Bacterial profile of surgical site infection and antimicrobial resistance patterns in Ethiopia: a multicentre prospective cross-sectional study

In the present study, a total of 752 patients from four different hospitals were investigated for SSIs. The number of patients from DTCSH was172, and the numbers from HUCSH, JUSTH, and TASH, were184, 193, and 203, respectively (Table 1). Of the 752 study participants whose SSI discharge was inoculated onto growth media, 65.5% (493 /752) showed bacterial growth (Table 1). DTCSH had the highest percentage of positive cultures (78.5%), followed by JUTSH (65.3%), and HUCSH and TASH, respectively, had 65.2% and 55.7% of SSI bacterial growth (Table 1). The study participants age ranged from 3 days to 85 years with median of 28 years and 418 (55.6%) were males. Approximately 487 (64.8%) of patients had deep SSI, 454 (60.4%) preoperative hospital stay > 7 days, 619 (82.4%) history of hospital admission, 388 (52.9%) had previous use of antibiotics, 448 (59.6%) had smoking history, 506 (67.2%) of surgical procedures were emergency surgery, 724 (96.2%) of patients with clean or clean contaminated wounds dominated the wound class, 548 (72.8%) required antimicrobial prophylaxis before the procedure, and 55.3% underwent surgeries lasting greater than an hour (Table 1).

Table 1 Socio-demographic characteristics and clinical data

Bivariate and multivariable logistic regression analyses were used to see the relationship between the independent variables over the dependent variable. On bivariate regression analysis, male sex, age ≥ 61, SSI type, preoperative hospital stays, history of hospital admission, previous use of antibiotics, smoking, emergency surgery, and duration of operation ≥ 1 h had a statistically significant association with the occurrence of SSI. The type of surgery (wound), alcohol history and the timing of prophylactic antibiotics ≥ 1 h had no statistically significant association (Table 2). The result of the multivariate regression showed that ages ≥ 61 years (AOR = 2.83, 95% CI: 1.02–7.99; P 0.046), prolonged duration of hospital stay (AOR = 4.15, 95% CI: 2.87–6.01; P 0.000), history of previous antibiotics use (AOR = 2.83, 95% CI: 1.06–2.80; P 0.028), history of smoking (AOR = 2.35, 95% CI:1.44–3.83; P 0.001), emergency surgery (AOR = 3.24, 95% CI: 2.29–4.77; P 0.000), and duration of operation (AOR = 0.27, 95% CI: 0.181–0.39; P 0.000) were significant risk factors (Table 2).

Table 2 Bivariate and multivariate analysis to identify factors associated with patient demographic and clinical characteristics with surgical site infection culture showed growthFrequency and distribution of identified bacterial isolates

The total number of pathogenic bacterial isolates were 65.7% (494/752) from all SSI culture (Figs. 3, 4A). Gram-negative were 57.9% (286/752), and Gram positive 42.1% (208/752) according to Fig. 2B, C). Of these, 2.6% (13/493) of cultures were a mixture of two colony types, while 2.4% (12/493) were commensals or contaminants and 97.4% showed single bacterial growth. Species of the mixed cultures were Raoultella ornithinolytica, Paenibacillus tylopili, S. aureus and coagulase negative staphylococci. Among the identified types of bacteria, Staphylococcus aureus was the predominant one (31%), followed by E. coli (20.7%) and Klebsiella pneumonia (9.8%) among SSIs (Fig. 1). Other less frequently detected species were Acinetobacter baumannii (7.6%), Enterobacter cloacae (5.1%), Pseudomonas aeruginosa (3.7%), Klebsiella variicola, and Enterobacter hormaeche (1% each). Diverse species of Acinetobacter, Enterobacter, Enterococcus, Staphylococcus, Aerococcus, Bacillus, Citrobacter, and Pseudomonas were identified. While Gram-positives was found at all four hospitals (42.1%), it was mainly detected at DTCSH (40.4%), with 21.6%, 21.6%, and 16.3% isolated at TASH, HUCSH, and JUTSH, respectively (Fig. 2B). In addition, Raoultella ornithinolytica, Stenotrophomonas maltophilia, Pantoea ecurina, Providencia rettgeri, Alcalignes faecalis, and Morganella morganii were detected as rare bacterial pathogens. Figure 2A shows the frequency and distribution of Gram-negative bacterial isolates at the four hospitals.

Fig. 3figure 3

Frequency and distribution of bacteria isolated from patients investigated for surgical site infection at four different hospitals in Ethiopia. GNB Gram-negative bacteria, GPB Gram-positive bacteria, Other GN and GP (n = 128): Raoultella ornithinolytica (n = 1), Stenotrophomonas maltophilia (n = 1), Acinetobacter soli (n = 2), Acinetobacter pitti (n = 2), Acinetobacter lactucae (n = 1), Pseudomonas plecoglossicida (n = 1), Pantoea ecurina (n = 1), Citrobacter freundii (n = 1), Citrobacter sedlakii (n = 2), Providencia rettgeri (n = 2), Alcalignes faecalis (n = 2), Proteus mirabilis (n = 4), Morganella morganii (n = 1), Aerococcus viridans (n = 3), Bacillus flexus(n = 1) Paenibacillus tylopili (n = 1), Enterobacter cloacae (n = 19), Enterobacter asburiae (n = 1), Enterobacter bugandensis (n = 4), Enterobacter hormaeche (n = 5), Enterococcus faecium (n = 8): Enterococcus gallinarum (n = 3), Enterococcus hirae (n = 2), Enterococcus durans (n = 2), Staphylococcus hominis (n = 4), Staphylococcus haemolyticus (n = 3), Staphylococcus warneri (n = 2), Staphylococcus sciuri (n = 6), S. epidermidis (n = 8)

Fig. 4figure 4figure 4

Frequency and distribution of bacterial isolates from the total number of bacteria isolated at each hospital A total identified bacteria at each site, B Gram-negative isolates and C Gram-positive isolates. DTCSH Debre Tabor Comprehensive Specialized Hospital, HUCSH Hawassa University Comprehensive Specialized Hospital, JUTSH Jimma University Teaching Specialized Hospital, TASH Tikur Anbessa Specialized Hospital, n number of bacterial isolates

Antibiotic resistance pattern of SSI bacterial isolates

The predominant isolate from Gram-positives, S. aureus, revealed a high level of resistance toward penicillin 90.1%, and ampicillin 76.5%, while 7.8%, 10.6%, and 12.4% of the isolates were resistant to clindamycin, chloramphenicol, and gentamicin respectively but 100% of S. aureus were sensitive to vancomycin (Table 3). All isolates of S. aureus showed multiple drug resistance (resistance to two or more drugs).

Table 3 Antimicrobial resistance pattern of Gram-positive bacteria isolated from patients diagnosed with surgical site infection in Ethiopia: a multicenter prospective cross-sectional study 2022

Cefoxitin, which is a surrogate marker of methicillin, showed 22.7% resistance against S. aureus. Enterococcus species showed 70.4% resistance to ampicillin and 66.7% to erythromycin. Table 3 shows the AMR pattern of Gram-positive bacteria.

The Enterobacteriaceae showed high resistance toward ampicillin (93.2%), ceftriaxone (90.5%), cefuroxime (88.7%), aztreonam (82.9%), ceftazidime (80.6%), cefepime (77%), ampicillin-sulbactam (76.1%), trimethoprim-sulfamethoxazole (77.5%), tetracycline (72.5%), amoxicillin-clavulanic acid (71.2%) (Table 4).

Table 4 Antibiotics resistance patterns of Gram-negative bacteria isolates among patients with surgical site infection in Ethiopia: a multicenter prospective cross-sectional study 2022

Low resistance frequency of Enterobacteriaceae was detected for amikacin (24.3%), imipenem (20.3%), meropenem (17.6%), and ertapenem (32.9%) (Table 4).

The resistance of Enterobacteriaceae to meropenem and imipenem was (11.6%,18.6%), (18%, 22.9%), (12.2%,13.5%) and (26.9%,25%) at DTCSH, HUCSH, JUTSH, and TASH, respectively (Fig. 5A).

Fig. 5figure 5

Frequency of antibiotic resistance at four hospitals; A Enterobacteriaceae B Acinetobacter species C Pseudomonas species. The percentage represents the numbers of resistant isolates, out of the total number of isolates at all hospitals. AMP ampicillin, AMC amoxicillin/clavulanate, AK amikacin, SXT trimethoprim-sulfamethoxazole, C chloramphenicol, CAZ ceftazidime, CTX cefotaxime, CRO ceftriaxone, CXM cefuroxime, CIP ciprofloxacin, CN gentamicin, TE tetracycline, ATM aztreonam, SAM ampicillin-sulbactam, FEP cefepime, IMP Impemene, MEM meropeneme, ET Ertapeneme, DTCSH Debre Tabor Comprehensive Specialized Hospital, HUCSH Hawassa University Comprehensive Specialized Hospital, JUTSH Jimma University Teaching Specialized Hospital, TASH Tikur Anbessa Specialized Hospital

The predominant isolate, E. coli (n = 102) revealed a high level of resistance to ampicillin (94.6%), ceftriaxone (99%), cefotaxime (93.8), ceftazidime (79.4%), cefepime (77%), cefuroxime (73.5%), ampicillin-sulbactam (72%), trimethoprim-sulfamethoxazole (71.5%), tetracycline (70.6%), and low-level resistance to gentamicin (57.8%), chloramphenicol (41.2%), ertapenem (24.5), imipenem (11.6%), amikacin (10.8%), meropenem (9.8).

K. pneumoniae (n = 48) were resistant to ampicillin (100%), ceftriaxone (100%), cefotaxime (93.8%), amoxicillin-clavulanic acid (91.7%), ceftazidime (88.5%), cefepime (81.2%), cefuroxime (77.1%), tetracycline (66.7%), ertapenem (43.8%), meropenem (41.7%), amikacin (33.3%), imipenem (29.2%). Amikacin and meropenem were 100% effective against all of the isolates of Klebsiella variicola and Proteus mirabilis. In the non-fermenter group, A. baumannii showed the highest resistance to cefotaxime (95.3%), ertapenem (92.1%), ceftazidime (89.5%), gentamicin (86.8%), cefepime (84.2%), meropenem (84.2%), and SXT (81.4%). In addition, A. baumannii has lower-level resistance to imipenem (65.9%) and ampicillin-sulbactam (63.1%) (Table 4). The resistance frequency of Acinetobacter species to meropenem at DRH, HUCSH, JUSTH, and TASH was 75%, 83.3%, 42.8%, and 46.2%, respectively (Fig. 3B). P. aeruginosa showed minimal resistance to ceftazidime (66.7%), cefepime (55.5%), gentamicin (47.8%), ciprofloxacin (22.2%), and amikacin (10.5%) (Table 4). In addition, 100% and 94.5% of Pseudomonas species were sensitive to meropenem and imipenem, respectively (Table 4, Fig. 5C).

Multidrug resistance

The overall Multidrug resistance (MDR) to three or more antibiotics was observed in 100% of S. aureus (Table 3) and 93.3% Enterobacteriaceae (Table 4). Enterobacteriaceae that showed MDR to eight (R-9), nine (R-10) and ten (R- ≥ 11) antibiotics from different groups had a frequency of 6.3%, 6.7%, and 64.9%, respectively. Only 0.5% Enterobacteriaceae showed zero resistance (R-0) to all antibiotic classes tested, whereas 3.1% Enterobacteriaceae showed resistance to one antibiotic (R-1) class. For Enterobacteriaceae, the MDR frequency at DTCSH, HUCSH, JUSTH, and TASH was 84.5%, 96.5%, 97.3%, and 94%, respectively (Fig. 6A). E. coli, K. pneumoniae, E. cloacae, S. dysenteriae, K. variicola, and P. mirabilis showed an overall MDR frequency of 96.1%, 95.9%, 79.3%, 82%, 100%, and 100%, respectively. The overall MDR frequency of A. baumannii and P. aeruginosa was 95% and 77.8%, respectively. The MDR frequency for Acinetobacter species was 73% at DTCSH, 83.3% at HUCSH, 100% at JUTSH, and 100% at TASH (Fig. 4B). On the other hand, MDR frequency for Pseudomonas species was 66.7%, 66.7%, 83.3% and 50% at DTCSH, HUCSH, and JUSTH and TASH, respectively (Fig. 6C).

Fig. 6figure 6

Frequency of multidrug resistance at four hospitals. A Enterobacteriaceae B Acinetobacter species C Pseudomonas species. Percentages represent the number of resistant isolates out of the total number of isolates at each hospital. Debre Tabor Comprehensive Specialized Hospital (DTCSH), HUCSH Hawassa University Comprehensive Specialized Hospital, and Jimma University Teaching Specialized Hospital (JUTH) and Tikur Anbessa Specialized Hospital (TASH), MDR multidrug resistance

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