal A, Hendrie D, Robinson S et al. Survey of the pattern of antibiotic dispensing in private pharmacies in Nepal. BMJ Open 2019; 9: e032422. 10.1136/bmjopen-2019-032422 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Alliance for Health Policy and Systems Research, WHO . Medicines in Health Systems. 2014. https://iris.who.int/bitstream/handle/10665/179197/9789241507622_eng.pdf?sequence=1.
- 47. Zeb S, Mushtaq M, Ahmad M et al. Self-medication as an important risk factor for antibiotic resistance: a multi-institutional survey among students. Antibiotics 2022; 11: 842. 10.3390/antibiotics11070842 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48. Alhomoud F, Aljamea Z, Almahasnah R et al. Self-medication and self-prescription with antibiotics in the Middle East—do they really happen? A systematic review of the prevalence, possible reasons, and outcomes. Int J Infect Dis 2017; 57: 3–12. 10.1016/j.ijid.2017.01.014 [DOI] [PubMed] [Google Scholar]
- 49. Kassie AD, Bifftu BB, Mekonnen HS. Self-medication practice and associated factors among adult household members in Meket district, northeast Ethiopia, 2017. BMC Pharmacol Toxicol 2018; 19: 15. 10.1186/s40360-018-0205-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50. Austin DJ, Kristinsson KG, Anderson RM. The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. Proc Natl Acad Sci U S A 1999; 96: 1152–6. 10.1073/pnas.96.3.1152 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51. Llor C, Bjerrum L. Antimicrobial resistance: risk associated with antibiotic overuse and initiatives to reduce the problem. Ther Adv Drug Saf 2014; 5: 229–41. 10.1177/2042098614554919 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52. Sokolović D, Drakul D, Vujić-Aleksić V et al. Antibiotic consumption and antimicrobial resistance in the SARS-CoV-2 pandemic: a single-center experience. Front Pharmacol 2023; 14: 1067973. 10.3389/fphar.2023.1067973 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53. Medic D, Bozic Cvijan B, Bajcetic M. Impact of antibiotic consumption on antimicrobial resistance to invasive hospital pathogens. Antibiotics 2023; 12: 259. 10.3390/antibiotics12020259 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54. Karakonstantis S, Kalemaki D. Antimicrobial overuse and misuse in the community in Greece and link to antimicrobial resistance using methicillin-resistant S. aureus as an example. J Infect Public Health 2019; 12: 460–4. 10.1016/j.jiph.2019.03.017 [DOI] [PubMed] [Google Scholar]
- 55. Nepal A, Hendrie D, Robinson S et al. Knowledge, attitudes and practices relating to antibiotic use among community members of the Rupandehi district in Nepal. BMC Public Health 2019; 19: 1558. 10.1186/s12889-019-7924-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56. Chigome A, Ramdas N, Skosana P et al. A narrative review of antibiotic prescribing practices in primary care settings in South Africa and potential ways forward to reduce antimicrobial resistance. Antibiotics 2023; 12: 1540. 10.3390/antibiotics12101540 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57. Massele A, Rogers AM, Gabriel D et al. A narrative review of recent antibiotic prescribing practices in ambulatory care in Tanzania: findings and implications. Medicina (B Aires) 2023; 59: 2195. 10.3390/medicina59122195 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58. Davari M, Khorasani E, Tigabu BM. Factors influencing prescribing decisions of physicians: a review. Ethiop J Health Sci 2018; 28: 795–804. 10.4314/ejhs.v28i6.15 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Lopez-Vazquez P, Vazquez-Lago JM, Figueiras A. Misprescription of antibiotics in primary care: a critical systematic review of its determinants. J Eval Clin Pract 2012; 18: 473–84. 10.1111/j.1365-2753.2010.01610.x [DOI] [PubMed] [Google Scholar]
- 60. Teixeira Rodrigues A, Roque F, Falcão A et al. Understanding physician antibiotic prescribing behaviour: a systematic review of qualitative studies. Int J Antimicrob Agents 2013; 41: 203–12. 10.1016/j.ijantimicag.2012.09.003 [DOI] [PubMed] [Google Scholar]
- 61. Pearson M, Chandler C. Knowing antimicrobial resistance in practice: a multi-country qualitative study with human and animal healthcare professionals. Glob Health Action 2019; 12: 1599560. 10.1080/16549716.2019.1599560 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62. Kimbowa IM, Eriksen J, Nakafeero M et al. Antimicrobial stewardship: attitudes and practices of healthcare providers in selected health facilities in Uganda. PLoS One 2022; 17: e0262993. 10.1371/journal.pone.0262993 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63. Otaigbe II, Elikwu CJ. Drivers of inappropriate antibiotic use in low- and middle-income countries. JAC Antimicrob Resist 2023; 5: dlad062. 10.1093/jacamr/dlad062 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64. Chabalenge B, Jere E, Nanyangwe N et al. Substandard and falsified medical product recalls in Zambia from 2018 to 2021 and implications on the quality surveillance systems. J Med Access 2022; 6: 27550834221141767. 10.1177/27550834221141767 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65. Mendelson M, Laxminarayan R, Limmathurotsakul D et al. Antimicrobial resistance and the great divide: inequity in priorities and agendas between the global north and the global south threatens global mitigation of antimicrobial resistance. Lancet Glob Heal 2024; 12: e516–21. 10.1016/S2214-109X(23)00554-5 [DOI] [PubMed] [Google Scholar]
- 66. Godman B, Haque M, McKimm J et al. Ongoing strategies to improve the management of upper respiratory tract infections and reduce inappropriate antibiotic use particularly among lower and middle-income countries: findings and implications for the future. Curr Med Res Opin 2020; 36: 301–27. 10.1080/03007995.2019.1700947 [DOI] [PubMed] [Google Scholar]
- 67. Rezal RS, Hassali MA, Alrasheedy AA et al. Prescribing patterns for upper respiratory tract infections: a prescription-review of primary care practice in Kedah, Malaysia, and the implications. Expert Rev Anti Infect Ther 2015; 13: 1547–56. 10.1586/14787210.2015.1085303 [DOI] [PubMed] [Google Scholar]
- 68. Zulu A, Matafwali SK, Banda M et al. Assessment of knowledge, attitude and practices on antibiotic resistance among undergraduate medical students in the school of medicine at the University of Zambia. Int J Basic Clin Pharmacol 2020; 9: 263–70. 10.18203/2319-2003.ijbcp20200174 [DOI] [Google Scholar]
- 69. Janssen J, Afari-Asiedu S, Monnier A et al. Exploring the economic impact of inappropriate antibiotic use: the case of upper respiratory tract infections in Ghana. Antimicrob Resist Infect Control 2022; 11: 53. 10.1186/s13756-022-01096-w [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70. Matee M, Mshana SE, Mtebe M et al. Mapping and gap analysis on antimicrobial resistance surveillance systems in Kenya, Tanzania, Uganda and Zambia. Bull Natl Res Cent 2023; 47: 12. 10.1186/s42269-023-00986-2 [DOI] [Google Scholar]
- 71. Tadesse BT, Ashley EA, Ongarello S et al. Antimicrobial resistance in Africa: a systematic review. BMC Infect Dis 2017: 17: 616. 10.1186/s12879-016-2105-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72. Cassini A, Högberg LD, Plachouras D et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European economic area in 2015: a population-level modelling analysis. Lancet Infect Dis 2019; 19: 56–66. 10.1016/S1473-3099(18)30605-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 73. Bumbangi FN, Llarena A-K, Skjerve E et al. Evidence of community-wide spread of multi-drug resistant Escherichia coli in young children in Lusaka and Ndola Districts, Zambia. Microorganisms 2022; 10: 1684. 10.3390/microorganisms10081684 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74. Mudenda S, Chabalenge B, Daka V et al. Global strategies to combat antimicrobial resistance: a One Health perspective. Pharmacol Pharm 2023; 14: 271–328. 10.4236/pp.2023.148020 [DOI] [Google Scholar]
- 75. McKenzie D, Rawlins M, Del Mar C. Antimicrobial stewardship: what’s it all about? Aust Prescr 2013; 36: 116–20. 10.18773/austprescr.2013.045 [DOI] [Google Scholar]
- 76. Mendelson M, Morris AM, Thursky K et al. How to start an antimicrobial stewardship programme in a hospital. Clin Microbiol Infect 2020; 26: 447–53. 10.1016/j.cmi.2019.08.007 [DOI] [PubMed] [Google Scholar]
- 77. Godman B, Egwuenu A, Haque M et al. Strategies to improve antimicrobial utilization with a special focus on developing countries. Life 2021; 11: 528. 10.3390/life11060528 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78. Siachalinga L, Mufwambi W, Lee I-H. Impact of antimicrobial stewardship interventions to improve antibiotic prescribing for hospital inpatients in Africa: a systematic review and meta-analysis. J Hosp Infect 2022; 129: 124–43. 10.1016/j.jhin.2022.07.031 [DOI] [PubMed] [Google Scholar]
- 79. Saleem Z, Godman B, Cook A et al. Ongoing efforts to improve antimicrobial utilization in hospitals among African countries and implications for the future. Antibiotics 2022; 11: 1824. 10.3390/antibiotics11121824 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80. Mudenda S, Chabalenge B, Kasanga M et al. Antifungal resistance and stewardship: a call to action in Zambia. PAMJ 2023; 45: 152. 10.11604/pamj.2023.45.152.41232 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81. Mudenda S, Chisha P, Chabalenge B et al. Antimicrobial stewardship: knowledge, attitudes and practices regarding antimicrobial use and resistance among non-healthcare students at the University of Zambia. JAC Antimicrob Resist 2023; 5: dlad116. 10.1093/jacamr/dlad116 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82. Mudenda S, Matafwali SK, Mukosha M et al. Antifungal resistance and stewardship: a knowledge, attitudes and practices survey among pharmacy students at the University of Zambia; findings and implications. JAC Antimicrob Resist 2023; 5: dlad141. 10.1093/jacamr/dlad141 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 83. Tembo N, Mudenda S, Banda M et al. Knowledge, attitudes and practices on antimicrobial resistance among pharmacy personnel and nurses at a tertiary hospital in Ndola, Zambia: implications for antimicrobial stewardship programmes. JAC Antimicrob Resist 2022; 4: dlac107. 10.1093/jacamr/dlac107 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84. Dyar OJ, Huttner B, Schouten J et al. What is antimicrobial stewardship? Clin Microbiol Infect 2017; 23: 793–8. 10.1016/j.cmi.2017.08.026 [DOI] [PubMed] [Google Scholar]
- 85. Earnshaw S, Mendez A, Monnet DL et al. Global collaboration to encourage prudent antibiotic use. Lancet Infect Dis 2013; 13: 1003–4. 10.1016/S1473-3099(13)70315-3 [DOI] [PubMed] [Google Scholar]
- 86. Keitoku K, Nishimura Y, Hagiya H et al. Impact of the world antimicrobial awareness week on public interest between 2015 and 2020: a Google Trends analysis. Int J Infect Dis 2021; 111: 12–20. 10.1016/j.ijid.2021.08.018 [DOI] [PubMed] [Google Scholar]
- 87. Wu D, Walsh TR, Wu Y. World Antimicrobial Awareness Week 2021—spread awareness, stop resistance. China CDC Wkly 2021; 3: 987–93. 10.46234/ccdcw2021.241 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 88. WHO . World Antimicrobial Awareness Week. 2021. https://www.who.int/campaigns/world-antimicrobial-awareness-week/2021.
- 89. Rawson TM, Moore LSP, Tivey AM et al. Behaviour change interventions to influence antimicrobial prescribing: a cross-sectional analysis of reports from UK state-of-the-art scientific conferences. Antimicrob Resist Infect Control 2017; 6: 11. 10.1186/s13756-017-0170-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 90. Borek AJ, Santillo M, Wanat M et al. How can behavioural science contribute to qualitative research on antimicrobial stewardship in primary care? JAC-Antimicrobial Resist 2022; 4: dlac007. 10.1093/jacamr/dlac007 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 91. Parveen S, Garzon-Orjuela N, Amin D et al. Public health interventions to improve antimicrobial resistance awareness and behavioural change associated with antimicrobial use: a systematic review exploring the use of social media. Antibiotics 2022; 11: 669. 10.3390/antibiotics11050669 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92. Kwabena O, Amponsah O, Courtenay A et al. Assessing the impact of antimicrobial stewardship implementation at a district hospital in Ghana using a health partnership model. JAC Antimicrob Resist 2023; 5: dlad084. 10.1093/jacamr/dlad084 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93. Hofer U. The cost of antimicrobial resistance. Nat Rev Microbiol 2019; 17: 3. 10.1038/s41579-018-0125-x [DOI] [PubMed] [Google Scholar]
- 94. Kalungia AC, Burger J, Godman B et al. Non-prescription sale and dispensing of antibiotics in community pharmacies in Zambia. Expert Rev Anti Infect Ther 2016; 14: 1215–23. 10.1080/14787210.2016.1227702 [DOI] [PubMed] [Google Scholar]
- 95. Li J, Zhou P, Wang J et al. Worldwide dispensing of non-prescription antibiotics in community pharmacies and associated factors: a mixed-methods systematic review. Lancet Infect Dis 2023; 23: e361–70. 10.1016/S1473-3099(23)00130-5 [DOI] [PubMed] [Google Scholar]
- 96. Loevinsohn G, Hardick J, Sinywimaanzi P et al. Respiratory pathogen diversity and co-infections in rural Zambia. Int J Infect Dis 2021; 102: 291–8. 10.1016/j.ijid.2020.10.054 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 97. Nakazwe C, Michelo C, Sandøy IF et al. Contrasting HIV prevalence trends among young women and men in Zambia in the past 12 years: data from demographic and health surveys 2002–2014. BMC Infect Dis 2019; 19: 432. 10.1186/s12879-019-4059-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 98. Mbewe N, Vinikoor MJ, Fwoloshi S et al. Advanced HIV disease management practices within inpatient medicine units at a referral hospital in Zambia: a retrospective chart review. AIDS Res Ther 2022; 19: 10. 10.1186/s12981-022-00433-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 99. Chizimu JY, Solo ES, Bwalya P et al. Genomic analysis of Mycobacterium tuberculosis strains resistant to second-line anti-tuberculosis drugs in Lusaka, Zambia. Antibiotics 2023; 12: 1126. 10.3390/antibiotics12071126 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 100. Qiao S, Zhang Y, Li X et al. Facilitators and barriers for HIV-testing in Zambia: a systematic review of multi-level factors. PLoS One 2018; 13: e0192327. 10.1371/journal.pone.0192327 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 101. Mweemba C, Hangoma P, Fwemba I et al. Estimating district HIV prevalence in Zambia using small-area estimation methods (SAE). Popul Health Metr 2022; 20: 8. 10.1186/s12963-022-00286-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 102. Nawa M, Hangoma P, Morse AP et al. Investigating the upsurge of malaria prevalence in Zambia between 2010 and 2015: a decomposition of determinants. Malar J 2019; 18: 61. 10.1186/s12936-019-2698-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 103. Lowa M, Sitali L, Siame M et al. Human mobility and factors associated with malaria importation in Lusaka district, Zambia: a descriptive cross-sectional study. Malar J 2018; 17: 404. 10.1186/s12936-018-2554-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 104. Mudenda S, Mukela M, Matafwali S et al. Knowledge, attitudes, and practices towards antibiotic use and antimicrobial resistance among pharmacy students at the university of Zambia: implications for antimicrobial stewardship programmes. Sch Acad J Pharm 2022; 11: 117–24. 10.36347/sajp.2022.v11i08.002 [DOI] [Google Scholar]
- 105. Mudenda S, Hankombo M, Saleem Z et al. Knowledge, attitude, and practices of community pharmacists on antibiotic resistance and antimicrobial stewardship in Lusaka, Zambia. J Biomed Res Environ Sci 2021; 2: 1005–14. 10.37871/jbres1343 [DOI] [Google Scholar]
- 106. Banda O, Vlahakis PA, Daka V et al. Self-medication among medical students at the Copperbelt University, Zambia: a cross-sectional study. Saudi Pharm J 2021; 29: 1233–7. 10.1016/j.jsps.2021.10.005 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 107. Chilawa S, Mudenda S, Daka V et al. Knowledge, attitudes, and practices of poultry farmers on antimicrobial use and resistance in Kitwe, Zambia: implications on antimicrobial stewardship. Open J Anim Sci 2023; 13: 60–81. 10.4236/ojas.2023.131005 [DOI] [Google Scholar]
- 108. Mudenda S, Malama S, Munyeme M et al. Awareness of antimicrobial resistance and associated factors among layer poultry farmers in Zambia: implications for surveillance and antimicrobial stewardship programs. Antibiotics 2022; 11: 383. 10.3390/antibiotics11030383 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 109. Yamba K, Lukwesa-Musyani C, Samutela MT et al. Phenotypic and genotypic antibiotic susceptibility profiles of Gram-negative bacteria isolated from bloodstream infections at a referral hospital, Lusaka, Zambia. PLOS Glob Public Heal 2023; 3: e0001414. 10.1371/journal.pgph.0001414 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 110. Samutela MT, Kalonda A, Mwansa J et al. Molecular characterisation of methicillin-resistant Staphylococcus aureus (MRSA) isolated at a large referral hospital in Zambia. Pan Afr Med J 2017; 26: 108. 10.11604/pamj.2017.26.108.10982 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 111. Chiyangi H, Muma B, Malama S et al. Identification and antimicrobial resistance patterns of bacterial enteropathogens from children aged 0–59 months at the University Teaching Hospital, Lusaka, Zambia: a prospective cross-sectional study. BMC Infect Dis 2017; 17: 117. 10.1186/s12879-017-2232-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 112. Mwansa TN, Kamvuma K, Mulemena JA et al. Antibiotic susceptibility patterns of pathogens isolated from laboratory specimens at Livingstone Central Hospital in Zambia. PLOS Glob Public Heal 2022; 2: e0000623. 10.1371/journal.pgph.0000623 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 113. Mwansa M, Mukuma M, Mulilo E et al. Determination of antimicrobial resistance patterns of Escherichia coli isolates from farm workers in broiler poultry production and assessment of antibiotic resistance awareness levels among poultry farmers in Lusaka, Zambia. Front Public Health 2023; 10: 998860. 10.3389/fpubh.2022.998860 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 114. Kasanga M, Kwenda G, Wu J, et al. Antimicrobial resistance patterns and risk factors associated with ESBL-producing and MDR Escherichia coli in hospital and environmental settings in Lusaka, Zambia: implications for One Health, antimicrobial stewardship and surveillance systems. Microorganisms 2023; 11: 1951. 10.3390/microorganisms11081951 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 115. Kabali E, Pandey GS, Munyeme M et al. Identification of Escherichia coli and related Enterobacteriaceae and examination of their phenotypic antimicrobial resistance patterns: a pilot study at a wildlife-livestock interface in Lusaka, Zambia. Antibiotics 2021; 10: 238. 10.3390/antibiotics10030238 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 116. Masich AM, Vega AD, Callahan P et al. Antimicrobial usage at a large teaching hospital in Lusaka, Zambia. PLoS One 2020; 15: e0228555. 10.1371/journal.pone.0228555 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 117. Republic of Zambia NAP on AMR . Multi-Sectoral National Action Plan on Antimicrobial Resistance. 2017. https://www.afro.who.int/publications/multi-sectoral-national-action-plan-antimicrobial-resistance-2017-2027.
- 118. Kapona O. Zambia successfully launches the first multi-sectoral national action plan on antimicrobial resistance (AMR). Health Press Zambia Bull 2017; 1: 5–7. https://www.flemingfund.org/app/uploads/ec74b8a828168c148bcba3700ace7989.pdf. [Google Scholar]
- 119. Census of Zambia . Census of Population and Housing. 2022. www.zamstats.gov.zm.
- 120. ZamStats . Population Size by Province, Zambia 2010 and 2022. 2022. https://www.zamstats.gov.zm/population-size-by-province-zambia-2010-and-2022/#.
- 121. Charan J, Biswas T. How to calculate sample size for different study designs in medical research? Indian J Psychol Med 2013; 35: 121–6. 10.4103/0253-7176.116232 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 122. Hosmer DW, Lemeshow S. Logistic Regression for Matched Case-Control Studies. In: Applied Logistic Regression. Wiley, 2005: 223–59. [Google Scholar]
- 123. Sindato C, Mboera LEG, Katale BZ et al. Knowledge, attitudes and practices regarding antimicrobial use and resistance among communities of Ilala, Kilosa and Kibaha districts of Tanzania. Antimicrob Resist Infect Control 2020; 9: 194. 10.1186/s13756-020-00862-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 124. Jani K, Srivastava V, Sharma P et al. Easy access to antibiotics; spread of antimicrobial resistance and implementation of One Health approach in India. J Epidemiol Glob Health 2021; 11: 444–52. 10.1007/s44197-021-00008-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 125. Carlet J, Pittet D. Access to antibiotics: a safety and equity challenge for the next decade. Antimicrob Resist Infect Control 2013; 2: 1. 10.1186/2047-2994-2-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 126. Chen J, Wang YM, Jie CX et al. Ease of access to antibiotics without prescription in Chinese pharmacies: a nationwide cross-sectional study. Lancet 2018; 392: S80. 10.1016/S0140-6736(18)32709-0 [DOI] [Google Scholar]
- 127. Mudenda S, Nsofu E, Chisha P et al. Prescribing patterns of antibiotics according to the WHO AWaRe classification during the COVID-19 pandemic at a teaching hospital in Lusaka, Zambia: implications for strengthening of antimicrobial stewardship programmes. Pharmacoepidemiology 2023; 2: 42–53. 10.3390/pharma2010005 [DOI] [Google Scholar]
- 128. Mudenda S, Chomba M, Chabalenge B et al. Antibiotic prescribing patterns in adult patients according to the WHO AWaRe classification: a multi-facility cross-sectional study in primary healthcare hospitals in Lusaka, Zambia. Pharmacol Pharm 2022; 13: 379–92. 10.4236/pp.2022.1310029 [DOI] [Google Scholar]
- 129. Jabeen N, Ullah W, Khalid J et al. Estimating antibiotics consumption in a tertiary care hospital in Islamabad using a WHO’s defined daily dose methodology. Antimicrob Resist Infect Control 2023; 12: 132. 10.1186/s13756-023-01311-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 130. Hodoșan V, Daina LG, Zaha DC et al. Pattern of antibiotic use among hospitalized patients at a level one multidisciplinary care hospital. Healthcare 2023; 11: 1302. 10.3390/healthcare11091302 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 131. Veerapa-Mangroo LP, Rasamoelina-Andriamanivo H, Issack MI et al. Point prevalence survey on antibiotic use in the hospitals of Mauritius. Front Antibiot 2023; 1: 1045081. 10.3389/frabi.2022.1045081 [DOI] [Google Scholar]
- 132. Dechasa M, Chelkeba L, Jorise A et al. Antibiotics use evaluation among hospitalized adult patients at Jimma Medical Center, southwestern Ethiopia: the way to pave for antimicrobial stewardship. J Pharm Policy Pract 2022; 15: 84. 10.1186/s40545-022-00490-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 133. Do NTT, Vu HTL, Nguyen CTK et al. Community-based antibiotic access and use in six low-income and middle-income countries: a mixed-method approach. Lancet Glob Heal 2021; 9: e610–9. 10.1016/S2214-109X(21)00024-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 134. Drakul D, Joksimovic BJ, Milic M et al. Public knowledge, attitudes, and practices towards antibiotic use and antimicrobial resistance in eastern region of Bosnia and Herzegovina in the COVID-19 pandemic. Antibiotics 2023; 12: 1274. 10.3390/antibiotics12081274 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 135. Wang W, Yu S, Zhou X et al. Antibiotic prescribing patterns at children’s outpatient departments of primary care institutions in southwest China. BMC Prim Care 2022; 23: 269. 10.1186/s12875-022-01875-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 136. Awad AI, Aboud EA. Knowledge, attitude and practice towards antibiotic use among the public in Kuwait. PLoS One 2015; 10: e0117910. 10.1371/journal.pone.0117910 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 137. Dache A, Dona A, Ejeso A. Inappropriate use of antibiotics, its reasons and contributing factors among communities of Yirgalem town, Sidama regional state, Ethiopia: a cross-sectional study. SAGE Open Med 2021; 9: 20503121211042460. 10.1177/20503121211042461 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 138. Surji K. Antibiotics misuse and factors leading to its’ abuse in Kurdistan region. J Health Med Nurs 2016; 24: 20–7. 10.7176/JHMN/24-2016-05 [DOI] [Google Scholar]
- 139. Mahajan M, Dudhgaonkar S, Deshmukh S. A questionnaire-based survey on the knowledge, attitude and practises about antimicrobial resistance and usage among the second year MBBS students of a teaching tertiary care hospital in central India. Int J Pharmacol Res 2014; 4: 175–9. 10.7439/ijpr.v4i4.120 [DOI] [Google Scholar]
- 140. Afari-Asiedu S, Oppong FB, Tostmann A et al. Determinants of inappropriate antibiotics use in rural central Ghana using a mixed methods approach. Front Public Heal 2020; 8: 90. 10.3389/fpubh.2020.00090 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 141. Ardillon A, Ramblière L, Kermorvant-Duchemin E et al. Inappropriate antibiotic prescribing and its determinants among outpatient children in 3 low- and middle-income countries: a multicentric community-based cohort study. PLoS Med 2023; 20: e1004211. 10.1371/journal.pmed.1004211 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 142. Mokwele RN, Schellack N, Bronkhorst E et al. Using mystery shoppers to determine practices pertaining to antibiotic dispensing without a prescription among community pharmacies in South Africa—a pilot survey. JAC Antimicrob Resist 2022; 4: dlab196. 10.1093/jacamr/dlab196 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 143. Gebeyehu E, Bantie L, Azage M. Inappropriate use of antibiotics and its associated factors among urban and rural communities of Bahir Dar city administration, northwest Ethiopia. PLoS One 2015; 10: e0138179. 10.1371/journal.pone.0138179 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 144. Lin L, Sun R, Yao T et al. Factors influencing inappropriate use of antibiotics in outpatient and community settings in China: a mixed-methods systematic review. BMJ Glob Health 2020; 5: e003599. 10.1136/bmjgh-2020-003599 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 145. Guo H, Hildon ZJL, Lye DCB et al. The associations between poor antibiotic and antimicrobial resistance knowledge and inappropriate antibiotic use in the general population are modified by age. Antibiotics 2022; 11: 47. 10.3390/antibiotics11010047 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 146. Fatokun O. Exploring antibiotic use and practices in a Malaysian community. Int J Clin Pharm 2014; 36: 564–9. 10.1007/s11096-014-9937-6 [DOI] [PubMed] [Google Scholar]
- 147. Rouusounides A, Papaevangelou V, Hadjipanayis A et al. Descriptive study on parents’ knowledge, attitudes and practices on antibiotic use and misuse in children with upper respiratory tract infections in Cyprus. Int J Environ Res Public Health 2011; 8: 3246–62. 10.3390/ijerph8083246 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 148. Napolitano F, Izzo MT, Di Giuseppe G et al. Public knowledge, attitudes, and experience regarding the use of antibiotics in Italy. PLoS One 2013; 8: e84177. 10.1371/journal.pone.0084177 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 149. Schmiege D, Evers M, Kistemann T et al. What drives antibiotic use in the community? A systematic review of determinants in the human outpatient sector. Int J Hyg Environ Health 2020; 226: 113497. 10.1016/j.ijheh.2020.113497 [DOI] [PubMed] [Google Scholar]
- 150. Arlinghaus KR, Johnston CA. Advocating for behavior change with education. Am J Lifestyle Med 2018; 12: 113–6. 10.1177/1559827617745479 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 151. Sartelli M, Barie PS, Coccolini F et al. Ten golden rules for optimal antibiotic use in hospital settings: the WARNING call to action. World J Emerg Surg 2023; 18: 50. 10.1186/s13017-023-00518-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
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