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Prevalence and antimicrobial susceptibility profile of multidrug-resistant bacteria among intensive care units patients at Ain Shams University Hospitals in Egypt—a retrospective study

Prevalence and antimicrobial susceptibility profile of multidrug-resistant bacteria among... Background: The nightmare of the rising numbers of multidrug-resistant organisms (MDROs) requires the implementation of effective stewardship programs. However, this should be preceeded by making available evidence-based knowledge regarding the local antimicrobial resistance pattern, which is fundamental. The aim of the current study is to determine the prevalence of MDRO among different Ain Shams University Hospitals (ASUHs) intensive care units (ICUs) and detect the resistance profile of the common pathogens. Results: The 1-year records of a total of 1280 pathogens were studied. The highest number of pathogens were isolated from blood cultures (44.84%), followed by urine (41.41%) then wound swabs (13.75%). Gram-negative isolates (57.5%) were more prevalent than gram-positive ones (31.1%). The most frequently isolated pathogens were Klebsiella spp. (22.5%), Escherichia coli (13.4%), and Coagulase-negative Staphylococci (12.5%). The highest percentage of resistance among gram-positive organisms was exhibited by penicillin (89.5%) followed by erythromycin (83.98%) and then cefoxitin (76.52%). None of the isolates showed resistance to linezolid and resistance to vancomycin was minimal (2.62%). Gram-negative isolates exhibited high overall resistance to all used antibiotic classes. The least frequency of resistance was recorded against nitrofurantoin (52.5%), amikacin (58.01%), followed by imipenem (59.78%) and meropenem (61.82%). All isolates of Pseudomonas and Acinetobacter showed 100% susceptibility to colistin. Conclusions: The prevalence of antibiotic resistance in Ain Shams University Hospitals (ASUHs) was high among both gram-negative and gram-positive organisms. This high resistance pattern foreshadows an inevitable catastrophe that requires continuous monitoring and implementation of effective antibiotic stewardship. Keywords: Multidrug resistance; Egypt, Prevalence, ICU, Susceptibility profile Correspondence: dr_nohaalaa@yahoo.com; dr_nohaalaa@med.asu.edu.eg Clinical Pathology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt © The Author(s). 2021 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://creativecommons.org/licenses/by/4.0/. Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 2 of 10 1 Background 2 Methods Antimicrobial resistance is rapidly becoming a global 2.1 Study design focus of attention, especially with the rising number of A record-based 1-year retrospective study—from March microorganisms resistant to available antimicrobials. It 2018 going through February 2019—was conducted at encompasses both the gram-positive and gram-negative ASUHs one of the largest tertiary hospitals in Egypt with bacteria, with global prevalence rates of 60% or more [1]. more than 3200-bed capacity. Multidrug-resistant organisms (MDROs) are described The records of the pathogenic organisms recovered as acquired non-sensitivity to one or more agents in at from different microbiological samples (blood, urine, least three groups of antimicrobials. This kind of resist- and wound) of ICU patients sent for routine diagnosis in ance essentially predominates in hospitals [2]. microbiology laboratory were retrieved from the micro- The lack of quick proper identification of pathogens biology laboratory information system at ASUHs and especially in patients with critical infection led to broad- reviewed. Information regarding the identified bacterial spectrum antibiotics overuse. As a result of this dilemma, isolate, specimen type, and antimicrobial susceptibility organisms became resistant to all available antimicrobial was collected and recorded. agents and susceptible only to older, likely more toxic anti- microbials, leaving less effective scanty alternatives [3, 4]. 2.2 Microbiological specimens processing and identification The Centers for Disease Control and Prevention (CDC) of isolated organisms declared that worldwide increasing infection rates with Sample processing and identification of the microorganism resistant pathogens strikingly endanger our healthcare were performed per the standard operating procedures of systems creating both negative universal economic effects our laboratory. All the used media were purchased from and a therapeutic challenge for clinicians hence delaying (Oxoid, UK). proper antibiotic therapy and increasing mortality rates [5]. The samples were cultured on the routinely used To combat this horrifying ascent in antimicrobial microbiological media and incubated for 24 h at 37 °C. resistance, the World Health Organization (WHO) If no growth, the plates were incubated for a total of 48 urges healthcare providers to adopt antimicrobial hours. stewardship to decrease the heavy cargo of antibiotic The isolated microorganisms' recognition was done resistance. However, before the implementation of according to colony morphology, Gram stain, and stand- any stewardship program, information on prevalent ard confirmatory biochemical tests were used. MDRO and their antimicrobial resistance profile are Gram-positive bacteria were identified via testing the required [6]. hemolytic activity on blood agar and further identification Data about the endemic antimicrobial resistance are using different biochemical tests as catalase reaction, slide generally difficult to find, particularly in countries and tube coagulase tests, culture on DNase agar, bile escu- where antibiotics are easily obtainable over the coun- lin, in addition to different differentiating antibiotic discs ter. Although numerous reports demonstrated the in- as optochin and bacitracin. For gram-negative bacteria, cidence and the patterns of resistance of many identification was conducted by biochemical tests such as pathogens, few studies about the endemic antimicro- oxidase, triple sugar iron, motility indole ornithine, citrate, bial resistance profile in developing countries were lysine iron arginine, and urease tests. They were further published [3, 7]. identified by Vitek2 system (Biomerieux, France). Hence, an evidence-based knowledge regarding the local antimicrobial resistance pattern is fundamental for guiding both antimicrobial treatment and empirical therapy 2.3 Antimicrobial susceptibility of specific pathogens [8]. This guide is also important for Antimicrobial susceptibilities of the bacterial isolates by effective antimicrobial stewardshipaswellasinthe design Kirby-Bauer disk diffusion method were performed and of local and universal research programs [3]. interpreted according to the Clinical Laboratory Standards Since the intensive care unit (ICU) patients are more Institute (CLSI) guidelines [9]. The tested antibiotic discs prone to nosocomial infections caused by aggressive path- were routinely supplied from Oxoid. Staphylococcus aur- ogens, therefore, the present study aimed to identify and eus ATCC 25923, Pseudomonas aeruginosa ATCC 27853, obtain a comprehensive idea about the current situation and Escherichia coli ATCC 25922 were used as controls in Ain Shams University Hospitals (ASUHs) regarding the for susceptibility testing. spectrum of microbes and the antimicrobial resistance Extended-spectrum beta-lactamase (ESBL) production pattern of the most prevalent pathogens isolated from was detected using the double-disc synergy test by pla- variable infection sites of ICU patients in addition to the cing amoxicillin/clavulanate disc adjacent to cefotaxime determination of the prevalence of multiple drug resist- and ceftazidime discs and looking for synergy between ance through a 1-year retrospective study. the clavulanic acid and the cephalosporin [10]. Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 3 of 10 Colistin resistance in both Acinetobacter spp. and information system of ASUH during the specified time Pseudomonas spp. was detected by Vitek2 system. period. The highest number of pathogens were isolated Methicillin resistance in Staphylococcus species both from blood cultures (44.84%, n = 574), followed by urine Staphylococcus aureus (MRSA) and coagulase-negative where (41.41%, n = 530) pathogens were recovered, while (MR-CONS) was detected using cefoxitin disc (30 μg). the least isolation rate was exhibited by wound swabs Vancomycin-resistant Enterococci (VRE) were initially (13.75%, n = 176). Gram-negative isolates (57.5%, n =736) screened for using agar dilution method on brain heart were more prevalent compared to gram-positive ones infusion agar (BHI) with 6 μg/ml vancomycin and further (31.1%, n = 399). The most frequently isolated pathogens confirmation for any suspected colonies was accomplished were Klebsiella spp. (22.5%, n =288), Escherichia coli by Vitek 2 system (Biomerieux, France). (E. coli)(13.4%, n = 172), and Coagulase-negative Staphylococci (CONS) (12.5%, n = 161), while Proteus, 2.4 Multiple drug resistance (MDR) non-hemolytic Streptococci, Enterobacter spp., and others MDR isolates were described by the CDC as acquired constituted the smallest group among the studied isolates non-sensitivity to one or more agents in at least three (Fig. 1). Bloodstream infections were caused mainly by groups of antimicrobials [11]. CONS (24.2%, n = 139/574) and Klebsiella spp. (23.8%, n = 137/574). Candida spp. (22.5%, n = 126/530), E. coli 2.5 Statistical analysis (20%, n = 106/530), and Klebsiella spp. (19%, n = 101/530) Data were presented as percentages and counts. Statistical were the main incriminated pathogens in urinary tract analysis was performed using the statistical package for infections. The frequently isolated pathogens from social sciences (SPSS) computer software (Version 25), wounds were Klebsiella spp. (28.4%, n = 50/176), Pseudo- IBM software, USA. Pearson chi-square test or Fisher’s monas spp. (17.6%, n = 31/176), and Acinetobacter spp. exact test—after checking the applicability conditions— (15.9%, n = 28/176). The distribution of pathogens were performed to identify the significant effect of each among the different types of specimens is summarized antibiotic on different isolates. A statistically significant in Table 1. difference was considered at p value ≤ 0.05. 3 Results 3.2 Antibiotic resistance pattern of isolates recovered 3.1 Spectrum of pathogens in different clinical specimens from various sites of infection The 1-year records of a total of 1280 pathogens from dif- The distribution of pathogens and their patterns of re- ferent clinical samples were retrieved from the laboratory sistance are presented in Table 2. Fig. 1 Distribution of different clinical isolates among patients admitted in ICU, March 2018–February 2019 Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 4 of 10 Table 1 Frequency of different pathogens within various clinical specimens collected from ICU patients, Ain Shams University Hospitals, Egypt, March 2018–February 2019 Name of organism Total N (%) Urine Blood Wound swab Klebsiella spp. 288 101 (35.06%) 137 (47.56%) 50 (17.38%) E.coli 172 106 (61.62%) 48 (27.91%) 18 (10.47%) Acinetobacter spp. 128 33 (25.78%) 67 (52.34%) 28 (21.88%) Pseudomonas spp. 114 49 (42.98%) 34 (29.82%) 31 (27.20%) Proteus spp. 23 5 (21.73%) 6 (26.10%) 12 (52.17%) Enterobacter spp. 11 2 8 1 (18.18%) (72.72%) (9.10%) Coagulase negative staphylococci (CONS) 161 20 (12.42%) 139 (86.33%) 2 (1.25%) Enterococcus spp. 151 74 (49.00%) 64 (42.38%) 13 (8.62%) Candida spp. 133 126 (94.73%) 6 (4.51%) 1 (%0.76) Staphylococcus aureus 69 5 (7.26%) 46 (66.66%) 18 (26.08%) Non-hemolytic Streptococci 18 6 (33.33%) 11 (61.11%) 1 (5.56%) Others 12 3 (25.00%) 8 (66.67%) 1 (8.33%) Total 1280 530 (41.41%) 574 (44.84%) 176 (13.75%) 3.2.1 Gram-positive isolates (6.62%). Data also revealed a statistically significant differ- The analysis of the antibiotic susceptibility profile of ence in the antimicrobial potentials to different isolates. different gram-positive organisms was conducted and The results of the antibiotic susceptibility profile of each of showed that the highest percentage of resistance was ex- the Gram-positive pathogens are summarized in Tables 2 hibited towards penicillin (89.5%) followed by erythro- and 4. mycin (83.98%) and then cefoxitin which is the representative of the different beta-lactams in Staphylo- 3.2.2 Gram-negative isolates coccus species (76.52%). On the other hand, linezolid dis- Table 3 shows that the least frequency of resistance was played no resistance (0%) and vancomycin resistance recorded against nitrofurantoin (52.5%), amikacin was minimal (2.62%) among gram-positive organisms. (58.01%), followed by imipenem (59.78%) and merope- With regards to the predominant resistance pheno- nem (61.82%). Colistin was the most promising types among different isolates, Staphylococcus aureus (S. antibiotic as all Acinetobacter and Pseudomonas isolates aureus) exhibited high resistance rates to many antibiotics showed 100% susceptibility to it. Data also revealed that where 97.1% of the isolates displayed resistance to penicil- some antimicrobials showed a statistically significant lin, and 73.91% were resistant to gentamicin and all beta- difference in their antimicrobial activities to different lactams. On the other hand, S. aureus isolates exhibited a bacterial isolates. suscepibility of more than 40% to the rest of antibiotics Table 3 also shows that among the obtained gram- with 100% susceptibility to linezolid, nitrofurantoin, and negative pathogens, Klebsiella was the one that dis- vancomycin where no vancomycin-intermediate S. aureus played the highest level of multidrug-resistance (VISA) or vancomycin-resistant S. aureus (VRSA) were (87.84%) followed by Acinetobacter (83.59%). E. coli found in this study. and Pseudomonas spp. showed almost identical levels Similarly, CONS showed comparable beta-lactam of multidrug-resistance (73.68%, 72.02%) respectively. resistance rates to S. aureus with a slightly higher level Although 70% or more of the E. coli isolates pos- of methicillin resistance (77.6%), as well as, 100% suscep- sessed resistance against the majority of the available tibility to linezolid and vancomycin. However, CONS antibiotic options, a few agents as amikacin, genta- displayed a higher level of resistance to the majority of micin, imipenem, meropenem, and nitrofurantoin the rest of the antibiotics. showed potential antimicrobial activity with percent- Enterococci expressed a high level of resistance to both age of resistance of (12.21%, 38.37%, 18.60%, 19.76%, beta-lactams and quinolones, ciprofloxacin (86.75%), 30.18%), respectively. levofloxacin (76.15%), penicillin (78.14%), and ampicillin Both Proteus and Enterobacter spp. isolates showed the (64.9%). In a similar pattern to Staphylococci, no linezo- least antibiotic resistance among gram-negative pathogens. lid resistance was detected and vancomycin-resistant In Enterobacter isolates, the highest level of resistance was Enterococci (VRE) were discovered in ten isolates recorded against cephalosporins, piperacillin/tazobactam, Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 5 of 10 Table 2 Distribution of pathogens associated with intensive care unit-associated infections and their antimicrobial resistance patterns, Ain Shams University Hospitals, Egypt, March 2018–February 2019 Pathogen type and pattern of resistance n Resistance, n (%) Klebsiella spp. 288 ESBL production 30 (10.4) Multidrug resistance 253 (87.84) Acinetobacter spp. 128 Multidrug resistance 107 (83.59) Pseudomonas spp. 114 Multidrug resistance 84 (73.68) Escherichia coli 172 ESBL production 80 (46.5) Multidrug resistance 124 (72.02) Proteus spp. 23 ESBL production 4 (17.4) Enterobacter spp. 11 ESBL production 4 (36.36) Staphylococcus aureus 69 MRSA 51 (73.9) Coagulase-negative staphylococci 161 MR-CONS 125 (77.6) Enterococcus spp. 151 VRE* 10 (6.6) Candida spp. 133 Non-hemolytic streptococci 18 Others 12 Total 1280 ESBL extended-spectrum β-lactamase, MRSA methicillin-resistant S aureus, VRE vancomycin-resistant Enterococcus *Vancomycin resistance was confirmed by Vitek 2C doxycycline, and tobramycin in contrast to the rest of anti- problem. The few available studies concerning ICUs microbials which still had considerable activity against suggest that they are hotbeds of emerging high-level Enterobacter. Proteus isolates had the maximum resistance resistance. Hence, additional studies in other countries levels observed towards ampicillin/sulbactam (60.08%), and healthcare settings are encouraged [14]. doxycycline (82.60%), levofloxacin (60.86%), tetracycline In this study, gram-negative isolates (57.5%, n = 736) (73.91%), and trimethoprim/sulfamethoxazole (69.56%). were more prevalent compared to gram-positive ones Fortunately, the rest of the antibiotics still had a favorable (31.1%, n = 399). Comparable results were found by potential against Proteus. Halim et al. [15] where gram-negative bacteria took the upper hand among all nosocomial pathogens (53%) 4 Discussion while gram-positive organisms represented 37.9%. Simi- The excessive use of antibiotics has led to a vast wide- larly, gram-negative organisms constituted 65.7% of spread prevalence of antimicrobial resistance. As time cases in a study conducted by Sawhney and col- passes, bacterial pathogens will defy every antibacterial op- leagues [16]. tion, thus, becoming extremely hard to control. Hence, Most of the isolates were recovered from blood the WHO identified it as an international health prime cultures (44.84%) followed by urine (41.41%), unlike the concern [12, 13]. results of Shebl and Mosaad who reported higher To control this mounting predicament, comprehensive recovery from urine specimens in comparison with antibiotic stewardship in poor countries is fundamental. blood cultures [3]. However, enough data regarding antimicrobial resistance Among gram-negative organisms, Klebsiella, repre- are unavailable to precisely measure the extent of the sented the majority (22.5%) followed by E. coli (13.4%). Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 6 of 10 Table 3 Antibiotic resistance pattern of the prevalent gram-negative pathogens isolated from patients admitted in ICU, Ain Shams University Hospitals, Egypt, March 2018-February 2019 Antibiotic Resistant isolates, n (%) Total , p value n/N(%) Acinetobacter Klebsiella E.coli spp. Pseudomonas Proteus Enterobacter (N = 736) spp. spp (n = 172) spp. spp. spp. (n = 128) (n = 288) (n = 114 (n = 23 (n = 11) Amikacin 113 (88.28) 208 (72.22) 21 (12.21) 76 (66.66) 6 (26.08) 3 (27.27) 427/736 p < 0.001* (58.01) Amoxicillin/clavulanate **NA 245 (85.06) 124 (72.09) **NA 12 (52.17) 3 (27.27) 384/494 p < 0.001* (77.73) Ampicillin/sulbactam 110 (85.93) 277 (96.18) 155 (90.11) **NA 14 (60.08) 4(36.36) 560/622 p < 0.001* (90.03) Cefepime 110 (85.93) 276 (96.83) 157 (91.27) 91 (79.82) 7 (30.43) 8 (72.72) 649/736 p < 0.001* (88.17) Cefotaxime 124 (96.87) 285 (98.95) 152 (88.37) **NA 12 (52.17) 10 (90.90) 583/622 p < 0.001* (93.72) Cefoxitin **NA 248 (86.11) 92 (53.48) **NA 7 (30.43) 10 (90.90) 357/494 p < 0.001* (72.26) Cefpodoxime **NA 282 (97.91) 160 (93.02) **NA 10 (43.47) 9 (81.81) 461/494 p < 0.001* (93.31) Ceftazidime 115 (89.84) 279 (96.87) 156 (90.69) 92 (80.70) 8 (34.78) 10 (90.90) 660/736 p < 0.001* (89.67) Ceftriaxone 127 (99.21) 285 (98.95) 152 (88.37) **NA 12 (52.17) 10 (90.90) 586/622 p < 0.001* (94.21) Ciprofloxacin 111 (86.71) 258 (89.58) 122 (70.93) 91 (79.82) 13 (56.52) 6 (54.54) 601/736 p < 0.001* (81.65) Doxycycline 85 (66.41) 235 (81.59) 123 (71.51) **NA 19 (82.60) 9 (81.81) 471/622 0.008* (75.72) Gentamicin 97 (75.78) 204 (70.83) 66 (38.37) 81 (71.05) 10 (43.47) 5 (45.45) 463/736 p < 0.001* (62.90) Imipenem 101 (78.91) 225 (78.12) 32 (18.60) 75 (65.78) 4 (17.39) 3 (27.27) 440/736 p < 0.001* (59.78) Levofloxacin 109 (85.15) 231 (80.21) 119 (69.18) 87 (76.31) 14 (60.86) 5 (45.45) 565/736 0.001* (76.76) Meropenem 103 (80.46) 228 (79.16) 34 (19.76) 81 (71.05) 4 (17.39) 5 (45.45) 455/736 p < 0.001* (61.82) Piperacillin/ 107 (83.59) 250 (86.81) 95 (55.23) 80 (70.17) 5 (21.73) 10 (90.90) 547/736 p < 0.001* tazobactam (74.32) Tetracycline 114 (89.06) 240 (83.33) 130 (75.58) **NA 17 (73.91) 3 (27.27) 504/622 p < 0.001* (81.02) Tobramycin 90 (70.31) 234 (81.25) 106 (61.62) 92 (80.70) 6 (26.08) 7 (63.63) 535/736 p < 0.001* (72.69) Trimethoprim/ 87 (67.96) 241 (83.68) 137 (79.65) **NA 16 (69.56) 3 (27.27) 484/622 p < 0.001* sulfamethoxazole (77.81) Colistin 0 **NA **NA 0 **NA **NA **NA – (0) (0) Nitrofurantoin NA 77 (76.23) 32 (30.18) **NA **NA 0 (0) 109/209 p < 0.001* (52.15) No of urine samples 33 101 106 49 5 2 296 **NA = not applicable * significant at p<0.05 On the other hand, CONS (12.5%) was the most com- 17] as well as from countries other than Egypt. Osifo, and mon gram-positive pathogen. Aghahowa from Nigeria reported that E. coli and Klebsi- These results were similar to the results reported by ella pneumoniae were the most frequently isolated patho- other researchers studying bacterial strains in Egypt [15, gens [18]. However, others reported a higher level of E. Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 7 of 10 Table 4 Antibiotic resistance pattern of the prevalent Gram-positive pathogens isolated from patients admitted in ICU, Ain Shams University Hospitals, Egypt, March 2018-February 2019 Antibiotic Resistant isolates, n (%) Total , p value n/N(%) Staphylococcus aureus Coagulase-negative Enterococcus spp. (N = 381) (n = 69) staphylococci (n = 151) (n = 161) Amikacin 34 61 **NA 95/230 0.108 (49.29) (37.88) (41.30) Ampicillin NA NA 98 321/381 – ***67 ***156 (64.90) (84.25) Cefoxitin 51 125 **NA 176/230 0.541 (73.91) (77.63) (76.52) Penicillin 67 156 118 341/381 p < 0.001* (97.10) (96.89) (78.14) (89.50) Clindamycin 36 97 **NA 133/230 0.256 (52.17) (60.2) (57.82) Erythromycin 43 130 147 320/381 p < 0.001* (62.31) (80.74) (62.31) (83.98) Ciprofloxacin 36 107 131 274/381 p < 0.00*1 (52.17) (66.45) (86.75) (71.91) Doxycycline 29 70 38 137/381 0.002* (42.02) (43.47) (25.16) (35.95) Gentamicin (low dose) 51 98 **NA 149/230 0.058 (73.91) (51.30) (64.78) Gentamicin (high dose) **NA **NA 95 95/151 – (62.91) (62.91) Linezolid 0 0 0 0/381 – (0) (0) (0) (0) Levofloxacin 33 97 115 245/381 0.001* (47.82) (60.24) (76.15) (64.30) Teicoplanin 6 25 26 57/381 0.250 (8.69) (15.52) (17.21) (14.96) Tetracycline 38 76 53 167/381 0.011* (55.07) (47.20) (35.09) (43.83) Tobramycin 40 117 **NA 157/230 0.028* (57.97) (72.67) (68.26 Trimethoprim/sulfamethoxazole 10 100 **NA 110/230 p < 0.001* (14.49) (62.11) (47.82) Nitrofurantoin 0 4 38 42/99 0.021* (0) (20.00) (28.12) (42.42) Vancomycin 0 0 10 10/381 – (0) (0) (6.62) (2.62) No. of urine samples 5 20 74 99 ***The resistance for ampicillin was deduced from cefoxitin **NA = not applicable * significant at p<0.05 coli than Klebsiella spp. [3, 19]and S. aureus was much blood cultures. Man et al. from Romania also stated that higher than CONS unlike our study [3]. The high preva- CONS were the most commonly isolated pathogens from lence of CONS was justified by Basiri and coworkers, who blood culture in their study; however, E. coli came before stated that it could be the overuse of invasive devices with Klebsiella spp. as a cause of bacteremia [21]. repeated manipulation by healthcare workers and inad- In this study, E. coli and Klebsiella spp. were the main equate infection control measures [20]. pathogens recovered from urine. Similarly, Duffa et al. [22] As regards the distribution of pathogens among the dif- reported that E. coli and Klebsiella spp. were highly en- ferent clinical specimens in the present work, CONS and countered pathogens in urine. As for the predominating Klebsiella spp. were the most frequently isolated from pathogens in wound specimens, Klebsiella, Pseudomonas, Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 8 of 10 and Acinetobacter spp. were highly recovered organisms in attributed to their massive use for the treatment of the current research. Ibrahim [23]fromSaudi Arabia no- enterococcal infections [31, 32]. ticed that most the common wound pathogens were Pro- In the present study, gram-negative isolates exhibited teus mirabilis followed by Klebsiella pneumoniae. However, high resistance to almost all the used antibiotic classes in a research by Magdy and colleagues [24], S. aureus was with the least frequency recorded against nitrofurantoin the most common followed by Pseudomonas aeruginosa, (52.5%), amikacin (58.01%), followed by imipenem Klebsiella pneumoniae,and E. coli. (59.78%) and meropenem (61.82%). All isolates of The difference between the current study and other Pseudomonas and Acinetobacter showed 100% suscepti- studies regarding type and frequency of pathogens could bility to colistin so it can be considered a good thera- be linked to several factors like environmental condi- peutic option [11]. These findings coincide well—with tions, health practices, patient conditions, personal hy- very few exceptions—with those of Eldomany and Abde- giene, number of patients involved in each study, and laziz [33] from Egypt who reported high antibiotic resist- laboratory procedures [3]. ance against their tested isolates of Acinetobacter, The highest percentage of resistance among gram- Pseudomonas, Klebsiella, Enterobacter, and E. coli from positive organisms was exhibited towards penicillin cancer patients. (89.5%) followed by erythromycin (83.98%) and cefoxi- It is worthy to point to the fact that the high level of tin (76.52%). Resistance to vancomycin was minimal resistance observed among the gram-negative organisms (2.62%) among gram-positive organisms while no re- in the current study agrees well with the results reported sistance was noted against linezolid (0%). Hove et al. by other researchers [33–35]. Such elevated resistance in [25] reported that the highest rates of resistance were Enterobacteriaceae may be attributed to β-lactamase observed against penicillin (90.0%) and oxacillin activity [36]. (64.0%). The overall resistance towards penicillin and Generally, the resistance patterns of Acinetobacter and cefoxitin among staphylococcal isolates of Magdy and Proteus in the current research were in concordance with colleagues [24] from Egypt was in agreement with the Ibrahim [23], although E. coli isolates in Ibrahim’sstudy present study. However, their S. aureus isolates dis- displayed similar results as regards amikacin, gentamycin, played higher resistance opposite to the current study imipenem, and piperacillin/tazobactam but with much where CONS was the species with higher resistance. lower resistance for the rest of antibiotics. Regarding Moreover, their results were much higher as regards Pseudomonas and Klebsiella, both showed lower resist- vancomycin resistance which displayed resistance ance rates in contrast to the present study [23]. Several rates of 32.4% and 41.2% by S. aureus isolates and causes can be responsible for the increased incidence of CONS respectively [24]. Results of Shebl and Mosaad drug-resistance detected in the present study. The prime [3] from Egypt were in contrast to the current study reason may be the common practice in Egypt where al- as regards vancomycin and linezolid with a resistance most all patients—before hospital admission—take diverse of 10.8% and 11.3%, respectively. However, the results of antibiotics either prescribed by doctors or self-medication other researchers regarding vancomycin and linezolid due to over-the-counter antibiotics administered mostly were in favor to that obtained in the present study where in an improper dose and for an inadequate period [37, Al-Zoubi and his colleagues reported that all their S. aur- 38]. Other potential causes are the geographical diver- eus isolates were 100% susceptible to vancomycin [26]. gence as well as the genetic variations among pathogens Also, Basak et al. [11] and Mahmoud et al. [27]reported from different studies. But unfortunately, data about the 100% susceptibility to both vancomycin and linezolid. The molecular characterization of the strains included in the higher antibiotic resistance rates reported by the above- current study are not available. mentioned researches in comparison to the current results It is obvious that the obtained results in the current might be attributable to inconvenient use of antimicro- study reflected the high prevalence of multidrug resistance bials, geographic and socioeconomic variations, sampling especially among gram-negative pathogens. Klebsiella dis- biases, and dissimilar patients’ characteristics [28]. played the highest degree of multidrug-resistance (87.84%) As regards Enterococci, the overall resistance pat- followed by Acinetobacter (83.59%). E. coli and Pseudo- tern was comparable to that reported by Said and monas spp. showed almost identical levels of multidrug- Abdelmegeed [29] with the exception of the higher resistance (73.68%, 72.02%) respectively, while Proteus and linezolid resistance reported (9.7%) in their study. Enterobacter spp. isolates exhibited the lowest resistance Likewise, the resistance pattern of ciprofloxacin, among all the gram-negative pathogens. erythromycin, gentamicin, and linezolid agrees with There is a tremendous increase in MDR gram-negative that reported by Zalipour and coworkers [30]. In- bacteria in hospitals and especially in the intensive care creased resistance to macrolides and quinolones units (ICU). Such resistance is most notable in ICUs due among enterococcal clinical isolates might be to the unrestrained usage of antibiotics in ICU in Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 9 of 10 comparison to other hospital departments and most of Received: 7 April 2020 Accepted: 17 December 2020 these infections were caused by gram-negative bacilli [39]. References It is important to note that the data presented in this 1. 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The challenge of antibiotic resistance. Sci Am. 1998;278(3):46–53. Acknowledgements 14. Bebell LM, Muiru AN. Antibiotic use and emerging resistance: how can None. resource-limited countries turn the tide? Glob Heart. 2014;9(3):347–58. 15. Halim MMA, Eyada IK, Tongun RM. Prevalence of multidrug drug resistant Author’s contributions organisms and hand hygiene compliance in surgical NICU in Cairo All of the work in this paper was done by Noha Alaa Eldin Fahim. The author University Specialized Pediatric Hospital. Egypt Pediatr Assoc Gaz. 2018;66(4): read and approved the final manuscript. 103–11. 16. Sawhney N, Shinu P, Singh VA. Bacteriological profile and antibiotic susceptibility pattern of neonatal septicaemia in a tertiary care hospital. Int J Funding Curr Microbiol App Sci. 2015;4(10):977–84. This research did not receive any specific grant from funding agencies in the 17. Khalifa HO, Soliman AM, Ahmed AM, Shimamoto T, Nariya H, Matsumoto T, public, commercial, or not-for-profit sectors. et al. High prevalence of antimicrobial resistance in gram-negative bacteria isolated from clinical settings in Egypt: recalling for judicious use of Availability of data and materials conventional antimicrobials in developing nations. Microb Drug Resist. 2019; All data generated or analyzed during this study are included in this 25(3):371–85. published article. 18. Osifo OD, Aghahowa SE. Audit of antibiotic therapy in surgical neonates in a tertiary hospital in Benin City. Nigeria Afr J Paediatr Surg. 2011;8(1):23–8. Ethics approval and consent to participate 19. Beyene D, Bitew A, Fantew S, Mihret A, Evans M. Multidrug-resistant profile This manuscript does not report on or involve the use of any animal or and prevalence of extended spectrum β-lactamase and carbapenemase human data or tissue. 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Acta Not applicable. Medica Marisiensis. 2014;60:89–93. 22. Merga Duffa Y, Terfa Kitila K, Mamuye Gebretsadik D, Bitew A. Prevalence Competing interests and antimicrobial susceptibility of bacterial uropathogens isolated from The author declares no competing interests. pediatric patients at Yekatit 12 Hospital Medical College. Addis Ababa Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 10 of 10 Ethiopia Int J Microbiol. 2018;2018:8492309. https://doi.org/10.1155/2018/ 23. Ibrahim ME. High antimicrobial resistant rates among gram-negative pathogens in intensive care units: a retrospective study at a tertiary care hospital in Southwest Saudi Arabia. Saudi Med J. 2018;39(10): 1035–43. 24. Bahgat MM, Elbialy AA, Zaky MM, Toubar SE. Prevalence of antibiotic resistant aerobic bacteria isolated from surgical wounds of inpatients at Zagazig University Hospitals. Egypt Int J Curr Microbiol App Sci. 2015;4(12): 460–72. 25. 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Emergence of multidrug resistance and extensive drug resistance among enterococcal clinical isolates in Egypt. Infect Drug Resist. 2019;7(12):1113–25. 30. Zalipour M, Esfahani BN, Havaei SA. Phenotypic and genotypic characterization of glycopeptide, aminoglycoside and macrolide resistance among clinical isolates of Enterococcus faecalis: a multicenter based study. BMC Res Notes. 2019;12(1):292. 31. Marosevic D, Kaevska M, Jaglic Z. Resistance to the tetracyclines and macrolide-lincosamide-streptogramin group of antibiotics and its genetic linkage- a review. Ann Agric Environ Med. 2017;24(2):338–44. https://doi. org/10.26444/aaem/74718. 32. Banerjee T, Anupurba S. Risk factors associated with fluoroquinolone- resistant enterococcal urinary tract infections in a tertiary care university hospital in North India. Indian J Med Res. 2016;144(4):604–10. https://doi. org/10.4103/0971-5916.200897. 33. Eldomany R, Abdelaziz N. Characterization and antimicrobial susceptibility of gram-negative bacteria isolated from cancer patients on chemotherapy in Egypt. Arch Clin Microbiol. 2011;2(6):2. 34. Zinner HS. New pathogens in neutropenic patients with cancer: an update for the new millennium. Int J Antimicrob Agents. 2000;16(2):97–101. 35. O’Neill E, Humphreys H, Phillips J, Smyth EG. Third generation cephalosporin resistance among gram-negative bacilli causing meningitis in neurosurgical patients: significant challenges in ensuring effective antibiotic therapy. J Antimicrob Chemother. 2006;57:356–9. 36. Wenzel PR, Sahm FD, Thornsberry C, Draghi DC, Jones EM, Karlowsky JA. In vitro susceptibilities of gram-negative bacteria isolated from hospitalized patients in four European countries, Canada, and the United States in 2000– 2001 to expanded-spectrum cephalosporins and comparator antimicrobials: implications for therapy. Antimicrob Agents Chemother. 2003;47:3089–98. 37. Elden NMK, Nasser HA, Alli A, Mahmoud N, Shawky MA, Ibrahim AAEA, et al. Risk factors of antibiotics self-medication practices among university students in Cairo, Egypt. Open Access Maced J Med Sci. 2020;5;8(E SE-Public Health Education and Training):7–12. 38. Ghazawy ER, Hassan EE, Mohamed ES, Emam SA. Self-medication among adults in Minia, Egypt: a cross sectional community-based study. Health. 2017;9:883–95. 39. Azim N, Al-Harbi M, Al-Zaban M, Nofal M, Somily A. Prevalence and antibiotic susceptibility among gram negative bacteria isolated from intensive care units at a tertiary care hospital in Riyadh. Saudi Arabia J Pure Appl Microbiol. 2019;13:201–8. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of the Egyptian Public Health Association Springer Journals

Prevalence and antimicrobial susceptibility profile of multidrug-resistant bacteria among intensive care units patients at Ain Shams University Hospitals in Egypt—a retrospective study

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Abstract

Background: The nightmare of the rising numbers of multidrug-resistant organisms (MDROs) requires the implementation of effective stewardship programs. However, this should be preceeded by making available evidence-based knowledge regarding the local antimicrobial resistance pattern, which is fundamental. The aim of the current study is to determine the prevalence of MDRO among different Ain Shams University Hospitals (ASUHs) intensive care units (ICUs) and detect the resistance profile of the common pathogens. Results: The 1-year records of a total of 1280 pathogens were studied. The highest number of pathogens were isolated from blood cultures (44.84%), followed by urine (41.41%) then wound swabs (13.75%). Gram-negative isolates (57.5%) were more prevalent than gram-positive ones (31.1%). The most frequently isolated pathogens were Klebsiella spp. (22.5%), Escherichia coli (13.4%), and Coagulase-negative Staphylococci (12.5%). The highest percentage of resistance among gram-positive organisms was exhibited by penicillin (89.5%) followed by erythromycin (83.98%) and then cefoxitin (76.52%). None of the isolates showed resistance to linezolid and resistance to vancomycin was minimal (2.62%). Gram-negative isolates exhibited high overall resistance to all used antibiotic classes. The least frequency of resistance was recorded against nitrofurantoin (52.5%), amikacin (58.01%), followed by imipenem (59.78%) and meropenem (61.82%). All isolates of Pseudomonas and Acinetobacter showed 100% susceptibility to colistin. Conclusions: The prevalence of antibiotic resistance in Ain Shams University Hospitals (ASUHs) was high among both gram-negative and gram-positive organisms. This high resistance pattern foreshadows an inevitable catastrophe that requires continuous monitoring and implementation of effective antibiotic stewardship. Keywords: Multidrug resistance; Egypt, Prevalence, ICU, Susceptibility profile Correspondence: dr_nohaalaa@yahoo.com; dr_nohaalaa@med.asu.edu.eg Clinical Pathology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt © The Author(s). 2021 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://creativecommons.org/licenses/by/4.0/. Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 2 of 10 1 Background 2 Methods Antimicrobial resistance is rapidly becoming a global 2.1 Study design focus of attention, especially with the rising number of A record-based 1-year retrospective study—from March microorganisms resistant to available antimicrobials. It 2018 going through February 2019—was conducted at encompasses both the gram-positive and gram-negative ASUHs one of the largest tertiary hospitals in Egypt with bacteria, with global prevalence rates of 60% or more [1]. more than 3200-bed capacity. Multidrug-resistant organisms (MDROs) are described The records of the pathogenic organisms recovered as acquired non-sensitivity to one or more agents in at from different microbiological samples (blood, urine, least three groups of antimicrobials. This kind of resist- and wound) of ICU patients sent for routine diagnosis in ance essentially predominates in hospitals [2]. microbiology laboratory were retrieved from the micro- The lack of quick proper identification of pathogens biology laboratory information system at ASUHs and especially in patients with critical infection led to broad- reviewed. Information regarding the identified bacterial spectrum antibiotics overuse. As a result of this dilemma, isolate, specimen type, and antimicrobial susceptibility organisms became resistant to all available antimicrobial was collected and recorded. agents and susceptible only to older, likely more toxic anti- microbials, leaving less effective scanty alternatives [3, 4]. 2.2 Microbiological specimens processing and identification The Centers for Disease Control and Prevention (CDC) of isolated organisms declared that worldwide increasing infection rates with Sample processing and identification of the microorganism resistant pathogens strikingly endanger our healthcare were performed per the standard operating procedures of systems creating both negative universal economic effects our laboratory. All the used media were purchased from and a therapeutic challenge for clinicians hence delaying (Oxoid, UK). proper antibiotic therapy and increasing mortality rates [5]. The samples were cultured on the routinely used To combat this horrifying ascent in antimicrobial microbiological media and incubated for 24 h at 37 °C. resistance, the World Health Organization (WHO) If no growth, the plates were incubated for a total of 48 urges healthcare providers to adopt antimicrobial hours. stewardship to decrease the heavy cargo of antibiotic The isolated microorganisms' recognition was done resistance. However, before the implementation of according to colony morphology, Gram stain, and stand- any stewardship program, information on prevalent ard confirmatory biochemical tests were used. MDRO and their antimicrobial resistance profile are Gram-positive bacteria were identified via testing the required [6]. hemolytic activity on blood agar and further identification Data about the endemic antimicrobial resistance are using different biochemical tests as catalase reaction, slide generally difficult to find, particularly in countries and tube coagulase tests, culture on DNase agar, bile escu- where antibiotics are easily obtainable over the coun- lin, in addition to different differentiating antibiotic discs ter. Although numerous reports demonstrated the in- as optochin and bacitracin. For gram-negative bacteria, cidence and the patterns of resistance of many identification was conducted by biochemical tests such as pathogens, few studies about the endemic antimicro- oxidase, triple sugar iron, motility indole ornithine, citrate, bial resistance profile in developing countries were lysine iron arginine, and urease tests. They were further published [3, 7]. identified by Vitek2 system (Biomerieux, France). Hence, an evidence-based knowledge regarding the local antimicrobial resistance pattern is fundamental for guiding both antimicrobial treatment and empirical therapy 2.3 Antimicrobial susceptibility of specific pathogens [8]. This guide is also important for Antimicrobial susceptibilities of the bacterial isolates by effective antimicrobial stewardshipaswellasinthe design Kirby-Bauer disk diffusion method were performed and of local and universal research programs [3]. interpreted according to the Clinical Laboratory Standards Since the intensive care unit (ICU) patients are more Institute (CLSI) guidelines [9]. The tested antibiotic discs prone to nosocomial infections caused by aggressive path- were routinely supplied from Oxoid. Staphylococcus aur- ogens, therefore, the present study aimed to identify and eus ATCC 25923, Pseudomonas aeruginosa ATCC 27853, obtain a comprehensive idea about the current situation and Escherichia coli ATCC 25922 were used as controls in Ain Shams University Hospitals (ASUHs) regarding the for susceptibility testing. spectrum of microbes and the antimicrobial resistance Extended-spectrum beta-lactamase (ESBL) production pattern of the most prevalent pathogens isolated from was detected using the double-disc synergy test by pla- variable infection sites of ICU patients in addition to the cing amoxicillin/clavulanate disc adjacent to cefotaxime determination of the prevalence of multiple drug resist- and ceftazidime discs and looking for synergy between ance through a 1-year retrospective study. the clavulanic acid and the cephalosporin [10]. Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 3 of 10 Colistin resistance in both Acinetobacter spp. and information system of ASUH during the specified time Pseudomonas spp. was detected by Vitek2 system. period. The highest number of pathogens were isolated Methicillin resistance in Staphylococcus species both from blood cultures (44.84%, n = 574), followed by urine Staphylococcus aureus (MRSA) and coagulase-negative where (41.41%, n = 530) pathogens were recovered, while (MR-CONS) was detected using cefoxitin disc (30 μg). the least isolation rate was exhibited by wound swabs Vancomycin-resistant Enterococci (VRE) were initially (13.75%, n = 176). Gram-negative isolates (57.5%, n =736) screened for using agar dilution method on brain heart were more prevalent compared to gram-positive ones infusion agar (BHI) with 6 μg/ml vancomycin and further (31.1%, n = 399). The most frequently isolated pathogens confirmation for any suspected colonies was accomplished were Klebsiella spp. (22.5%, n =288), Escherichia coli by Vitek 2 system (Biomerieux, France). (E. coli)(13.4%, n = 172), and Coagulase-negative Staphylococci (CONS) (12.5%, n = 161), while Proteus, 2.4 Multiple drug resistance (MDR) non-hemolytic Streptococci, Enterobacter spp., and others MDR isolates were described by the CDC as acquired constituted the smallest group among the studied isolates non-sensitivity to one or more agents in at least three (Fig. 1). Bloodstream infections were caused mainly by groups of antimicrobials [11]. CONS (24.2%, n = 139/574) and Klebsiella spp. (23.8%, n = 137/574). Candida spp. (22.5%, n = 126/530), E. coli 2.5 Statistical analysis (20%, n = 106/530), and Klebsiella spp. (19%, n = 101/530) Data were presented as percentages and counts. Statistical were the main incriminated pathogens in urinary tract analysis was performed using the statistical package for infections. The frequently isolated pathogens from social sciences (SPSS) computer software (Version 25), wounds were Klebsiella spp. (28.4%, n = 50/176), Pseudo- IBM software, USA. Pearson chi-square test or Fisher’s monas spp. (17.6%, n = 31/176), and Acinetobacter spp. exact test—after checking the applicability conditions— (15.9%, n = 28/176). The distribution of pathogens were performed to identify the significant effect of each among the different types of specimens is summarized antibiotic on different isolates. A statistically significant in Table 1. difference was considered at p value ≤ 0.05. 3 Results 3.2 Antibiotic resistance pattern of isolates recovered 3.1 Spectrum of pathogens in different clinical specimens from various sites of infection The 1-year records of a total of 1280 pathogens from dif- The distribution of pathogens and their patterns of re- ferent clinical samples were retrieved from the laboratory sistance are presented in Table 2. Fig. 1 Distribution of different clinical isolates among patients admitted in ICU, March 2018–February 2019 Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 4 of 10 Table 1 Frequency of different pathogens within various clinical specimens collected from ICU patients, Ain Shams University Hospitals, Egypt, March 2018–February 2019 Name of organism Total N (%) Urine Blood Wound swab Klebsiella spp. 288 101 (35.06%) 137 (47.56%) 50 (17.38%) E.coli 172 106 (61.62%) 48 (27.91%) 18 (10.47%) Acinetobacter spp. 128 33 (25.78%) 67 (52.34%) 28 (21.88%) Pseudomonas spp. 114 49 (42.98%) 34 (29.82%) 31 (27.20%) Proteus spp. 23 5 (21.73%) 6 (26.10%) 12 (52.17%) Enterobacter spp. 11 2 8 1 (18.18%) (72.72%) (9.10%) Coagulase negative staphylococci (CONS) 161 20 (12.42%) 139 (86.33%) 2 (1.25%) Enterococcus spp. 151 74 (49.00%) 64 (42.38%) 13 (8.62%) Candida spp. 133 126 (94.73%) 6 (4.51%) 1 (%0.76) Staphylococcus aureus 69 5 (7.26%) 46 (66.66%) 18 (26.08%) Non-hemolytic Streptococci 18 6 (33.33%) 11 (61.11%) 1 (5.56%) Others 12 3 (25.00%) 8 (66.67%) 1 (8.33%) Total 1280 530 (41.41%) 574 (44.84%) 176 (13.75%) 3.2.1 Gram-positive isolates (6.62%). Data also revealed a statistically significant differ- The analysis of the antibiotic susceptibility profile of ence in the antimicrobial potentials to different isolates. different gram-positive organisms was conducted and The results of the antibiotic susceptibility profile of each of showed that the highest percentage of resistance was ex- the Gram-positive pathogens are summarized in Tables 2 hibited towards penicillin (89.5%) followed by erythro- and 4. mycin (83.98%) and then cefoxitin which is the representative of the different beta-lactams in Staphylo- 3.2.2 Gram-negative isolates coccus species (76.52%). On the other hand, linezolid dis- Table 3 shows that the least frequency of resistance was played no resistance (0%) and vancomycin resistance recorded against nitrofurantoin (52.5%), amikacin was minimal (2.62%) among gram-positive organisms. (58.01%), followed by imipenem (59.78%) and merope- With regards to the predominant resistance pheno- nem (61.82%). Colistin was the most promising types among different isolates, Staphylococcus aureus (S. antibiotic as all Acinetobacter and Pseudomonas isolates aureus) exhibited high resistance rates to many antibiotics showed 100% susceptibility to it. Data also revealed that where 97.1% of the isolates displayed resistance to penicil- some antimicrobials showed a statistically significant lin, and 73.91% were resistant to gentamicin and all beta- difference in their antimicrobial activities to different lactams. On the other hand, S. aureus isolates exhibited a bacterial isolates. suscepibility of more than 40% to the rest of antibiotics Table 3 also shows that among the obtained gram- with 100% susceptibility to linezolid, nitrofurantoin, and negative pathogens, Klebsiella was the one that dis- vancomycin where no vancomycin-intermediate S. aureus played the highest level of multidrug-resistance (VISA) or vancomycin-resistant S. aureus (VRSA) were (87.84%) followed by Acinetobacter (83.59%). E. coli found in this study. and Pseudomonas spp. showed almost identical levels Similarly, CONS showed comparable beta-lactam of multidrug-resistance (73.68%, 72.02%) respectively. resistance rates to S. aureus with a slightly higher level Although 70% or more of the E. coli isolates pos- of methicillin resistance (77.6%), as well as, 100% suscep- sessed resistance against the majority of the available tibility to linezolid and vancomycin. However, CONS antibiotic options, a few agents as amikacin, genta- displayed a higher level of resistance to the majority of micin, imipenem, meropenem, and nitrofurantoin the rest of the antibiotics. showed potential antimicrobial activity with percent- Enterococci expressed a high level of resistance to both age of resistance of (12.21%, 38.37%, 18.60%, 19.76%, beta-lactams and quinolones, ciprofloxacin (86.75%), 30.18%), respectively. levofloxacin (76.15%), penicillin (78.14%), and ampicillin Both Proteus and Enterobacter spp. isolates showed the (64.9%). In a similar pattern to Staphylococci, no linezo- least antibiotic resistance among gram-negative pathogens. lid resistance was detected and vancomycin-resistant In Enterobacter isolates, the highest level of resistance was Enterococci (VRE) were discovered in ten isolates recorded against cephalosporins, piperacillin/tazobactam, Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 5 of 10 Table 2 Distribution of pathogens associated with intensive care unit-associated infections and their antimicrobial resistance patterns, Ain Shams University Hospitals, Egypt, March 2018–February 2019 Pathogen type and pattern of resistance n Resistance, n (%) Klebsiella spp. 288 ESBL production 30 (10.4) Multidrug resistance 253 (87.84) Acinetobacter spp. 128 Multidrug resistance 107 (83.59) Pseudomonas spp. 114 Multidrug resistance 84 (73.68) Escherichia coli 172 ESBL production 80 (46.5) Multidrug resistance 124 (72.02) Proteus spp. 23 ESBL production 4 (17.4) Enterobacter spp. 11 ESBL production 4 (36.36) Staphylococcus aureus 69 MRSA 51 (73.9) Coagulase-negative staphylococci 161 MR-CONS 125 (77.6) Enterococcus spp. 151 VRE* 10 (6.6) Candida spp. 133 Non-hemolytic streptococci 18 Others 12 Total 1280 ESBL extended-spectrum β-lactamase, MRSA methicillin-resistant S aureus, VRE vancomycin-resistant Enterococcus *Vancomycin resistance was confirmed by Vitek 2C doxycycline, and tobramycin in contrast to the rest of anti- problem. The few available studies concerning ICUs microbials which still had considerable activity against suggest that they are hotbeds of emerging high-level Enterobacter. Proteus isolates had the maximum resistance resistance. Hence, additional studies in other countries levels observed towards ampicillin/sulbactam (60.08%), and healthcare settings are encouraged [14]. doxycycline (82.60%), levofloxacin (60.86%), tetracycline In this study, gram-negative isolates (57.5%, n = 736) (73.91%), and trimethoprim/sulfamethoxazole (69.56%). were more prevalent compared to gram-positive ones Fortunately, the rest of the antibiotics still had a favorable (31.1%, n = 399). Comparable results were found by potential against Proteus. Halim et al. [15] where gram-negative bacteria took the upper hand among all nosocomial pathogens (53%) 4 Discussion while gram-positive organisms represented 37.9%. Simi- The excessive use of antibiotics has led to a vast wide- larly, gram-negative organisms constituted 65.7% of spread prevalence of antimicrobial resistance. As time cases in a study conducted by Sawhney and col- passes, bacterial pathogens will defy every antibacterial op- leagues [16]. tion, thus, becoming extremely hard to control. Hence, Most of the isolates were recovered from blood the WHO identified it as an international health prime cultures (44.84%) followed by urine (41.41%), unlike the concern [12, 13]. results of Shebl and Mosaad who reported higher To control this mounting predicament, comprehensive recovery from urine specimens in comparison with antibiotic stewardship in poor countries is fundamental. blood cultures [3]. However, enough data regarding antimicrobial resistance Among gram-negative organisms, Klebsiella, repre- are unavailable to precisely measure the extent of the sented the majority (22.5%) followed by E. coli (13.4%). Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 6 of 10 Table 3 Antibiotic resistance pattern of the prevalent gram-negative pathogens isolated from patients admitted in ICU, Ain Shams University Hospitals, Egypt, March 2018-February 2019 Antibiotic Resistant isolates, n (%) Total , p value n/N(%) Acinetobacter Klebsiella E.coli spp. Pseudomonas Proteus Enterobacter (N = 736) spp. spp (n = 172) spp. spp. spp. (n = 128) (n = 288) (n = 114 (n = 23 (n = 11) Amikacin 113 (88.28) 208 (72.22) 21 (12.21) 76 (66.66) 6 (26.08) 3 (27.27) 427/736 p < 0.001* (58.01) Amoxicillin/clavulanate **NA 245 (85.06) 124 (72.09) **NA 12 (52.17) 3 (27.27) 384/494 p < 0.001* (77.73) Ampicillin/sulbactam 110 (85.93) 277 (96.18) 155 (90.11) **NA 14 (60.08) 4(36.36) 560/622 p < 0.001* (90.03) Cefepime 110 (85.93) 276 (96.83) 157 (91.27) 91 (79.82) 7 (30.43) 8 (72.72) 649/736 p < 0.001* (88.17) Cefotaxime 124 (96.87) 285 (98.95) 152 (88.37) **NA 12 (52.17) 10 (90.90) 583/622 p < 0.001* (93.72) Cefoxitin **NA 248 (86.11) 92 (53.48) **NA 7 (30.43) 10 (90.90) 357/494 p < 0.001* (72.26) Cefpodoxime **NA 282 (97.91) 160 (93.02) **NA 10 (43.47) 9 (81.81) 461/494 p < 0.001* (93.31) Ceftazidime 115 (89.84) 279 (96.87) 156 (90.69) 92 (80.70) 8 (34.78) 10 (90.90) 660/736 p < 0.001* (89.67) Ceftriaxone 127 (99.21) 285 (98.95) 152 (88.37) **NA 12 (52.17) 10 (90.90) 586/622 p < 0.001* (94.21) Ciprofloxacin 111 (86.71) 258 (89.58) 122 (70.93) 91 (79.82) 13 (56.52) 6 (54.54) 601/736 p < 0.001* (81.65) Doxycycline 85 (66.41) 235 (81.59) 123 (71.51) **NA 19 (82.60) 9 (81.81) 471/622 0.008* (75.72) Gentamicin 97 (75.78) 204 (70.83) 66 (38.37) 81 (71.05) 10 (43.47) 5 (45.45) 463/736 p < 0.001* (62.90) Imipenem 101 (78.91) 225 (78.12) 32 (18.60) 75 (65.78) 4 (17.39) 3 (27.27) 440/736 p < 0.001* (59.78) Levofloxacin 109 (85.15) 231 (80.21) 119 (69.18) 87 (76.31) 14 (60.86) 5 (45.45) 565/736 0.001* (76.76) Meropenem 103 (80.46) 228 (79.16) 34 (19.76) 81 (71.05) 4 (17.39) 5 (45.45) 455/736 p < 0.001* (61.82) Piperacillin/ 107 (83.59) 250 (86.81) 95 (55.23) 80 (70.17) 5 (21.73) 10 (90.90) 547/736 p < 0.001* tazobactam (74.32) Tetracycline 114 (89.06) 240 (83.33) 130 (75.58) **NA 17 (73.91) 3 (27.27) 504/622 p < 0.001* (81.02) Tobramycin 90 (70.31) 234 (81.25) 106 (61.62) 92 (80.70) 6 (26.08) 7 (63.63) 535/736 p < 0.001* (72.69) Trimethoprim/ 87 (67.96) 241 (83.68) 137 (79.65) **NA 16 (69.56) 3 (27.27) 484/622 p < 0.001* sulfamethoxazole (77.81) Colistin 0 **NA **NA 0 **NA **NA **NA – (0) (0) Nitrofurantoin NA 77 (76.23) 32 (30.18) **NA **NA 0 (0) 109/209 p < 0.001* (52.15) No of urine samples 33 101 106 49 5 2 296 **NA = not applicable * significant at p<0.05 On the other hand, CONS (12.5%) was the most com- 17] as well as from countries other than Egypt. Osifo, and mon gram-positive pathogen. Aghahowa from Nigeria reported that E. coli and Klebsi- These results were similar to the results reported by ella pneumoniae were the most frequently isolated patho- other researchers studying bacterial strains in Egypt [15, gens [18]. However, others reported a higher level of E. Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 7 of 10 Table 4 Antibiotic resistance pattern of the prevalent Gram-positive pathogens isolated from patients admitted in ICU, Ain Shams University Hospitals, Egypt, March 2018-February 2019 Antibiotic Resistant isolates, n (%) Total , p value n/N(%) Staphylococcus aureus Coagulase-negative Enterococcus spp. (N = 381) (n = 69) staphylococci (n = 151) (n = 161) Amikacin 34 61 **NA 95/230 0.108 (49.29) (37.88) (41.30) Ampicillin NA NA 98 321/381 – ***67 ***156 (64.90) (84.25) Cefoxitin 51 125 **NA 176/230 0.541 (73.91) (77.63) (76.52) Penicillin 67 156 118 341/381 p < 0.001* (97.10) (96.89) (78.14) (89.50) Clindamycin 36 97 **NA 133/230 0.256 (52.17) (60.2) (57.82) Erythromycin 43 130 147 320/381 p < 0.001* (62.31) (80.74) (62.31) (83.98) Ciprofloxacin 36 107 131 274/381 p < 0.00*1 (52.17) (66.45) (86.75) (71.91) Doxycycline 29 70 38 137/381 0.002* (42.02) (43.47) (25.16) (35.95) Gentamicin (low dose) 51 98 **NA 149/230 0.058 (73.91) (51.30) (64.78) Gentamicin (high dose) **NA **NA 95 95/151 – (62.91) (62.91) Linezolid 0 0 0 0/381 – (0) (0) (0) (0) Levofloxacin 33 97 115 245/381 0.001* (47.82) (60.24) (76.15) (64.30) Teicoplanin 6 25 26 57/381 0.250 (8.69) (15.52) (17.21) (14.96) Tetracycline 38 76 53 167/381 0.011* (55.07) (47.20) (35.09) (43.83) Tobramycin 40 117 **NA 157/230 0.028* (57.97) (72.67) (68.26 Trimethoprim/sulfamethoxazole 10 100 **NA 110/230 p < 0.001* (14.49) (62.11) (47.82) Nitrofurantoin 0 4 38 42/99 0.021* (0) (20.00) (28.12) (42.42) Vancomycin 0 0 10 10/381 – (0) (0) (6.62) (2.62) No. of urine samples 5 20 74 99 ***The resistance for ampicillin was deduced from cefoxitin **NA = not applicable * significant at p<0.05 coli than Klebsiella spp. [3, 19]and S. aureus was much blood cultures. Man et al. from Romania also stated that higher than CONS unlike our study [3]. The high preva- CONS were the most commonly isolated pathogens from lence of CONS was justified by Basiri and coworkers, who blood culture in their study; however, E. coli came before stated that it could be the overuse of invasive devices with Klebsiella spp. as a cause of bacteremia [21]. repeated manipulation by healthcare workers and inad- In this study, E. coli and Klebsiella spp. were the main equate infection control measures [20]. pathogens recovered from urine. Similarly, Duffa et al. [22] As regards the distribution of pathogens among the dif- reported that E. coli and Klebsiella spp. were highly en- ferent clinical specimens in the present work, CONS and countered pathogens in urine. As for the predominating Klebsiella spp. were the most frequently isolated from pathogens in wound specimens, Klebsiella, Pseudomonas, Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 8 of 10 and Acinetobacter spp. were highly recovered organisms in attributed to their massive use for the treatment of the current research. Ibrahim [23]fromSaudi Arabia no- enterococcal infections [31, 32]. ticed that most the common wound pathogens were Pro- In the present study, gram-negative isolates exhibited teus mirabilis followed by Klebsiella pneumoniae. However, high resistance to almost all the used antibiotic classes in a research by Magdy and colleagues [24], S. aureus was with the least frequency recorded against nitrofurantoin the most common followed by Pseudomonas aeruginosa, (52.5%), amikacin (58.01%), followed by imipenem Klebsiella pneumoniae,and E. coli. (59.78%) and meropenem (61.82%). All isolates of The difference between the current study and other Pseudomonas and Acinetobacter showed 100% suscepti- studies regarding type and frequency of pathogens could bility to colistin so it can be considered a good thera- be linked to several factors like environmental condi- peutic option [11]. These findings coincide well—with tions, health practices, patient conditions, personal hy- very few exceptions—with those of Eldomany and Abde- giene, number of patients involved in each study, and laziz [33] from Egypt who reported high antibiotic resist- laboratory procedures [3]. ance against their tested isolates of Acinetobacter, The highest percentage of resistance among gram- Pseudomonas, Klebsiella, Enterobacter, and E. coli from positive organisms was exhibited towards penicillin cancer patients. (89.5%) followed by erythromycin (83.98%) and cefoxi- It is worthy to point to the fact that the high level of tin (76.52%). Resistance to vancomycin was minimal resistance observed among the gram-negative organisms (2.62%) among gram-positive organisms while no re- in the current study agrees well with the results reported sistance was noted against linezolid (0%). Hove et al. by other researchers [33–35]. Such elevated resistance in [25] reported that the highest rates of resistance were Enterobacteriaceae may be attributed to β-lactamase observed against penicillin (90.0%) and oxacillin activity [36]. (64.0%). The overall resistance towards penicillin and Generally, the resistance patterns of Acinetobacter and cefoxitin among staphylococcal isolates of Magdy and Proteus in the current research were in concordance with colleagues [24] from Egypt was in agreement with the Ibrahim [23], although E. coli isolates in Ibrahim’sstudy present study. However, their S. aureus isolates dis- displayed similar results as regards amikacin, gentamycin, played higher resistance opposite to the current study imipenem, and piperacillin/tazobactam but with much where CONS was the species with higher resistance. lower resistance for the rest of antibiotics. Regarding Moreover, their results were much higher as regards Pseudomonas and Klebsiella, both showed lower resist- vancomycin resistance which displayed resistance ance rates in contrast to the present study [23]. Several rates of 32.4% and 41.2% by S. aureus isolates and causes can be responsible for the increased incidence of CONS respectively [24]. Results of Shebl and Mosaad drug-resistance detected in the present study. The prime [3] from Egypt were in contrast to the current study reason may be the common practice in Egypt where al- as regards vancomycin and linezolid with a resistance most all patients—before hospital admission—take diverse of 10.8% and 11.3%, respectively. However, the results of antibiotics either prescribed by doctors or self-medication other researchers regarding vancomycin and linezolid due to over-the-counter antibiotics administered mostly were in favor to that obtained in the present study where in an improper dose and for an inadequate period [37, Al-Zoubi and his colleagues reported that all their S. aur- 38]. Other potential causes are the geographical diver- eus isolates were 100% susceptible to vancomycin [26]. gence as well as the genetic variations among pathogens Also, Basak et al. [11] and Mahmoud et al. [27]reported from different studies. But unfortunately, data about the 100% susceptibility to both vancomycin and linezolid. The molecular characterization of the strains included in the higher antibiotic resistance rates reported by the above- current study are not available. mentioned researches in comparison to the current results It is obvious that the obtained results in the current might be attributable to inconvenient use of antimicro- study reflected the high prevalence of multidrug resistance bials, geographic and socioeconomic variations, sampling especially among gram-negative pathogens. Klebsiella dis- biases, and dissimilar patients’ characteristics [28]. played the highest degree of multidrug-resistance (87.84%) As regards Enterococci, the overall resistance pat- followed by Acinetobacter (83.59%). E. coli and Pseudo- tern was comparable to that reported by Said and monas spp. showed almost identical levels of multidrug- Abdelmegeed [29] with the exception of the higher resistance (73.68%, 72.02%) respectively, while Proteus and linezolid resistance reported (9.7%) in their study. Enterobacter spp. isolates exhibited the lowest resistance Likewise, the resistance pattern of ciprofloxacin, among all the gram-negative pathogens. erythromycin, gentamicin, and linezolid agrees with There is a tremendous increase in MDR gram-negative that reported by Zalipour and coworkers [30]. In- bacteria in hospitals and especially in the intensive care creased resistance to macrolides and quinolones units (ICU). Such resistance is most notable in ICUs due among enterococcal clinical isolates might be to the unrestrained usage of antibiotics in ICU in Fahim Journal of the Egyptian Public Health Association (2021) 96:7 Page 9 of 10 comparison to other hospital departments and most of Received: 7 April 2020 Accepted: 17 December 2020 these infections were caused by gram-negative bacilli [39]. References It is important to note that the data presented in this 1. 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