Abstract
Purpose
Diabetic foot infection (DFI) is one of the most feared complications of diabetes. In Sudan, the number of cases and the problems associated with diabetic foot infections increased in recent years. This study aimed to assess the bacteriological profile of patients with DFIs and their antibiotic susceptibility pattern.
Methods
A descriptive retrospective cross-sectional study was carried out at Surgery Department of Ribat University Hospital. All medical records of patients with DFIs during the period from September 2017 to February 2019 were reviewed using data collection sheet. The collected data were analyzed using Statistical Package for Social Sciences.
Results
Out of 250 DFI patients, 73.2% of them were males, and 86.4% of them had type 2 diabetes mellitus, and most of them suffered from diabetes for more than 10 years. Regarding culture results, 64.7% and 35.3% of the samples revealed presence of single microorganism and mixed infections, respectively. A total of 335 bacterial isolates were identified, gram-negative were more prevalent than gram-positive organisms. The most frequently isolated organisms were Proteus spp. Staphylococcus aureus, and Escherichia coli. Furthermore, antibiotic susceptibility pattern showed that imipenem, amikacin and vancomycin have the highest activity against isolated bacteria, and all isolates were found to be completely resistant to different cephalosporin drugs.
Conclusion
Among the studied samples, gram-negative bacteria were found to be more common in DFI patients, Proteus spp. and S. aureus were the most common microorganisms. Moreover, different isolated microorganisms showed to have different degrees of resistance and sensitivity to various antibacterial drugs.
Keywords: Diabetic foot infection, Antimicrobial agents, Bacteriological profile, Antibacterial susceptibility, Sudan
Introduction
Diabetic foot is one of the most critical complications of diabetes mellitus (DM), and is a leading cause of morbidity and disability, especially in developing countries (1). The World Health Organization (WHO) defines the diabetic foot as infection, ulceration, and/or destruction of deep tissues associated with neurological and various degrees of peripheral vascular disease in the lower limb (2). Furthermore, diabetic ulcers have 30 times higher risk of limb amputation when compared with foot ulcers due to other causes (3). The number of cases and the problems associated with diabetic foot infections (DFIs) have dramatically increased in recent years [4]. Many approaches are used to classify DFIs as the Infectious Disease Society of America (IDSA) system, the University of Texas System, and Wagner system [5]. Wagner system has been widely used for 25 years ago for the classification of DFIs. This classification system assesses ulcer depth and the presence of osteomyelitis or gangrene by using the following six grades: grade 0 (pre-or post-ulcerative lesion), grade 1 (partial/full-thickness ulcer), grade 2 (probing to tendon or capsule), grade 3 (deep with osteitis), grade 4 (partial foot gangrene), grade 5 (whole foot gangrene) [5–7].
The microbial etiology of diabetic foot ulcers is usually complex. Many of these infections are either mono-microbial or poly-microbial. In recent years, multidrug-resistant organisms have been reported very frequently, which has further complicated the treatment regimens [8, 9]. Pathogenic bacteria that cause these infections either originated from the external environment or physiological microflora of the skin (10). Furthermore, most of foot ulcerations may contain mixed flora, that consist of aerobic strains such as S. aureus, Streptococcus pyogenes, E. coli, Proteus mirabilis, Pseudomonas aeruginosa, E. fecalis, Klebsiella spp., and anaerobic bacteria, for example, Bacteroides fragilis Clostridium perfringens and Peptostreptococcus spp. [11].
Up to 60% of diabetic patients who are treated for a foot ulcer receive antibiotic therapy [12]. Initial therapy for infected wounds is usually empirical and based on the severity of the infection, gram-stained smear findings, and recent culture results [13]. For severe infections to chronic moderate infections, it is recommended to start with parenteral broad-spectrum agents, and after the infection is responding, most patients can have their treatments switched to oral therapy. Whereas mild and moderate infections can be treated with narrow-spectrum antibiotics [14–17]. However, although there are many advantages for topical antimicrobial therapy, including high local drug levels and avoidance of systemic adverse effects, only limited data supports the use of local antimicrobial therapy for mildly infected foot ulcers [18, 19]. Because antibiotics use may result in antimicrobial resistance, high financial cost, and drug-related adverse effects, many published evidence discourage therapy of uninfected ulcers with antibiotics, either to enhance wound healing or as prophylaxis against infection [14, 18].
Recently, DFIs are among the major diabetic complications in Sudanese diabetic patients that cause high morbidity and mortality [20, 21]. Multidrug resistance represents one of the main challenges in managing and treating these infections, as it further complicated the treatment regimens and increased the hospital stay and the cost [22, 23]. Therefore, there is an urgent need to study the prevalence and the causative microorganisms of DFIs in Sudanese hospitals. Hence, this study aimed to determine the bacteriological profile and antimicrobial susceptibility pattern of organisms isolated from patients with DFIs. To the best of our knowledge, no study has been made in Ribat University hospital about DFIs. Hence, this study aimed to determine the bacteriological profile and antimicrobial susceptibility pattern of organisms isolated from patients with DFIs.
Methods
Study setting
This study was a retrospective descriptive cross-sectional hospital-based survey involving the review of patients’ laboratory records and files. The study was conducted at the surgery unit at Ribat University Hospital, Khartoum, Sudan.
Study population and selection criteria
The study included all hospital records of diabetic patients with diabetic foot infections (DFIs) in Ribat University Hospital in the period from September 2017 to February 2019. The records of diabetic patients with DFIs did not perform culture, and sensitivity testing or those with unavailable sensitivity testing results were excluded from the study.
Sample size
Total coverage of all reports of diabetic patients with DFIs in the period from September 2017 to February 2019 was carried out; consequently, the study was no borne to sampling bias. The sample size in this study was 250 records.
Data collection tool
The data were collected from the patient files using a pre-designed validated checklist. It included the following variables; age, gender, economic condition, duration of DM, type of DM, level of HgbA1c, grade of DFI according to Wagner classification, duration of symptoms, the bacteriological profile of the isolated microorganisms, and antibiotic susceptibility data.
Data analysis
Data were analyzed by the International Business Machines [IBM]. Statistical Package for Social Sciences [SPSS] for Windows, Version 24.0 software [Armonk, NY: IBM Corp]. Descriptive statistics (frequency tables) and bivariate analysis (Chi-square) was done. P value ≤0.05 was considered significant in comparative data.
Ethical consideration
The ethical clearance (FPEC-17-2019) was obtained from the Ethical Committee of the Faculty of Pharmacy, University of Khartoum. Additional approval was obtained from Ribat University Hospital. All collected data were coded with ensuring confidentiality throughout the study.
Results
During the study period and based on the inclusion criteria, a total of 250 patients were included, as summarized in Table 1, the frequencies of males were 183(73.2%), the most frequent age range was 46–65 years (56.3%), followed by the age group of 66–85 years (26.3%). In addition, 99 (39.6%) participants were with low socioeconomic status, and only 34 (13.6%) were with high socioeconomic status. Clinically, most of the participants (86.4%) were have type 2 DM. Furthermore, about 45.2% of the patients had DM for 10–19 years. Moreover, Assessment of HbgA1c to evaluate DM control in participants revealed that 87.2% of participants had an HbgA1c level of more than 7%. Regarding the DFIs, the duration of diabetic foot ulcers ranged from less than one month 90 (36%), and one month or more 160 (64%).
Table 1.
Socio-demographic and clinical characteristics of the participants (n = 250)
| Variable | Number (frequency %) |
|---|---|
| Gender | |
| Male | 183 (73.2%) |
| Female | 67 (26.8%) |
| Age (years) | |
| 25–45 | 42 (16.8%) |
| 46–65 | 141 (56.4%) |
| 66–85 | 66 (26.4%) |
| > 86 | 1 (0.4%) |
| Economic condition | |
| Low | 99 (39.6%) |
| Moderate | 117 (46.8%) |
| High | 34 (13.6%) |
| Duration of DM (years) | |
| <10 | 73 (29.2%) |
| 10–19 | 113 (45.2%) |
| ≥20 | 64 (25.6%) |
| HbgA1c | |
| <7% | 32 (12.8%) |
| ≥7% | 218 (87.2%) |
| Duration of Diabetic foot ulcer | |
| <1 month | 90 (36%) |
| ≥1 month | 160 (64%) |
According to bacteriological profile results, 224 (89.6%) of the isolated samples were culture positive, and 26 (10.4%) showed no growth (Table 2). More than half of the cultures 145(58%) revealed the presence of single microorganisms, whereas 79(31.6%) of samples had mixed infections. Thus, a total of 335 microorganisms were isolated from the cultured-positive samples. Moreover, the classification of DFI ulcers based on Wagner system, and the association between Wagner classification and microbial flora was summarized in Table 3, in which we found 4.5%, 34.9%, 36.6%, 22.7%, 1.3% of DFI were distributed into grade 1, grade 2, grade 3, grade 4, and grade 5, respectively. Importantly, the results showed a significant association (p = 0.001) between the type of microbial flora and the grade of ulcer, as the deeper the ulcer was more likely to be infected with poly-microbial infection.
Table 2.
Bacteriological profile of isolated microorganisms among the studied population (n = 250)
| Variable | Number (frequency %) |
|---|---|
| Bacterial growth (250) | |
| Positive | 224 (89.6%) |
| Negative | 26 (10.4%) |
| Kind of infection (224) | |
| Single microorganism (Single infection) | 145 (64.7%) |
| Combined microorganism (Mixed infection) | 79 (35.3%) |
| Microorganisms’ type (335) | |
| Gram-positive bacteria | 138 (41.2%) |
| Gram-negative bacteria | 197 (58.8%) |
| Isolated microorganisms (335) | |
| Proteus species | 63 (18.8%) |
| Staphylococcus aureus | 61 (18.2%) |
| Escherichia coli | 52 (15.5%) |
| Enterococcus faecalis | 49 (14.6%) |
| Klebsiella species | 47 (14%) |
| Pseudomonas species | 35 (10.5%) |
| Methicillin resistant S. aureus (MERSA) | 28 (8.4%) |
Table 3.
Classification of DFI ulcers based on Wagner system, and the association between Wagner classification and the type of infection (single or mixed infection)
| Type of infection | Wagner classification of DFI, N(%) | Total N(%) | ||||
|---|---|---|---|---|---|---|
| Grade 1 | Grade 2 | Grade 3 | Grade 4 | Grade 5 | ||
| Single infection | 8 (3.6%) | 70 (31.3%) | 47 (21%) | 20 (8.9%) | 0 (0%) | 145 (64.7%) |
| Mixed infection | 2 (0.9%) | 8 (3.6%) | 35 (15.6%) | 31 (13.8%) | 3 (1.3%) | 79 (35.3%) |
| Total N(%) | 10 (4.5%) | 78 (34.9%) | 82 (36.6%) | 51 (22.7%) | 3 (1.3%) | 224 (100%) |
| P value | 0.001 | |||||
Furthermore, as shown in Table 2, all bacterial isolates were aerobic. Among them, the gram-negative organisms were more frequent and isolated from about 197(58.8%) cultures. Gram-negative organisms included Proteus spp. 63(18.8%), E. coli (15.5%), Klebsiella spp. 47(14%), and Pseudomonas aeruginosa 35(10.5%). On the other hand, isolated gram-positive strains were found in 183(41.2%) that included S. aureus 61(18.2%), Methicillin resistant S. aureus (MERSA) 28(8.4%), and E. fecalis 49(14.6%).
Concerning the antimicrobial sensitivity among bacterial isolates, 22 antimicrobial drugs were studied against the seven isolated bacteria, and the results are summarized in Tables 4 and 5 for gram-negative and gram-positive types of bacteria, respectively. Our findings showed that all tested the gram-negative and gram-positive microorganisms were 100% sensitive to imipenem, with the exception of Pseudomonas aeruginosa that exhibited 93.3% sensitivity to imipenem. All tested gram-negative and gram-positive, and bacteria were found to be 100% resistant to a different cephalosporin (cefepime, cefixime, cefuroxime, cefotaxime).
Table 4.
Sensitivity and resistance pattern of gram-negative microorganisms
| Microorganism | Antibiotics (number of tested isolate) | Sensitivity test | |
|---|---|---|---|
| Sensitive N(%) | Resistant N(%) | ||
| Klebsiella species (n = 47) |
Imipenem (12) Meropenem (21) Cefipime (22) Ceftixime (22) Cefaroxin (12) Ceftriaxone (11) Ceftazidine (18) Cephalexin (25) Ampicillin (8) Amoxicillin/Clavulanic acid (34) Co-trimoxazole (30) Fucidic acid (3) Amikacin (17) Gentamicin (28) Ciprofloxacin (42) Oxacillin (3) Doxacycline (1) Erythromycin (2) |
12 (100%) 13 (65%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 4 (16.7%) 0 (0%) 3 (9.1%) 12 (41.4%) 2 (66.7%) 16 (100%) 14 (51.9%) 23 (56.1%) 3 (100%) 0 (0%) 1 (50%) |
0 (0%) 7 (35%) 21 (100%) 21 (100%) 12 (100%) 11 (100%) 17 (100%) 20 (83.3%) 8 (100%) 30 (90.1%) 17 (58.6%) 1 (33.3%) 0 (0%) 13 (48.1%) 18 (43.9%) 0 (0%) 1 (100%) 1 (50%) |
| Pseudomonas species (n = 35) |
Imipenem (16) Meropenem (3) Cefipime (2) Ceftixime (1) Cefaroxin (1) Ceftazidine (16) Cephalexin (3) Amoxicillin/Clavulanic acid (6) Ticaracilin (4) Co-trimoxazole (4) Amikacin (27) Gentamicin (22) Ciprofloxacin (32) Doxacycline (3) Tetracycline (4) |
14 (93.3%) 1 (33.3%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (25%) 26 (100%) 12 (57.1%) 22 (71%) 1 (33.3%) 0 (0%) |
1 (3.7%) 2 (66.7%) 2 (100%) 1 (100%) 1 (100%) 15 (100%) 3 (100%) 6 (100%) 4 (100%) 3 (75%) 0 (0%) 9 (42.9%) 9 (29%) 2 (66.7%) 4 (100%) |
| Escherichia coli (n = 52) |
Imipenem (20) Meropenem (24) Cefipime (31) Ceftixime (38) Cefaroxin (20) Ceftriaxone (18) Ceftazidine (28) Cephalexin (22) Ampicillin (9) Amoxicillin/Clavulanic acid (39) Vancomycin (2) Co-trimoxazole (27) Fucidic acid (2) Amikacin (33) Gentamicin (33) Ciprofloxacin (45) |
19 (100%) 23 (100%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (100%) 1 (4.8%) 0 (0%) 1 (2.6%) 2 (100%) 9 (34.6%) 2 (100%) 32 (100%) 17 (53.1%) 16 (36.4%) |
0 (0%) 0 (0%) 30 (100%) 37 (100%) 19 (100%) 17 (100%) 27 (0%) 20 (95.2%) 9 (100%) 37 (97.4%) 0 (0%) 17 (65.4%) 0 (0%) 0 (0%) 15 (46.9%) 28 (63.6%) |
| Proteus species (n = 63) |
Imipenem (20) Meropenem (19) Cefipime (28) Ceftixime (30) Cefaroxin (12) Ceftriaxone (9) Ceftazidine (16) Cephalexin (40) Ampicillin (13) Amoxicillin/Clavulanic acid (51) Vancomycin (3) Co-trimoxazole (31) Fucidic acid (3) Amikacin (20) Gentamicin (38) Ciprofloxacin (55) Doxacycline (2) Tetracycline (4) Erythromycin (2) |
19 (100%) 17 (94.4%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 16 (31%) 1 (7.7%) 19 (38%) 3 (100%) 9 (30%) 2 (66.7%) 19 (100%) 16 (43.2%) 37 (68.5%) 2 (100%) 0 (0%) 2 (100%) |
0 (0%) 1 (5.6%) 27 (100%) 29 (100%) 12 (100%) 9 (100%) 15 (100%) 23 (69%) 12 (92.3%) 31 (62%) 0 (0%) 21 (70%) 1 (33.3%) 0 (0%) 21 (56.8%) 17 (31.5%) 0 (0%) 4 (100%) 0 (0%) |
Table 5.
Sensitivity and resistance pattern of gram-positive microorganisms
| Microorganism | Antibiotics (number of tested isolate) | Sensitivity test | |
|---|---|---|---|
| Sensitive N(%) | Resistant N(%) | ||
| Staphylococcus aureus (n = 61) |
Imipenem (1) Meropenem (1) Cefipime (1) Ceftixime (1) Cefaroxin (1) Ceftazidine (1) Cephalexin (1) Amoxicillin/Clavulanic acid (2) Vancomycin (50) Co-trimoxazole (32) Fucidic acid (59) Amikacin (2) Gentamicin (24) Ciprofloxacin (3) Oxacillin (19) Doxacycline (47) Tetracycline (54) Erythromycin (55) |
1 (100%) 1 (100%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 45 (91.8%) 22 (71%) 46 (78%) 2 (100%) 8 (34.8%) 3 (100%) 18 (100%) 29 (63%) 29 (54.7%) 20 (37%) |
0 (0%) 0 (0%) 1 (100%) 1 (100%) 1 (100%) 1 (100%) 0 (0%) 2 (100%) 4 (8.2%) 9 (29%) 13 (22%) 0 (0%) 15 (65.2%) 0 (0%) 0 (0%) 17 (37%) 24 (45.3%) 34 (53%) |
|
Methicillin-resistant Staphylococcus aureus (MRSA) (n = 28) |
Imipenem (6) Meropenem (3) Cefipime (6) Ceftixime (6) Cefaroxin (3) Ceftriaxone (3) Ceftazidine (3) Cephalexin (1) Ampicillin Amoxicillin/Clavulanic acid (9) Vancomycin (16) Co-trimoxazole (9) Fucidic acid (16) Gentamicin (12) Ciprofloxacin (11) Oxacillin (2) Doxacycline (8) Tetracycline (16) Erythromycin (16) |
6 (100%) 3 (100%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (100%) 1 (100%) 1 (33.3%) 3 (33.3%) 15 (100%) 3 (33.3%) 8 (53.3%) 6 (50%) 7 (63.6%) 2 (100%) 2 (25%) 8 (53.3%) 4 (26.7%) |
0 (0%) 0 (0%) 6 (100%) 6 (100%) 3 (100%) 3 (100%) 3 (0%) 0 (0%) 2 (66.7%) 6 (66.7%) 0 (0%) 6 (66.7%) 7 (46.7%) 6 (50%) 4 (36.4%) 0 (0%) 6 (75%) 7 (46.7%) 11 (73.3%) |
|
Enterococcus faecalis (n = 49) |
Meropenem (1) Cefipime (4) Ceftixime (2) Cefaroxin (2) Ceftriaxone (11) Ceftazidine (18) Cephalexin (4) Penicillin (6) Ampicillin (14) Amoxicillin/Clavulanic acid (43) Vancomycin (43) Co-trimoxazole (24) Fucidic acid (9) Amikacin (1) Gentamicin (7) Ciprofloxacin (47) Doxacycline (2) Tetracycline (5) Erythromycin (3) |
1 (100%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (20%) 6 (100%) 9 (64.3%) 29 (69.1%) 38 (90.5%) 7 (30.4%) 5 (55.6%) 1 (100%) 2 (28.6%) 21 (45.7%) 1 (50%) 0 (0%) 2 (66.7%) |
0 (0%) 4 (100%) 2 (100%) 2 (100%) 1 (100%) 1 (100%) 4 (80%) 0 (0%) 5 (35.7%) 13 (30.9%) 4 (9.5%) 16 (69.6%) 4 (44.4%) 0 (0%) 5 (71.4%) 25 (54.3%) 1 (50%) 5 (100%) 1 (33.3%) |
Furthermore, Klebsilla isolates showed 100% sensitivity to imipenem, amikacin and oxacillin, but very high resistance rates to doxycycline, amoxicillin/clavulanic acid (Table 4). Pseudomonas aeruginosa isolates revealed sensitivity to imipenem and amikacin, and all isolates were resistant to tetracycline and amoxicillin/clavulanic acid (Table 4). Whereas all Proteus isolates showed were sensitive to imipenem, doxycycline, erythromycin, amikacin, and vancomycin (Table 4). Interestingly, E. coli showed 100% sensitivity to imipenem, meropenem, amikacin, and Vancomycin. However, E. coli was highly resistant to different penicillins and cephalosporins (Table 4).
Regarding gram-positive isolates, all S. aureus isolates were sensitive to imipenem, ciprofloxacin, meropenem, oxacillin, and amikacin. Whereas, vancomycin sensitivity rate was 91%. In addition, resistance rates of S. aureus isolates were 65.2%, 63%, and 45.3 to gentamicin, erythromycin, and tetracycline, respectively (Table 5). Methicillin-resistant S. aureus (MERSA) showed 100% sensitivity to imipenem, meropenem, oxacillin, and vancomycin. However, 75% of MERSA isolates were resistant to doxycycline, and erythromycin (Table 5). Moreover, meropenem, amikacin, and penicillin were showed 100% sensitivity against E. fecalis. Whereas, vancomycin, amoxicillin/clavulanic acid had 90% and 70% of sensitivity, respectively (Table 5).
Discussion
Diabetic foot infections represent one of the leading causes of morbidity and disability among people with diabetes, it could lead to amputation and requires extreme care during treatment [1]. However, clinicians have a greater role to play, as they involve in rational and effective management, through determining the causative microorganisms involved and their antibiotic susceptibility pattern [24]. In the current study, DFIs among Sudanese diabetic patients were assessed, in which we found that DFIs were higher in males (73.2%) than in females (26.8%). This could be attributed to the fact that males are more exposed to hard works in the outer environment. Moreover, most DFIs patients were aged between 45 and 65 years and had diabetes for more than 10 years, this because the age increases the chance of getting DFIs, and diabetic complications are directly proportional to the duration of DM [1]. These findings are similar to the results of studies conducted by Umasankari et al. and Bentkover et al. [25, 26]. On the other hand, most of the participants in the current study have poor to moderate socioeconomic status, which may contribute to the development of antimicrobial-resistant due to the high cost of antimicrobial drugs in Sudan; therefore, many of them may ignore to complete the antibiotic course.
Regarding the type of diabetes, more than 80% of the participants had type 2 DM, and this could be because mostly type 2 DM have already developed complications, particularly peripheral neuropathy and peripheral vascular diseases upon diagnosis because most of them go undiagnosed for an extended period [2, 27]. Moreover, 87.2% of participants had HgbA1c levels of more than 7%, indicating poor control of blood glucose. It is known that hyperglycemia increases pathogenic bacteria’s virulence and may contribute to the development of severe infection, immune system impairment, and antibiotic resistance [28].
Even though many reports indicated that DFIs are mostly poly-microbial in the Middle East and North Africa countries [3, 27, 29–36] as shown in Table 4. In this study, we observed a higher percentage of mono-microbial infections (64%), this finding is in line with the results of studies conducted by Dhanasekaran et al. and Tiwari et al. [37, 38]. Moreover, there is a significant association between the presence of polymicrobial infection and the grade of the ulcer, and it is quite logical as the deepness and severity of the ulcer increase the risk of poly-microbial infections, these results similar to those shown by Shankar et al. and by Gadepalli et al. [8, 39]. Furthermore, as many previous reports, our study indicated that gram-negative organisms were present in higher numbers than gram-positive organisms [39–41]. Thus in order to treat DFIs, it is essential to select antimicrobial drugs that are more effective against gram-negative bacteria. Among gram-negative isolates, Proteus spp. was the most frequent bacterium, followed by E. coli. In contrast to our findings, previous studies by Citron et al. and Sivanmaliappan et al. [10, 42], reported that Pseudomonas aeruginosa was the most predominant microorganism. On the other hand, S. aurerus was the major causative gram-positive bacterium comparable with the findings of Lipsky et al. and Gu et al. [19, 43]. Importantly, in agreement with the study, which concluded that diabetic foot ulcers had a high frequency of colonization with antimicrobial-resistant organisms, including MRSA, in this study, MRSA was observed in 12.5% case [44].
Concerning the sensitivity to different antibacterial drugs, unexpectedly, all tested gram-positive and gram-negative bacteria were found to be 100% resistant to different cephalosporin drugs such as cefepime, cefixime, cefuroxime, and cefotaxime. This could be attributed to the irrational use of these antibiotics. Antimicrobial susceptibility Klebsilla isolates are partially similar to those reported in the previous literature, as all isolates were sensitive to imipenem and amikacin and highly resistant to erythromycin, amoxicillin/clavulanic acid and co-tirmoxazole [45, 46]. Results of the susceptibility of Pseudomonas aeruginosa isolates are partially in agreement with those reported by Shanmugam et al. [42], who reported that more than 50% of Pseudomonas aeruginosa were resistant to gentamicin, quinolones and third-generation cephalosporin’s. Also, another study by Girish et al. reported that Pseudomonas infections respond better to imipenem [46]. Furthermore, Proteus isolates showed complete sensitivity to imipenem, doxycycline, erythromycin, amikacin and vancomycin, and 94.4% sensitivity to meropenem, and 68.52% sensitivity to ciprofloxacin. These findings agree with a study conducted by Hefni AA el al. who reported 95% sensitivity to imipenem, 89% to meropenem, but contradictory to our findings in that he reported 100% sensitivity to amoxicillin-clavulanic acid [31]. Among gram-negative microorganisms, E. coli was the only bacterium that showed 100% sensitivity to fusidic acid. This finding may support the value of topical fusidic acid for the treatment of DFIs.
Regarding gram-positive bacteria, S. aureus isolates showed complete sensitivity to imipenem, ciprofloxacin, meropenem, and amikacin, and 91.84% sensitivity to vancomycin. These results are quite similar to the findings of Hefni AA el al who reported 100% sensitivity to imipenem, vancomycin, and amikacin [31]. Although MERSA sensitivity to results is in line with those reported by Abdulrazaka et al., in that both studies showed 100% sensitivity to vancomycin, imipenem, meropenem, a difference was observed for susceptibility to amikacin [30]. While they reported high sensitivity of MRSA to amikcacin, in the current study, resistance to amikacin was about 67%. Finally, E. fecalis isolates showed high resistance to tetracycline, gentamicin, co-trimoxazole, and ciprofloxacin, and highly sensitive to vancomycin, this sensitivity pattern is similar to those reported by Lee JH et al. and Shahid M et al. [47, 48]. The emergence of resistance to this group of antibiotics leaves little options for treating such life-threatening infections, as seen in the current study (Table 6).
Table 6.
Common isolated microorganisms, sensitivity and resistance pattern of microorganisms for different studies about DFIs in the Middle East and North Africa region
| Country | Common Organisms isolated | Most active antibiotics | Most resistant antibiotics | Ref |
|---|---|---|---|---|
| Sudan | S. aureus, Coagulase negative staphylococci, E. fecalis, E.coli, Klebsiella spp., Proteus spp., Pseudomonas aeruginosa | Ciprofloxacin, Vancomycin, Imipenem, Amikacin | Chloramphenicol, Azetreonam, Tetracycline, Oxacillin, Amoxicillin/clavulanic acid (Co-amoxiclav), Penicillin. | 29 |
| Kuwait | S. aureus, MERSA, Group B streptococci, Enterococcus spp., E. coli, Klebslella pneumonia, Proteus mirabilis, Psudeumonus areginosa, Some anaerobes | Imipenem, Piperacillin-Tazobactum, Vancomycin | Tetracycline, Penicillin, Erythromycin, Fucidic acid, Ampicillin, Trimethoprim, Piperacillin and Ciprofloxacillin. | 30 |
| Egypt | S. aureus, MERSA, S. pyogens, Group D streptococcus, Streptococcus pneumonia, Pseudomonas argionosa, Klebsiella pneumonia, Proteus mirabilis, E. coli | Amikacin, Vancomycin, Levofloxacin, Imepenem | Penicillin, Tetracycline, Cephalexin, Ampicillin, cefuroxime, Co-amoxiclav | 31 |
| Iran | S. aureus, E. coli, Proteus mirabilis, Staph-epidermis, Pseudomonas aeruginosa, Klebsiella spp. | Ciprofloxacin, Ceftriaxone, Clindamycin | Cloxacillin, Clindamycin, Amoxicillin, Cloxacillin, Ceftazidime | 3 |
| Tunis | S. aureus, E. coli, Entrobacter spp., Klebsiella, Proteus mirabilis, Proteus vulgaris, Group C, G streptococci | Ertapenem, Ceftazidime, Cefepime, Fosfomycin | Amoxicilin, ticoplanin, cotrimoxazole, netimicin and ofloxacin | 32 |
| Saudi Arabia |
S. aureus, MERSA, Enterococcus fecalis, Group B Streptococcus, Pseudomonas aeruginosa, Klebsiella Proteus mirabilis, Enterobacter cloacae |
Gentamycin, Ciprofloxacin, Erythromycin | Penicillin, Clindamycin, Ceftazidine, Imepenem, Levofloxacin, Amikacin, chlothromycin. | 33 |
| Egypt | S. aureus, Streptococcus, Staphylococcus epidermis, E. coli, Proteus mirabiis, Klebsiella, Pseudomonas aeruginosa | Clindamycin, Gentamicin, Vancomycin, Oxacillin | Ampicillin, Cephalexin, Cefuroxime, Tetracycline, Gentamicin | 34 |
| Saudi Arabia | S. aureus, MERSA, Enterococcus spp., Group B streptococci, E. coli, Pseudomonas aeruginosa, Klebsiella, Proteus mirabilis, Morganella spp., Clostridium prefringens | Co-amoxiclav, Ampicillin, Ceftriaxone, Trimethoprim/sulfamethoxazole | Amikacin, Aztreonam, Ceftazidime, Meropenem, Cefuroxime, Imepenem | 35 |
| Southern Iran |
Enterococcus spp., S. aureus, E. coli Proteus, Diphtheroid spp., Pseudomonas aeruginosa, Klebsiella |
Impenem, Amikacin, Meropenem, Gentamicin |
Tetracycline, Ampicillin, Trimethoprim/sulfamethoxazole, Ciprofloxacin, Co-amoxiclav acid, Cephalexin, Cefotaxime |
36 |
In the developing countries, community-acquired and hospital-acquired infections are characterized by high rate antibiotic resistance, which may lead to continuous changes in the selection of empirical therapy [49]. Furthermore, there is a direct relationship between the total amount of a specific antibiotic used in a particular hospital during a certain period of time and the number of resistant strains that emerge [50]. In Sudan, the high resistance rates could be due to the irrational use of antibiotics [51]. In addition, low cost and availability of antibiotics in community pharmacies without restricting regulations may cause some patients with DFIs to skip the culture and sensitivity testing, resort to cheap antibiotics, or even do the test but never complete the antibiotic course [52]. Even though no optimal antimicrobial therapy was established for DFIs up to date, management of these infections requires isolation and identification of the microbial flora, appropriate antibiotic therapy, according to the sensitivity patterns, and precise selection and identification of the chronic complications and rational surgical intervention for complications.
The limitations of the current study are, firstly the cross-sectional design in one hospital may not allow generalization of the findings to all hospitals in Sudan. Secondly, the missed data about the sensitivity testing of many drugs against isolated organisms have a significant impact on this study. Despite these limitations, this surveillance is essential, as it provides the situation of the causative microorganisms for DFIs in Sudanese patients, which will help a lot in constructing the proper hospital guidelines for the rational treating of DFIs. However, prospective studies are urgently needed in other Sudanese hospitals to assess the current situation of DFIs,
Conclusion
Among DFIs studied samples, gram-negative bacteria were more commonly isolated than gram-positive bacteria. The most frequently isolated organisms were Proteus spp. and E. coli. For the gram-negative bacteria and S. aureus for gram-positive bacteria. All isolates were found to be completely resistant to different cephalosporin drugs and highly sensitive to imipenem, meropenem, amikacin, and vancomycin. The surveillance of antimicrobial resistance is necessary, and antibiotic policy should be formulated in the hospital.
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