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Background Antimicrobial resistance (AMR) is widely acknowledged as a global health problem, yet its extent is not well evaluated, especially in low-middle income countries. It is challenging to promote policies without focusing on healthcare systems at a local level, therefore a baseline assessment of the AMR occurrence is a priority. This study aimed to look at published papers relating to the availability of AMR data in Zambia as a means of establishing an overview of the situation, to help inform future decisions. Methods PubMed, Cochrane Libraries, Medical Journal of Zambia and African Journals Online databases were searched from inception to April 2021 for articles published in English in accordance with the PRISMA guidelines. Retrieval and screening of article was done using a structured search protocol with strict inclusion/exclusion criteria. Results A total of 716 articles were retrieved, of which 25 articles met inclusion criteria for final analysis. AMR data was not available for six of the ten provinces of Zambia. Twenty-one different isolates from the human health, animal health and environmental health sectors were tested against 36 antimicrobial agents, across 13 classes of antibiot- ics. All the studies showed a degree of resistance to more than one class of antimicrobials. Majority of the studies focused on antibiotics, with only three studies (12%) highlighting antiretroviral resistance. Antitubercular drugs were addressed in only five studies (20%). No studies focused on antifungals. The most common organisms tested, across all three sectors, were Staphylococcus aureus, with a diverse range of resistance patterns found; followed by Escherichia coli with a high resistance rate found to cephalosporins (24–100%) and fluoroquinolones (20–100%). Conclusions This review highlights three important findings. Firstly, AMR is understudied in Zambia. Secondly, the level of resistance to commonly prescribed antibiotics is significant across the human, animal, and environmental sec- tors. Thirdly, this review suggests that improved standardization of antimicrobial susceptibility testing in Zambia could help to better delineate AMR patterns, allow comparisons across different locations and tracking of AMR evolution over time. Keywords Antimicrobial resistance, One Health, Zambia, Review Antimicrobial resistance (AMR) has been highlighted Background by the World Health Organization (WHO) as a promi- The SARS-COV-2 pandemic has highlighted the impor - nent threat to global health [1]. There is specific con - tance of implementing working systems at a local level cern of low-middle income countries (LMICs) where to mitigate and prevent spread of infectious diseases. there is poor surveillance, poor diagnosis measure and a lack of guidelines indicating therapy procedures [2]. A *Correspondence: regional and national understanding of AMR is needed Avis A. Nowbuth anyanowbuth@gmail.com to improve human health, animal health and agricultural Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Nowbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 2 of 12 productivity per country [3]. A 2022 study highlights agriculture sectors. We conducted a systematic review that bacterial AMR is the most prevalent cause of death assessing the prevalence of AMR in Zambia as a means of related to drug resistance [4]. Given the global impor- establishing an overview of the situation, to help inform tance of bacterial AMR, there is an urgent need to high- future decisions as there are currently no guidelines in light the clinically relevant resistance related to bacteria, place to monitor the use of antimicrobials, nor is there especially in LMICs [4]. LMICs have unique socioeco- standardized testing procedures in place, to date. This nomic and cultural settings that challenge the strategies review will assist in creating a more tailored approach from policy makers on the world stage [5], as a result of in implementing interventions by highlighting the levels this, antimicrobial stewardship strategies must be tai- of resistance and lack of data that need to be addressed lored specifically from the ground level. In many LMICs, across all sectors. the use of antimicrobials for treatment remain undocu- mented and unregulated [6]. Methods The One Health Approach is the ‘collaborative effort Search strategy of multiple disciplines – working locally, nationally, and A systematic review was performed in accordance with globally – to attain optimal health for people, animals PRISMA (Preferred Reporting Items for Systematic and our environment…’ [7] and recognizes that there is a Reviews and Meta-Analysis) guidelines (Fig. 1) [15]. The link between these three domains. The WHO has stated search terms [(multiresistant OR multi-drug resistant OR that the One Health approach is critical to addressing antimicrobial resistance OR drug resistance OR bacterial health threats across all three interfaces [8]. The con - resistance) AND (Zambia)] were used to identify relevant cept focuses on the consequences, responses and actions literature from Cochrane Libraries, PubMed, Medical across the human-animal-environment sectors highlight- Journal of Zambia and African Journals Online data- ing the importance of balance and interconnectedness. A bases. Various spellings of the search terms were con- solo approach only focusing on health education will not sidered. A total of 994 articles were identified from the lead to effective results because these three sources are four databases that were searched using Boolean search interrelated. AMR understanding and control should be strategies to obtain English articles relating to AMR and approached ideally from a One Health perspective since Zambia. No limitation on publication dates were set. resistance can arise in the human, animal or the environ- Literature search began in March 2021, with an update ment and spread from one to another [9]. on April 30, 2021. Reference list of relevant articles were A report was developed by the Zambian National checked for additional titles for inclusion in the review. Public Health Institute (ZNHPI) and the Centre for Sci- No limitation was set on the bacteria in animal and ence and Environment (CSE) India highlighting the need human health sectors. to prepare a surveillance system for Zambia [10]. This report mentions the need for interventions, however, Inclusion and exclusion criteria does not reflect the rate of AMR data and studies in Zam - Full-text articles on the prevalence of antibiotic resistance bia to date. Zambia faces a generalized HIV epidemic, among clinical pathogenic bacteria isolated from humans with most deaths resulting from opportunistic infections. (inpatients, outpatients, healthy volunteers), animals Malaria is considered to be the main cause for hospi- (avian, cattle, sheep, swine, and fish) and environment talization, and the biggest contributor to morbidity and (non-healthcare: water, markets, outbreak studies; and mortality rates [10, 11]. There have also been outbreaks healthcare: hospital surfaces, health care tools,) in Zam- of cholera, meningococcal meningitis, pneumonia, and bia were used for the review. Publications were initially typhoid in Zambia [10]. Standard infections are becom- screened independently by three reviewers (AAN, NNT, ing increasingly difficult to treat with standard first-line OYM) to determine eligibility. Articles were reviewed by antibiotics because of AMR, leading to the necessary use at least two reviewers and disagreements were resolved of newer, more targeted, but also more expensive antibi- by a third author. Studies related to human sector otics [12, 13]. included both adult and pediatric populations, inpatients A consolidated approach is needed to address the com- and outpatients, and healthy volunteers in institutions plexity and scale of the problem which includes incor- such as prisons and schools. There were no limitations on porating the various fields of governance and policy the disease or microorganism tested. Publications iden- makers [14]. When an overview of antimicrobial prac- tified through the literature search that reported AMR tice is known, more tailored implementations and con- in human, animal, and environment but that did not trol measures can be planned; and understood. Unique report prevalence data were not included; specific site of insight into antibiotic prescribing, ideas about AMR, genetic mutations resulting in AMR were not included. and insights into use of antimicrobials in the animal and Studies that mentioned insecticide resistance, assessed No wbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 3 of 12 Fig. 1 PRISMA flow-chart illustrating the study selection process on antimicrobial resistance in Zambia the quality of the drug (drug composition, generic com- cross-sectional design, or longitudinal study). The spe - pounds and imported medications compared to local cific information extracted for the human sector con - medications) were excluded as the studies did not men- sidered: category of patients (in- or out-patients, healthy tion resistance rates. Studies that tested the most appro- persons and reason admitted if inpatient), and type priate diagnostic testing tools were excluded. Studies that of samples extracted (pus, blood, throat swabs, stool, made mention of compliance of chronic medicines such nasal swabs, urine, vaginal or wound swabs). Regard- as in HIV, and treatment failures were rejected. Any pub- ing the animal sector: species, number of sites (includ- lication that did not report data on AMR were consid- ing farms, sanctuaries, and veterinary sites), number of ered not relevant and were excluded. animals sampled in analysis, sample type (feces, meat, milk, blood), sampling point (farm, slaughterhouse, or Data extraction retail market) were extracted. The environmental/agri - Data was extracted from each study using a database cultural sector included information of interest such as developed by AAN for the purpose of this review using water, outbreak studies, vegetables, markets, clinic/hos- Microsoft Office 365: Excel. The data extraction was pital surfaces and medical tools were considered. Arti- independently done by AAN and verified by co-authors cles that studied more than one sector were classified as a NNT and OYM. Articles that met the inclusion criteria One Health paper and extracted to the subsections men- and reported prevalence data for AMR were included in tioned above. The type of organism, organism numbers, the systematic review. antibiotics tested, and interpretation of the findings was Information extracted included article information extracted into each of the abovementioned category. The (first author, year of publication, duration of study, loca - samples that were studied had to have undergone a labo- tion, and specific sites), and study design (samples size, ratory procedure in which the type of microorganism Nowbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 4 of 12 was identified, and prevalence of antibiotic-resistant bac - reflected on the outcomes of AMR within the human and teria was taken into consideration for the human, animal, environmental sector (Table 1a and Table 2). Across the and environment articles. Specific site of genetic muta - sectors, 21 (84%) of studies were focused on antibacte- tions was noted, highlighting the degree of resistance a rial, with 5 studies specific for antitubercular drugs, and microorganism has, however the specific sites were not 3 studies focused on antiretrovirals. The antimicrobials included in this systematic review. that underwent surveillance were antibiotics (antibiotic classes were aminoglycosides, cephalosporins, penicil- Data analysis lin, sulfonamides, fluoroquinolones, macrolides, tetra - Articles were characterized based on Zambia as a geo- cyclines, chloramphenicol and glycopeptides), antivirals graphic location (including the region and specific site if (nucleoside reverse transcriptase inhibitors (NRTI), non- this information was available; if the study included other nucleoside reverse transcriptase inhibitors (NNRTIs) and countries, specific information regarding Zambia was protease inhibitors (PIs). Only one paper reported data extracted if available), the type of antimicrobial resistance on antimalarials. No antifungals were surveilled. All the described in the study (antibacterial, antiviral, antifungal studies relayed information about surveillance, highlight- or antimalarial), context of the study (human, animal or ing zero studies on policy making. environmental; or a combination of any of the sectors i.e. The largest number of studies originated from Lusaka One Health), study design, and outcome of the studies Province (n = 12), followed by Copperbelt Province (specifically prevalence rate of antimicrobial resistance). (n = 6), Western Province (n = 2), Southern Province Meta-analysis was not conducted due to the diversity of (n = 1), Eastern Province (n = 1), while three studies the study types and identified data, and therefore present mentioned multiple sites within the regions of the coun- descriptive findings. Visualizations were performed using try (Fig. 2.) however, it was noted that several provinces Microsoft Office 365. had no studies conducted. From these studies, there were multiple samples taken, and multiple microorganisms Results sampled and tested (Table 2). These studies investigated Data isolates from diarrheal diseases (2; 10%), breast abscesses The initial search of the online databases identified a total (1; 5%), chronic supportive otitis media (1; 5%), hospital of 994 publications (PubMed (n = 234), Cochrane Librar- acquired infections (1; 5%), malaria (1; 5%), neonatal sep- ies (n = 376), African Journals Online (AJOL) (n = 377) sis (1; 5%), typhoid (1; 5%), HIV (4; 20%), and tuberculo- and Medical Journal of Zambia (MJZ) (n = 7)) from sis (4, 25%) (Table 1b). Overall, 27 samples were reported inception of database to April 2021. A total of 5 duplicates from the human and animal studies, the most abun- were removed. Additional 4 records were retrieved after dant being blood (7; 26%) followed by sputum samples screening references. The African Journals Online iden - (5; 19%), stool samples (4; 15%), wound swabs (4; 15%), tified 377 studies, of which only 100 articles were acces - nasal swabs (2; 7%), aspirates (1; 4%), rectal swabs (1; 4%), sible from the database due to an internal error within urine samples (1; 4%) and oral swabs (2; 7%) (Table 1c) AJOLs system. A total of 716 studies were screened for Two animal studies did not provide the source of samples eligibility based on the title and abstract contents. Over- for culture. Samples from the environmental sector were all, 614 articles were excluded for non-relevance to this obtained from fish markets, veterinary hospital surfaces, systematic review. 102 full-text articles were assessed for healthcare white coats and the hydrotherapy bathtub of eligibility with 25 articles meeting the inclusion criteria the burns unit at the Department of Surgery (Table 2). for the study (Fig. 1). Table 1 summarizes the characteris- Twenty-one types of pathogens across all sectors were tics of the analyzed articles; a full list of the included arti- isolated from samples with the most common organ- cles and breakdown of findings is provided in Table 2 and isms isolated being Staphylococcus aureus (13; 17%) fol- further details of specific antimicrobial results is found in lowed by Escherichia coli (11; 14%), Klebsiella species (7; Additional file 1/Supplementary Data. 9%), Mycobacterium tuberculosis (5; 7%), Proteus species (4; 5%), Streptococcus species (4; 5%), Pseudomonas spe- Study characteristics cies (4, 5%), Enterobacter species (4; 5%), Coliform (3; 4%), A total of 18 studies reported on the outcome of AMR Shigella species (3; 4%), coagulase negative Staphylococci in humans, two reported on the outcome of AMR in (3; 4%), HIV (3; 4%), Vibrio cholerae (2; 3%), Salmonella animals and two on the environment (Table 1a). Three Typhi (2; 3%), Salmonella paratyphi B (1; 1%), Non- studies used a One Health approach; with one study Typhoidal Salmonella (NTS) (1; 1%), Citrobacter species reporting outcomes of AMR in both human and animal (1; 1%), Yersinia species (1; 1%), Plasmodium falciparum sectors, while one study reporting on the outcome of (1; 1%), Campylobacter jejuni (1; 1%) and Staphylococcus AMR in animals and environmental sectors, one study pseudointermedius (2; 3%) as summarized in Fig. 3 and No wbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 5 of 12 Table 1 Summary of the articles included in the systematic review Resistance type Number of AMR context (Samples studied) Output Articles Human (H) Animal (A) Environmental (E) One Health (AHE) Policy Surveillance Antibacterial 16 9 (+ 2) 2 (+ 2) 2 (+ 2) 3 (AE, HE, HA) 0 16 Antimalarial 1 1 0 0 0 0 1 Antiviral 3 3 0 0 0 0 3 Antitubercular 5 5 0 0 0 0 5 Antifungal 0 0 0 0 0 0 0 Total 25 18 (20) 2 (4) 2 (4) 3 0 25 Pathology in human samples n (%) (n = 20) Study 1 Breast abscess 1 (5) Kapatamoyo et al. [16] 2 Cholera 1 (5) Mwape et al. [17] 3 Chronic suppurative otitis media 1 (5) Matundwelo and Mwansasu [18] 4 Diarrheal disease 2 (10) Mainda et al. [19, 20], Chiyangi et al. [21] 5 HIV 4 (20) Gill et al. [22], Bennett et al. [23], Inzaule et al. [24], Miti et al. [25] 6 Hospital acquired infections 1 (5) Chanda et al. [26] 7 Malaria 1 (5) Bijl et al. [27] 8 Neonatal sepsis 1 (5) Kabwe et al. [28] 9 Not mentioned 2 (10) Ziwa et al. [29], Nagelkerke et al. [30] 10 Tuberculosis 5 (25) Mulenga et al. [31], Habeenzu et al. [32], Kapata et al. [33, 34], Masenga et al. [35], Kapata et al. [33, 34] 11 Typhoid 1 (5) Hendriksen et al. [36] Samples Human studies Animal studies Total Studies (A + E) Total % 1 Blood 7 7 26 2 Sputum 5 5 19 3 Stool 4 4 15 4 Wound Swab 3 1 4 15 5 Aspirates 1 1 4 6 Nasal swab 1 1 2 7 7 Rectal swab 1 1 4 8 Urine 1 1 4 9 Oral swab 1 1 2 7 detailed in Table 2. The susceptibility of these isolates or management. No studies were conducted that relayed towards 36 antimicrobial agents across 13 classes of anti- information about antifungal resistance. biotics was tested. The animal, environmental and One Health studies Discussion focused on bacterial pathogens and resistance patterns. Antimicrobial Resistance has been highlighted by the The most found pathogens isolated were E. coli and S. World Health Organization (WHO) as a global health aureus. Salmonella was only studied in the human sec- threat that needs urgent intervention [13, 41]. Zambia tor. The 25 included studies focused on resistance profiles has a National Action Plan (NAP), aimed to have been of microbes. No articles included described the process implemented by 2020 [10], however the effects of these or outcomes of AMR stewardship programs at a local interventions may be inaccurate without a baseline level or focused on policy aspects of AMR prevention investigation. As an LMIC, there are multiple challenges Nowbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 6 of 12 Table 2 Characteristics of articles included in the systematic review Type of study Author Year published Location Human `Animal Environmental Sample SOURCE Microorganism Species Sample type Microorganism Sample Source Microorganism One Health Mainda et al. [20] 2019 Lusaka, LP Stool E. coli Cattle E. coli Ziwa et al. [29] 2018 Lusaka, LP Wound swabs S. aureus Hydrotherapy S. aureus K. pneumoniae Bathtub K. pneumoniae Youn et al. [37] 2014 Lusaka, LP Dogs Wound swabs S. aureus Door handles, S. aureus Cats S. pseudinterme- Desk Examination S. pseudintermedius dius table, Medical Devices, Scale, Floor, Tray surface, Operation table Environ Songe et al. [38] 2016 Mongu, WP Mongu Fish E. coli Markets: Flies Mwamungule 2015 Lusaka, LP Doctors White S. aureus et al. [39] Coats K. pneumoniae Animal Mainda et al. [19] 2015 Zambia Cattle E. coli Schaumburg et al. 2012 Chingola, CoP Chimpanzees Oral swabs S. aureus [40] Nasal swabs No wbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 7 of 12 Table 2 (continued) Type of study Author Year published Location Human `Animal Environmental Sample SOURCE Microorganism Species Sample type Microorganism Sample Source Microorganism Human Kapatamoyo et al. 2010 Lusaka, LP Pus Aspirates S. aureus [16] Matundwelo and 2016 Ndola, CoP Pus Swab S. aureus Mwansasu [18] P. vulgaris Miti et al. [25] 2020 Ndola, CoP Blood HIV Nagelkerke et al. 2017 Eastern EP Nasal Swab S. aureus [30] Rectal Swab Enterobacteriaceae Inzaule et al. [24] 2020 Zambia Blood HIV Bennett et al. [23] 2020 Lusaka, LP Dried Blood Spots HIV Mwape et al. [17] 2020 Lusaka, LP Stool V. cholerae Kapata et al. [34] 2015 Lusaka, LP Sputum M. tuberculosis Hendriksen et al. 2014 Lusaka, LP Stool S. typhi [36] Blood Masenga et al. [35] 2017 Livingstone, SP Sputum M. tuberculosis Kapata et al. [33] 2013 Lusaka, LP M. tuberculosis Mulenga et al. [31] 2010 Ndola, CoP Sputum M. tuberculosis Bijl et al. [27] 2000 Kaoma, WP Blood P. falciparum Chiyangi et al. [21] 2017 Lusaka, LP Stool V. cholerae NTS E. coli, S.Typhi S.paratyphi B, Shigella flexinari, Shigella dysente- riae, Shigella boydii, Campylobacter jejuni Habeenzu et al. 2007 Zambia Sputum M. tuberculosis [32] Kabwe et al. [28] 2016 Lusaka, LP Blood Klebsiella sp, S. aureus, E.coli Chanda et al. [26] 2019 Ndola, CoP Blood, Urine, E. coli, Citrobacter Wound swabs species, Coliform, Streptococcus Enterobacteriaceae, S. aureus, coan Staphylococci, Pseudomonas sp. Proteus species Klebsiella sp. Gill et al. [22] 2008 Ndola, CoP Nasal Swabs S. pneumoniae Nowbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 8 of 12 Fig. 2 Map of Zambia showing study sites and number of articles used in the review Zambia must overcome, such as the unavailability of antibiotics used in Zambia. Lusaka province had majority diagnostic tests, lack of microbiologists at teaching hos- of the studies, with various provinces having no data on pitals, lack of reagents or inadequate equipment within AMR, indicative that more AMR data is needed for sev- hospitals and laboratories. Availability of routine and eral provinces to have a more complete understanding of research data on antimicrobial resistance is an impor- the status of AMR in the country. A possible explanation tant step in the development of local strategies to curb for why studies are conducted in Lusaka could be because the global AMR crisis [42]. The One Health approach is Lusaka has the highest population density, with the biggest a progressive development of multi-disciplinary action of the teaching hospitals in Zambia located in this prov- across the human health sector with animal and envi- ince. There are more resources, more sites, and greater ronmental health [43]. A report was developed by the ease to collaborate in a One Health approach in Lusaka, ZNHPI and the CSE India highlighting the need to pre- compared to the smaller, distanced cities in Zambia. A pare a surveillance system for Zambia [10]. An integrated couple of articles mentioned Zambia in a multi-country baseline using information collected from secondary study, however in these cases, the specific region or loca - research was developed with the hope to accurately tion of the study or sample collection was rarely men- implement a NAP. The report mentions commonly used tioned, resulting in limitations of the study in findings antimicrobials, disease burdens and estimates the trends specific to the Zambian context. A 2017 systematic review of AMR from secondary studies conducted in Zambia reported that about 42% of African countries do not have [10]. published studies on AMR [44], and the lack of informa- This current review describes published data on anti - tion available in Zambia is evident. Many LMICs, such as microbial drug resistance from Zambia, revealing a high Zambia, are resource limited. The allocation of resources is rate of resistance of microorganisms isolated in hospital crucial hence an up-to-date baseline is needed to develop, settings, animal health and environment against typical coordinate and apply surveillance systems at all levels [10]. No wbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 9 of 12 Fig. 3 Microorganisms isolated across human, animal, and environmental sectors in Zambia Many studies in sub-Saharan Africa focus on antibac- slaughtered were infected with BTB [47]. The spill-over terial resistance with few studies on antivirals and anti- effect from the animal sector to the human sector has fungals. Countries with high prevalence of HIV, TB and not yet been established in Zambia. A recent study found malaria had high numbers of studies on these diseases that there is a need for routine laboratory surveillance [10]; this does not align with our observations from Zam- and better case managements to prevent and limit multi- bia. Despite Zambia having an HIV epidemic, only four drug resistant TB in Zamia [48]. In Copperbelt Province, studies made mention of HIV, with one study testing the Zambia, Monde et al. [48] shows that there is emergence resistance to opportunistic infections in HIV patients: S. of Mycobacterium tuberculosis complex which are resist- pneumoniae. HIV prevalence in Zambia was estimated ant to one or more anti-tuberculosis drugs. 11.3% among adults ages 15 to 49 as of 2018 [45]. This Most studies on AMR in Zambia focused on resist- represents a substantial burden of disease, and it was sur- ance in the human sector, with a handful of studies in the prising to identify only three studies focusing on preva- animal and environmental sectors, despite the known lence to antiretroviral resistance in Zambia: particularly importance of the interconnectedness of all three sec- because of the emerging resistance to antiretroviral regi- tors and the vital role they play in preventing and miti- mens across Africa [46]. Zambia has a high prevalence of gating AMR. The One Health approach should assist and tuberculosis with 455/100,000 cases recorded in a study encourage future researchers to consider the methodolo- in 2019 [47]. Despite the tuberculosis epidemic, only gies that explicitly look at the interlink across human- five studies showed specific resistance to antitubercular animal-environment frameworks, specifically focusing drugs. The detection of M. bovis in Zambia and LMICs on the zoonotic diseases that have the high potential of is limited due to poor laboratory facilities and lack of resulting in resistance to antimicrobials. With only three trained personnel [47]. Bovine tuberculosis (BTB) has studies focusing on multiple sectors, yet these studies are been reported in traditional cattle in Zambia, with a high on microorganisms that are not epidemiological micro- prevalence of 49.8% within the Kafue basin region; while organisms, it was noted that there are not enough studies abattoirs in Namwala district found that 16.8% of cattle using the ‘One Health’ approach in Zambia. More studies Nowbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 10 of 12 Fig. 4 One Health approach to antimicrobial resistance highlighting the spill-over effect will be needed to estab - resistance has emerged and been detected for K. pneumo- lish a better overview and a better way to combat AMR nia and E. coli. The results vary widely, however majority in Zambia. Understanding these elements and addressing shows resistance greater than 50% for both these organ- them from the ground-level is necessary to change the isms. These findings demonstrate antibiotic resistance, modifiable interactions to reduce or interrupt the spread regardless of testing method, site, year and region, to new of resistance from the environment into clinical, and ani- and extended spectrum, more efficacious antibiotics. mal settings; and vice versa (Fig. 4). Figure 4 shows the The most common pathogen identified across the relationship between the sectors, and the importance of human-animal-environmental sectors was S. aureus. S. recognizing this collaboration. aureus is frequently found on the human skin and is rec- Numerous studies found resistance of more than 50% sug- ognized as the main contributor of infections in humans gesting high resistance or possible sampling/testing errors. It [50]. There are high rates of AMR to gentamycin, ceftazi - was observed that studies are diverse in samples type, study dime, amoxicillin-clavulanic acid, cotrimoxazole, nali- design and identified data and no standardized tool was used dixic acid, norfloxacin and oxacillin found in this study. across the studies. Antibiograms were not found in the sys- Gentamycin, ceftazidime (third generation cephalo- tematic review, and the most recent antibiogram found in sporin) and the fluoroquinolones (nalidixic acid and nor - a ZNHPI report was from 2016 for only one hospital [10]. floxacin) are considered second line for Staphylococcus Recent communication with the laboratory mentioned a spp. This finding is a serious concern as we see a promi - shortage of reagents hence the main third level hospital can- nent resistance rate across multiple studies. not conduct yearly antibiograms, as recommended by the Special consideration needs to be addressed in Zam- Clinical and Laboratory Standards Institute (CLSI) [49]. bia regarding the surveillance techniques across the sev- Several studies showed a 100% resistance to commonly eral regions. It is imperative to include rural and urban prescribed drugs in Zambia, as well as multidrug resist- informal settlements, as well as community studies. To ance amongst clinical isolates. This review highlights prevent an AMR pandemic, it is important to establish concerns relating to the use of common antimicrobials as surveillance systems that also address and incorporate the choice for optimal therapy of common pathogens in investigations into the knowledge, attitudes and practices Zambia. Our study highlights concern regarding second- across the human, animal and environmental sectors. It line treatment options, such as azithromycin for cholera, is also recommended to establish systems to map antimi- in the country have also been highlighted by this study. crobial use, resistance profiles and genetics. No known However, the high rate of antimicrobial resistance does system to address AMR mapping is in place in Zambia bring into question the testing methods and accuracy at the time of this review. Studies on antifungals, a group of the testing in Zambia as there may have been sam- that is neglected, should be considered a field of interest. ple contaminations at certain studies since there were a Researchers should be encouraged to collaborate within variety of contradicting results, as seen with penicillin, the human-animal-environmental sectors and conduct cephalosporins, monobactams, and carbapenems use for studies from a One Health perspective; as well as estab- S. aureus ranging from 0% resistance to 100% resistance lish appropriate means to ensure a system can be in place for second line antibiotics (gentamicin, ceftazidime, nali- to potentiate future studies on AMR in Zambia. dixic acid and norfloxacin). Similarly, it was noted that No wbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 11 of 12 the manuscript. LRS and AWA provided critical review of the manuscript and Our research is one of the first systematic reviews to contributed to the final version. All the authors read and approved the final assess antimicrobial resistance in Zambia. Our results version of the manuscript. provide critical information that can be used towards Funding policy development and patient management. The dif - No funding was received for this study. ferent sectors should be more involved and share infor- mation to ensure that there is a holistic approach when it Availability of data and materials The data and materials of the study will be available from the corresponding comes to combatting AMR. author on reasonable request. Declarations Conclusion To safeguard our current collection of antibiotics it is Ethics approval and consent to participate Not applicable. imperative to address the gaps in AMR diagnostic stand- ardization and reporting; and improve surveillance, stew- Consent for publication ardship, infection control, and implementations of updated Not applicable. treatment guidelines and monitoring. Overall, this review Competing interests suggests that improved standardization of antimicrobial The authors declare that they have no competing interests. susceptibility testing in Zambia could help to better delin- Author details eate AMR patterns and allow comparisons across different 1 2 Lusaka Apex Medical University, Lusaka, Zambia. School of Medicine, locations and allow tracking of AMR evolution over time. University of Missouri-Columbia, Columbia, MO, USA. Pan-African Organiza- The findings further emphasize the need to address and tion for Health, Education and Research, Manchester, USA. Present Address: Massachusetts General Hospital, Boston, USA. Central Administration implement effective AMR surveillance through contin - University of Buea, Buea, Cameroon. Obafemi Awolowo University, Ife, Osun ued data sharing, multidisciplinary collaborations, and State, Nigeria. coordination of all stakeholders—using the One Health Received: 10 May 2022 Accepted: 23 February 2023 Approach. This is essential to understand and manage the AMR national burden especially in Zambia. Abbreviations References AJOL African Journals Online 1. WHO. AMR and Covid-19. World Health Organization. 2020 [cited 2021 AMR Antimicrobial Resistance Feb 28]. Available from: https:// www. euro. who. int/__ data/ assets/ pdf_ BTB Bovine tuberculosis file/ 0004/ 441751/ COVID- 19- AMR. pdf . CLSI Clinical and Laboratory Standards Institute 2. Iskandar K, Molinier L, Hallit S, Sartelli M, Hardcastle TC, Haque M, et al. CSE Centre for Science and Environment Surveillance of antimicrobial resistance in low- and middle-income coun- LMIC Low-middle income countries tries: a scattered picture. Antimicrob Resist Infect Control. 2021;10(1):1– MJZ Medical Journal of Zambia 19. https:// doi. org/ 10. 1186/ s13756- 021- 00931-w. NAP National Action Plan 3. Caudell MA, Dorado-Garcia A, Eckford S, Creese C, Byarugaba DK, NRTI Nucleoside r everse transcriptase inhibitors Afakye K, et al. Towards a bottom-up understanding of antimicrobial NNRTI Non-nucleoside reverse transcriptase inhibitors use and resistance on the farm: a knowledge, attitudes, and practices PI Protease inhibitors survey across livestock systems in five African countries. PLoS ONE. PRISMA Preferred reporting items for systematic reviews and meta-analysis 2020;15(1):e0220274. https:// doi. org/ 10. 1371/ journ al. pone. 02202 74. WHO World Health Organization 4. Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray ZNHPI Zambian National Public Health Institute A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55. 5. Haque M, Rahman NAA, McKimm J, Sartelli M, Kibria GM, Islam MZ, et al. Supplementary Information Antibiotic use: a cross-sectional study evaluating the understanding, The online version contains supplementary material available at https:// doi. usage and perspectives of medical students and pathfinders of a public org/ 10. 1186/ s13756- 023- 01224-0. defence university in Malaysia. Antibiotics. 2019;8(3):154. https:// doi. org/ 10. 3390/ antib iotic s8030 154 6. Gilbert M, Pullano G, Pinotti F, Valdano E, Poletto C, Boëlle PY, et al. Pre- Additional file 1. Table S1: Detailed findings of antimicrobial resistance paredness and vulnerability of African countries against importations of rates across the studies included. COVID-19: a modelling study. Lancet. 2020;395(10227):871–7. 7. Mackenzie JS, Jeggo M. The One Health approach—Why is it so Acknowledgements important? Trop Med Infect Dis. 2019;4(2). Available from: /pmc/articles/ The authors would like to thank Dr Seth Bloom for critical review at work in PMC6630404/. progress meetings. The Pan-African Organization for Health, Education and 8. McEwen SA, Collignon PJ. Antimicrobial Resistance: a One Health Research (POHER) for the support for the duration of the study. perspective. In: Antimicrobial resistance in bacteria from livestock and companion animals [Internet]. American Society of Microbiology; 2018 Author contributions [cited 2021 Jun 26]. pp. 521–47. Available from: https:// pubmed. ncbi. nlm. AAN, AWA and LRS conceived the idea. AAN prepared the systematic review nih. gov/ 29600 770/. protocol and was involved in the literature search, screening, extraction of 9. WHO. WHO, FAO, and OIE Unite in the Fight Antimicrobial Resistance. data, data analysis and developed the drafts of the manuscript. OYM and NNT 2021. Available from: https:// www. who. int/ foods afety/ areas_ work/ antim performed the screening, extraction of data and developed the first draft of icrob ial- resis tance/ amr_ tripa rtite_ flyer. pdf? ua=1. Nowbuth et al. Antimicrobial Resistance & Infection Control (2023) 12:15 Page 12 of 12 10. Zambia National Public Health Institute. Baseline information for inte- 30. Nagelkerke MMB, Sikwewa K, Makowa D, et al. Prevalence of antimicro- grated antimicrobial resistance surveillance in Zambia; 2020. bial drug resistant bacteria carried by in- and outpatients attending a 11. Zamstats. Zambia 2020 Census. 2020. Available from: https:// census. secondary care hospital in Zambia. BMC Res Notes. 2017;10:1–6. zamst ats. gov. zm/. 31. Mulenga C, Chonde A, Bwalya IC, et al. Low occurrence of tuberculosis drug 12. Pearson M, Doble H-R, Nabila S, Reynolds C, Chandler C. Antibiotic pre- resistance among pulmonary tuberculosis patients from an urban setting, with scribing and resistance: views from low-and middle-income prescribing a long-running DOTS program in Zambia. Tuberc Res Treat. 2010;2010:1–6. and dispensing professionals Report to the World Health Organization, 32. Habeenzu C, Mitarai S, Lubasi D, et al. Tuberculosis and multidrug researched and compiled by students and staff of the Antimicrobial Resist - resistance in Zambian prisons, 2000–2001. Int J Tuberc Lung Dis. ance Centre at the London Sc [Internet]. London; 2017 [cited 2021 Mar 3]. 2007;11:1216–20. Available from: http:// www. who. int/ antim icrob ial- resis tance/ LSHTM-. 33. Kapata N, Chanda-Kapata P, Bates M, et al. Multidrug-resistant TB in 13. WHO. WHO|Global action plan on antimicrobial resistance. WHO [Inter- Zambia: review of national data from 2000 to 2011. Trop Med Int Health. net]. 2017 [cited 2021 Feb 28]; Available from: http:// www. who. int/ antim 2013;18:1386–91. icrob ial- resis tance/ publi catio ns/ global- action- plan/ en/ 34. Kapata N, Mbulo G, Cobelens F, et al. The second Zambian national 14. Borek AJ, Wanat M, Sallis A, Ashiru-Oredope D, Atkins L, Beech E, et al. tuberculosis drug resistance survey - a comparison of conventional and How can national antimicrobial stewardship interventions in primary care molecular methods. Trop Med Int Health. 2015;20(11):1492–500. be improved? A stakeholder consultation. Antibiotics. 2019;8(4):207. 35. Masenga SK, Mubila H, Hamooya BM. Rifampicin resistance in mycobacte- 15. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, rium tuberculosis patients using GeneXpert at Livingstone Central Hospital et al. The PRISMA 2020 statement: an updated guideline for reporting for the year 2015: a cross sectional explorative study. BMC Infect Dis 2017;640. systematic reviews. Syst Rev. 2021;10(1):1–11. https:// doi. org/ 10. 1186/ 36. Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, et al. Genomic s13643- 021- 01626-4. signature of multidrug-resistant salmonella enterica serovar Typhi isolates 16. Kapatamoyo B, Andrews B, Bowa K. Association of HIV with breast related to a massive outbreak in Zambia between 2010 and 2012. J Clin abscess and altered microbial susceptibility patterns. Med J Zambia. Microbiol. 2015;53:262–72. 2010;37:58–63. 37. Youn JH, Park YH, Hang’ombe B, et al. Prevalence and characterization 17. Mwape K, Kwenda G, Kalonda A, et al. Characterisation of Vibrio cholerae of Staphylococcus aureus and Staphylococcus pseudintermedius isolated isolates from the 2009, 2010 and 2016 cholera outbreaks in Lusaka prov- from companion animals and environment in the veterinary teach- ince, Zambia. Pan Afr Med J. 2020;35:1–10. ing hospital in Zambia, Africa. Comp Immunol Microbiol Infect Dis. 18. Matundwelo N, Mwansasu CS. Bacteriology of chronic suppurative otitis 2014;37:123–30. media among children at the arthur davidson children’s hospital, Ndola, 38. Songe MM, Hang’ombe B, Knight-Jones TJD, et al. Antimicrobial resistant Zambia. Med J Zambia. 2016;43(1):36–40. enteropathogenic Escherichia coli and Salmonella spp. in houseflies 19. Mainda G, Bessell PR, Muma JB, et al. Prevalence and patterns of antimi- infesting fish in food markets in Zambia. Int J Environ Res Public Health. crobial resistance among Escherichia coli isolated from Zambian dairy 2016. https:// doi. org/ 10. 3390/ ijerp h1401 0021. cattle across difference production systems. Nature. 2015. https:// doi. org/ 39. Mwamungule S, Chimana HM, Malama S, et al. Contamination of health 10. 1038/ srep1 2439. care workers’ coats at the University Teaching Hospital in Lusaka, Zambia: 20. Mainda G, Lupolova N, Sikakwa L, et al. Whole Genome sequence analysis the nosocomial risk. J Occup Med Toxicol. 2015;10:1–7. reveals lower diversity and frequency of acquired antimicrobial resistance 40. Schaumburg F, Mugisha L, Peck B, et al. Drug-resistant human staphylo- (AMR) genes in E. coli from dairy hers compared with human isolates coccus aureus in sanctuary apes pose a threat to endangered wild ape from the same Region of Central Zambia. Front Microbiol 2019;1–10.36. populations. Am J Primatol. 2012;74:1071–5. 21. Chiyangi H, Muma JB, Malama S, et al. Identification and antimicrobial 41. Mayor S. First WHO antimicrobial surveillance data reveal high levels of resistance patterns of bacterial enteropathogens from children aged resistance globally. BMJ. 2018;360:k462. 0–59 months at the University Teaching Hospital, Lusaka, Zambia: a 42. Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multi- prospective cross sectional study. BMC Infect Dis. 2017;17:1–9. faceted phenomenon. Pathog Glob Health. 2015;109(7):309. 22. Gill CJ, Mwanakasale V, Fox MP, Chilengi R, Tembo M, Nsofwa M, et al. 43. Collignon PJ, McEwen SA. One Health-its importance in helping to better Eec ff t of presumptive co-trimoxazole prophylaxis on pneumococ- control antimicrobial resistance. Trop Med Infect Dis [Internet]. 2019 Jan cal colonization rates, seroepidemiology and antibiotic resistance in 29 [cited 2021 Jun 26];4(1). Available from: http:// www. ncbi. nlm. nih. gov/ Zambian infants: a longitudinal cohort study. Bull World Health Organ. pubmed/ 30700 019. 2008;86(12):929–38. 44. Tadesse BT, Ashley EA, Ongarello S, Havumaki J, Wijegoonewardena M, 23. Bennett SJ, Chunda-Liyoka C, Poppe LK, et al. High nonnucleoside González IJ, et al. Antimicrobial resistance in Africa: a systematic review. reverse transcriptase inhibitor resistance levels in HIV-1-infected Zambian BMC Infect Dis. 2017;17(1):1–17. mother-infant pairs. AIDS. 2020;34:1833–42. 45. UNICEF. UNICEF Zambia Statistics [Internet]. UNICEF. 2018 [cited 2021 Jul 24. Inzaule SC, Jordan MR, Cournil A, et al. Tenofovir resistance in early and 7]. Available from: https:// www. unicef. org/ zambia/ hivai ds. long-term treated patients on first-line antiretroviral therapy in eight low- 46. Moreno M, Caballero E, Mateus RM, Samba F, Gil E, Falcó V. HIV drug income and middle-income countries. AIDS. 2020;34:1965–9. resistance in Africa: an emerging problem that deserves urgent attention. 25. Miti S, Handema R, Mulenga L, et al. Prevalence and characteristics of AIDS. 2017;31(11):1637–9. HIV drug resistance among antiretroviral treatment (ART ) experienced 47. Mutembo S, Mutanga JN, Musokotwane K, Kanene C, Dobbin K, Yao X, adolescents and young adults living with HIV in Ndola, Zambia. PLoS et al. Urban-rural disparities in treatment outcomes among recurrent ONE. 2020;15:1–15. TB cases in Southern Province, Zambia. BMC Infect Dis. 2019;19(1):1–8. 26. Chanda W, Manyepa M, Chikwanda E, et al. Evaluation of antibiotic suscep-https:// doi. org/ 10. 1186/ s12879- 019- 4709-5. tibility patterns of pathogens isolated from routine laboratory specimens at 48. Monde N, Zulu M, Tembo M, Handema R, Munyeme M, Malama S. Drug Ndola Teaching Hospital: a retrospective study. PLoS ONE. 2019;14(12):1–14. resistant tuberculosis in the Northern Region of Zambia: a retrospective 27. Bijl HM, Koetsier DW, van der Werf TS. Chloroquine- and sulfadoxine- study. Front Trop Dis. 2021;3:36. pyrimethamine-resistant falciparum malaria in vivo– a pilot study in rural 49. Joshi S. Hospital antibiogram: a necessity. Indian J Med Microbiol. Zambia. Trop Med Int Heal. 2000;5:692–5. 2010;28(4):277–80. 28. Kabwe M, Tembo J, Chilukutu L, Chilufya M, Ngulube F, Lukwesa C, Kapasa 50. Otto M. Staphylococcus colonization of the skin and antimicrobial pep- M, Enne V, Wexner H, Mwananyanda L, Hamer DH, Sinyangwe S, Ahmed tides. Expert Rev Dermatol. 2010;5(2):183. Y, Klein N, Maeurer M, Zumla A, Bates M. Etiology antibiotic resistance and risk factors for neonatal sepsis in a large referral center in zambia. Pediatr Publisher’s Note Infect Dis J. 2016;35(7):e191–8. https:// doi. org/ 10. 1097/ INF. 00000 00000 Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. 29. Ziwa M, Jovic G, Ngwisha CLT, et al. Common hydrotherapy practices and the prevalence of burn wound bacterial colonisation at the University Teaching Hospital in Lusaka, Zambia. Burns. 2019;45:983–9.
Antimicrobial Resistance and Infection Control – Springer Journals
Published: Mar 3, 2023
Keywords: Antimicrobial resistance; One Health; Zambia; Review
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