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 Table of Contents  
Year : 2019  |  Volume : 21  |  Issue : 1  |  Page : 69-74

Antimicrobial susceptibility profile of surgical site infection isolates from a tertiary care center in West India

1 Department of Microbiology, Army Hospital (R and R), New Delhi, India
2 Officer Commanding, SHO, Jalandhar, Punjab, India
3 Research Associate, UPMC Pinnacle, Harrisburg, PA, USA
4 Department of Surgery, Military Hospital (Bathinda), Punjab, India

Date of Submission06-May-2018
Date of Acceptance06-Dec-2018
Date of Web Publication19-Jun-2019

Correspondence Address:
Maj Gurpreet Singh Bhalla
Department of Microbiology, Army Hospital (R and R), New Delhi - 110 010
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmms.jmms_32_18

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Introduction: Surgical site infection (SSI) is an infection that develops within 30 days after a surgical procedure or 1 year if an implant is placed and the infection appears to be related to surgery. SSIs are associated with complications such as increased readmission rates, increased hospital length of stay, increased overall costs, and increased morbidity and mortality rates. There is a dearth of data from India regarding SSI and susceptibility profile of the isolates. Therefore, this study was undertaken to determine the rate of SSIs, and the antimicrobial susceptibility profile of the isolates was obtained at a tertiary care center. Materials and Methods: A cross-sectional study was conducted for 2 years where all patients who underwent a surgical procedure were followed up and evaluated if they showed features of SSI. Requisite samples were taken and processed. Biochemical tests and susceptibility testing identified the isolated organisms and reporting was done as per the Clinical Laboratory Standards Institution guidelines. Results: Of 7675 surgeries, 303 developed SSI. The most common isolate was Staphylococcus aureus followed by Gram-negative bacteria. Antimicrobial profile of Gram-positive isolates revealed a high degree of resistance to methicillin and high susceptibility to vancomycin, teicoplanin, and linezolid; whereas among Gram-negative isolates, both Enterobacteriaceae and nonfermenters showed a high degree of resistance to various drugs including the cephalosporins. Susceptibility was seen for carbapenems and polymyxins. Conclusion: A close collaboration between microbiologists and surgeons is required. Strict hand hygiene and antimicrobial stewardship protocols need to be followed to prevent and reduce SSI.

Keywords: Antibiotic stewardship, antimicrobial resistance, infection control, surgical site infection

How to cite this article:
Bhalla GS, Grover N, Singh G, Sarao MS, Mishra D. Antimicrobial susceptibility profile of surgical site infection isolates from a tertiary care center in West India. J Mar Med Soc 2019;21:69-74

How to cite this URL:
Bhalla GS, Grover N, Singh G, Sarao MS, Mishra D. Antimicrobial susceptibility profile of surgical site infection isolates from a tertiary care center in West India. J Mar Med Soc [serial online] 2019 [cited 2022 Aug 13];21:69-74. Available from: https://www.marinemedicalsociety.in/text.asp?2019/21/1/69/260660

  Introduction Top

Surgical site infection (SSI) is an infection that develops within 30 days after a surgical procedure or 1 year if an implant is placed and the infection appears to be related to surgery.[1],[2] SSI is divided into three types, depending on the depth of infection penetration into the wounds: superficial incisional, deep incisional, and organ/space.[3] Even though every surgical site is contaminated with bacteria by the end of the procedure, few become clinically infected depending on the interplay of inoculum and virulence of the pathogen, adjuvant effects of microenvironment such as ischemia or foreign body and innate and acquired host defenses.

Infectious agents may cause SSI by from endogenous or exogenous sources. Endogenous sources are body sites, such as the skin, nose, mouth, gastrointestinal tract, or vagina that are usually inhabited by microorganisms. Exogenous sources are those external to the patient, such as patient care personnel, visitors, patient care equipment, medical devices, or the health-care environment.

SSI contributes to approximately 20% of (health-care-associated infection) preceded by 36% due to urinary tract infection (UTI) and followed by pneumonia and bloodstream infections (BSI), both at 11%.[4],[5] However, the highest mortality is associated with hospital-acquired pneumonia, followed by BSI, UTI, and SSI. The occurrence of SSI following surgery depends on the type of wound (clean, clean-contaminated, contaminated or dirty), immune status of the host, presence or absence of a foreign body/prosthesis, and core body temperature fluctuations. Health-care workers should identify the patients with risk factors amenable to intervention early and strive to minimize the risk of wound contamination in all surgical cases as well as to support host defenses throughout the continuum of care. SSIs have been associated with complications such as increased readmission rates, increased hospital length of stay, enhanced overall costs, and increased morbidity and mortality rates.[6]

Surveillance data suggest that the types of causative organisms associated with SSI have not significantly changed over the past 10–15 years; however, the proportion of different types of causative organisms has changed. Antimicrobial-resistant organisms are causing an increasing proportion of SSIs, and there has been a rise in the number of infections caused by atypical bacterial and fungal organisms. These changing proportions have been attributed to the increasing acuity of surgical patients, the increase in the number of immunocompromised patients, and the increasing use of broad-spectrum antibiotics.[7]

Due to the paucity of data from India, this study was undertaken to determine the rate of SSIs and the antimicrobial susceptibility profile of the isolates obtained at a tertiary care center, which would help to institute better prophylactic measures and appropriate, timely and accurate therapeutic measures to reduce the cost of treatment and morbidity of the disease.

  Materials and Methods Top

A cross-sectional study was performed by analyzing 303 consecutive, nonrepeat clinical samples of postoperative SSI cases from all surgical specialties (after obtaining informed consent and clearance from the Institutional Ethics Committee) from our center for two consecutive years. Patients were actively followed up, and relevant samples (pus, pus swab, pus and explanted mesh, and tissue margin scrapings) from postoperative SSI cases were collected aseptically. Samples were examined by Gram stain and Ziehl–Neelsen (ZN) stain. All the samples were inoculated on blood agar, MacConkey agar, and also on Lowenstein–Jensen medium (for the isolation and identification[8] of mycobacteria). Final identification of the isolates was made by interpretation of direct Gram's stain or ZN stain from sample, colony morphology, and biochemical tests from the isolates. Antimicrobial susceptibility testing was performed, and the results were reported as per the Clinical Laboratory Standards Institution (CLSI) guidelines.[9] Phenotypic methods were used to detect and report methicillin-resistant Staphylococcus aureus, extended-spectrum beta-lactamases (ESBL), and carbapenemase production in Gram-negative bacteria as per the CLSI guidelines.[9]

The data were tabulated and statistically analyzed using SPSS software Version 20.0. (IBM Corp., Armonk, NY, USA). Pearson's Chi-square test was used to test the strength of association between the variables with P < 0.05 taken as statistically significant.

  Results Top

Of 7675 multispecialty surgeries performed in the study period, 303 were reported as SSI, which translates to the overall SSI rate at our center to be 3.95%.

Age group-wise distribution of SSI is shown in [Table 1]. Gender-wise distribution of SSI is shown in [Table 2].
Table 1: Age group-wise distribution of surgical site infection

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Table 2: Gender-wise distribution of surgical site infection

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In our study population, 30 (9.9%) patients underwent laparoscopic surgery and 273 (90.1%) had open surgery. Age, gender, and type of surgery were not statistically significant variables in the development of SSI (P > 0.05).

The most frequently received sample was pus swab (56.44%) followed by pus (39.93%), pus and explanted mesh (3.30%), and tissue margin scrapings (0.33%). Test of significance for the best sample for isolation of pathogens could not be applied as one of the cells included zero.

Implants/prostheses were placed in 97 (32%) of the cases and were a significant factor in the development of SSI (P < 0.05) following surgery.

Organisms isolated in the present study are listed in [Table 3]. A noteworthy finding is 66 (21.78%) of samples were culture negative despite the clinical diagnosis of SSI.
Table 3: Distribution of various organisms isolated (n=303)

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Antimicrobial susceptibility patterns of isolates belonging to Enterobacteriaceae family (n = 82), nonfermenter Gram-negative Bacilli (n = 48), genus Staphylococcus (n = 68), and genus Enterococcus (n = 4) are depicted in [Figure 1], [Figure 2], [Figure 3], [Figure 4], respectively.
Figure 1: Antimicrobial susceptibility of isolates belonging to the Enterobacteriaceae family (n = 82)

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Figure 2: Antimicrobial susceptibility of nonfermenter Gram-negative Bacilli (n = 48)

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Figure 3: Antimicrobial susceptibility of isolates belonging to the genus Staphylococcus (n = 68)

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Figure 4: Antimicrobial susceptibility of isolates belonging to the genus Enterococcus (n = 4)

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  Discussion Top

In the study period, a total of 7675 surgeries were performed, including elective and emergency procedures. During the study period, a total of 303 SSIs were reported and included in the study leading to an overall SSI rate of 3.95%. Our findings correlate with studies done in other Indian hospitals which reported an overall SSI rate ranging from 3.03% to 22.41%.[10],[11],[12],[13],[14]

The most frequent sample received was pus swab (56.44%) which was followed by pus (39.95%), pus and explanted mesh (3.30%), and tissue margin scrapings (0.33%). Of these, no growth was observed in 25.73% of pus swabs, 15.7% of pus, and 3% of pus with explanted mesh. These findings suggest that pus is a better sample for culture than a swab.

In corroboration with earlier studies, we also found that age group, gender, and type of surgery are not significant factors in the development of SSI following surgery. However, placement of implant or prosthesis is a significant factor for the same.

The most common cause of SSI per our study was S. aureus (20.46%) followed by E. coli (11.55%), nontuberculous mycobacteria (NTM) (10.9%), Klebsiella spp. (9.57%), Pseudomonas aeruginosa (8.58%), Acinetobacter baumannii (6.93%), and others (10.3%). Of the NTM, the most common was Mycobacterium fortuitum followed by Mycobacterium abscessus and Mycobacterium chelonae (published elsewhere).[15] Elgohari et al., in his Surveillance of Surgical Infections in NHS hospitals in England 2013–2014, also reported S. aureus (16%) as the most frequent species causing SSI.[16] He also reported an increasing trend of Enterobacteriaceae which accounted for 21% SSI in his study.

Of the samples collected from SSI in the present study, 21.78% were culture negative, which suggests other causes of SSI such as anaerobic organisms, Mycoplasma hominis, or Ureaplasma urealyticum which are not looked for routinely. Reddy,[17] in his work from Hyderabad, also reported that up to 30% SSI could be labeled as culture negative if the organisms as mentioned earlier are not looked for specifically. A limitation of the present study is that anaerobic organisms were not investigated which may have been a cause of culture-negative SSI.

The increasing reports of multidrug-resistant organisms being isolated from SSI are a cause for concern. More than 85% of the isolates belonging to Enterobacteriaceae family [Figure 1] were resistant to ampicillin, amoxicillin-clavulanic acid, piperacillin-tazobactam, and even the third-generation cephalosporins like ceftriaxone and were phenotypically ESBL producers. High degree (>50%) of resistance was also seen against fluoroquinolones, gentamicin, cotrimoxazole, and amikacin, thus precluding the use of all these drugs as prophylactic and therapeutic agents. Another alarming finding is that >20% of the isolates were resistant to carbapenems, and spread of these organisms or their resistance genes in and outside hospital environment is a cause of concern. Almost all isolates were susceptible to polymyxins. Various Indian and Southeast Asian workers have reported similar findings.[11],[12],[18],[19]

Nonfermenting Gram-negative Bacilli are ubiquitous and are notoriously multidrug resistant. In the present study [Figure 2], more than 65% of isolates were resistant to piperacillin-tazobactam, ceftazidime, cefepime, amikacin, gentamicin, and ciprofloxacin, and 58% were resistant to tobramycin. Only 58% were susceptible to imipenem, 75% to meropenem, and 88% to colistin. Injudicious use of antimicrobial agents may lead to such a pattern, and we recommend combination therapy when such pathogens are isolated along with meticulous wound care and barrier nursing precautions to avoid the spread of these bugs. Although Indian workers have reported similar findings,[11],[19] European workers reported a better susceptibility of >90% toward carbapenems.[20]

Organisms belonging to the genus Staphylococcus form the largest group of isolates from SSI in a majority of the studies. An increase in the number of drug-resistant isolates is a global problem. In the present study [Figure 3], 97% isolates were resistant to penicillin, and notably, 78% were cefoxitin (and therefore, methicillin) resistant. About 62% were resistant to erythromycin with 41% being resistant to clindamycin including inducible resistance. Isolates were moderately susceptible to quinolones and cotrimoxazole. All isolates were susceptible to linezolid and vancomycin with 100% susceptibility to teicoplanin.[19]

Four isolates of Enterococcus faecalis were isolated [Figure 4], and 100% resistance was seen against penicillin and ampicillin. All isolates were susceptible to linezolid, vancomycin, and teicoplanin. Two isolates of Candida spp. were also isolated, which were susceptible to amphotericin B, azoles, echinocandins, and flucytosine. The results about isolated NTM are under publication elsewhere.

Our findings reiterate those of previous workers[10],[11],[12],[21] except for those of a high degree of methicillin resistance in staphylococci.

The drug susceptibility findings of the present study show that antibiotics such as fluoroquinolones and third-generation cephalosporins would have minimal usefulness for the prophylaxis or treatment of infections caused by Enterobacteriaceae since most of the patients receive third-generation cephalosporins as prophylactic agents. Nonfermenters are reported to be highly resistant, and due to their ability to survive easily and form biofilms, infections caused by them are challenging to treat. Beta-lactam antibiotics would be poor choices as prophylactic/empirical therapy agents since a majority of staphylococcal strains are resistant to methicillin. It is known that perioperative prophylaxis can decrease the incidence of wound infection;[11],[12],[18],[22],[23],[24],[25] isolation of such multidrug-resistant strains is a cause of concern due to a limited repertoire of available antimicrobial agents.

  Conclusion Top

Based on our findings, we recommend a few protocols to be followed to prevent and reduce SSI, first – hand hygiene and thorough infection control protocol to reduce the spread of microbes and plasmid-mediated drug resistance, the second – antibiotic stewardship and tailor-made prophylactic policies based on local susceptibility data, the third – maintenance of the infrastructure of operation theater and wards, and finally – a close collaboration between microbiologists and surgeons.[25],[26],[27]

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Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2], [Table 3]

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