Antimicrobial susceptibility pattern of Acinetobacter isolates from patients in Kenyatta National Hospital, Nairobi, Kenya

Antimicrobial susceptibility pattern of Acinetobacter isolates from patients in Kenyatta National Hospital, Nairobi, Kenya

Victor Moses Musyoki^1,&, Moses Muia Masika¹, Winnie Mutai¹, Gitau Wilfred¹, Antony Kuria², Felista Muthini¹

 

¹Department of Medical Microbiology, School of Medicine, University of Nairobi, Nairobi, Kenya, ²Department of Medical Microbiology, Kenyatta National Hospital, Nairobi, Kenya

 

 

^&Corresponding author
Victor Moses Musyoki, Department of Medical Microbiology, School of Medicine, University of Nairobi, Nairobi, Kenya

 

 

 

 

The genus Acinetobacter comprises of non-motile gram-negative coccobacilli bacteria. The colonies are 1 to 2mm, non-hemolytic, mucoid, smooth and round on sheep's blood agar after 24 hours of incubation at 37ºC (Figure 1) [1-3]. Most species in this genus have emerged as common pathogens causing community as well as hospital-acquired infections [4, 5]. Hospital-acquired infections are common among patients admitted in the intensive care unit (ICU) and those patients not admitted in the ICU but are immunocompromised. Infections linked to these species include wound infections, urinary tract infections, pneumonia and bacteremia subsequent to trauma, urinary catheters, mechanical ventilators and central venous access catheters respectively. These infections increase the length of hospital stay and risk of hospital death [6]. As a health concern, Acinetobacter associated infections are difficult to treat due to the natural tendency of acquisition and spread of multidrug-resistant strains among hospitalized patients and the organisms' different mechanism of antimicrobial resistance [7, 8]. This has contributed to the high morbidity and mortality rate ranging from 27% and 91% especially in immunocompromised patients in the last three decades [9]. Globally, the occurrence of MDR Acinetobacter, particularly A. baumannii has been reported through several epidemiological studies [10] with a documentation of 10-15% prevalence of Acinetobacter resistance to carbapenem, penicillins and fluoroquinolones [11, 12]. Acinetobacter species have relatively high resistance to carbapenems, even in countries with high level of awareness and vibrant national nosocomial infection surveillance with an overall low antibiotic resistance [11-13]. However, carbapenems remain the treatment of choice for Acinetobacter infections [14]. In two separate studies conducted in Kenya, one study noted that 10% of community-acquired bacteremia was associated with Acinetobacter species [13] while in another study that recruited hospitalized patients, A. baumannii accounted for 0.9% in wound infections [15]. Management of nosocomial infections remains a challenge in healthcare settings due to the increasing resistance to antimicrobials [16]. Therefore the aim of this study was to evaluate the antimicrobial susceptibility of Acinetobacter species isolated from patients in Kenyatta National Hospital (KNH). Previous studies done in Kenya focused on critical care units, we however explored other hospital units.

 

 

This was a retrospective study. We analyzed electronic laboratory records of Acinetobacter isolates from clinical specimens analyzed between 2013 and 2015 at KNH microbiology laboratory. Identification and antimicrobial susceptibility data were retrieved from the VITEK-2 antimicrobial susceptibility system and exported to WHONET through BACLINK. Analysis was done using WHONET version 5.6 and IBM SPSS Statistics version 21. Identification of Acinetobacter isolates was done using VITEK-2 Gram Negative identification card (GN83). Clinical specimens were mainly tracheal aspirates, pus, and urine and were analyzed according to the 2015 Clinical and Laboratory Standards Institute guidelines (CLSI M100-S25). The panel of antibiotics tested included amoxicillin/clavulanic acid (20/10 μg), amikacin (30 μg), ampicillin (10 μg), aztreonam (30 μg), ceftazidime (30 μg), ciprofloxacin (5 μg), cefpodoxime (10 μg), ceftriaxone (30 μg), cefotaxime (30 μg), cefuroxime axetil (30 μg), cefuroxime (30 μg), cefazolin (30 μg), cefepime (30 μg), cefoxitin (30 μg), gentamicin (10 μg), meropenem (10 μg), nitrofurantoin (300 μg), norfloxacin (10 μg), piperacillin (100 μg), ampicillin/sulbactam (10/10 μg), trimethoprim/sulfamethoxazole (1.25/23.75 μg), tobramycin (10 μg) and piperacillin/tazobactam (100/10 μg). The laboratory participates in external quality assurance (EQA) coordinated by United Kingdom National External Quality Assurance (UKNEQAS) and World Health Organization-National Institute for Communicable Diseases (WHO-NICD). This helps to evaluate reliability of methods, materials, equipment and staff training impact. The study was approved by the Kenyatta National Hospital-University of Nairobi Ethics and Research Committee.

 

 

The study analyzed 590 Acinetobacter isolates. Majority of the isolates were from male patients, 380 (52%). The isolates were mainly from tracheal aspirates (273; 46%), pus (130; 22%), urine (93; 16%) and blood (35; 6%). The specimen type for thirty-five (6%) of the isolates was unknown. Other isolates were obtained from peritoneal fluid, pleural fluid, cerebral spinal fluid and tissue. The most frequently isolated Acinetobacter species in this study was Acinetobacter baumannii (95%); the other isolates included Acinetobacter lwoffii (3%) and Acinetobacter haemolyticus (1%) (Table 1). Most of the isolates were obtained from samples collected from critical care unit (48%) and internal medicine (13%) with the least obtained from accident and emergency unit (9%) and burns unit (3%). Acinetobacter baumannii (n=560) showed high susceptibility to amikacin (77%) and poor susceptibility to tobramycin (37%), meropenem (27%), penicillins (1-27%), fluoroquinolones (13-24%), cephalosporins (0-11%) and trimethoprim-sulfamethoxazole (15%) (Figure 2). Although Acinetobacter lwoffii (n=15), A. haemolyticus (n=5), A. junii (n=1) and other Acinetobacter species (n=8) did not meet the CLSI threshold for antibiogram reporting (≥30 isolates each), their AST results were reported due to their microbiological significance. Both A. lwoffii and A. haemolyticus had high susceptibility to amikacin (80-100%), meropenem (75-100%), ciprofloxacin (80-85%), gentamicin (80-100%) and piperacillin/tazobactam (75-80%); poor susceptibility to aztreonam (23-25%), cefuroxime axetil (20-31%), cefazolin (23-25%) and cefoxitin (20-39%) (Table 2). Acinetobacter baumannii isolates from tracheal aspirates, pus, and urine, showed high level of resistance to cephalosporins (65-85%), ciprofloxacin (69-76%) and moderate resistance to meropenem (51-59%) (Table 3). Isolates obtained from blood and other specimens had moderate resistance to cephalosporins (49-63%). Acinetobacter baumannii isolates from all specimens showed relatively high sensitivity to amikacin (77-89%). Antibiotic susceptibility varied with hospital units. High resistance to cephalosporins (65-86%) was seen in A. baumannii isolates from critical care unit, obstetrics and gynecology, internal medicine ward, accident and emergency, and surgery (Table 4). In summary, A. baumannii was the most common species isolated and showed high susceptibility to amikacin (77%), high resistance to cephalosporins (89-100%), fluoroquinolones (76-87%) and meropenem (72%).

 

 

In this study, we recorded 95% of Acinetobacter baumannii from all the samples analyzed. Other species were detected in low numbers and included Acinetobacter lwoffii (3%), A. haemolyticus (1%), A. calcoaceticus (n=1) and A. junii (n=1). A similar observation was noted in similar studies in India [17, 18] and Nigeria [19] where A. baumannii and A. lwoffii were the predominant species. The predominance of Acinetobacter baumannii is most likely due to its ability to survive for a long period in the hospital environment, the potential to respond to selective environment pressure and its non-fastidious nature. Based on hospital units and specimen type, majority of the isolates were obtained from samples collected from the critical care unit (48%) and tracheal aspirates (46%) respectively. Consequently, high level of resistance (71-86%) to the commonly used antibiotics was noted in isolates from these units. These findings concur with results from similar studies conducted in India [18], Iran [20] and Sudan [21]. Several factors including immunosuppressed hosts, previous use of antibiotics, patients with severe underlying diseases, duration of hospital stay, the increasingly invasive diagnostic procedures and more frequent use of antibiotics in ICU have been shown to contribute to the occurrence of Acinetobacter and especially A. baumannii [1, 22]. The highest number of isolates were recovered from tracheal aspirates, pus and urine samples, consistent with results from studies in several hospitals in India [17, 22] and Morocco [9]. These results were in contrast with those reported in two separate studies done in India [23, 24] which showed highest number of isolates were from tracheal aspirate followed by blood and pus respectively. The rate of isolation from different clinical samples is mostly influenced by the differences in the sample types, antibiotic usage, previous history of specific site colonization, infection control practices and a times the type of health facility.

 

Generally, A. baumannii exhibit resistance to multiple antibiotics. Third and fourth generation cephalosporins, carbapenems and fluoroquinolones are the most commonly used antibiotics in treating infections in hospitalized patients. In our study, a total of 502 (85%) Acinetobacter isolates, mostly A. baumannii were multidrug resistant. Multi-drug resistant (MDR) was defined as non-susceptibility to at least one agent in three or more antimicrobial classes. The high proportion of multidrug resistant A. baumannii have been reported in other studies globally with major impact reported in Asian countries including Malaysia, India, and Pakistan [25-27]. A. baumannii isolated showed high resistance to majority of the antibacterial agents tested and high susceptibility to amikacin (77%). Our findings on resistance to the commonly prescribed cephalosporins are consistent with results from several previous studies in other parts of the world showing high resistance to third and fourth generation cephalosporins, for instance a survey in tertiary hospitals in Colombia, Turkey, Romania, and Sudan reported resistance to cefotaxime, ceftazidime, and cefepime with proportions ranging from 84% to 98% [21, 22, 27, 28]. In contrast, similar studies in the Netherlands and India reported resistance rate of 16%-56% to ceftazidime and cefepime [29, 30]. The high resistance to Beta-lactam antibiotics in Acinetobacter species especially A. baumannii is most likely associated with the production of B-lactamases including TEM-1, TEM-2 and CARB-5, AR-1, ACE-1, 2, 3, 4 and the ESBL whose genes are either chromosomally or plasmid located. This may lead to alteration of penicillin-binding proteins and reduction in permeability to antimicrobials conferring some inherent resistance [1, 31]. On fluoroquinolones, we observed a high level of ciprofloxacin resistance (69-76%) in A. baumannii similar to findings of studies done in different referral hospitals in Turkey (90%), India (86%), Iran (80-82%) and Sudan (91%) [16, 21, 24, 32, 33]. This observation is contrary to what was initially reported in the same Hospital (KNH) in 2009 where they reported up to 100% susceptibility to ciprofloxacin [15]. The A. baumannii resistance to fluoroquinolones could be attributed to the structural modifications of the DNA gyrase subunits by gyrA and parC gene mutations. Additional explanation to this is the decreased uptake of the antimicrobials due to altered outer membrane (protein) leading to the early development of gyrA and parC resistance genes [1, 34] and the efflux systems that decrease intracellular drug accumulation [35].

 

Carbapenems for a long time have been the most potent drugs in the treatment of A. baumannii infection. In several parts of sub-Sahara Africa and other parts of the world, A. baumannii has been reported to exhibit resistance to carbapenems which is not the case with other Acinetobacter species. In our study, A. baumannii was resistant to meropenem (72%), compared to A. lwoffii and A. haemolyticus which recorded a high susceptibility of 100% and 75% respectively. Studies in other countries have however reported a slightly higher rate of resistance to meropenem (80-87%) in A. baumannii [28, 35, 36]. These findings are in contrast with several reports from previous studies where A. baumannii resistance to meropenem was remarkably lower (52-62%) than what we observed [17, 19, 37]. The high resistance to carbapenems and especially meropenem is attributed to prolonged empirical treatment duration with the drug. Further, resistance is also driven by production of carbapenemase enzymes categorically class B Metallo-beta-Lactamases (MBLs) and class D oxacillinases. Additional mechanisms involve efflux pump and impermeability associated mutations altering the porins expression [9, 28, 38]. Although aminoglycosides like amikacin and tobramycin retain activity against Acinetobacter species and especially A. baumannii, resistance to these drugs is emerging as demonstrated in this study where 23% of A. baumannii isolates exhibited resistance to amikacin. Similar findings have been reported in India [15] and Iran [31]. Previous studies have noted moderate (55%) to high resistance (78%) to amikacin [25, 35, 37, 38-40]. This study therefore highlights the occurrence of antibiotic resistant Acinetobacter species in a hospital setup considerably A. baumannii which showed high resistance to first line treatment regime of Acinetobacter associated infections. The major limitation in this study was the missing socio-demographics, clinical, and previous antibiotic use information which strongly underpins the importance of an integrated laboratory information management system in data capture. Another limitation is the fact that we were not able to confirm if all Acinetobacter isolates were causing infection or were just colonizers. This requires the correlation of laboratory results with the clinical presentation of the patient.

 

 

We report a high proportion of Acinetobacter isolates from samples obtained from critical care unit (48%) and tracheal aspirates (46%). Besides, A. baumannii was the most common species isolated and it demonstrated high susceptibility to amikacin (77%) and high resistance to commonly administered antibiotics such as cephalosporins, fluoroquinolones, penicillins, and meropenem. With the emergence and increase of MDR Acinetobacter, this study provides further evidence of the need for continuous surveillance of A. baumannii resistance patterns and enforcement of antibiotic stewardship programs in healthcare settings. There is need for further research on molecular mechanisms of resistance to monitor the epidemiology of MDR A. baumannii and combat antimicrobial resistance.

 

 

The authors declare no competing interests.

 

 

All the authors were involved in designing, data interpretation, and manuscript preparation. Victor Musyoki, Moses Masika and Gitau Wilfred also participated in data retrieval and data analysis. All the authors read and approved the final manuscript.

 

 

The authors would like to acknowledge all the staff, Department of Medical Microbiology of the University of Nairobi, Kenyatta National Hospital Microbiology Laboratory, the Research Coordinator and Head of Department, Department of Laboratory Medicine, Kenyatta National Hospital for their support during this study.

 

 

Table 1: distribution of Acinetobacter isolates by species

Table 2: antibiotic susceptibility profile of Acinetobacter isolates

Table 3: antibiotic resistance of Acinetobacter baumannii isolates by specimen type

Table 4: antibiotic resistance of Acinetobacter baumannii isolates by hospital unit

Figure 1: Acinetobacter species growing on blood agar

Figure 2: antimicrobial susceptibility pattern of clinical isolates of Acinetobacter baumannii

 

 

1. Bergogne-Bérézin E, Towner KJ. Acinetobacter spp as nosocomial pathogens: microbiological, clinical and epidemiological features. Clin Microbiol Rev. 1996; 9(2): 148-65. PubMed | Google Scholar


2. Chan JZ-M, Halachev MR, Loman NJ, Constantinidou C, Pallen MJ. Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol. 2012; 12: 302. PubMed | Google Scholar


3. Jain R, Danziger LH. Multidrug-resistant Acinetobacter infections: an emerging challenge to clinicians. Ann Pharmacother. 2004 Sep; 38(9): 1449-59. Epub 2004 Jul 27. PubMed | Google Scholar


4. Sohail M, Rashid A, Aslam B, Waseem M, Shahid M, Akram M et al. Antimicrobial susceptibility of Acinetobacter clinical isolates and emerging antibiogram trends for nosocomial infection management. Rev Soc Bras Med Trop. 2016 May-Jun; 49(3): 300-4. PubMed | Google Scholar


5. Begum S, Hasan F, Hussain S, Shah AA. Prevalence of multi drug resistant Acinetobacter baumannii in the clinical samples from tertiary care hospital in Islamabad, Pakistan. Pakistan J Med Sci. 2013 Sep; 29(5): 1253-8. PubMed | Google Scholar


6. Gandra S, Mojica N, Klein EY, Ashok A, Nerurkar V, Kumari M et al. Trends in antibiotic resistance among major bacterial pathogens isolated from blood cultures tested at a large private laboratory network in India, 2008-2014. Int J Infect Dis. 2016; 50: 75-82. Epub 2016 Aug 10. PubMed | Google Scholar


7. Joly-Guillou ML. Clinical impact and pathogenicity of Acinetobacter. Clin Microbiol Infect. 2005 Nov; 11(11): 868-73. PubMed | Google Scholar


8. Park KH, Shin JH, Lee SY, Kim SH, Jang MO, Kang SJ et al. The clinical characteristics, carbapenem resistance and outcome of Acinetobacter bacteremia according to genospecies. PLoS One. 2013 Jun 3; 8(6): e65026. PubMed | Google Scholar


9. Uwingabiye J, Frikh M, Lemnouer A, Bssaibis F, Belefquih B, Maleb A et al. Acinetobacter infections prevalence and frequency of the antibiotics resistance: a comparative study of intensive care units versus other hospital units. Pan Afr Med J. 2016 Apr 15; 23: 191. PubMed | Google Scholar


10. Almasaudi SB. Acinetobacter spp. As nosocomial pathogens: epidemiology and resistance features. Saudi J Biol Sci. 2018 Mar; 25(3): 586-596. Epub 2016 Feb 11. PubMed | Google Scholar


11. Lee K, Kim MN, Kim JS, Hong HL, Kang JO, Shin JH et al. Further increases in carbapenem-, amikacin-and fluoroquinolone-resistant isolates of Acinetobacter spp. and P. aeruginosa in Korea: KONSAR study 2009. Yonsei Med J. 2011 Sep; 52(5): 793-802. PubMed | Google Scholar


12. Gales AC, Jones RN, Forward KR, Liñares J, Sader HS, Verhoef J. Emerging importance of multidrug-resistant Acinetobacter species and stenotrophomonas maltophilia as pathogens in seriously Ill patients: geographic patterns, epidemiological features and trends in the SENTRY antimicrobial surveillance prog. Clin Infect Dis. 2001; 32 Suppl 2: S104-13. PubMed | Google Scholar


13. Chaudhary M, Payasi A. Molecular characterization and antimicrobial susceptibility study of Acinetobacter baumannii clinical isolates from middle east, African and Indian patients. J Proteomics Bioinforma. 2012; 5: 265-9.


14. Awad E, Osman I, El N, El M. High prevalence of multidrug-resistant Acinetobacter species in Khartoum Intensive Care Units (ICUs). Am J Res Commun. 2015; 3(2): 35-42.


15. Karimi PN, Bururia JM, Odhiambo PA, Bamugune BK, Museve GO. Enterobacteriaceae members are primary inhabitants of the lower gastrointestinal tract of man and animals. East Cent Africa J Pharm Sci. 2009; 12: 42-5.


16. Akalin H, Sinirta M, Ocakolu G, Yilmaz E, Heper Y, Kelebek N et al. Nosocomial Acinetobacter pneumonia: treatment and prognostic factors in 356 cases. Respirology. 2016 Feb; 21(2): 363-9. Epub 2015 Dec 3. PubMed | Google Scholar


17. Nath H, Barkataki D. Study of Acinetobacter isolates from clinical specimens in tertiary care hospital and their antimicrobial susceptibility pattern. Int J Curr Microbiol Applied Sci. 2016; 5(10): 842-8.


18. Bansal A, Singhal A, Sharma R et al. Antimicrobial susceptibility pattern and detection of metallobetalactamase production in Acinetobacter species isolated from clinical samples. Indian J Appl Res. 2016; 6: 6-9.


19. Ugochukwu V, Kingsley C, Iche E. Multidrug-resistant Acinetobacter infection and their antimicrobial susceptibility pattern in a Nigerian Tertiary Hospital ICU. Department of Medical Microbiology, Federal Medical Centre, Owerri, Imo State, Nigeria. Africa J Infect Dis. 2014; 8(1): 14-8. PubMed | Google Scholar


20. Fazeli H, Taraghian A, Kamali R, Poursina F, Nasr B. Molecular Identification and antimicrobial resistance profile of Acinetobacter baumannii isolated from nosocomial infections of a teaching Hospital in Isfahan, Iran. Avicenna J Clin Microb Infect. 2014; 1: 1-5.


21. Omer MI, Gumaa SA, Hassan AA, Idris KH, Ali OA, Mustafa M et al. Prevalence and resistance profile of Acinetobacter baumannii clinical isolates from a private hospital in Khartoum, Sudan. Am J Microbiol Res. 2015; 3: 76-9. Google Scholar


22. Maragakis LL, Perl TM. Antimicrobial resistance: Acinetobacter baumannii: epidemiology, antimicrobial resistance and treatment options. Clin Infect Dis. 2008 Apr 15; 46(8): 1254-63. PubMed | Google Scholar


23. Guckan R, Kilinc C, Capraz A, Yanik K. Antimicrobial susceptibility of Acinetobacter baumannii complex isolated from different clinical samples in a tertiary care hospital. J Antibiot Res. 2015; 1: 1-5. Google Scholar


24. Islahi S, Ahmad F, Khare V, Mishra N, Yaqoob S, Shukla P et al. Prevalence and resistance pattern of Acinetobacter species in hospitalized patients in a tertiary care centre. J Evol Med Dent Sci. 2014; 3(17): 4629-35. Google Scholar


25. Dash M, Padhi S, Pattnaik S, Mohanty I, Misra P. Frequency, risk factors and antibiogram of Acinetobacter species isolated from various clinical samples in a tertiary care hospital in Odisha, India. Avicenna J Med. 2013 Oct; 3(4): 97-102. PubMed


26. Nazmul MHM, Jamal H, Fazlul MKK. Acinetobacter species-associated infections and their antibiotic susceptibility profiles in Malaysia. Biomed Res. 2012; 23: 571-5. Google Scholar


27. Biglari S, Hanafiah A, Ramli R, Rahman MM, Nizam Khaithir TM. Clinico-epidemiological nature and antibiotic susceptibility profile of Acinetobacter species. Pakistan J Med Sci. 2013 Apr; 29(2): 469-73. PubMed | Google Scholar


28. Reguero MT, Medina OE, Hernández MA, Flórez DV, Valenzuela EM, Mantilla JR. Antibiotic resistance patterns of Acinetobacter calcoaceticus-A baumannii complex species from Colombian hospitals. Enferm Infecc Microbiol Clin. 2013 Mar; 31(3): 142-6. Epub 2012 Sep 26. PubMed | Google Scholar


29. Lazureanu V, Porosnicu M, Gândac C, Moisil T, Baditoiu L, Laza R et al. Infection with Acinetobacter baumannii in an intensive care unit in the Western part of Romania. BMC Infect Dis. 2016 Mar 8; 16 Suppl 1: 95. PubMed | Google Scholar


30. Broek PJ, Van Der Reijden TJK, Van Strijen E, Helmig-Schurter AV, Bernards AT, Dijkshoorn L. Endemic and epidemic Acinetobacter species in a university hospital: an 8-year survey. J Clin Microbiol. 2009 Nov; 47(11): 3593-9. Epub 2009 Sep 30. PubMed | Google Scholar


31. Mushtaq S, Javeid I, Hassan M. Antibiotic sensitivity pattern of Acinetobacter species isolated from clinical specimens in a tertiary care hospital. Biomed Res. 2013; 29: 23-6. Google Scholar


32. Ghasemian R, Ahanjan M, Fatehi E, Shokri M. Prevalence and antibiotic resistance pattern of Acinetobacter isolated from patients admitted in ICUs in Mazandaran, Northern Iran. Glob J Heal Sci. 2016; 8: 112-9. Google Scholar


33. Japoni S, Farshad S, Ali AA, Japoni A. Antibacterial susceptibility patterns and cross-resistance of Acinetobacter, isolated from hospitalized patients, Southern Iran. Iran Red Crescent Med J. 2011 Nov; 13(11): 832-6. Epub 2011 Nov 1. PubMed | Google Scholar


34. Rabirad N, Mohammadpoor M, Lari AR, Shojaie A, Bayat R. Antimicrobial susceptibility patterns of the gram-negative bacteria isolated from septicemia in Children's Medical Center, Tehran, Iran. J Prev Med Hyg Italy. 2014; 55(1): 23-6. PubMed | Google Scholar


35. Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. The global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother. 2007 Oct; 51(10): 3471-84. Epub 2007 Jul 23. PubMed | Google Scholar


36. Altun HU, Yagci S, Bulut C, Sahin H, Kinikli S, Adiloglu K et al. Antimicrobial susceptibilities of clinical Acinetobacter baumannii isolates with different genotypes. Jundishapur J Microbiol. 2014 Dec 7; 7(12): e13347. PubMed


37. Sanjeev H, Swathi N, Pai A, Rekha R, Vimal K, Ganesh HR. Systematic review of urinary tract infection caused by Acinetobacter species among hospitalized patients. Nitte Univ J Heal Sciences. 2013; 3: 7-9. Google Scholar


38. Hasan B, Perveen K, Olsen B, Zahra R. Emergence of carbapenem-resistant Acinetobacter baumannii in hospitals in Pakistan. J Med Microbiol. 2014 Jan; 63(Pt 1): 50-5. Epub 2013 Oct 1. PubMed | Google Scholar


39. Sadeghifard N, Ranjbar R, Zaeimi J, Alikhani MY, Ghafouryan S, Raftari M. Antimicrobial susceptibility, plasmid profiles, and RAPD-PCR typing of Acinetobacter bacteria. Asian Biomed. 2010; 4(6): 901-11. Google Scholar


40. Eldomany R, Abdelaziz NA. Characterization and antimicrobial susceptibility of gram-negative bacteria isolated from cancer patients on chemotherapy in Egypt. iMedPub Journals. 2011; 2(6): 1-13.