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 ~ Introduction
 ~ Methods
 ~ Results
 ~ Discussion
 ~ Conclusion
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  Table of Contents  
Year : 2020  |  Volume : 38  |  Issue : 3  |  Page : 344-350

Predominance of multidrug-resistant Gram-negative organisms as cause of surgical site infections at a private tertiary care hospital in Mumbai, India

Department of Infection Prevention and Control, Kokilaben Dhirubhai Ambani Hospital and Medical Research Institute, Mumbai, Maharashtra, India

Date of Submission24-Jun-2020
Date of Decision29-Jun-2020
Date of Acceptance20-Aug-2020
Date of Web Publication4-Nov-2020

Correspondence Address:
Dr. Tanu Singhal
Department of Infection Prevention and Control, Kokilaben Dhirubhai Ambani Hospital and Medical Research Institute, Mumbai, Maharashtra
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmm.IJMM_20_284

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 ~ Abstract 

Background: This study aims to study the incidence, microbial aetiology and antimicrobial susceptibility of surgical site infections (SSIs) at a private tertiary care hospital in Mumbai, India, and compare it with previously published data from the same institute as well as literature. Methods: This is a prospective observational study done over 6 years (January 2013–December 2018) at a 750-bed private multi-specialty hospital in Mumbai, India, among all patients undergoing clean and clean-contaminated surgeries. Standard guidelines for preventing, diagnosing and classifying SSIs were followed. The incidence rates of SSI (overall and specialty specific), microbial aetiology and antibiotic susceptibility of SSI were calculated and expressed as percentages. Results: A total of 55,553 patients underwent clean and clean-contaminated surgeries during the study period. The overall SSI rate was 1.0% (555 cases). The SSI rate in clean surgeries was 0.97% and in clean-contaminated surgeries was 1.03%. Sixty-five per cent of SSIs were due to Gram-negative bacilli, 30% were due to Gram-positive cocci and 4% were due to Candida. Klebsiella pneumoniae (19%), Escherichia coli (17%), Pseudomonas aeruginosa (13%), Staphylococcus aureus(12%) and Enterococcus (10%) were the top five organisms. The overall susceptibility rate of the Gram-negative isolates to beta-lactam–beta-lactamase inhibitor combinations was 60% and carbapenems was 73%. The prevalence of methicillin resistance in S. aureus was 44% and coagulase-negative Staphylococcus was 84%. The crude mortality rate was 1%. Conclusions: Although the SSI rate is comparable to established international benchmarks, the predominance of multidrug-resistant Gram-negative organisms is a matter of serious concern.

Keywords: Gram-negative, India, surgical site infections

How to cite this article:
Shah S, Singhal T, Naik R, Thakkar P. Predominance of multidrug-resistant Gram-negative organisms as cause of surgical site infections at a private tertiary care hospital in Mumbai, India. Indian J Med Microbiol 2020;38:344-50

How to cite this URL:
Shah S, Singhal T, Naik R, Thakkar P. Predominance of multidrug-resistant Gram-negative organisms as cause of surgical site infections at a private tertiary care hospital in Mumbai, India. Indian J Med Microbiol [serial online] 2020 [cited 2021 Jan 25];38:344-50. Available from:

 ~ Introduction Top

Healthcare-associated infections (HCAI) are an important cause of increased morbidity, mortality, treatment costs, length of stay and antimicrobial resistance in low-and middle-income countries (LMIC).[1] The pooled incidence of HCAI in LMIC is around 10% with surgical site infections (SSIs) being the most common HCAI contributing to around 30% of all HCAI.[1] Approximately 10% of all patients undergoing surgery in LMIC develop SSI.[1] In contrast, the prevalence of SSI in developed countries ranges from 1.2 to 5%.[2] A large multicentric study by the International Nosocomial Infection Control Consortium which amalgamated data from multiple hospitals from 6 Indian cities reported the average SSI rate from India as 4.2%.[3] We previously reported the incidence of SSI in approximately 24,000 surgical procedures performed in our hospital from 2009 to 2013 as 1.6%.[4] The current study was conducted to study the temporal evolution in incidence rates, aetiology and antimicrobial susceptibility of SSIs.

 ~ Methods Top

The study was conducted in a private tertiary care hospital in Mumbai, India. The infection control bundle for preventing SSI is detailed in [Table 1]. In this prospective observational cohort study, all patients undergoing clean and clean-contaminated surgical procedures from January 2013 and December 2018 were included. The patients undergoing contaminated surgeries and dirty surgeries were excluded from the study. The study was approved by the institutional research and ethics committee vide letter number IEC Code: C-3/15/2018 dated 2 May 2018. Patient details recorded included age, sex, type of surgical procedure, presence of risk factors, modality of hair removal, receipt of chlorhexidine bath, type of surgery (clean/clean-contaminated), prophylactic antibiotic used, dose, time of antibiotic administration in relation to incision, duration of surgery and receipt of repeat dose if so indicated and duration of antibiotic therapy.
Table 1: Salient features if the hospital infection control policy to prevent surgical site infections

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Standard CDC criteria proposed in 1999 were used to define and classify SSI.[5] Stitch abscess was not included as SSI. Patients were monitored for 30 days following surgery, and those with implants were followed up for 1 year. The patients were followed up daily during hospital stay for SSI. The occurrence of any SSI in the post-discharge period was tracked by keeping record of all pus samples received by the microbiology laboratory, readmissions for wound debridement and calling telephonically a random sample of 10% of the patients who had undergone surgery at the end of the 30-day surveillance period. All specimens including pus, tissue and swabs from the surgical wounds were plated on 5% sheep blood agar and MacConkey agar. In addition, pus or tissue samples (not swabs) were also inoculated in aerobic blood culture bottles of the BacT Alert blood culture system from Biomerieux. After performing preliminary identification tests such as Gram stain, oxidase and catalase, identification and susceptibility testing were done by VITEK 2 from Biomerieux, France. ESBL detection was noted from VITEK 2. Colistin susceptibility testing was done using VITEK 2 till December 2017. From January 2018 onwards, microbroth dilution test, Mikrolatest, Erba, European Union, was used for colistin susceptibility testing. An increase in the incidence of SSI rate beyond 1% in the previous month triggered an audit of the operating room and compliance to the prevention bundle with feedback to those concerned and rectification of the gaps.

Outcomes studied included incidence rates of SSI, percentage compliance to the hospital prevention bundle, microbial aetiology and susceptibility of SSI as well as need for additional antibiotics/dressing/surgical debridement and mortality in patients with SSI.

 ~ Results Top

A total of 55,553 patients underwent clean and clean-contaminated surgeries during the study period. Five hundred and fifty-five patients developed SSI, translating into an overall SSI rate of 1.0% (95% confidence interval [CI]: 0.9%–1.1%). The SSI rate in clean surgeries was 0.97% (95% CI: 0.9%–1.1%) and in clean-contaminated surgeries was 1.03% (95% CI: 0.9%–1.2%). The yearly rate declined from 1.23% in 2013 to 0.94% in 2018; the trend in incidence rate of SSI for clean and clean-contaminated surgeries is depicted in [Figure 1]. [Table 2] depicts the SSI rate in various specialties. The highest rate was seen in coronary artery bypass graft surgeries in adults (3.7%). Overall, 66% of infections were superficial incisional type, 25% were deep incisional type and 9% were organ space type (prosthetic joint infections and meningitis). The variation in the annual distribution of types of SSI is depicted in [Figure 2]. The compliance to clipper use for hair removal and chlorhexidine bath was calculated on a monthly basis, and it varied from 90% to 95%. The compliance to hospital antibiotic policy as far as choice of the antibiotic, administration of the first dose within 60 min of surgical incision and repeating the antibiotic if surgery was prolonged for more than 4 h was more than 90%. However, the duration of antibiotic use following surgery varied from 2 to 7 days.
Figure 1: Year-wise incidence of surgical site infection of clean surgeries and clean-contaminated surgeries

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Table 2: Specialty-wise distribution of surgical site infection cases

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Figure 2: Year-wise segregation of type of surgical site infections in percentage

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A total of 612 isolates were obtained from 510 study patients. One hundred and seven patients had 2 or more isolates causing SSI. Microorganisms could not be isolated in 45 (8%) cases. The microbial aetiology of SSI is depicted in [Figure 3]; predominant being Gram-negative bacilli (GNB) (65%), followed by Gram-positive cocci (30%) and yeast in 4% of isolates. There has been no significant change in the type of microorganisms over the years. Klebsiella pneumoniae (19%), Escherichia coli (17%), Pseudomonas aeruginosa (13%), Staphylococcus aureus (12%) and Enterococcus (10%) were the top five organisms. Of the enterococcal isolates, 53% were Enterococcus faecalis and 47% were Enterococcus faecium. A total of 27 Candida species were isolated (Candida albicans [n = 15], Candida tropicalis [n = 7], Candida parapsilosis [n = 2] and one each Candida guilliermondii, Candida kefyr and Candida haemulonii). The single isolate of C. haemulonii was identified by VITEK in 2013 and was probably Candida auris. No non-tuberculous mycobacteria (NTM) infections were identified.
Figure 3: Microbial aetiology of surgical site infections (n = 612)

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The susceptibility of GNB isolates is depicted in [Table 3] and [Table 4]. The resistance in Enterobacteriaceae has not changed significantly through the years and average ESBL rates were 85%; susceptibility rates to beta-lactam–beta-lactamase inhibitor (BL-BLI) combinations were 57% and carbapenems 79% [Table 3]. Two isolates (K. pneumoniae and Enterobacter cloacae one each) were colistin resistant but susceptible to other antibiotics and treated accordingly successfully. The year-wise susceptibility of P. aeruginosa and Acinetobacter baumannii is depicted in [Table 4]a and [Table 4]b, respectively. The A. baumannii isolates though constituting only 4.4% of the total isolates showed very high rates of resistance to both BL-BLI and carbapenems. The overall susceptibility rate of the Gram-negative isolates to BL-BLI combinations was 60% and carbapenems was 73%.
Table 3: Year-wise and average sensitivity (in %) for Enterobacteriaceae*

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Forty-four per cent of S. aureus were methicillin resistant as against 84% of the CONS which were methicillin resistant. All the E. faecalis were vancomycin sensitive, but 4 (8.5%) of the E. faecium were vancomycin resistant. All the isolates of Candida were fluconazole susceptible except for the one isolate of C. haemulonii/C. auris in 2013.

In terms of outcomes of SSI, additional antibiotics were given to 88% of the patients. Twenty-nine per cent of the patients needed frequent dressings and 20% needed a repeat operative procedure. 15.0% of the patients had to stay in the hospital for a longer duration. Five patients with SSI died, translating into a crude mortality of 1%.

 ~ Discussion Top

To our knowledge, this is one of the largest prospective single-centre studies on the incidence and microbial aetiology of SSI. [Table 5] compares the SSI rates in our hospital with other reported studies. While there are a handful of Indian studies that have reported SSI rates ranging from 1.2 to 39%, these studies are limited by small sample size, retrospective nature, limited follow-up, etc.[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20] The SSI rate of 1% reported by us is at par with the developed world and can be attributed to surgical expertise, standardised SSI prevention protocols, world-class Central Sterile Supply Department services, state-of-the-art OT complex with HEPA filters that maintain 25 air exchanges per hour, strict OT cleaning and disinfection procedures and an ongoing sturdy infection prevention and control program. While overall SSI rates were low, 9% of the study patients (50 patients) had organ space SSI (including prosthetic joint infections and meningitis). Since these organ space infections are responsible for significant morbidity, increased length of stay, excessive antibiotic use and increased cost of treatment in the study population, there is scope to reduce them further. Some of these strategies in joint replacement surgeries could include using antibiotic impregnated bone cement/silver-coated implants in high-risk patients.[21],[22] Similarly, a reduction of organ space SSI in high-risk neurosurgical patients could include the use of antibiotic-impregnated shunts.[23]
Table 5: Summary of surgical site infections rates as percentage of surgical procedures

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The highest specialty-specific SSI rate of 3.7% was seen with coronary bypass grafting (CABG) surgeries. These rates can possibly be attributed to the advanced age of these patients and the presence of multiple comorbidities such as diabetes and renal impairment. However, this rate compares favourably with the rate of 11.6% reported by Sahu et al. in adult cardiac surgeries in India.[13] The SSI rate following CABG surgeries in Australia has been reported to be 11.7% (of which sternal site infections occurred in 3.6%) and the USA as 1% (including only deep incisional and organ space infections).[24],[25] The rate of infection in knee replacement surgeries of 0.6% compares favourably with the 1.1% rate reported from New Delhi in knee replacement surgeries.[26]

We report a predominance of Gram-negative pathogens as cause of SSI in our current study. This is in agreement with our previous study, other Indian studies on SSI and from other developing countries.[1],[4],[15],[16] Some Indian studies have, however, reported S. aureus and especially MRSA as the predominant cause of SSI.[9],[12],[14],[17] Studies from resource-rich settings report a predominance of Gram-positive organisms including S. aureus as the predominant pathogens.[27] So why do patients in resource-limited settings/developing countries get Gram-negative SSI? Is it from the skin that gets quickly colonised by Gram-negative pathogens soon after hospital admission or is it from the operation theatre environment? The latter seems more likely as the vast majority of patients undergoing elective surgery in our study were admitted just the day before admission. Further research is needed to determine skin-colonising flora of pre-surgical patients. Unlike many other Indian studies which have reported rapidly growing non-tuberculous mycobacteria (NTM) as an emerging cause of SSI, we did not report any NTM infection.[28],[29] This can be attributed to strict procedures for cleaning, disinfection and rinsing of laparoscopes/arthroscopes.

Although our SSI rate is comparable to international standards, the high incidence of antimicrobial resistance is of great concern. The resistance rates reported by us in Gram-negative pathogens (ESBL rates of 80%, BL-BLI 57% and carbapenems 79%) and Gram-positive pathogens (MRSA 44% and MR CONS 84%) are higher than reported by us in the previous study (ESBL rate of 64%, BL-BLI 66% and carbapenems 92%, MRSA 17%).[4] Rising antimicrobial resistance in nosocomial pathogens including those causing SSI has been reported from other studies from India and across the world, especially from low- and middle-income countries.[14],[15],[17],[20],[27],[30],[31] However, rates of antimicrobial resistance noted in this study are significantly lower than those reported by us in CLABSI at our centre where carbapenem resistance rates were 50%.[31] The lower resistance rates in SSI as compared to CLABSI in the same institute are possibly due to the fact that patients undergoing surgeries are less antibiotic experienced and usually have a shorter hospital stay than patients in the intensive care unit who develop CLABSI.

While the compliance to surgical prophylaxis policy of the hospital as far as choice of the antimicrobial was concerned was good, antimicrobials were used for longer than necessary. All standard guidelines recommend only a single dose of antibiotic as perioperative prophylaxis in most surgeries.[32] However, the surgeons at the study site continued antibiotics in the post-operative period of 2–7 days due to practices followed in the institutions they trained or worked at earlier and worry that the 'milieu' in Indian hospitals is not clean enough as those in resource-rich settings. Other Indian studies have also reported prolonged antibiotic use in surgical prophylaxis.[33],[34] There are now studies from Indian hospitals which have also shown no benefit of extended prophylaxis over single dose/48-h prophylaxis.[35],[36],[37] Hence the duration of antibiotic prophylaxis should be shortened to mitigate problems of drug adverse effects. C. difficile infection, cost of therapy and antimicrobial resistance.

It is also important to discuss the use of aminoglycosides/ciprofloxacin as perioperative prophylaxis in addition to cefazolin/cefuroxime at our centre for some surgeries [Table 1]. This is based on the predominance of Gram-negative organisms causing SSI in our setting and international guidelines on surgical prophylaxis that recommend tailoring of the prophylaxis to cover the flora causing SSI at a particular centre.[32] However, the use of even single/short course of aminoglycosides is likely to be associated with nephrotoxicity and possibly increased resistance. Therefore, it is the felt need of the authors to study SSI rates at our centre after dropping the Gram-negative cover.

It is now known that risk of SSI is the same whether hair is removed or not.[38] However, at the study site, hair is routinely removed before surgery since surgeons insist on it. Clippers are used at the study site instead of shaving, since clippers are associated with lower risk of SSI as compared to shaving.[38] However, it is worthwhile to move away from the practice of routine hair removal before surgery after regular dialogues with the surgeons.

The main limitation of the study is the inability to follow up each patient for the entire follow-up period. Hence, some SSIs could have been missed, especially in those patients that did not need hospitalisation and in those who approached other hospitals for treatment. This would have led to underestimation of the SSI rate. Improving the follow-up of these patients through enhanced use of mobile phones/customised mobile applications/reminders is a feasible option.[39] The study was also not designed to evaluate risk factors for SSI, extra burden of SSI in terms of length of hospital stay/cost of treatment and the attributable mortality from SSI. On the other hand, the strength of the study lies in its prospective nature, large sample size and involvement of the same infection control team throughout the length of the study. While the low rates of SSI provide confidence in our infection control bundle, the high resistance rates underscore the need for comprehensive antimicrobial stewardship initiatives.

 ~ Conclusion Top

In a nutshell, the rate of SSI in this prospective study involving more than 55,000 surgical procedures from 2013 to 2018 was 1%. Gram-negative organisms were responsible for 65% of the infections, followed by Gram-positive in 30% and Candida in 4%. A significant percentage of the study isolates were drug resistant. Crude mortality in patients with SSI was 1%.

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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]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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