Menoufia Medical Journal

: 2017  |  Volume : 30  |  Issue : 4  |  Page : 1005--1013

Surgical site infections: Problem of multidrug-resistant bacteria

Wafaa A Zahran1, Ashraf A Zein-Eldeen1, Sanaa S Hamam2, Mona S Elsayed Sabal1,  
1 Department of Microbiology, Faculty of Medicine, Menoufia University, Ashmoun, Menoufia Governorate, Egypt
2 Department of General Surgery, Faculty of Medicine, Menoufia University, Ashmoun, Menoufia Governorate, Egypt

Correspondence Address:
Mona S Elsayed Sabal
Department of Microbiology, Faculty of Medicine, Menoufia University, Ashmoun, Menoufia Governorate


Objectives The present study aimed (a) to determine the prevalence and risk factors of surgical site infections (SSIs) at Menoufia University Hospitals; (b) to determine bacterial pathogens and their antimicrobial susceptibility patterns frequently causing SSIs; (c) to determine the prevalence of multidrug-resistant (MDR) bacteria; and (d) to assess infection control practices related to surgeries. Background SSI is the most surveyed and frequent type of healthcare-associated infection. A high prevalence of MDR strains has been observed in patients with SSIs. Patients and methods This study involved 148 patients who were admitted and chosen randomly from the General Surgery and Orthopedics Departments of Menoufia University Hospitals. Isolated organisms and antimicrobial susceptibility were identified. Detection of and phenotypic confirmation of MDR strains were carried out according to Clinical and Laboratory Standards Institute guidelines. Correlation between compliance rate of the surgical team to infection control measures in operating theater and SSI rate was determined. Results Prevalence of SSI was found to be 67.6%. The most common type of operative wounds were contaminated wounds and the most common wound infections were superficial wounds. The most frequently isolated species was Staphylococcus aureus (27.4%). Methicillin resistance was detected in S. aureus and coagulase-negative staphylococci by 88.3 and 62.5%, respectively. Extended spectrum β-lactamases were detected in 65.1% of Enterobacteriaceae isolates and metallo-β-lactamases in 73% of Gram-negative isolates. MDR isolates were detected in 37.2%. Furthermore, a reverse correlation between compliance rate and infection rate was detected. Conclusion In our study, there was a high prevalence of SSI and great problem of MDR bacteria with reflected difficulty in managing SSIs. Focused efforts should be directed to support infection control strategies.

How to cite this article:
Zahran WA, Zein-Eldeen AA, Hamam SS, Elsayed Sabal MS. Surgical site infections: Problem of multidrug-resistant bacteria.Menoufia Med J 2017;30:1005-1013

How to cite this URL:
Zahran WA, Zein-Eldeen AA, Hamam SS, Elsayed Sabal MS. Surgical site infections: Problem of multidrug-resistant bacteria. Menoufia Med J [serial online] 2017 [cited 2020 Apr 1 ];30:1005-1013
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Full Text


Healthcare-associated infections (HAIs) are acquired by patients while receiving care in healthcare facilities and represent the most frequent adverse events affecting patients' safety worldwide. Of every 100 hospitalized patients at any given time, seven in developed and 15 in developing countries will acquire at least one HAI. The endemic burden of HAI is also significantly (at least 2–3 times) higher in low-income and middle-income countries than in high-income nations, particularly in patients admitted to ICUs and neonates[1].

A recent study by the WHO shows that surgical site infection (SSI) is the most surveyed and frequent type of HAI in low-income and middle-income countries and affects up to one-third of patients who have undergone a surgical procedure. Although SSI incidence is lower in high-income countries, it remains the second most frequent type of HAI in Europe and the USA[1].

There are three different types of SSIs defined by the Centers for Disease Control and Prevention: superficial infections, deep incisional infections, and infections involving organs or body spaces. The degree of surgical site contamination at the time of surgery influences the probability of SSI. According to the presence and degree of contamination, wounds can be classified as clean, clean contaminated wounds, contaminated wounds, and dirty or infected wounds[2].

Staphylococcus aureus is the most commonly isolated organism in SSI, accounting for 15–20% of SSI occurring in hospitals; other organisms regularly isolated from SSIs include coagulase-negative staphylococci (CoNS), Enterococcus spp., and Escherichia coli, Pseudomonas aeruginosa, and Enterobacter spp. Methicillin-resistant Staphylococcus aureus (MRSA) is an increasingly important pathogen that causes more than 50% of S. aureus HAIs in the USA and Europe, and presents a challenge to treatment due to multiple antibiotic resistance[2].

Risk factors for SSI are typically separated into patient-related (preoperative), procedure-related (perioperative), and postoperative categories. In general, patient-related risk factors for the development of SSI can be categorized as either unmodifiable or modifiable. The most prominent unmodifiable risk factor is age. Modifiable patient-related risk factors include poorly controlled diabetes mellitus, obesity, tobacco use, use of immunosuppressive medications, and length of preoperative hospitalization. Procedure-related risk factors include wound class, length of surgery, shaving of hair, hypoxia, and hypothermia[3].

Strategies for the prevention of SSIs are based both on reducing the risk for bacterial contamination and improving the patient's defenses against infection. This requires a 'bundle' approach through preoperative, perioperative, and postoperative strategies. Preoperative strategies focus on controlling patient-related risk factors, for example, smoking cessation, controlling blood glucose level, decreasing body weight, and appropriate patient's skin antisepsis, and appropriate hand/forearm antisepsis for the surgical team. Perioperative strategies depend on good surgical technique, for example, maintenance of hemostasis, removal of devitalized tissue and foreign bodies, and elimination of dead space at the surgical site, and on aseptic precautions, for example, use of gloves, facemasks, caps, gowns, and sterile instruments. The Centers for Disease Control and Prevention guidelines recommended that incisions that have been closed by primary intention should be protected by sterile dressings for 24–48 h, and that personnel should use sterile technique when changing dressings on any kind of skin incision. Surveillance of SSIs, and reporting appropriate data back to surgeons, has been shown to be effective components of strategies to reduce SSI risk[4].

Despite the new antibiotics available today, SSI still remains a threat due to secondary bacterial contamination and widespread use of prophylactic antibiotics that lead to emergence of multidrug-resistant (MDR) bacteria. Over the past decade, Gram-positive bacteria, such as MRSA and vancomycin-resistant enterococci have attracted attention in the battle against MDR microorganisms. In addition, MDR Gram-negative bacilli as extended spectrum-β-lactamases (ESBL)-producing Enterobacteriaceae and metallo-β-lactamases (MBLs) have become a growing problem[5].

Vancomycin and teicoplanin are glycopeptide antibiotics used to treat MRSA infections. Linezolid, quinupristin/dalfopristin, daptomycin, ceftaroline, and tigecycline are used to treat infections of higher severity that do not respond to vancomycin. The therapeutic options for ESBLs-producing organisms are very limited. ESBLs confer on them the ability to be resistant to most β-lactam antibiotics except cephamycins and carbapenems. In addition, the plasmids bearing genes-encoding ESBLs frequently also carry genes-encoding resistance to other antimicrobial agents, such as aminoglycosides, trimethoprim, sulfonamides, tetracyclines, and chloramphenicol. The number of antimicrobial agents reliably effective against these often MDR organisms is very limited. Cefepime, colistin (polymyxin E), tigecycline, and fosfomycin may be options under certain circumstances. Tigecycline may have activity against some carbapenemase-producing organisms[5].

 Patients and Methods

This study was carried out during the period from February 2016 to November 2016. It included 148 patients who were chosen randomly from those who were admitted for surgery in General Surgery and Orthopedic Departments of Menoufia University hospitals. The study protocol was approved by the local ethics committee of the Menoufia University. All subjects gave written informed consent before inclusion into the study. Patient's personal history was taken, as name, age, sex, occupation, socioeconomic status, residence, presence of comorbidities (e.g., diabetes, obesity, or immunosuppressive disorders). Furthermore, patient's operation data as type of surgery (emergent or elective), type of wound (clean, clean contaminated, contaminated, or dirty), use of antimicrobial prophylaxis, length of the procedure, presence of foreign material in the surgical site (e.g., drainage), and length of postoperative stay were recorded.

The specimens collected were wound swabs by dry sterile cotton tipped swabs or aspirated pus by sterile disposable syringes from the surgical wounds. The specimens were processed according to standard microbiological methods. Antimicrobial susceptibility was determined by using the disk-diffusion method and results were interpreted according to the guidelines of the Clinical and Laboratory Standard Institute. S. aureus strains with cefoxitin (30 μg) disk-diffusion zones of 21 mm or less were reported as oxacillin resistant. Those with cefoxitin zones of at least 22 were reported as oxacillin susceptible. CoNS with cefoxitn disk-diffusion zones of 24 mm or less were reported as oxacillin resistant. Those with cefoxitin zones of at least 25 were reported as oxacillin susceptible. All staphylococcal isolates were tested by using the vancomycin minimum inhibitory concentration method[6].

ESBLs producers were screened by using the disk-diffusion test by using ceftazidime (30 μg), cefotaxime (30 μg), ceftriaxone (30 μg), and aztreonam (30 μg) with resulted inhibition zone diameters [ceftazidime (30 μg) ≤22 mm, cefotaxime (30 μg) ≤27 mm, ceftriaxone (30 μg) ≤25 mm, and aztreonem (30 μg) ≤27 mm were considered resistant]. They were confirmed by using the combined disk-diffusion test by using ceftazidime (30 μg) and ceftazidime/clavulanic acid (30/10 μg). Organism was considered as ESBL producer if there was at least 5 mm increase in the diameter of ceftazidime/clavulanic acid disk compared with ceftazidime disk alone[6].

MBLs producers were screened by using the disk-diffusion method by using imipenem disk (10 μg) with resulted inhibition zone diameters of 19 mm or less were considered resistant. They were confirmed by using the imipenem/EDTA combined disk test by using the imipenem and imipenem plus EDTA disks. If the increase in inhibition zone with the imipenem plus EDTA disk was 7 mm or more than that of imipenem disk alone, it was considered as MBL positive[6].

Infection control practice assessment

Establishment and implementation of infection control surveillance system and scoring according to Infection Control and Nurses Association (2004): it includes a sterile dressing of wounds and the use of operating theater safety checklist to assess safety measures in operating roomsProvision of training program in infection control principles to the surgical team (doctors and nurses of operation room)Assessment of post-training compliance was attained by using the same scoring system of Infection Control and Nurse Association (2004) audit tools for monitoring infection control standardsCorrelation between SSI rate and compliance rate of medical team in operation theater was determined before training and after training.


The prevalence of SSI among studied patients was 67.6% [Figure 1]. About 69% of patients with SSI belonged to the age group 40–75 years old, 54% were from rural areas, and 74% were smokers. Regarding comorbid conditions, 75% of patients with SSI were receiving immunosuppressive drugs, 54% were diabetics, and 61% were obese. The majority of the patients with SSI received antimicrobial prophylaxis (91%), 80% had drain at surgical site, the duration of surgery extended more than 2 h in 87% of SSI cases, and 60% stayed more than 2 weeks in the hospital [Table 1].{Table 1}{Figure 1}

Regarding type of operative wound, 57% of studied patients with SSI had contaminated wounds, 21% had dirty wounds, 12% had clean, and 10% had clean contaminated wounds [Figure 2]. Regarding type of surgical wound infection, 51% of patients had superficial SSI while 32% of them had deep wound infection, and only 17% had organ/space wound infection [Figure 3].{Figure 2}{Figure 3}

The most frequently isolated species from patients with SSI were S. aureus (27.4%) followed by CoNS (19.4%), Klebseilla pneumoniae) 12.1%), E. coli and Enterobacter spp. (each 9.7%), Proteus mirabilis and P. aeruginosa (each 5.62%), Citrobacter spp. and Acinetobacter spp. (each 4.03%), and lastly, anerobic isolates (two Gram-positive cocci and one Gram-negative coccus) (2.4%) [Figure 4].{Figure 4}

Both S. aureus and CoNS isolates showed 100% resistance to penicillin and ampicillin. Both showed 100 and 91.7% resistance to oxacillin, respectively. Sensitivity to new therapeutic drugs was 88.2 and 87.5% for linezolid, respectively, and 94.1 and 91.7% for teicoplanin, respectively [Table 2].{Table 2}

MRSA was detected in 88.2% of S. aureus isolates, whereas methicillin-resistant coagulase-negative staphylococci (MRCoNS) was detected in 62.5% of CoNS. S. aureus and CoNS were sensitive to vancomycin by 55.8 and 50%, respectively; 14.7 and 12.5% were intermediately resistant and 29.4 and 37.5% were completely resistant to vancomycin, respectively [Table 3].{Table 3}

Enterobacteriaceae isolates showed 100% resistance to ceftazidime, cefepime, cefotaxime, ceftriaxone, cefoxitin, aztreonam, and chloramphenicol. Resistance to carbapenems was 88.2% to imipenem and 82.4% to ertapenem and meropenem. Sensitivity to the new therapeutic drug tigecycline was 96.1% [Table 4].{Table 4}

ESBLs were detected in 65.1% of Enterobacteriaceae isolates [Table 5] and MBLs in 73% of Gram-negative isolates [Table 6].{Table 5}{Table 6}

From all isolates, MDR and pandrug-resistant isolates (45/121; 37.2% for each), were more common compared with extreme drug-resistant isolates, which represented only 25.6% (31/121) [Figure 5].{Figure 5}

Regarding infection control assessment, there was a reverse correlation between SSI rate and compliance rate of surgical team in the operating theater to infection control practice regarding pretraining and post-training assessment [Table 7].{Table 7}


The present study revealed that the prevalence of SSI among studied patients was 67.6%. This was in agreement with the study carried out by Bhatt et al.[7], where 62.4% of samples showed positive growth, and in contrast to Hafez et al.[8] and Labib et al.[9] who reported that rate of SSI to be 17 and 9%, respectively, which is much lower than that reported in the current study. The lower rates noted in these studies can be attributed to standardized SSI prevention protocols, strict operation theater cleaning, and disinfection procedures, and a strict infection prevention and control program, which includes intensive training, surveillance, data dissemination, and feedback.

In the present study, 69% of patients with SSIs belonged to the age group 40–75 years old, which was in agreement with Wu et al.[10] who reported a predominance of SSI in the older age group. On the other hand, Malinzak et al.[11]have determined predominance of SSI in a younger age group. This can be explained by the difference in the type of operations performed in each study population and presence of other comorbid conditions in old age that predispose to infection. In the present study, 58% of patients with SSI were male patients with no significant difference between patients with and without SSI. This was in agreement with Labib et al.[9] who reported that sex is not a risk factor for infection after operation. In contrast, another study by Dale et al.[12]showed increased incidence of infection with male sex. The reason may be that male patients are highly exposed to external environment than do female patients.

Moreover, 74% of SSI patients were smokers. This was in agreement with Sorensen et al.[13]but in disagreement with Labib et al.[9]. As for comorbid conditions, most of the patients who had SSI were obese (61%) and this was in agreement with a study conducted by Labib et al.[9] whose results of SSI in obese patients were 65%.

SSI was higher in diabetic patients (54%). This was in agreement with Neumayer et al.[14]and Latham et al.[15]who found a higher incidence of SSI among diabetic patients, and in contrast to Maksimovic et al.[16]who did not reveal significant association between diabetes mellitus and SSI. A possible explanation of higher incidence in diabetic patients may be related to a deficiency of vasoactive neuropeptides in patients with neuropathy, which may impair normal soft tissue and osseous healing[17]. In this study, malignancy and immunosuppressive drugs increased the risk for SSI, a finding that was in agreement with those reported by Biondo et al.[18]; they reported malignancy was one of the predictive variables for increasing SSI risk. The incidence of SSI in emergency surgery cases was higher than that in elective surgery cases (65 vs. 35%, respectively) and this result was in agreement with Mulu et al.[19]. In our study, 80% patients had drains in surgical site, which was in agreement with Manian[20]. In the present study, 91% received antimicrobial prophylaxis with no significant difference between patients with SSI and those without SSI. This was in contrast to the study done by Labib et al.[9] that reported that the administration of prophylactic antibiotic half an hour before the operation would bring about the best results and the lowest SSI. In the present study, contaminated surgical wounds were the most frequent surgical incisions to increase risk to develop SSI by 57%, followed by dirty wound (21%). Similar findings were reported by Labib et al.[9] and Hafez et al.[8] in Egypt. Frequencies of SSI according to type were 51, 32, and 17% in superficial, deep, and organ/space, respectively. This finding was in agreement with the study done by Labib et al.[9] in Egypt that revealed that the frequencies of SSI were 62, 36, and 2%, respectively. However, the results of our study were in contrast to a study done in Egypt by Afifi and Baghagho[21] in which majority of the patients (70%) developed deep infection.

The predominant bacteria isolated from wound infection were Gram-positive S. aureus (27.4%), followed by CoNS (19.4%), Gram-negative K. pneumoniae (12.2%), E. coli and Enterobacter spp. (each 9.7%), P. mirabilis and P. aeruginosa (each 5.6%), Citrobacter spp. and Acinetobacter spp. (each 4.0%), and lastly, anerobic organism (2.4%). As reported by the present study, S. aureus (27.4%) was the predominant organism. Similar finding was found in the study by Sonawane et al.[22]who reported that S. aureus was the predominant organism (29.26%) and Mulu et al.[19]who showed that S. aureus was the most common isolate.

In the present study 88.3% of S. aureus isolates were MRSA, which was in agreement with the findings by Mama et al.[23]and Etok et al.[24]where 83 and 74.2% isolates, respectively, were MRSA. But this was lower than the100% resistant S. aureus reported by Yishak et al.[25]. About 62.5% of CoNS isolates in this study were MRCoNS; this was in agreement with the results of Mama et al.[24]who found that 60% of CoNS isolates were MRCoNS, and with the higher rates of MRCoNS (80%) recorded by Yishak et al.[25]. In this study, 44.1% of S. aureus and 50% of CoNS were completely or intermediately resistant to vancomycin by using the MIC tube dilution confirmatory method. Similar results were reported by Etok et al.[24]in Italy (40 and 47.2%, respectively). Lower results were obtained by Mehdinejad et al.[26]as16.4% of isolates were vancomycin-resistant S. aureus.

About 100% of Enterobacteriaceae isolated in this study were ESBL producers, as shown by using the disk-diffusion test, compared with 65.1%, as shown by using the confirmatory combined disk test. These results were in agreement with Shittu et al.[27] who found 82% ESBL producers by using the disk-diffusion test compared with 58% by using the confirmatory combined disk test. About 92.1% of Gram-negative bacilli isolated in this study were MBL producers, as shown by using the disk-diffusion test, compared with 73%, as shown by using the confirmatory combined disk test. This was in agreement with Anoar et al.[28]who revealed 70% of MBL by using the imipenem/EDTA synergy test.

Out of 121 isolates, the majority of the isolated organisms were MDR and pandrug-resistant strains (each 37.2%), whereas extreme drug-resistant strains accounted for 25.6%. This was in agreement with Vinodkumar et al.[29].

In the present study, we assessed compliance of healthcare workers to infection control measures related to surgeries. In the operating theater, compliance rate of surgical team to infection control practice was assessed before and after training. The assessment revealed that the infection rate decreased after training of surgical team with no significant statistical difference between pretraining and post-training assessment. Another study by Mortada and Zalat[30]showed adequate compliance to standard precautions (57.5%) in the operation room.

To our knowledge, this is the first study carried out in Menoufia University Hospitals on the issue of correlation between compliance of surgical team and SSI rate.


In our study, there was high prevalence of SSI and a great problem of MDR bacteria with reflected difficulty in managing SSIs. The high incidence of β-lactamases production due to multiple mechanisms in SSI is alarming and urgent action needs to be taken. Training of surgical team toward implementation of infection control practice has been shown to lead to a significantly decreased SSI rate. Great efforts should be directed to support infection control strategies to combat this problem.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.


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