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Hindawi International Journal of Microbiology Volume 2018, Article ID 8964958, 1 page https://doi.org/10.1155/2018/8964958

Retraction Retracted: Prevalence of and Antimicrobial Susceptibility Patterns among Diabetic and Nondiabetic Patients Attending at Debre Tabor Hospital, Northwest Ethiopia

International Journal of Microbiology

Received 15 May 2018; Accepted 15 May 2018; Published 6 June 2018

Copyright © 2018 International Journal of Microbiology. !is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

At the request of the authors, the article titled “Prevalence of Bacteriuria and Antimicrobial Susceptibility Patterns among Diabetic and Nondiabetic Patients Attending at Debre Tabor Hospital, Northwest Ethiopia” [1] has been retracted. !e article was found to contain a substantial amount of material from a previously unpublished thesis. !e first author Seble Worku takes the full responsibility and apologizes for the error. References [1] S. Worku, A. Derbie, M. Alemneh Sinishaw, Y. Adem, and F. Biadglegne, “Prevalence of bacteriuria and antimicrobial susceptibility patterns among diabetic and nondiabetic patients attending at Debre Tabor Hospital, Northwest Ethiopia,” International Journal of Microbiology, vol. 2017, Article ID 5809494, 8 pages, 2017. Hindawi International Journal of Microbiology Volume 2017, Article ID 5809494, 8 pages https://doi.org/10.1155/2017/5809494

Research Article Prevalence of Bacteriuria and Antimicrobial Susceptibility Patterns among Diabetic and Nondiabetic Patients Attending at Debre Tabor Hospital, Northwest Ethiopia

Seble Worku,1 Awoke Derbie,2 Mulusew Alemneh Sinishaw,3 Yesuf Adem,2 and Fantahun Biadglegne2

1 Department of Medical Laboratory Sciences, College of Health Sciences, Debre Tabor University, Debre Tabor, Ethiopia 2Department of Microbiology, Immunology and Parasitology, College of Medicine and Health Sciences, Bahir Dar University, Bahir Dar, Ethiopia 3Bahir Dar Regional Health Research Laboratory Center, Bahir Dar, Ethiopia

Correspondence should be addressed to Seble Worku; [email protected]

Received 29 November 2016; Revised 6 February 2017; Accepted 7 February 2017; Published 1 March 2017

Academic Editor: Joseph Falkinham

Copyright © 2017 Seble Worku et al. Tis is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Background. is a major health problem especially in developing countries. Information about bacterial pathogens isolated from urinary tract infection in diabetic patients and their antimicrobial susceptibility patterns is limited in Ethiopia. Terefore, this study aimed at isolating bacterial pathogens and their antimicrobial susceptibility patterns. Methods.A hospital based comparative cross-sectional study was conducted at Debre Tabor. sample was inoculated onto cysteine lysine electrolyte defcient (CLED) medium. Bacterial pathogens were identifed using standard bacteriological methods. Te data were cleaned and entered into SPSS version 20. � value less than 0.05 is considered statistically signifcant. Result. A total of 384 study participants were included in the study. Of them, 21 (10.9%) were from diabetics and 9 (4.7%) of them were from nondiabetics. Large proportion of gram positive at 18 (58.1%) were isolated compared to gram negatives at 13 (41.9%). Gram positive isolates were resistant to cotrimoxazole 10 (58.8%). Conclusion. Te rates of bacterial pathogens were higher in diabetic than nondiabetic patients. Bacteriuria was signifcantly associated with sex and type of . Multidrug resistance to two or more was observed in 56.7% of bacterial isolates. Rational use of antimicrobial agent should be thought of to prevent the emergence of multidrug resistance.

1. Background developing countries, incidence of DM is becoming a serious public health problem [3]. Diabetes mellitus (DM) is a chronic metabolic disorder Urinary tract infections (UTIs) are caused by growth of characterized by hyperglycemia resulting from impairments microorganisms anywhere in the urinary tract. It is usually in insulin secretion, defects in insulin action, or both which duetobacteriafromthedigestivetractwhichclimbthe in turn damageRETRACTED many of the body’s systems and also cause opening of the urethra and begin to multiply to cause several abnormalities of the host defense system that might infection [4]. Urinary tract infections have been the major increase the risk of certain infections [1]. Based on pathogenic problem in the tropics and also a common problem seen process, DM has two broad categories. Type 1 diabetes is in communities as well as in hospitals [5] and the most the result of complete or near-total insulin defciency. Type common conditions causing individuals to seek medical care 2 DM is a heterogeneous group of disorders characterized and results in a signifcant morbidity and high medical costs. by variable degrees of insulin resistance, impaired insulin It occurs in all age groups, in both genders, and usually secretion,andincreasedglucoseproduction[2].DMis requires urgent treatment [6]. Globally the prevalence of a worldwide public health problem considering its high UTI is high in healthy populations during the last 25 years prevalence and extremely high economic and social costs. In and the morbidity and mortality due to UTI have remained 2 International Journal of Microbiology static. It is most common particularly in females and a and nondiabetic patients that was expected to come to the signifcant number have recurrent infections at young age hospital for service was 660 (�1) and 4224 (�2), respectively. [7]. In developing countries, UTIs are commonly encoun- Te following form is used �1(fordiabetic)=�1/�1 = tered diseases by clinicians with an estimated annual global 660/192 = 3.4, so approximately every 4th Diabetic patient incidence of at least 250 million and also has been estimated that was included in the sample until the required sample thatgloballysymptomaticUTIsresultinasmanyas7million was achieved. Similarly �2 (for nondiabetic) = �2/�2 = visits to outpatient’s clinics, 1 million visits to emergency 4224/192 = 22 for nondiabetic patients, so every 22nd of the departments, and 100,000 hospitalizations annually [8]. nondiabetic patients was included until the required sample Both gram positive and gram negative bacteria are impli- size was achieved. cated as common causes of UTI. E. coli is the most common causative agent of UTIs in both DM and non-DM patients. 2.5. Data Collection and Laboratory Methods. Sociodemo- Other organisms reported include members of the fam- graphic data were collected from each study participant using ily Enterobacteriaceae (i.e., Proteus, Klebsiella, Enterobacter, structured questionnaire by trained nurses. To know the and Citrobacter species), Pseudomonas species, controls (nondiabetic) to be free from DM, history was taken species, streptococci, staphylococci, and C. albicans [9]. Te from each patient and blood level was checked. emergences of resistant bacterial strains in hospitals pose a continued challenge to treat and control the spread of infec- 2.6. Specimen Collection. Each diabetic patient and control tions. Moreover, indiscriminate use of antibiotics ofen results group were instructed how to collect a “clean-catch” mid- in the increased resistance of urine pathogens to most com- stream urine specimen by laboratory personnel or staf. monly used antimicrobial agents [10]. Antimicrobial resis- About 10 to 20 ml urine specimen was collected in a sterile tance is becoming an important public health problem in dia- screw-capped and wide-mouthed container. Te container betic urinary tract infection. Information about the etiologies was labeled with unique sample number, date, and time of UTI and among diabetic patients of collection. Following collection, it was delivered to the is limited in the study area. Terefore, this study was under- bacteriology laboratory of Debre Tabor Hospital for culture taken to analyze prevalence of bacterial etiologic agents, and drug susceptibility testing. antimicrobial susceptibility patterns, and risk factors among diabetic and nondiabetic patients in Debre Tabor Hospital. 2.7. Isolation and Identifcation of Bacteria. For the detec- tion of , collected urine specimens were 2. Methods inoculated onto cysteine lysine electrolyte defcient agar (CLED) (Oxoid, Ltd., Basingstoke, Hampshire, England) 2.1. Study Design and Period. Ahospitalbasedcomparative using calibrated loop (0.001 ml). Te inoculated plate was ∘ cross-sectional study was conducted from February to June incubated in aerobic atmosphere at 37 Cfor18–24hours 2015. (hrs). Ten, the plate was inspected for growth. Signifcant 5 bacteriuria was defned as colony count ≥ 10 cfu/ml, sub- 2.2. Study Area. Te study was conducted in Debre Tabor cultureontoMacconkeyandbloodagar.Teinoculated ∘ town, which is located 666 km far from Addis Ababa, in plate was incubated at 37 Cfor18–24hrs.Aferobtaining South Gondar Zone of the Amhara Region. It is 100 km from pure colonies, further identifcation was done by using the Bahir Dar, the capital city of Amhara regional state. In the standard microbiological technique, which includes gram town there are three Governmental Health Centers, 3 private stain, colony morphology, and biochemical tests (Oxoid, clinics; and one hospital. Based on fgures from 2007 Central LTD). Preliminary identifcation of bacteria was based on StatisticalAgencyofEthiopia(CSA),DebreTabortownhas gram reaction, colony characteristics of the bacteria like a total population of 55,596. Te hospital serves as a teaching on blood agar, and enzyme activities of the bacteria as well as patient-care providing center for the region. Te on diferent substrates. hospital has 91 beds. Close to 192 patients visit the hospital every day. Te hospital has diabetic treatment center that Biochemical Tests. Biochemical tests were performed on serves about 2149 diabetic patients. colonies from pure cultures for fnal identifcation of the isolates. Gram negative rods were identifed afer performing 2.3. Sample Size Determination. Te sample size was cal- a series of biochemical tests, which includes gas production, culated using comparison of two population proportion sugar fermentation, H2S production, indole production, cit- formula in epidemiologicalRETRACTED statistics (Open Epi version 2.3) rate utilization, lysine decarboxylase production, hydrolysis considering the following assumptions: 95% level of con- of urea, and motility tests. Te bacterial isolates were iden- fdence interval, ratio of diabetic to nondiabetic 1 : 1, and tifed by combination of diferent biochemical tests. Gram hypothetical proportion of controls to exposure �1 is 17.8% positive cocci were identifed based on their gram reaction, UTI in diabetic patients which was conducted in Gondar , , bacitracin, and test results [11]. University Hospital, Ethiopia [10]. Te fnal sample size with 10% nonresponse rate expectation was 385. Antimicrobial Susceptibility Testing. Antimicrobial suscepti- bility testing was carried out on each identifed organism by 2.4. Sampling Technique. Te sample collection period for disc difusion method on Muller Hinton agar (MHA) [11]. this study was for one month the total amount of diabetic Aferapureculturewasobtained,aloopfullofbacteria International Journal of Microbiology 3 was taken from a colony and was transferred to a tube Table 1: Sociodemographic characteristics of diabetic and nondia- containing 5 ml sterile normal saline (0.85% NaCl) and betic patients attending Debre Tabor Hospital, Northwest Ethiopia, mixed gently until it formed a homogenous suspension. Te 2015. turbidity of suspension was determined in comparison with Diabetic Characteristic 0.5 MacFarland standard [11]. A sterile swab was dipped in Number (%) Number (%) the broth suspension and excess suspension was removed Age (year) by pressing the swab against the wall of the tube. Te swab was used to distribute the bacteria suspension evenly 10–20 34 (17.7) 35 (18.2) over the entire surface of MHA (Oxoid). For antimicrobial 21–35 50 (26.0) 50 (26.0) testing of streptococci, 5% defbrinated sterile sheep blood was 36–45 36 (18.8) 39 (20.3) aseptically added to Mueller-Hinton medium. Te inoculated 46–55 35 (18.2) 31 (16.0) plates were lef at room temperature until dry. Te antimicro- ≥56 37 (19.3) 37 (19.3) bial impregnated disks were placed with sterile forceps on the Sex agar surface at least 24 mm away from each other to avoid the Male 102 (53.1) 100 (52.1) overlapping zone of inhibition. Afer placing the disk the plate Female 90 (46.9) 92 (47.9) was allowed to stand for 30 minutes to dissolve the Residence inthemedia.Ten,theplateswereinvertedandincubatedat ∘ Rural 114 (59.4) 122 (63.5) 37 C for 24 hrs and were read for the diameter of zone of inhi- Urban 78 (40.6) 70 (36.5) bition. Grades of susceptibility pattern were recognized as sensitive, intermediate, and resistant by comparison of zone Educational status of inhibition as indicated in the manufacturer’s guide [12]. Illiterate 110 (57.3) 124 (64.6) Te antimicrobial agents tested were obtained from Literate 82 (42.7) 68 (35.4) Oxoid in the following concentrations: Occupation For gram negative ampicillin (AMP) (10 �g), amoxicillin- Civil servant 40 (20.8) 23 (12.0) clavulanic acid (AMC) (30 �g), cefriaxone (CRO) (30 �g), Housewife 35 (18.0) 20 (10.4) � � ciprofoxacin (CIP) (5 g), gentamicin (CN) (10 g), cotri- Student 8 (4.1) 30 (15.6) � � moxazole (25 g), and tetracycline (TTC) (30 g) [10]. Farmer 66 (34.3) 92 (47.9) � For gram positive ampicillin (AMP) (10 g), amoxicillin- Merchant 14 (7.2) 6 (3.1) clavulanic acid (AMC) (30 �g), cefriaxone (CRO) (30 �g), Dailylabor 17(8.8) 12(6.3) chloramphenicol (C) (30 �g), ciprofoxacin (CIP) (5 �g), ∗ � � Other 12 (6.3) 9 (4.7) erythromycin (E) (15 g), gentamicin (CN) (10 g), penicillin ∗ (P) (10 IU), cotrimoxazole (25 �g), and tetracycline (TTC) jobless,driver. (30 �g) [10].

2.8. Quality Control. All specimens were collected and tested Te purpose and importance of the study were explained to according to the standard operating procedure of each phase. each study participant. Te laboratory fndings of study par- Te sterility of culture media was ensured by incubating 5% of ∘ ticipants were communicated with the responsible clinicians each batch of the prepared media at 37 C for 24 hours. Perfor- assigned at the OPD class. Above all the data were collected mance of all prepared media was also checked by inoculating afer full informed and written consent was obtained from international standard-strains such as E. coli (ATCC 25922) each participant. and S. aureus (ATCC 25923). To standardize the inoculum density of bacterial suspension for the susceptibility test, 0.5 3. Results MacFarland standard was used [11]. To ensure the accuracy of data, double data entry method was used. 3.1. Sociodemographic Characteristics of Study Participants. Of the total study participants, 384 (192 diabetic and 192 non- 2.9. Data Analysis. Data were entered, cleaned, and edited, diabetics), included in the study, 204 (53.1%) were males and using Epi info version 3.7, and were exported into SPSS 180 (46.9%) were females. Te age of the study participants version 20 for data analysis. Frequencies and cross tabulations ranged from 10 to 86 years for diabetic with a mean age of were used to summarize descriptive statistics. Tables were 39.8 ± 17.3years and nondiabetic patients also ranged from 10 used for data presentation.RETRACTED Odd ratio and adjusted odds ratio to 86 years with a mean age of 39.2 ± 17.2 years. Among the were used in the analysis. Both bivariate and multiple logistic diabetic patients 114 (59.4%) lived in rural areas, of whom 70 regressions were employed to assess the association between (36.4%) were farmers (Table 1). outcome and explanatory variables. � values < 0.05 were considered statistically signifcant. 3.2. Prevalence of Bacterial Urinary Tract Infection in Dia- betic and Nondiabetic Patients. Twenty-one (10.9%) and nine 2.10. Ethical Considerations. Ethical clearance was obtained (4.7%) bacterial isolates were recovered from diabetic and from ethical review committee of the School of health science nondiabetic study participants, respectively (Tables 2 and 3). of Debre Tabor University. A permission and supportive letter Among the diabetic patients who were culture positive 4 were obtained from Debre Tabor Hospital administration. (19%) and 17 (80.9%) had symptomatic and asymptomatic 4 International Journal of Microbiology

Table 2: Frequency and types of bacterial species isolated from symptomatic and asymptomatic diabetic patients’ urine culture attending Debre Tabor Hospital, Northwest Ethiopia, 2015.

Diabetic patient Number (%) Total Bacterial isolates � value Symptomatic Asymptomatic Number (%) E. coli 1 (25.0) 3 (75.0) 4 (19.1) 0.030 S. aureus 0 (0.0) 6 (28.6) 6 (28.6) 0.999 S. saprophyticus 2 (33.3) 4 (66.6) 6 (28.6) 0.011 Enterococcus spp. 1 (50.0) 1 (50.0) 2 (9.5) 0.011 K. pneumoniae 0 (0.0) 3 (100.0) 3 (14.3) 0.999 Total 4 (100.0) 17 (100.0) 21 (100.0)

Table 3: Prevalence bacterial urinary tract infection in diabetic and nondiabetic patients attending Debre Tabor Hospital, Northwest Ethiopia, 2015. Patient Status Number (%) Urine culture Diabetic Nondiabetic Total Odd ratio � value Urine culture positive 21 (10.9) 9 (4.7) 30 (7.8) 2.5 (1.11–5.60) 0.026 Urine culture negative 171 (89.1) 183 (95.3) 354 (91.5) 1

bacteriuria in that order. Majority, 171 (89.1%), of the diabetic of the isolates of S. aureus were sensitive to cefriaxone patients were asymptomatic and culture negative. Te preva- 7(77.8%). lence of asymptomatic bacteriuria among diabetic patients Te second predominant gram positive isolate, S. wassix(6%)and15(16.3%)ofmaleandfemalecorrespond- saprophyticus also showed low level of resistance to oxacillin ingly. Female diabetic patients were at more risk for UTI than 3(50%),cotrimoxazole3(50%),nitrofurantoinand males. Te prevalence of UTI among diabetic patients within cephalothin to 1 (16.7%), and tetracycline 2 (33.3%). All of the age group of 46–55 was 6 (17.1%). DM patients are more the isolates of S. saprophyticus were sensitive to doxycycline, likely to develop UTI (� = 0.026)thannon-DMpatients erythromycin, and cefriaxone 6 (100%). (Table 3). Te frst predominant gram negative isolate, E. coli,sho- Nine (4.7%) of nondiabetic study participants were wed high resistance to amoxicillin 8 (100%) and low level culture positive for UTI while four (44.4%) of them had resistant to tetracycline 3 (37.5%)and ampicillin 3 (37.5%).All symptomatic urinary tract infection. Te prevalence of UTI of the isolates of E. coli were 100% sensitive to gentamicin, was 1 (1%) and 8 (8.7%) in males and females of nondiabetic chloramphenicol,andcefriaxoneandfoundsensitiveto patients, respectively. Females were more at risk for UTI than 7 (87.5%), cotrimoxazole 7 (87.5%), and tetra- their male counter parts. Te prevalence of UTI in the age cycline 6 (66.6%). K. pneumoniae showed intermediate level range 46–55 years was 2 (6.5%) which is higher than other of resistance to amoxicillin 3 (75%) and low level of resistant age ranges. to tetracycline 2 (50%), cotrimoxazole, nitrofurantoin and Statistically signifcant associations were observed bet- chloramphenicol to each 1 (25%). All of the isolates of K. ween patient status (� = 0.024)andsex(� = 0.002)and pneumoniae were sensitive to gentamicin and cefriaxone urinary tract infection among diabetic and nondiabetic 4 (100%) to each and it was also found to be sensitive to patients using multivariate logistic regression assessment. ciprofoxacin, nitrofurantoin, cotrimoxazole, and chloram- Diabetic patients were 2.5 times as likely to develop UTI phenicol 4 (75%). during the follow-up period as nondiabetic patients (Table 5). One Enterobacter spp. showed resistant to amoxicillin whereas sensitive to ampicillin, tetracycline, cotrimoxazole, 3.3. Antimicrobial Susceptibility Patterns of Bacterial Isolates nitrofurantoin, chloramphenicol, gentamicin, cefriaxone, from Urine Culture.RETRACTEDAntibiotic sensitivity patterns of the and ciprofoxacin. isolates of bacteria were determined following the Kirby- Bauer disk difusion technique. Te antimicrobial susceptibil- 3.4. Comparison of Antimicrobial Resistance Patterns of Bac- ity patterns of the gram positive and gram negative bacterial terial Isolates from Diabetic and Nondiabetic Patients. Antibi- isolates were presented, in Tables 6 and 7, respectively. Te otic resistance of S. aureus isolates to penicillin and cotrimox- predominant isolate, S. aureus, revealed intermediate level of azole was 66.6% while cephalothin and nitrofurantoin was resistance to cotrimoxazole 7 (77.8%)and penicillin 6 (66.7%) 0%oftheisolatesfromdiabeticpatientswhereasisolatesfrom and low level resistance to oxacillin 5 (55.6%), tetracycline nondiabetic patients for cotrimoxazole and nitrofurantoin 5 (55.6%), doxycycline 4 (44.4%), erythromycin 4 (44.4%), were 100% and 0%, respectively. Antibiotic resistance of cephalothin 2 (22.2%), and nitrofurantoin 1 (11.1%). Most CoNS isolates to oxacillin and cotrimoxazole each is at 50% International Journal of Microbiology 5

Table 4: Frequency and types of bacterial species isolated from symptomatic and asymptomatic nondiabetic patients urine culture attending Debre Tabor Hospital, Northwest Ethiopia, 2015.

Nondiabetic patients Number (%) Bacterial isolates Total � value Symptomatic Asymptomatic E. coli 2 (50.0) 2 (50.0) 4 (44.4) 0.008 S. aureus 1 (33.3) 2 (66.7) 3 (33.3) 0.113 K. pneumoniae 1 (100.0) 0 (0.0) 1 (11.1) 0.995 Enterobacter spp. 0 (0.0) 1 (100.0) 1 (11.1) 0.999 Total 4 (44.4) 5 (55.5) 9 (100.0)

Table 5: Univariate and bivariate analysis of urinary tract infection among diabetic and nondiabetic patients attending Debre Tabor, Northwest Ethiopia, 2015.

Bacterial isolation Characteristic Crude-OR (95% CI) Adjusted-OR (95% CI) � value Yes � (%) No � (%) Patient status Diabetic 21 (10.9) 171 (89.1) 4.00 (0.178–0.899) 2.562 (1.130–5.809) 0.024 Nondiabetic 9 (4.7) 183 (95.3) 1 1 Sex Male 7 (3.5) 183 (96.5) 1 1 Female 23 (12.5) 161 (87.5) 3.939 (1.648–9.416) 4.011 (1.669–9.636) 0.002

and TTC and nitrofurantoin at 33.3% and 16.7%, respectively 4. Discussion (Table 6). Antibiotic resistance of E. coli isolates resistant to AMP In this study the isolation rates of bacterial pathogens among and TTC each was found to be at 50% in diabetics patients diabetic patients were found lower than previous studies done whereas in nondiabetic patients it was 40% for AMP and in Gondar (17.8%) [10] and India (37%) [7]. It was similar to 20% for TTC. However, E. coli isolates were 100% resistant the fndings of a study conducted in Addis Ababa (10.9%) [13] to amoxicillin isolates from both diabetic and nondiabetic Ethiopia. patients (Table 8). Cotrimoxazole was 100% efective in In the present study the isolation rates of bacterial diabetic patient isolates of E. coli whereas, in nondiabetic pathogens were (6%) and (16.3%) in male and female diabetic patient isolates, only 50% of the strains were sensitive. E. coli patients and also (1%) and (8.7%) in male and female was sensitive to ciprofoxacin, chloramphenicol, gentamicin, nondiabetic patients; these fndings were consistent with the nitrofurantoin, and cefriaxone 100% to each for both diabetic previous reports in Gondar (14%) [10] and (21.2%) [10] in and nondiabetic patient. males and females diabetic patients and in Italy (12.8% versus Te Antibiotic resistance of K. pneumoniae isolates to 11.4%) [9] and (15% versus 13.1%) [9] in male and female AMP,TTC, and AMOX each was at 33.3% in diabetic patients; diabetic versus nondiabetic patients. Te prevalence of UTI however, in nondiabetic patients it was 100% resistance to among female is high this may be due to low acidic pH AMP, TTC, chloramphenicol, MOX, and cotrimoxazole. K. of vaginal surface, poor hygienic conditions, and short and pneumoniae isolates from both diabetic and nondiabetic wide urethra and proximity to anus [10]. Te present fnding patients were 100% sensitive to ciprofoxacin, gentamicin and showed that the isolation rates of gram positive bacteria were cefriaxone antibiotics. foundtobehigherthanthepreviousstudydoneinCameroon Enterobacter spp. isolate was sensitive for most antimi- (41.2%) [14] and in Gondar (42.7%) [10]. crobial except amoxicillin. In the present study, S. aureus was the predominant isolate among diabetic patients. Tis fnding was similar 3.5. Multiple AntimicrobialRETRACTED Resistance Patterns. Of the 10 withastudyinNigeria(26.03%)[15].However,thisfnding (30%) S. aureus isolates 7 (77.8%)showed multidrug resistant is higher as compared with previous report from Gondar strain while two of them were sensitive to all antimicrobial University Hospital (8.5%) [10]. Tis discrepancy might be agents tested. Te six isolates of S. saprophyticus showed 3 poor personal hygiene condition. (50%) of multidrug resistant isolates. Te overall multiple Te isolation rate of S. saprophyticus (33.3%) in this study drug resistance patterns were 17 (56.7%). Among two isolates was consistent with a study fnding from Gondar University of Enterococci spp. only one was found to be resistant to one Hospital (22%) [10]. However, it is lower than a report from antibiotic. Of the eight E. coli isolates four isolates showed Cameroon (36.3%) [14]. Tis could be due to the appropriate multidrug resistant and the other three were resistant to only use of antibiotics that may reduce the proliferation of S. one antibiotic (Table 9). saprophyticus bacteria or good personal hygiene practice. 6 International Journal of Microbiology

Table 6: Antimicrobial resistance pattern of gram-positive bacteria isolated from urine of diabetic and nondiabetic patients attending Debre Tabor Hospital, Northwest Ethiopia, 2015.

Gram positive isolates Total Antibiotics tested S. aureus (�=9) � (%) CoNs (�=6) � (%) Enterococcus spp. (�=2) � (%) � (%) Oxacillin 5 (55.5) 3 (50.0) 0 (0.0) 8 (47.1) Nitrofurantoin 1 (11.1) 1 (16.7) 1 (50.0) 3 (17.7) Doxycycline 4 (44.4) 0 (0.0) 0 (0.0) 4 (23.5) Ampicillin 0 (0.0) — 0 (0.0) 0 (0.0) Cotrimoxazole 7 (77.7) 3 (50.0) 0 (0.0) 10 (58.8) Tetracycline 5 (55.5) 2 (33.3) 0 (0.0) 7 (41.2) Chloramphenicol 0 (0.0) — 0 (0.0) 0 (0.0) Penicillin 6 (66.7) 1 (16.7) 0 (0.0) 7 (41.2) Erythromycin 4 (44.4) 0 (0.0) 0 (0.0) 4 (23.5) Cefriaxone 2 (22.2) 0 (0.0) 0 (0.0) 2 (11.8) Cephalothin 2 (22.2) 1 (16.7) 0 (0.0) 3 (17.7)

Table 7: Antimicrobial resistance pattern of gram-negative bacteria isolated from urine of diabetic and nondiabetic patients attending Debre Tabor Hospital, Northwest Ethiopia, 2015.

Gram Negative isolates Total Antibiotics tested E. coli (�=8) � (%) K. Pneumoniae (�=4) � (%) Enterobacter spp. (�=1) � (%) � (%) Amoxicillin 8 (100) 3 (75.0) 1 (100) 12 (92.3) Ampicillin 3 (37.5) 2 (50.0) 0 (0.0) 5 (38.5) Ciprofoxacin 0 (0.0) 1 (25.0) 0 (0.0) 1 (7.7) chloramphenicol 0 (0.0) 1 (25.0) 0 (0.0) 1 (7.7) Gentamicin 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) Nitrofurantoin 1 (12.5) 1 (25.0) 0 (0.0) 2 (15.4) Cotrimoxazole 1 (12.5) 1 (25.0) 0 (0.0) 2 (15.4) Tetracycline 3 (37.5) 2 (50.0) 0 (0.0) 5 (38.5) Cefriaxone 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

Table 8: Comparison of antimicrobial resistance pattern of common bacterial isolates from urine of diabetic and nondiabetic patients attending Debre Tabor Hospital, Northwest, Ethiopia, 2015.

Isolates form diabetic patients Isolate from nondiabetic patient Antibiotics E. coli K. Pneumoniae S. aureus E. coli K. Pneumoniae S. aureus (�=4) (�=3) (�=6) (�=4) (�=1) (�=3) � (%) � (%) � (%) � (%) � (%) � (%) Oxacillin — — 2 (33.3) — — 2 (66.6) Penicillin — — 4 (66.6) — — 2 (66.6) Erythromycin — — 2 (33.3) — — 2 (66.6) Doxycycline — — 2 (33.3) — — 2 (66.6) Cephalothin — — 0 (0.0) — — 2 (66.6) NitrofurantoinRETRACTED 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (100.0) 1 (33.3) Cefriaxone 0 (0.0) 0 (0.0) 2 (33.3) 0 (0.0) 0 (0.0) 0 (0.0) Cotrimoxazole 0 (0.0) 1 (100.0%) 4 (66.6) 1 (25.0) 1 (100.0) 3 (100.0) Tetracycline 2 (50.0) 1 (33.3%) 3 (50.0) 1 (25.0%) 1 (100.0) 2 (66.6) Chloramphenicol 0 (0.0) 0 (0.0) — 0 (0.0) 1 (100.0) — Gentamicin 0 (0.0) 0 (0.0) — 0 (0.0) 0 (0.0) — Amoxicillin 4 (100.0) 2 (66.6) — 4 (100.0%) 1 (100.0) — Ciprofoxacin 0 (0.0) 1 (33.3) — 0 (0.0) 0 (0.0) — International Journal of Microbiology 7

Table 9: Multiple antimicrobial resistance pattern of bacterial isolates from urine of diabetic and nondiabetic patients attending Debre Tabor Hospital, Northwest Ethiopia, 2015.

Antibiogram patterns � (%) Bacterial isolates Number (%) �0 �1 �2 �3 �4 ≥R5 S. aureus 10 (32.2) 2 (22.2) 1 (11.1) 1 (11.1) 0 (0.0) 2 (22.2) 4 (44.4) S. saprophyticus 6 (19.3) 1 (16.7) 2 (33.3) 1 (16.7) 0 (0.0) 2 (33.3) 0 (0.0) Enterococcus spp. 2 (6.4) 1 (50.0) 1 (50.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) E. coli 8 (25.8) 1 (12.7) 3 (37.5) 2 (25.0) 1 (12.5) 1 (12.5) 0 (0.0) K. pneumoniae 4 (12.9) 1 (25.0) 0 (0.0) 1 (25.0) 1 (25.0) 0 (0.0) 1 (25.0) Enterobacter spp. 1 (3.2) 0 (0.0) 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) Total 31 (100.0) 5 (16.7) 8 (26.7) 5 (16.7) 2 (6.7) 5 (16.7) 5 (16.7)

�0 is no antibiotic resistance, R1 is resistant to one antibiotic, R2 is resistant to two antibiotic, R3 is resistant to three antibiotic, R4 is resistant to four antibiotic, and R5 is resistant to fve and more than fve.

Te current study fnding showed that 43.3% of the susceptibility to this drug might be due to self-medication isolates were gram negative bacteria which was lower than and indiscriminate use of antibiotics in the study area. the previous report in Gondar (57.3%) [10]. Tis inconsistency In this investigation, E. coli isolates were 100% sensitive to would be probably due to study design or sample size ciprofoxacin, gentamicin, chloramphenicol, and cefriaxone deference. On the other hand, this study was consistent with which was higher than the report from Addis Ababa (85%) thepreviousreportinCameroon(45.1%)[14]. [17]. On the other hand, in the present study, E. coli isolates Te second predominant bacterial isolate next to S. aureus that were resistant to amoxicillin 100% that was also similar was E. coli (Tables 2 and 4) in diabetic and nondiabetic with a study done in Gondar have been shown to increase patients, respectively. Tis fndings was higher than the the resistance of E. coli to amoxicillin; clavulanic acid is the study done in Libya (13%) versus (18%) [13] from diabetic result of hyperproduction of TEM-� lactamase, production and nondiabetic patients. However, it was lower than study of penicillinase resistant to inhibitors, and production of fndings reported from Italy (54.1%) versus (58.2%) [16] and cephalosporinase [10], ampicillin 50% versus 40%, and tetra- Nepal (41.7%) versus (40) in the above order. In addition, the cycline 50% versus 20%. isolation rates of K. pneumoniae in the present study were In the present study K. pneumonia isolates were 100% 14.3% versus 11.1% which was similar to those reported from sensitive to chloramphenicol, gentamicin, nitrofurantoin, Cameroon (15.9%) [14] and Libya (13% versus 14%) [13]. cefriaxone, and cotrimoxazole for diabetic patients and In the present study signifcant bacteriuria was detected gentamicin, ciprofoxacin, and cefriaxone for nondiabetic in symptomatic diabetic patients (80%) which was higher patients. Tis result depicted similar fnding with the report than reports from Gondar (51.4%) [10] and Addis Ababa from Addis Ababa [17] and Gondar. However, inconsistent (13.6%) [17]. Te fnding of this study also showed that report was reported from Libya more than (20%) of K. diabetic patients were more likely prone to UTIs than non- pneumoniae isolates were resistant to ciprofoxacin [13]. diabetic patients (10.9% versus 4.7%). Tis could be due to Tis discrepancy could be study setting, geography, and diabetes afecting many systems that protect against infection population diference. in general and against urinary tract infections specifcally. Multidrug resistance (MDR) to two or more drugs was In the present study, signifcant bacteriuria was detected observed in (56.7%) of the isolates in this study. Tis was in asymptomatic diabetic patients (9.1%) which were consis- consistent with the previous report from Gondar (59.8%) [10] tent with the reports in Addis Ababa (10.4%) [18] and Gondar and, however, lower than the previous report from Addis (14.7%) [10]. However, the fnding was lower than the report Ababa(71.7%)[17].Telowermultidrugresistanceratefrom from Cameroon (33.2%) [14]. theisolatesinthisstudycouldberationaluseofantimicrobial Urinary tract infection appears to be multifactorial in agents. subjects with diabetes and various diabetes-related risk fac- tors. Te risk ofRETRACTED acquiring bacteriuria is higher in diabetic 5. Conclusion patients (P-0.024) and females (P-0.002) [AOR: 4.011; 95% CI: 1.669–9.636 and AOR: 2.562; 95% CI: 1.130–5.809], respec- Te isolation rates of bacterial pathogens were higher in tively. Similar fndings have been reported in studies con- diabetic than nondiabetic patients. Statistically signifcant ducted elsewhere [10, 16]. In this study the susceptibility pat- UTI was observed between sex diference and becoming tern of S. aureus isolates demonstrated low and intermediate diabetic patient. Te predominant isolates were S. aureus, E. level of resistance to the commonly used antimicrobial agents. coli and K. pneumoniae from both diabetic and nondiabetic Most of the gram negative isolates (Table 7) were resistant patients. Most of the isolates showed intermediate to low level to amoxicillin. Tis showed as sensitivity was decreased in of resistance to one or more antimicrobials tested. Tis indi- contrast with the report from Gondar (59.6%) [10]. Decreased cates that regular monitoring is required to establish reliable 8 International Journal of Microbiology information about resistance pattern of urinary pathogens for in Vandavasi, Tamil Nadu, India,” International Journal of optimal empirical therapy of diabetic patients with UTIs. UTI Biological Technology,vol.2,no.2,pp.42–45,2011. in asymptomatic diabetic patients should not be neglected. [8] M. L. Wilson and L. Gaido, “Laboratory diagnosis of urinary Tough appropriate laboratory diagnosis establishment takes tract infections in adult patients,” Clinical Infectious Diseases, the leading point, nitrofurantoin, gentamicin, and cefriaxone vol. 38, no. 8, pp. 1150–1158, 2004. were the choice of antimicrobial agents against gram positives [9] S. E. Geerlings, “Urinary tract infections in patients with and ciprofoxacin, gentamicin, and cefriaxone were relatively diabetes mellitus: epidemiology, pathogenesis and treatment,” sensitive for most of gram negative isolates. International Journal of Antimicrobial Agents,vol.31,no.1,pp. 54–57, 2008. [10] G. Yismaw, D. Asrat, Y. Woldeamanuel, and C. G. Unakal, Competing Interests “Urinary Tract Infection: bacterial etiologies, drug resistance profle and associated risk factors in diabetic patients attending Te authors declare no competing interests with respect to Gondar University Hospital, Gondar, Ethiopia,” European Jour- the authorship and/or publication of this research paper. nal of Experimental Biology,vol.2,no.4,pp.889–898,2012. [11] M. Cheesbrough, “Biochemical tests to identify bacteria,” in Authors’ Contributions District Laboratory Practice in Tropical Countries Part II,pp. 45–58, Cambridge University Press, New York, NY, USA, 2nd Seble Worku was the primary researcher, conceived the edition, 2009. study, data collection, analysis, interpretation of the fndings, [12] Clinical and Laboratory Standards Institute (CLSI), Perfor- and drafing of the manuscript, and wrote the manuscript. mance Standards for Antibiotic Susceptibility Testing Tewenty Awoke Derbie, Mulusew Alemneh Sinishaw, and Yesuf Adem First Informational Supplement, CLSI Document M100-S21, substantially participated in collection and interpretation Clinical and Laboratory Standards Institute (CLSI), Wayne, Pa, of data. Fantahun Biadglegne substantially participated in USA, 2011. the design of the study, analysis, and interpretations of the [13]K.S.Ghenghesh,E.Elkateb,N.Berbashetal.,“Uropathogens fndings. 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