Review Article | Open Access
Birhan Alemnew, Habtamu Biazin, Asmamaw Demis, Melese Abate Reta, "Bacterial Profile among Patients with Suspected Bloodstream Infections in Ethiopia: A Systematic Review and Meta-Analysis", International Journal of Microbiology, vol. 2020, Article ID 8853053, 12 pages, 2020. https://doi.org/10.1155/2020/8853053
Bacterial Profile among Patients with Suspected Bloodstream Infections in Ethiopia: A Systematic Review and Meta-Analysis
Introduction. The burden of bloodstream infections (BSIs) has been warranted in Ethiopia. Globally, the emergency and raised resistance rate of bacterial antimicrobial resistance is becoming a prominent problem, and it is difficult to treat patients having sepsis. In this review, we aimed to determine the pooled prevalence of bacterial isolates among presumptive patients with bloodstream infections in Ethiopia. Methods. A systematic search was performed from PubMed/MEDLINE, Scopus, HINARI, ScienceDirect, and Google Scholar electronic databases using PRISMA guidelines. The data analysis was carried out using STATATM version 14 after the records were cleaned and sorted out. Results. A total of 26 studies with 8,958 blood specimens and 2,382 culture-positive bacterial isolates were included for systematic review and meta-analysis. The meta-analysis derived a pooled culture-positive bacterial prevalence which was 25.78% (95% CI: 21.55–30.01%). The estimated pooled prevalence of Gram-positive and Gram-negative bacterial isolates was 15.50% (95% CI: 12.84–18.15%) and 10.48 % (95% CI: 8.32–12.63%), respectively. The two common Gram-positive bacteria isolated from patients suspected of BSIs were coagulase-negative Staphylococcus with a pooled prevalence of 5.75% (95% CI: 4.58–6.92%) and S. aureus 7.04 % (95% CI: 5.37–8.72%). Similarly, the common Gram-negative bacterial isolates and their estimated pooled prevalence were E. coli 1.69% (95% CI: 1.21–2.16%), Klebsiella species 7.04 % (95% CI: 5.37–8.72%), Pseudomonas species 0.39% (95% CI: 0.08–0.70%), Salmonella species 1.09% (95% CI: 0.79–1.38%), and Streptococcus pyogenes 0.88% (95% CI: 0.54–1.22%). Conclusion. The prevalence of bacterial isolates among presumptive patients suspected to BSIs in Ethiopia remains high. Furthermore, we found a remarkable variation in the pathogen distribution across the study setting.
Bloodstream infections are the leading cause of morbidity and mortality throughout the world . Globally, around 200,000 cases of BSIs with mortality of rates ranging from 20 to 50% were reported annually . In low- and middle-income countries including Ethiopia, BSIs are a major public health concern and cause illnesses and deaths in all groups of population , especially in immunocompromised individuals such as patients in an intensive care unit (ICU), elders, children , cancer patients [5, 6], neonates , and patients living with human immunodeficiency virus (HIV) .
Bacterial bloodstream infections are defined as the presence of viable bacteria in the bloodstream that can elicit an immune response . Bacteria may enter the bloodstream invasion, normally sterile parts of the body, in different ways. It is a serious, life-threatening infection that gets worse very quickly due to the spread of microorganisms and their toxins in blood . Both Gram-negative and positive bacteria in a wide range of bacteria species cause BSIs . As many previous studies highlighted, the common types of bacteria causing bloodstream infections are Gram-positive bacteria such as Staphylococcus aureus, coagulase-negative Staphylococci (CoNS), Streptococcus pyogenes, Streptococcus pneumoniae, Streptococcus agalactiae, and Enterococcus faecium and Gram-negative bacteria such as Escherichia coli, Pseudomonas aeruginosa, and Klebsiella species [4, 11, 12].
Blood is normally a sterile site, in which a blood culture has a high positive predictive value and is a key laboratory diagnostic tool/or specimen for an accurate bacteremia diagnosis . Furthermore, blood culture is considered a highly sensitive test to identify such bacterial isolates that can cause bloodstream infection; also, it is easy to perform . Thus, rapid detection and identification of these possible bacterial pathogens in blood culture are very essential, and the determination of their antimicrobial resistance profile has a key role to diminish the impact of bacteria associated with bloodstream infections .
Treatment of BSI is usually done by the timely administration of appropriate antimicrobial agents based on the sensitivity profile of the causative agents. However, due to the emergency and wide distribution of resistant bacteria to most of the currently prescribed antibiotics, it has become a serious health problem with many economic and social inferences all over the world .
Clinical disease caused by multidrug-resistant bacteria prolongs the duration of illness, hospital stays, and healthcare-associated costs and makes patients lose protection to invasive procedures; besides, it lowers productivity and harms the global economy .
On the contrary, bloodstream infections have an impact on dental prechemotherapy and transplant prescribed antimicrobial agents due to developing resistance; as a result, it is difficult to treat dental/oral health, transplantation, hematological diseases, and viral diseases such as coronavirus through reducing the immune systems and increasing the risk of morbidity and mortality due to underline BSIs [18–21].
Extensive use and misuse of antibiotics in clinical, environmental, and agricultural areas, empirical treatment, and taking the drug without prescription are the major contributors to the emergence of antimicrobial resistance (AMR) and the development of different antibiotic-resistant gene mutations [22–24]. Additionally, the global movement of people and the extensive use of antibiotics as the last sort of drug for extended-spectrum antibiotics give rise to carbapenem resistance [24, 25]. Furthermore, prolonged hospital stay, presence of underline medical conditions, and invasive procedures contribute to the rise of AMR .
The spread of drug resistance for many antibiotics makes the treatment options for bacterial bloodstream infections difficult. For this reason, in 2015, the World Health Organization (WHO) set strategies for detection, prevention, and control of AMR [27–29]. This strategy comprises improving awareness and understanding of AMR, performing surveillance and research to increase the knowledge and strengthen the evidence about AMR, improving the use of antimicrobial agents in human and animal health, and developing new drugs, vaccines, diagnostic tools, and other interventions in all countries [30, 31].
Despite many efforts that have been undergoing, many bacterial pathogens have become resistant to the most common antibiotics and become a serious public health concern with economic and social implications. Globally, antimicrobial resistance is a major challenge, particularly in resource-limited countries including Ethiopia. Even though timely and appropriate use of antibiotics is the only way to treat bacterial bloodstream infection, there are no strict antibiotic stewardship practices and information showing the countrywide pooled prevalence of bloodstream infection-causing bacterial isolates and their antimicrobial resistance patterns, which may halt the resistance pattern. Therefore, this systematic review and meta-analysis aimed to determine pooled estimates of the prevalence of bacterial isolates causing bloodstream infections among presumptive patients of bloodstream infections in Ethiopia. Besides, this will help as a benchmark for developing antimicrobial stewardship programs and generating evidence-based selection of antimicrobial agents for proper treatment.
2.1. Protocol and Registration
We strictly follow the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) tool to report the findings of this systematic review and meta-analysis . The completed PRISMA checklist is provided as a supplementary file (additional file: Table S1). The protocol for this study was submitted to the International Prospective Register of Systematic Reviews (PROSPERO) in February 2020 and was assigned the identification number (ID#149999).
2.2. Data Sources and Search Strategies
A systematic search was carried out using the following electronic databases: PubMed/Medline, HINARI, Scopus, ScienceDirect, and Google Scholar. Medical subject headings and related keywords were used extensively to search the appropriate articles from these databases using the following combinations of keywords: “bacterial isolates,” “bacterial pathogen,” “bacteria,” “bloodstream infection,” “bacteremia,” “sepsis,” “septicemia,” “antibiotic resistance pattern,” “antimicrobial resistance,” “antimicrobial susceptibility,” “antimicrobial susceptibility test,” and “Ethiopia.” These search words/phrases were further paired with each other or combined using “AND” and “OR” Boolean operators. Furthermore, reference lists of all included studies were screened to identify further potentially eligible studies and gray literature studies. Only those articles written in the English language and conducted in Ethiopia were considered.
2.3. Inclusion and Exclusion Criteria
Observational studies fulfilling the following criteria were included: (a) studies reporting bloodstream infections across all age groups and conducted in Ethiopia; (b) articles published in the English language and published from 2000 to 2020. Additionally, case reports, policy statements, reviews, and inaccessible full texts or those unable to receive from the corresponding author communicated through e-mail were excluded from the study.
2.4. Study Selection and Quality Assessment
All retrieved studies were exported into EndNote reference manager software version 8 (Thomson Reuters, London), and duplicated studies were removed. Four reviewers (BA, HB, AD, and MAR) independently screened the titles and abstracts, and full texts were reviewed to determine the eligibility of each study. Where there was disagreement, a decision was reached after discussion and consensus among all reviewers. On the contrary, the critical quality assessment checklist recommended by the “Joanna Briggs Institute (JBI)” was used to evaluate the quality of the included studies . Two reviewers (BA and MAR) independently assessed the quality of the full-text articles. The discrepancy was resolved through discussion to reach on consensus and to include articles to the final analysis. The domain paper quality assessment criteria were clear inclusion criteria, details of study subjects, the study settings, reliable/valid measurements for exposure, outcome variables, and appropriate statistical analysis (additional file, Table S2). The cutoff point was declared after reviewing the relevant literature. Disagreements between the two authors were resolved by taking the mean score of the two authors’ evaluations.
2.5. Data Extraction
All articles included in the final analysis were reviewed by two authors independently using standardized data extraction tools prepared in the Microsoft Excel sheet. The following data were extracted from each original article using the data abstraction form: author’s name, year of publication, study region, study area, study design, study period, sample size, the prevalence of bacterial BSI, type of bacterial isolates, and prevalence of bacterial isolates.
2.6. Data Processing and Analysis
The extracted data using Microsoft Excel sheet 2016 were transferred into STATA version 14 software (Stata Corporation, College Station, Texas) for final analysis. Due to the presence of significant heterogeneity across studies, the random-effect model was applied to estimate the pooled effect size, odds ratios (ORs), and 95% confidence intervals (CIs) across studies. Subgroup analysis was conducted by sample size, year of publication, and study region. Heterogeneity of all included studies was assessed using the I2-statistical test. A value of less than 0.05 was used to declare heterogeneity. Heterogeneity across the studies examined using the I2 statistics was categorized to 25%, 50%, and 75% which represent low, moderate, and high, respectively . The source of heterogeneity was examined through sensitivity analysis and subgroup analysis. The presence of publication bias was evaluated using Egger’s regression test with a value of less than 0.05 as a cutoff point to declare the presence of publication bias .
3.1. Search Results
As illustrated in Figure 1, we identified a total of 285 potentially relevant studies from electronic databases, and 39 articles were excluded due to duplication. After reviewing the titles and abstracts, 128 articles were excluded because they did not meet the objectives and the inclusion criteria of the review. Accordingly, 128 full-text articles were reviewed in-depth based on the preset inclusion criteria, of which 102 articles were excluded with reasons. Finally, 26 studies were considered and used for the final quantitative analysis (meta-analysis).
3.2. Characteristics of Included Studies
As illustrated in Table 1, all the included studies in the final quantitative analysis were observational, 20 were cross-sectional [7, 14, 16, 35, 36, 38, 39, 42–47, 49–53, 55] and 6 were retrospective [11, 16, 40, 41, 48, 52] by study design. The included studies were conducted in four regions (Amhara, Tigray, Oromia, and Southern Nations, Nationalities, and Peoples’ Region (SNNPR)) and from the two self-administrative cities (Addis Ababa and Dire Dawa). Of the 26 studies that fulfilled the review inclusion criteria [7, 11, 14, 16, 35, 36, 38–52, 55], eleven studies were conducted in Amhara region [7, 8, 11, 14, 36, 40, 44, 45, 52–54], nine in Addis Ababa [16, 41, 43, 46, 48–50, 55, 56], three in Oromia region [35, 38, 42], and a single study from Tigray , Dire Dawa , and SNNPR . The sample size of individual studies ranged from 83  to 856 .
ATRH: Asella Teaching and Referral Hospital, UoGTH: University of Gondar Teaching Hospital, TASH: Tikur Anbessa Specialized Hospital, YH: Yekatit 12 Hospital, TUSH: Jimma University Specialized Hospital, MK: Mekelle Hospital, BRHRLC: Bahir Dar Regional Health Research Laboratory Center, FHCSH: Felege Hiwot Comprehensive Specialized Hospital, AARL: Addis Ababa Regional Laboratory, GUH: Gondar University Hospital, HUCSH: Hawassa University Comprehensive Specialized Hospital, ZMH: Zewuditu Memorial Hospital, and DCRH: Dil Chora Referral Hospital.
3.3. Culture-Positive Bacterial Profile among Patients with Suspected Bloodstream Infections in Ethiopia
In this meta-analysis, a total of 2,382 positive bacteria cultures obtained from 8,958 blood samples were included. The meta-analysis-derived pooled culture-positive bacterial prevalence from all blood samples was 25.78 % (95% CI: 21.55–30.01%) (Figure 2). Pooled prevalence of Gram-positive and Gram-negative bacterial isolates was 15.50 % (95% CI: 12.84–18.15%) (Figure 3) and 10.48 % (95% CI: 8.32–12.63%) (Figure 4), respectively. The two common Gram-positive bacteria among patients suspected for bloodstream infections were recovered. The pooled prevalence of CoNS was 5.75 % (95% CI: 4.58–6.92%) (Figure 5). Similarly, the pooled estimated prevalence of S. aureus from these groups was 7.04 % (95% CI: 5.37–8.72%) (Figure 6). Likewise, we found five Gram-negative bacterial isolates among patients suspected for bloodstream infection in Ethiopia. The pooled estimates of Klebsiella species isolates were found to be 7.04 % (95% CI: 5.37–8.72%) (additional file: Figure S1 and Table 2) followed by E. coli 1.69% (95% CI: 1.21–2.16%) (additional file: Figure S2 and Table 2), Salmonella species 1.09% (95% CI: 0.79–1.38%) (additional file: Figure S3 and Table 2), S. pyogenes 0.88% (95% CI:0.54–1.22%) (additional file: Figure S4 and Table 2), and Pseudomonas species 0.39% (95% CI: 0.08–0.70%) (additional file: Figure S5 and Table 2).
3.4. Heterogeneity and Publication Bias
The existence of heterogeneity and publication bias was assessed within the included studies. Consequently, there was considerable heterogeneity across twenty six included studies (I2 = 95.8%). Egger’s regression test for publication bias revealed marginally significant (), which indicated the presence of publication bias (additional file: Figure S6). Moreover, heterogeneity across studies considered for Gram-positive isolates was I2 = 92.9% and Gram-negative isolates was I2 = 92.6%. The publication bias of Gram-positive and Gram-negative bacterial isolates was found to be and , respectively, using Egger’s regression test.
3.5. Subgroup Analysis
Due to the presence of high heterogeneity across or within the included studies, we conducted subgroup analysis based on the study area (region), sample size, and year of publication to sort out the possible source of heterogeneity across the studies. However, the subgroup analysis result revealed that the source of heterogeneity was not due to the study region, sample size, and year of publication disparities (Table 3 and Supplementary Figures S7–S9).
Others: Tigray, Southern Nations, Nationalities, and Peoples’ Region, and Dire Dawa.
3.6. Sensitivity Analysis
The sensitivity analysis showed that the effect of individual studies on the pooled estimate was insignificant, suggesting the robustness of the aggregated estimate. Therefore, the pooled prevalence of bacterial isolates was steady and reliable when examined by neglecting one study at a time (additional file: Figure S10).
To our knowledge, the result of this review documented that the pooled prevalence of bacterial isolates causing bloodstream infections in Ethiopia remains high. The overall pooled prevalence of BSIs by bacterial isolates from blood cultures was 27.78%. The finding was relatively lower as compared to findings from meta-analysis done in West Africa in which the pooled prevalence of BSIs was 31.70% . On the contrary, our finding was higher than a study done in low- and middle-income countries that the prevalence of bacterial isolates from community-acquired pediatric bloodstream infection was 19.1% . Moreover, previous studies reported that bacterial positive blood culture ranged from 7 to 13.9% [59, 60]. Similarly, a systematic review done in Africa reported that the pooled prevalence of bacterial isolates from blood specimens among bloodstream infections was 17.4% . Moreover, significant bloodstream infections and antibiotic resistance in the ICU were observed in North India, in which the blood culture positivity was estimated at 12% . Bacterial isolates in a blood sample with a pooled prevalence of 7.4% were reported in Harare, Zimbabwe . Furthermore, a previous systematic review and meta-analysis study done in Africa and Asia region indicated that the median prevalence of BSIs was 12.50% . The possible explanation for the discrepancies might be due to the drug stewardship program, geographical location, epidemiological difference of the etiological agents, and nature of the patients.
The current review revealed that the pooled prevalence of Gram-positive bacterial isolates was 15.50 %. A study conducted in resource-limited countries revealed that the prevalence of Gram-positive bacterial isolates in the blood culture was relatively lower, 6.2% .
Similarly, in this meta-analysis, the pooled prevalence of Gram-negative bacterial isolates was 10.48 %. This finding was relatively similar to the previously conducted systematic review report which revealed that the pooled prevalence of Gram-negative bacterial isolates in blood specimens from children was 7.7% .
Furthermore, the rapid rise of bacterial bloodstream infections and evidence of resistance to commonly prescribed antimicrobial agents have been a warranted public health problem in prevention and treatment of oral health/dental care transplantation process, cancer chemotherapy, hematological diseases, and others due to presensitized and existence of the resistance gene and suppressed host immune systems as a result of bacterial BSIs [18–21].
4.1. Limitations of the Study
Our review had many limitations. First, there was no documented history of antimicrobial therapy and history of antibiotic intake. Second, in this study, only the English language articles were considered for the analysis. Third, due to the lack of documented antibiogram data, we were unable to review and evaluate BSI causing bacteria multidrug resistance profile. Last, antimicrobial susceptibility standards and interpretive criteria change over time, which may have variations in interpretations and findings.
Generally, in this meta-analysis, we found a wide variety of bacterial isolates with the high pooled prevalence of both Gram-negative and Gram-positive bacteria, in particular S. aureus, CoNS, Klebsiella species, E. coli, S. pyogenes, Salmonella species, and Pseudomonas species. Therefore, strengthening of the tool to diagnose BSIs should be a routine practice to detect pathogenic bacteria in blood to select the appropriate/better antibiotics to treat the bacteria causing BSIs. Besides, an effort should be given to the resistance pattern, molecular genetics to detect specific resistance gene mutations associated with different antibiotics, and characterizations of its phylogenetic parameters for those commonly identified bacteria l isolates causing bloodstream infections.
|HIV:||Human immunodeficiency virus|
|MeSH:||Medical subject headings|
|MOOSE:||Meta-analysis of observational studies in epidemiology|
|PRISMA:||Preferred Reporting Items for Systematic Reviews and Meta-Analyses|
|PROSPERO:||International Prospective Register of Systematic Reviews|
|WHO:||World Health Organization.|
All generated data and research materials used during this systematic review and meta-analysis are available from the corresponding author upon reasonable request.
Conflicts of Interest
The authors declare that they have no conflicts of interest.
BA, HB, AD, and MAR developed the protocol and were involved in the design, selection of studies, data extraction, statistical analysis, writing the initial draft of the manuscript, data curation, investigation, formal statistical analysis, quality assessment, writing the original draft, and editing/critical review of the manuscript for publication. All authors read and approved the final draft of the manuscript.
The data (PRISMA check list and additional findings) are available in the supplementary file. (Supplementary Materials)
- K. B. Laupland and D. L. Church, “Population-based epidemiology and microbiology of community-onset bloodstream infections,” Clinical Microbiology Reviews, vol. 27, no. 4, pp. 647–664, 2014.
- D. R. Bhatta, A. Gaur, and H. Supram, “Bacteriological profile of blood stream infections among febrile patients attending a tertiary care centre of Western Nepal,” Asian Journal of Medical Sciences, vol. 4, no. 3, pp. 92–98, 2013.
- A. M. Aiken, N. Mturi, P. Njuguna et al., “Risk and causes of paediatric hospital-acquired bacteraemia in Kilifi District Hospital, Kenya: a prospective cohort study,” The Lancet, vol. 378, no. 9808, pp. 2021–2027, 2011.
- H. Bhabhor, U. Bhabhor, H. Shingala, and M. Sinha, “Bacteriological study of blood stream infection (BSI) in ICU patients,” Indian Journal of Microbiology Research, vol. 5, no. 3, pp. 368–373, 2018.
- A. Fentie, Y. Wondimeneh, A. Balcha, A. Amsalu, and B. Adankie, “Bacterial profile, antibiotic resistance pattern and associated factors among cancer patients at University of Gondar Hospital, Northwest Ethiopia,” Infection and Drug Resistance, vol. 11, pp. 2169–2178, 2018.
- B. Arega, Y. Woldeamanuel, K. Adane, A. Abubeker, and D. Asrat, “Microbial spectrum and drug-resistance profile of isolates causing bloodstream infections in febrile cancer patients at a referral hospital in Addis Ababa, Ethiopia,” Infection and Drug Resistance, vol. 11, pp. 1511–1519, 2018.
- A. Gebrehiwot, W. Lakew, F. Moges et al., “Bacterial profile and drug susceptibility pattern of neonatal sepsis in Gondar university hospital, Gondar Northwest Ethiopia,” Der Pharmacia Lettre, vol. 4, no. 6, pp. 1811–1816, 2012.
- M. Jemal, Bacterial Bloodstream Infections and Their Antimicrobial Susceptiblity Pattern Among HIV/AIDS Patients at Felege Hiwot Referral Hospital, Bahir Dar, Amahara Regional State, North West Ethiopia, Addis Ababa University, Addis Ababa, Ethiopia, 2017.
- G. Singh and S. G. Wulansari, “Pattern of bacterial and fungal pathogen in patients with high risk for invasive fungal disease in an Indonesian tertiary care hospital: an observational study,” Pan African Medical Journal, vol. 29, 2018.
- L. K. Archibald, L. C. McDonald, O. Nwanyanwu et al., “A hospital-based prevalence survey of bloodstream infections in febrile patients in Malawi: implications for diagnosis and therapy,” The Journal of Infectious Diseases, vol. 181, no. 4, pp. 1414–1420, 2000.
- M. Dagnew, G. Yismaw, M. Gizachew et al., “Bacterial profile and antimicrobial susceptibility pattern in septicemia suspected patients attending Gondar university hospital, Northwest Ethiopia,” BMC Research Notes, vol. 6, no. 1, 2013.
- S. Khurana, N. Bhardwaj, M. Kumari, R. Malhotra, and P. Mathur, “Prevalence, etiology, and antibiotic resistance profiles of bacterial bloodstream infections in a tertiary care hospital in Northern India: a 4-year study,” Journal of Laboratory Physicians, vol. 10, no. 4, pp. 426–431, 2018.
- J. P. Buttery, “Blood cultures in newborns and children: optimising an everyday test,” Archives of Disease in Childhood Fetal and Neonatal Edition, vol. 87, no. 1, pp. F25–F28, 2002.
- D. Hailu, B. Abera, G. Yitayew, D. Mekonnen, and A. Derbie, “Bacterial blood stream infections and antibiogram among febrile patients at Bahir dar regional health research laboratory center, Ethiopia,” Ethiopian Journal of Science and Technology, vol. 9, no. 2, p. 103, 2016.
- D. Murty and M. Gyaneshwari, “Blood cultures in paediatric patients: a study of clinical impact,” Indian Journal of Medical Microbiology, vol. 25, no. 3, pp. 220–224, 2007.
- T. Seboxa, W. Amogne, W. Abebe et al., “High mortality from blood stream infection in Addis Ababa, Ethiopia, is due to antimicrobial resistance,” PloS One, vol. 10, no. 12, 2015.
- CDC, Antibiotic Resistance Threats in the United States, US Department of Health and Human Service, Washington, DC, USA, 2013.
- P. Bollero, P. C. Passarelli, A. D’Addona et al., “Oral management of adult patients undergoing hematopoietic stem cell transplantation,” European Review for Medical and Pharmacological Sciences, vol. 22, no. 4, pp. 876–887, 2018.
- D. Azzolino, P. C. Passarelli, P. De Angelis, G. B. Piccirillo, A. D’Addona, and M. Cesari, “Poor oral health as a determinant of malnutrition and sarcopenia,” Nutrients, vol. 11, no. 12, p. 2898, 2019.
- P. C. Passarelli, M. De Leonardis, G. B. Piccirillo et al., “The effectiveness of chlorhexidine and air polishing system in the treatment of Candida albicans infected dental implants: an experimental in vitro study,” Antibiotics, vol. 9, no. 4, p. 179, 2020.
- L. Santacroce, P. C. Passarelli, G. Passarelli, I. A. Charitos, E. Rella, and A. D’Addona, “COVID-19 and oral diseases: how can we manage hospitalized and quarantined patients while reducing risks?” Electronic Journal of General Medicine, vol. 17, no. 6, 2020.
- D. J. Morgan, I. N. Okeke, R. Laxminarayan, E. N. Perencevich, and S. Weisenberg, “Non-prescription antimicrobial use worldwide: a systematic review,” The Lancet Infectious Diseases, vol. 11, no. 9, pp. 692–701, 2011.
- H. D. Marston, D. M. Dixon, J. M. Knisely, T. N. Palmore, and A. S. Fauci, “Antimicrobial resistance,” JAMA, vol. 316, no. 11, pp. 1193–1204, 2016.
- J. O. Sekyere and M. Abate Reta, “Phylogeography and resistome epidemiology of gram-negative bacteria in Africa: a systematic review and genomic meta-analysis from a one-health perspective,” medRxiv, 2020.
- P. M. Hawkey, “Multidrug-resistant gram-negative bacteria: a product of globalization,” Journal of Hospital Infection, vol. 89, no. 4, pp. 241–247, 2015.
- P. Torres-Gonzalez, M. E. Cervera-Hernandez, M. D. Niembro-Ortega et al., “Factors associated to prevalence and incidence of carbapenem-resistant Enterobacteriaceae fecal carriage: a cohort study in a Mexican tertiary care hospital,” PLoS One, vol. 10, no. 10, 2015.
- N. Sabtu, D. Enoch, and N. Brown, “Antibiotic resistance: what, why, where, when and how,” British Medical Bulletin, vol. 116, no. 1, 2015.
- M. Akova, “Epidemiology of antimicrobial resistance in bloodstream infections,” Virulence, vol. 7, no. 3, pp. 252–266, 2016.
- J. Carlet, V. Jarlier, S. Harbarth, A. Voss, H. Goossens, and D. Pittet, “Ready for a world without antibiotics? the pensières antibiotic resistance call to action,” Antimicrobial Resistance and Infection Control, vol. 1, no. 1, 2012.
- World Health Organization, Global Action Plan on Antimicrobial Resistance, World Health Organization, Geneva, Switzerland, 2015.
- Ethiopian Public Health Institute, Ethiopia Antimicrobial Resistance Surveillance Plan, Ethiopian Public Health Institute, Addis Ababa, Ethiopia, 2017.
- D. L. A. Moher, J. Tetzlaff, D. G. Altman, and P. Group, “Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement,” PLoS Medicine, vol. 6, no. 7, 2009.
- Joanna Briggs Institute, The Joanna Briggs Institute Critical Appraisal Tools for Use in JBI Systematic Reviews: Checklist for Prevalence Studies, Joanna Briggs Institute, Adelaide, Australia, 2018.
- J. L. Peters, A. J. Sutton, D. R. Jones, K. R. Abrams, L. Rushton, and S. G. Moreno, “Assessing publication bias in meta-analyses in the presence of between-study heterogeneity,” Journal of the Royal Statistical Society: Series A (Statistics in Society), vol. 173, no. 3, pp. 575–591, 2010.
- A. Sorsa, J. Früh, L. Stötter, and S. Abdissa, “Blood culture result profile and antimicrobial resistance pattern: a report from neonatal intensive care unit (NICU), Asella teaching and referral hospital, Asella, south East Ethiopia,” Antimicrobial Resistance and Infection Control, vol. 8, no. 1, pp. 42–46, 2019.
- A. A. Abebaw Shiferaw, H. Tesera, T. Belachew, and G. D. Mihiretie, “The bacterial profile and antibiotic susceptibility pattern among patients with suspected bloodstream infections, Gondar, north-west Ethiopia,” Pathology and Laboratory Medicine International, vol. 10, pp. 1–7, 2018.
- A. Negussie, G. Mulugeta, A. Bedru et al., “Bacteriological profile and antimicrobial susceptibility pattern of blood culture isolates among septicemia suspected children in selected hospitals Addis Ababa, Ethiopia,” International Journal of Biological and Medical Research, vol. 6, no. 1, pp. 4709–4717, 2015.
- A. Abrha, A. Abdissa, G. Beyene, G. Getahun, and T. Girma, “Bacteraemia among severely malnourished children in Jimma university hospital, Ethiopia,” Ethiopian Journal of Health Sciences, vol. 21, no. 3, pp. 175–182, 2011.
- A. G. Wasihun, L. N. Wlekidan, S. A. Gebremariam et al., “Bacteriological profile and antimicrobial susceptibility patterns of blood culture isolates among febrile patients in Mekelle Hospital, Northern Ethiopia,” Springer Plus, vol. 4, p. 314, 2015.
- F. Moges, S. Eshetie, W. Abebe et al., “High prevalence of extended-spectrum beta-lactamase-producing gram-negative pathogens from patients attending Felege Hiwot comprehensive specialized hospital, Bahir dar, Amhara region,” PloS One, vol. 14, no. 4, 2019.
- K. Terfa Kitila, B. D. Taddese, T. K. Hailu et al., “Assessment of bacterial profile and antimicrobial resistance pattern of bacterial isolates from blood culture in Addis Ababa regional laboratory, Addis Ababa, Ethiopia,” Clinical Microbiology: Open Access, vol. 7, no. 2, 2018.
- T. Zenebe, S. Kannan, D. Yilma, and G. Beyene, “Invasive bacterial pathogens and their antibiotic susceptibility patterns in jimma university specialized hospital, Jimma, southwest Ethiopia,” Ethiopian Journal of Health Sciences, vol. 21, no. 1, pp. 1–8, 2011.
- S. Eshetu, A. Bitew, T. Getachew, D. Abera, and S. Gizaw, “Multi-drug resistance profile of bacteria isolated from blood stream infection at Tikur anbessa specialized hospital, Addis Ababa, Ethiopia,” EC Microbiology, 2018.
- T. G/eyesus, F. Moges, S. Eshetie, B. Yeshitela, and E. Abate, “Bacterial etiologic agents causing neonatal sepsis and associated risk factors in Gondar, Northwest Ethiopia,” BMC Pediatrics, vol. 17, no. 1, 2017.
- G. Alebachew, B. Teka, M. Endris, Y. Shiferaw, and B. Tessema, “Etiologic agents of bacterial sepsis and their antibiotic susceptibility patterns among patients living with human immunodeficiency virus at Gondar university teaching hospital, Northwest Ethiopia,” BioMed Research International, vol. 2016, Article ID 5371875, 8 pages, 2016.
- B. Arega, Y. Wolde-Amanuel, K. Adane, E. Belay, A. Abubeker, and D. Asrat, “Rare bacterial isolates causing bloodstream infections in Ethiopian patients with cancer,” Infectious Agents and Cancer, vol. 12, no. 1, 2017.
- T. Alemayehu, E. Tadesse, S. Ayalew et al., “High burden of Nosocomial infections caused by multi-drug Re-sistant pathogens in pediatric patients at Hawassa university comprehensive specialized hospital,” Ethiopian Medical Journal, 2019.
- Y. Adib and B. Worku, “Descriptive cross –sectional study on neonatal sepsis in the neonatal intensive care unit of Tekur Anbessa hospital, Addis Ababa , Ethiopia,” Earth, Planets and Space, 2012.
- M. Mitiku, Z. Ayenew, and K. Desta, “Multi-drug resistant, extended spectrum beta-lactamase and carbapenemase producing bacterial isolates among children under five years old with suspected bloodstream infection in a specialized hospital in Ethiopia: Cross-sectional study,” 2019.
- D. Tsega, K. Desta, and Y. Woldekidan, Bacterial Profile, Antimicrobial Susceptibility Pattern and Associated Risk Factors Among Septicemia Suspected Pediatrics Patients at Zewuditu Memorial Hospital, Addis Ababa, Ethiopia, Addis Ababa University Institutional Repository, Addis Ababa, Ethiopia, 2017.
- D. Demissie, B. Seyoum, M. Demena, and B. Yeshitila, “Septicemia, bacterial isolates and drug susceptibility among women attending delivery at dilchora hospital, Dire Dawa, Eastern Ethiopia,” 2019, Ethiopian Medical Journal.
- J. Ali and Y. Kebede, “Frequency of isolation and antimicrobial susceptibility pattern of bacterial isolates from blood culture, Gondar University teaching hospital, Northwest Ethiopia,” Ethiopian Medical Journal, vol. 46, no. 2, pp. 155–161, 2008.
- M. Endris, Y. Takele, D. Woldeyohannes et al., “Bacterial sepsis in patients with visceral leishmaniasis in Northwest Ethiopia,” BioMed Research International, vol. 2014, Article ID 361058, 7 pages, 2014.
- S. T. Gebre-Egziabher, F. M. Yehuala, Z. T. Kebede, and A. G. Mehari, “Bacterial profile and their antibiotic resistance patterns from blood culture in intensive care unit patients at the university of Gondar comprehensive specialized hospital, Northwest Ethiopia,” General Microbiology, 2019.
- A. Negussie, G. Mulugeta, A. Bedru et al., “Bacteriological profile and antimicrobial sensitivity pattern of blood culture isolates among septicemia-suspected children at Tikur Anbessa Specialized Hospital and Yekatit 12 Hospital, Addis Ababa, Ethiopia,” Critical Care, vol. 17, no. 4, 2013.
- M. Hailu, G. Mulugeta, and D. Asrat, “Prevalence and antimicrobial resistance pattern of bacterial isolates among children suspected for septicemia and urinary tract infections at Tikur Anbessa specialized hospital, Addis Ababa, Ethiopia,” International Journal of Scientific and Engineering Research, vol. 7, no. 10, pp. 1431–1444, 2016.
- K. J. Bernabé, C. Langendorf, N. Ford, J.-B. Ronat, and R. A. Murphy, “Antimicrobial resistance in West Africa: a systematic review and meta-analysis,” International Journal of Antimicrobial Agents, vol. 50, no. 5, pp. 629–639, 2017.
- N. Droz, Y. Hsia, S. Ellis, A. Dramowski, M. Sharland, and R. Basmaci, “Bacterial pathogens and resistance causing community acquired paediatric bloodstream infections in low- and middle-income countries: a systematic review and meta-analysis,” Antimicrobial Resistance & Infection Control, vol. 8, 2019.
- K. Le Doare, J. Bielicki, P. T. Heath, and M. Sharland, “Systematic review of antibiotic resistance rates among gram-negative bacteria in children with sepsis in resource-limited countries,” Journal of the Pediatric Infectious Diseases Society, vol. 4, no. 1, pp. 11–20, 2015.
- J. Deen, L. von Seidlein, F. Andersen, N. Elle, N. J. White, and Y. Lubell, “Community-acquired bacterial bloodstream infections in developing countries in south and southeast Asia: a systematic review,” The Lancet Infectious Diseases, vol. 12, no. 6, pp. 480–487, 2012.
- B. T. Tadesse, E. A. Ashley, S. Ongarello et al., “Antimicrobial resistance in Africa: a systematic review,” BMC Infectious Diseases, vol. 17, no. 1, p. 616, 2017.
- C. Wattal, R. Raveendran, N. Goel, J. K. Oberoi, and B. K. Rao, “Ecology of blood stream infection and antibiotic resistance in intensive care unit at a tertiary care hospital in North India,” The Brazilian Journal of Infectious Diseases, vol. 18, no. 3, pp. 245–251, 2014.
- M. Mhondoro, N. Ndlovu, D. Bangure et al., “Trends in antimicrobial resistance of bacterial pathogens in Harare, Zimbabwe, 2012-2017: a secondary dataset analysis,” BMC Infectious Diseases, vol. 19, no. 1, 2019.
- C. S. Marchello, A. P. Dale, S. Pisharody, M. P. Rubach, and J. A. Crump, “Prevalence of community-acquired bloodstream infections among hospitalized patients in Africa and Asia: a systematic review and meta-analysis,” Antimicrobial Agents and Chemotherapy, vol. 64, no. 1, 2019.
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