American Journal of Infectious Diseases and Microbiology
ISSN (Print): 2328-4056 ISSN (Online): 2328-4064 Website: Editor-in-chief: Maysaa El Sayed Zaki
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American Journal of Infectious Diseases and Microbiology. 2021, 9(2), 39-47
DOI: 10.12691/ajidm-9-2-2
Open AccessArticle

Prevalence of Carbapenemase Encoding Genes and Antimicrobial Resistance Pattern of Enterobacteriaceae Isolated from Hospitalized Patients in Khartoum State, Sudan

Omnia M. Hamid1, , Omer M. Omer2 and Magdi A. Bayoumi3

1Faculty of Medical Laboratory Sciences-Medical Microbiology, University of Medical Sciences & Technology, Khartoum, Sudan

2Faculty of Medical Laboratory Sciences-Medical Microbiology, National university of Sudan, Khartoum, Sudan

3Faculty of Postgraduate Studies, Scientific Research, and Publication, Ibn Sina University, Khartoum, Sudan

Pub. Date: April 16, 2021

Cite this paper:
Omnia M. Hamid, Omer M. Omer and Magdi A. Bayoumi. Prevalence of Carbapenemase Encoding Genes and Antimicrobial Resistance Pattern of Enterobacteriaceae Isolated from Hospitalized Patients in Khartoum State, Sudan. American Journal of Infectious Diseases and Microbiology. 2021; 9(2):39-47. doi: 10.12691/ajidm-9-2-2


Carbapenem-resistant Enterobacteriaceae strains have been responsible for an increasing number of hospital-acquired infections globally. This study aimed to determine the prevalence of carbapenemase-producing Enterobacteriaceae and their frequency of antimicrobial-resistant patterns among hospitalized patients across three Khartoum State Teaching Hospitals, Sudan. Materials and Methods. A cross-sectional study was conducted at Khartoum State Teaching Hospitals from April 2018 to October 2019. A total of 384 non-duplicative Enterobacteriaceae strains were isolated from1062 clinical samples obtained from hospitalized patients receiving treatment across three main teaching hospitals. The samples were cultured into a MacConkey agar plate. The Enterobacteriaceae strains were differentiated by specific colony color and again by biochemical test. Antimicrobial susceptibility testing was performed by the disc diffusion method. The minimum inhibitory concentration (MIC) of imipenem and meropenem was performed by the agar dilution method. Multiplex polymerase chain reaction (PCR) was performed to investigate the presence of carbapenemase-encoding genes. Data analysis was carried out using SPSS version 21. Results. Of the 36.2% (384/10.62) nonduplicate of Enterobacteriaceae strains isolated from clinical samples, 122 (31.8%) were carbapenemase-producing Enterobacteriaceae (CPE). Of these isolates, 37 (30.3%) harbored the blaIMP followed by; 29 (23.8%) blaNDM, 21 (17.2%) blaOXA-48, 6 (4.9%) blaGES, 5 (4.1%) were blaKPC, 3(2.5%) blaGIM-1, 2(1.6%) blaVIM and 1 (0.8%) blaSIM-1, while the remaining 19(15.6%) isolates carried combinations carbapenemase blagenes. The most predominant CPE strains were Escherichia coli 40 (32.8%) followed by Klebsiella pneumoniae 24 (19.7%) and Enterobacter aerogenes 14(11.5%). Most of the CPE isolates were isolated from wound swab 40(32.8), sputum 33(27.0), and urine 22(18.0) samples. Furthermost strains showed high resistance rates (>70%) to the antibiotics tested. Resistance to amikacin, tetracycline, co-trimoxazole, and nalidixic acid was 36.9%, 43.4%, 62.3%, and 63.9%, respectively and 82.8 % of CPE strains were susceptible to colistin. The detection of blagenes carbapenemases in CPE strains had a significant effect on both imipenem and meropenem MICs. Conclusion. The most prevalent carbapenemase-producing blagenes among clinical Enterobacteriaceae clinical isolates from the three Khartoum state regions were blaIMP, blaNDM, and blaOXA-48. In contrast, the propensity of the multidrug-resistant profile that has been associated with producing carbapenemase blagenes is alarming. Therefore, it is very important to establish a routine screening of carbapenemase-producing blagenes in clinical isolates to prevent the dissemination of resistant strains among both inpatients and outpatients in hospital settings.

carbapenemase Enterobacteriaceae Khartoum prevalence resistance

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[1]  Guh AY, Bulens SN, Mu Y, Jacob JT, Reno J, Scott J, Wilson LE, Vaeth E, Lynfield R, Shaw KM: Epidemiology of carbapenem-resistant Enterobacteriaceae in 7 US communities, 2012-2013. Jama 2015, 314(14):1479-1487.
[2]  Nordmann P, Dortet L, Poirel L: Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends in molecular medicine 2012, 18(5):263-272.
[3]  Potter RF, D’Souza AW, Dantas G: The rapid spread of carbapenem-resistant Enterobacteriaceae. Drug Resistance Updates 2016, 29:30-46.
[4]  Meletis G: Carbapenem resistance: overview of the problem and future perspectives. Therapeutic advances in infectious disease 2016, 3(1): 15-21.
[5]  Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, Westblade LF: Carbapenemase-producing organisms: a global scourge. Clinical Infectious Diseases 2018, 66(8):1290-1297.
[6]  Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, Nisar MA, Alvi RF, Aslam MA, Qamar MU: Antibiotic resistance: a rundown of a global crisis. Infection and drug resistance 2018, 11: 1645.
[7]  Guh AY, Limbago BM, Kallen AJ: Epidemiology and prevention of carbapenem-resistant Enterobacteriaceae in the United States. Expert review of anti-infective therapy 2014, 12(5):565-580.
[8]  Shrivastava SR, Shrivastava PS, Ramasamy J: World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. Journal of Medical Society 2018, 32(1):76.
[9]  Nordmann P, Gniadkowski M, Giske C, Poirel L, Woodford N, Miriagou V, on Carbapenemases EN: Identification and screening of carbapenemase-producing Enterobacteriaceae. Clinical Microbiology and Infection 2012, 18(5):432-438.
[10]  Doi Y, Paterson DL: Carbapenemase-producing enterobacteriaceae. In: Seminars in respiratory and critical care medicine: 2015. NIH Public Access: 74.
[11]  Elbadawi HS, Elhag KM, Mahgoub E, Altayb HN, Ntoumi F, Elton L, McHugh TD, Osman M, Tembo J, Vairo F: Detection and Characterisation of Carbapenem Resistant Gram-negative Bacilli Isolates Recovered From Hospitalised Patients at Soba University Hospital, Sudan. 2020.
[12]  Mahrach Y, Mourabit N, Arakrak A, Bakkali M, Laglaoui A: Phenotypic and molecular study of carbapenemase-producing Enterobacteriaceae in a regional hospital in northern Morocco. J Clin Med Sci 2019, 3:113.
[13]  Perovic O, Ismail H, Quan V, Bamford C, Nana T, Chibabhai V, Bhola P, Ramjathan P, Swe-Han KS, Wadula J: Carbapenem-resistant Enterobacteriaceae in patients with bacteraemia at tertiary hospitals in South Africa, 2015 to 2018. European Journal of Clinical Microbiology & Infectious Diseases 2020, 39(7): 1287-1294.
[14]  Soliman AM, Zarad HO, Nariya H, Shimamoto T, Shimamoto T: Genetic analysis of carbapenemase-producing Gram-negative bacteria isolated from a university teaching hospital in Egypt. Infection, Genetics and Evolution 2020, 77:104065.
[15]  Reyes JA, Melano R, Cárdenas PA, Trueba G: Mobile genetic elements associated with carbapenemase genes in South American Enterobacterales. Brazilian Journal of Infectious Diseases 2020, 24(3): 231-238.
[16]  Satir S, Elkhalifa A, Ali M, El Hussein A, Elkhidir I: Detection of Carbepenem resistance genes among selected Gram Negative bacteria isolated from patients in-Khartoum State, Sudan. Clin Microbiol 5: 266. doi: 10.4172/2327-5073. 1000266 Page 2 of 4 Clin Microbiol, an open access journal ISSN: 2327-5073 Volume 5• Issue 6• 1000266. Figure 2016016, 2:3.
[17]  Jung SH: Stratified Fisher's exact test and its sample size calculation. Biometrical Journal 2014, 56(1):129-140.
[18]  Abbey TC, Deak E: What's New from the CLSI Subcommittee on Antimicrobial Susceptibility Testing M100. Clinical Microbiology Newsletter 2019, 41(23):203-209.
[19]  Wikler MA: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard. CLSI (NCCLS) 2006, 26:M7-A7.
[20]  Poirel L, Walsh TR, Cuvillier V, Nordmann P: Multiplex PCR for detection of acquired carbapenemase genes. Diagnostic microbiology and infectious disease 2011, 70(1):119-123.
[21]  Ellington MJ, Kistler J, Livermore DM, Woodford N: Multiplex PCR for rapid detection of genes encoding acquired metallo-β-lactamases. Journal of Antimicrobial Chemotherapy 2007, 59(2): 321-322.
[22]  Castanheira M, Toleman MA, Jones RN, Schmidt FJ, Walsh TR: Molecular characterization of a β-lactamase gene, blaGIM-1, encoding a new subclass of metallo-β-lactamase. Antimicrobial agents and chemotherapy 2004, 48(12):4654-4661.
[23]  Hamid O, Gumaa S, Ibrahim A: Extended spectrum beta-lactamase producing Enterobacteriaceae: hospital-acquired urinary tract infections, Khartoum-Sudan. Ann Microbiol Res 2019, 3(1): 76-82.
[24]  Mahamat OO, Lounnas M, Hide M, Dumont Y, Tidjani A, Kamougam K, Abderrahmane M, Benavides J, Solassol J, Bañuls A-L: High prevalence and characterization of extended-spectrum ß-lactamase producing Enterobacteriaceae in Chadian hospitals. BMC infectious diseases 2019, 19(1):1-7.
[25]  Ghotaslou R, Sadeghi MR, Akhi MT, Hasani A, Asgharzadeh M: Prevalence and antimicrobial susceptibility patterns of ESBL, ampC and carbapenemase-producing enterobactericeae isolated from hospitalized patients in Azerbaijan, Iran. Iranian journal of pharmaceutical research: IJPR 2018, 17(Suppl):79.
[26]  Singh-Moodley A, Perovic O: Antimicrobial susceptibility testing in predicting the presence of carbapenemase genes in Enterobacteriaceae in South Africa. BMC infectious diseases 2016, 16(1): 1-10.
[27]  Khalil HS, Wahab MAAE: Risk factors, phenotypic and genotypic characterization of carpabenem resistant Enterobacteriaceae in Tanta University Hospitals, Egypt. International Journal of Infection Control 2016, 12(2).
[28]  Okoche D, Asiimwe BB, Katabazi FA, Kato L, Najjuka CF: Prevalence and characterization of carbapenem-resistant Enterobacteriaceae isolated from Mulago National Referral Hospital, Uganda. PLoS One 2015, 10(8):e0135745.
[29]  Mushi MF, Mshana SE, Imirzalioglu C, Bwanga F: Carbapenemase genes among multidrug resistant gram negative clinical isolates from a tertiary hospital in Mwanza, Tanzania. BioMed research international 2014, 2014.
[30]  Hu L, Zhong Q, Shang Y, Wang H, Ning C, Li Y, Hang Y, Xiong J, Wang X, Xu Y: The prevalence of carbapenemase genes and plasmid-mediated quinolone resistance determinants in carbapenem-resistant Enterobacteriaceae from five teaching hospitals in central China. Epidemiology & Infection 2014, 142(9):1972-1977.
[31]  Ehrhard I, Karaalp A, Hackel T, Höll G, Rodewald N, Reif U, Kaase M, Eckmanns T, Sydow W: Prevalence of carbapenemase-producing bacteria in hospitals in Saxony, Germany. Bundesgesundheitsblatt, Gesundheitsforschung, Gesundheitsschutz 2014, 57(4):406-413.
[32]  Lerner A, Solter E, Rachi E, Adler A, Rechnitzer H, Miron D, Krupnick L, Sela S, Aga E, Ziv Y: Detection and characterization of carbapenemase-producing Enterobacteriaceae in wounded Syrian patients admitted to hospitals in northern Israel. European Journal of Clinical Microbiology & Infectious Diseases 2016, 35(1): 149-154.
[33]  Miró E, Agüero J, Larrosa M, Fernández A, Conejo M, Bou G, González-López J, Lara N, Martínez-Martínez L, Oliver A: Prevalence and molecular epidemiology of acquired AmpC β-lactamases and carbapenemases in Enterobacteriaceae isolates from 35 hospitals in Spain. European journal of clinical microbiology & infectious diseases 2013, 32(2): 253-259.
[34]  Wilson H, Török ME: Extended-spectrum β-lactamase-producing and carbapenemase-producing Enterobacteriaceae. Microbial genomics 2018, 4(7).
[35]  Temkin E, Adler A, Lerner A, Carmeli Y: Carbapenem‐resistant Enterobacteriaceae: biology, epidemiology, and management. Annals of the New York Academy of Sciences 2014, 1323(1): 22-42.
[36]  Bogaerts P, Cuzon G, Evrard S, Hoebeke M, Naas T, Glupczynski Y: Evaluation of a DNA microarray for rapid detection of the most prevalent extended-spectrum β-lactamases, plasmid-mediated cephalosporinases and carbapenemases in Enterobacteriaceae, Pseudomonas and Acinetobacter. International journal of antimicrobial agents 2016, 48(2):189-193.
[37]  Aoki K, Harada S, Yahara K, Ishii Y, Motooka D, Nakamura S, Akeda Y, Iida T, Tomono K, Iwata S: Molecular characterization of IMP-1-producing Enterobacter cloacae complex isolates in Tokyo. Antimicrobial agents and chemotherapy 2018, 62(3).
[38]  Adam MA, Elhag WI: Prevalence of metallo-β-lactamase acquired genes among carbapenems susceptible and resistant Gram-negative clinical isolates using multiplex PCR, Khartoum hospitals, Khartoum Sudan. BMC infectious diseases 2018, 18(1): 1-6.
[39]  Mohamed E, Ahmed AO, Kidir E-SB, Sirag B, Ali MA: Phenotypic and genotypic characterization of carbapenems-resistant clinical gram-negative bacteria from Sudan. Edorium Journal of Microbiology 2019, 23(12): 457-464.
[40]  Hamprecht A, Poirel L, Göttig S, Seifert H, Kaase M, Nordmann P: Detection of the carbapenemase GIM-1 in Enterobacter cloacae in Germany. Journal of Antimicrobial Chemotherapy 2013, 68(3): 558-561.
[41]  Lü Y, Zhao S, Liang H, Zhang W, Liu J, Hu H: The first report of a novel IncHI1B blaSIM-1-carrying megaplasmid pSIM-1-BJ01 from a clinical Klebsiella pneumoniae isolate. Infection and drug resistance 2019, 12: 2103.
[42]  Zowawi HM, Sartor AL, Balkhy HH, Walsh TR, Al Johani SM, AlJindan RY, Alfaresi M, Ibrahim E, Al-Jardani A, Al-Abri S: Molecular characterization of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in the countries of the Gulf cooperation council: dominance of OXA-48 and NDM producers. Antimicrobial agents and chemotherapy 2014, 58(6): 3085-3090.
[43]  Jeong SH, Kim H-S, Kim J-S, Shin DH, Kim HS, Park M-J, Shin S, Hong JS, Lee SS, Song W: Prevalence and molecular characteristics of carbapenemase-producing Enterobacteriaceae from five hospitals in Korea. Annals of laboratory medicine 2016, 36(6):529.
[44]  O’Riordan J, Bhally HS, Salmon AH, de Zoysa JR: Successful treatment of carbapenemase producing Enterobacteriaceae peritonitis: Old therapy for a new bug’. Peritoneal Dialysis International 2020, 40(1): 100-102.