|Year : 2015 | Volume
| Issue : 2 | Page : 195-200
|A study of organisms causing surgical site infections and their antimicrobial susceptibility in a tertiary care Government Hospital
Aniruddha S Mundhada, Sunita Tenpe
Department of Microbiology, Indira Gandhi Government Medical College, Nagpur, Maharashtra, India
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|Date of Web Publication||17-Apr-2015|
| Abstract|| |
Background: Surgical site infection (SSI) is one of the most common postoperative complication and causes significant postoperative morbidity and mortality. Patients: A prospective study was carried out in a total of 100 patients operated for clean and clean-contaminated surgeries from department of orthopedics, surgery and obstetrics & gynecology. Materials and Methods: Relevant details were noted in clinical history. Each patient was followed from the time of admission till discharge from the hospital and also for 30 days postoperatively (CDC, 1999). The identification of the infecting organism was done by staining, and culture and antibiotic susceptibility by Disc Diffusion method. Results: Out of 100 patients, 32 patients got infected post-operatively. Staphylococcus aureus was the most common organism isolated. None of the strains were Methicillin resistant. Drug resistance was widespread, especially in Enterobacteriaceae, where the Cefotaxime resistant strains of Escherichia coli and Klebsiella pneumoniae were ESBL producing. Another concern in recent times is the isolation of Acinetobacter from surgical wounds. Various patient factors and hospital protocol were analyzed with regard to the treatment outcome. Judicious use of antibiotics along with evidence-based medicine is the need of the hour to stop the rise of these superbugs.
Keywords: Antibiotic susceptibility, nosocomial infection, surgical site infection
|How to cite this article:|
Mundhada AS, Tenpe S. A study of organisms causing surgical site infections and their antimicrobial susceptibility in a tertiary care Government Hospital. Indian J Pathol Microbiol 2015;58:195-200
|How to cite this URL:|
Mundhada AS, Tenpe S. A study of organisms causing surgical site infections and their antimicrobial susceptibility in a tertiary care Government Hospital. Indian J Pathol Microbiol [serial online] 2015 [cited 2019 Dec 13];58:195-200. Available from: http://www.ijpmonline.org/text.asp?2015/58/2/195/155313
| Introduction|| |
Hospital-acquired infections are the most common type of nosocomial infection among surgical patients.  Surgery has made great advances in last 3 quarters of this century and postoperative wound infection is the most common complication faced by surgeon since the advent of surgery. Results of infection cause delayed recovery and may leave permanent disability. But, despite efforts to control it and better understanding of sepsis, wound infection is still a clinical problem and some infections in clean wounds still remain unexplained. Wound access to bacteria can be prevented by aseptic surgical techniques, or bacteria can be removed substantially by early wound toilet and uncomplicated healing can be expected. However, if by any reason, microorganisms gain a foothold and infection becomes established, antibiotics contribute to prevention and treatment of infection. With the influx of the voluminous number of antibiotics, the clinician often finds himself overwhelmed by the variety of the options. Determination of the etiologic agent is vital in the final choice of the antibiotics. Most especially in the situation where empirical treatment has to be started without the benefit of the Gram-stain or culture and sensitivity results, a working knowledge of the most likely organism and the prevailing antibiotic sensitivity/resistance pattern will be of great help. Apart from bacterial contamination of the wound, there are many other factors within the patient and his environment, both local and general, which ultimately determine the outcome. These local factors such as hematomas, seromas, suture material, poor surgical technique, degree of contamination and also age, nutrition, hygiene, and other associated disease play an important role in the etiology of postoperative wound infection.
Thus, the identification of factors that cause or predict these infections continues to be an important area of research. A wide variety of aerobic and anaerobic species of bacteria may be present, either singly or in combination. Infections of wounds, are generally associated with the production of pus and the bacteria involved are said to be "pyogenic" (pus producing). The incidence of surgical site infection (SSI) varies from hospital to hospital and also varies in different studies that have been reported from time to time. The treatment depends on determining its susceptibility to antibiotics. Extended-spectrum β-lactamases (ESBLs) are enzymes produced by Gram-negative bacilli that mediate resistance to penicillin, cephalosporins, and monobactams and are commonly recognized in Enterobacteriaceae and Pseudomonas aeruginosa. 
Wounds were classified as clean/Class 1 or clean-contaminated/Class 2 according to Centers for Disease Control (CDC) classification based on the degree of microbial contamination. 
In the view of these observations, the present study was undertaken with the following aims:
- To find the incidence of postoperative surgical wound infections in clean and clean-contaminated surgeries in orthopedic, surgery and obstetric-gynecology wards;
- To determine factors related to patient and surgical procedures influencing the rate of postoperative surgical wound infections;
- To determine bacteriological profile and antimicrobial susceptibility patterns of the isolates.
| Materials and Methods|| |
The present prospective study was conducted in the Department of Microbiology at Indira Gandhi Government Medical College and Hospital, Nagpur. The study period was from May 2011 to June 2011. Institutional ethics committee approval was obtained prior to the start of the study.
Totally, 100 patients operated for clean and clean-contaminated surgeries from Department of Orthopedics, Surgery and Obstetrics and Gynecology. The details of the patients were recorded as per the proforma. Each patient was followed from the time of admission till discharge from the hospital (CDC, 1999). 
Clean surgeries (Class I operative wounds) and Clean-contaminated surgeries (Class II operative wounds). 
- Contaminated surgeries (Class III operative wounds) and dirty surgeries (Class IV operative wounds);
- Stitch abscess;
- Episiotomy and circumcision wounds.
A wound was considered to be infected if any one of the following criteria was fulfilled: ,
- Serous or nonpurulent discharge from the wound;
- pus discharge from the wound;
- serous or nonpurulent discharge from the wound with signs of inflammation (edema, redness, warmth, raised local temperature, tenderness, induration).
Sample collection and transport
The swabs were obtained from deep inside the wound avoiding contact with skin under all aseptic precautions. , The surgical wound was inspected at the time of first dressing and weekly thereafter till discharge (CDC 1999). 
A smear was prepared and stained by Gram-staining method for early presumptive diagnosis and inoculated on Blood agar and McConkey's agar by streak method using Nichrome wire loop. The plates were incubated at 37°C overnight for 18-24 h. Identification of isolates was done by morphology and colony characteristics according to CLSI guidelines. Antimicrobial susceptibility was done using disk diffusion tests according to CLSI guidelines. 
The isolates of Escherichia More Details coli, Klebsiella pneumoniae showing resistance to cefotaxime were further tested for ESBL production. Double Disk Diffusion Test was used for detection of ESBL production. 
A clear extension of the edge of inhibition zone of cephalosporin disk toward amoxicillin-clavulanic acid disk incubated for 18 h on Mueller-Hinton agar was interpreted as positive for ESBL production. 
| Results|| |
Infection rates after various surgical procedures at surgical sites were observed. [Table 1] shows the high infection rate in appendectomy, gastric, small and large bowel surgeries (50%). The infection rate in uterus and adnexal structures (33.33%), urinary tract and genitalia (33.33%) and lower segment caesarean structure (LSCS) (31.81%) are comparatively lower. The infection rate after breast surgery is 25% [Table 1].
Overall postoperative SSI rate was 32% [Table 1]. It was higher (50%) in age group above 60 years. There was no sex predilection. Totally, 34 (34%) wounds were classified as clean wounds. Of these, 6 cases developed wound infection with an infection rate of 17.65%. Rest of the 66 (66%) cases were classified as clean contaminated wounds and out of which 26 cases (39.39%) got infected postoperatively (χ2 = 13.08; P = 0.0003). Rate of infection was higher in emergency cases (45%) than elective cases (21%) (χ2 = 6.54; P = 0.0106). There is an increase in infection rate with increase in preoperative hospital stay (χ2 = 9.88; P = 0.019). The highest infection rate is seen among the patients with preoperative stay of more than 21 days (66.67%) while it is 27.78% in patients with preoperative stay up to 7 days. Infection rate is 18.52% in patients who received preoperative antibiotics compared to 47.83% in patients who did not (χ2 = 9.81; P = 0.0017).
The infection rate in patients operated under general anesthesia is 45% and under subarachnoid block anesthesia is 25% while one of the patients operated under local anesthesia is infected (12.5%) (χ2 = 7.72; P = 0.0211). Infection rate varied with duration of operation with rate of 10.75% in surgeries those lasted for >1 h, which is higher than the rate in surgeries which lasted between 30 min to 1 h (2.04%) (χ2 = 6.56; P = 0.0377). None of the wound is infected in surgeries that lasted for <30 min. Use of drain is associated with more infection rate (14.28%). The nondrained wounds have less rate of infection (5.22%) (χ2 = 5.83; P = 0.0157).
Surgical site infection was more in patients with preexisting illness such as diabetes (66%), hypertension (66%), sickle cell disease (33%) and other past medical/surgical history (tuberculosis, anemia, malaria, jaundice, other high risk surgery in the past 1-year.
Polymicrobial infection was experienced by 16 (50%) patients, 14 (29.16%) had Staphylococcus aureus, 10 (20.83%) had E. coli and 9 (18.75%), had P. aeruginosa 7 (14.58%), had K. pneumoniae 6 (12.5%) had Acinetobacter and 2 (4.16%) cases had Staphylococcus epidermidis. Gram-negative organisms were mostly isolated from surgeries on bowel, urinary tract and appendix.
Staphylococcus aureus is the predominant organism infecting LSCS surgeries. No other organism is particularly associated with specific surgery [Table 2] and [Table 3].
Antibiotic susceptibility testing showed that all the strains of S. aureus resistant to penicillin, moderately sensitive to erythromycin (42.8%), tetracycline (28.5%), gentamicin (35.7%) and ciprofloxacin (42.8%). All the strains were sensitive to cefoxitin, means none of the strains were methicillin resistant.
Escherichia coli was moderately sensitive to ampicillin (33.3%), gentamicin (50%), ciprofloxacin (50%), amikacin (66.6%) and cefotaxime (33.3%) and extensive resistance to tetracycline (90%). In case of K. pneumoniae, poor sensitivity to ampicillin and gentamicin (14.28%), moderately sensitive to cefotaxime (28.57%), amikacin and ciprofloxacin (42.85%) was observed. None of the strains were sensitive to tetracycline.
Pseudomonas aeruginosa was moderately sensitive to ciprofloxacin (44.44%), gentamicin (77.78%) and all the strains sensitive to ceftazidime, amikacin and imipenem.
The 2 strains of Acinetobacter isolated were sensitive to Amikacin, Imipenem and resistant to Ciprofloxacin, Ceftazidime, Tetracycline and Gentamicin. The 2 strains of S. epidermidis isolated were sensitive to all the antibiotics-gentamicin, tetracycline, ciprofloxacin, cefotaxime, cefoxitin except penicillin and erythromycin.
Cefotaxime resistant strains of E. coli (7 strains) and K. pneumoniae (5 strains) were tested for ESBL production by Double Disk Diffusion Test. All the 12 strains tested were ESBL producing.
Organisms isolated from postoperative wound
Staphylococcus aureus was the predominant organism isolated (29%) followed by Gram-negative organisms. Other studies have also implicated S. aureus as the predominant cause of postoperative wound infections. ,[ 10],, Among the Gram-negative organisms E. coli was the predominant organism (21%), followed by P. aeruginosa (19%), K. pneumoniae (15%), Acinetobacter (12%) and S. epidermidis (4%) [Table 2] and [Table 3].
Antibiotic susceptibility of isolates
Staphylococcal isolates were 100% resistant to penicillin. Totally, 6 strains (42.8%) are sensitive to erythromycin, 4 strains (28.5%) are sensitive to tetracycline, 5 strains (35.7%) are sensitive to gentamicin, 6 strains (42.8%) are sensitive to ciprofloxacin and all are sensitive to cefotaxime. All the strains are sensitive to cefoxitin, means none of the strains are methicillin resistant.
In this study, 3 strains (33.33%) of E. coli were sensitive to ampicillin, 5 strains (50%) were sensitive to gentamicin and ciprofloxacin, 6 strains (66.66%) were sensitive to amikacin, 3 strains (33.33%) were sensitive to cefotaxime and only 1 strain (10%) was sensitive to tetracycline. In case of K. pneumoniae 1 strain (14.28%), each shows susceptibility to ampicillin and gentamicin, 2 strains (28.57%) were sensitive to cefotaxime and 3 strains (42.85%) to amikacin and ciprofloxacin. None of the strains were sensitive to tetracycline. Cefotaxime resistant strains of E. coli (7 strains) and K. pneumoniae (5 strains) were tested for ESBL production by Double Disk Diffusion Test. All the 12 strains tested were ESBL producing. The 2 strains of Acinetobacter isolated were sensitive to amikacin, imipenem and resistant to ciprofloxacin, ceftazidime, tetracycline and gentamicin.
Three strains (75%) of P. aeruginosa were sensitive to gentamicin, and 2 strains (50%) were sensitive to ciprofloxacin. All the strains were sensitive to ceftazidime, amikacin, imipenem and piperacillin. The 2 strains of S. epidermidis isolated were sensitive to all the antibiotics-gentamicin, tetracycline, ciprofloxacin, cefotaxime, cefoxitin except penicillin and erythromycin.
| Discussion|| |
The problem of postoperative wound infection is seen in both developed and developing countries, despite introduction of meticulous antiseptic regime in surgical practice. It can occur from either an endogenous or an exogenous source. In this study, 32 patients got infected postoperatively with the postoperative SSI rate of 32%. This is comparable with the rates reported by various authors. ,, Low infection rate in developed countries may be due to vast differences in working conditions prevailing in these countries. ,, The higher rates reported by some authors may be due to the inclusion of contaminated and dirty wound types and also emergency surgeries in their studies. ,
Contaminated and dirty wounds were excluded, but the emergency surgeries were included, which is the reason for the high infection rate in the present study.
It was reported by many authors that antibiotic coverage during the preoperative period lowers the incidence of postoperative SSI. , In the present study also, it was observed that preoperative antibiotic administration significantly reduces the rate of postoperative SSI (χ2 = 9.81; P = 0.0017).
The higher rate of infection in elderly patients observed in the present study is in conformity with the findings of several workers. , Increasing age is correlated with a greater likelihood of certain chronic conditions, malnutrition and a fall in the body immunological efficiency, predisposing to SSI. ,[ 22]
The reason for obtaining a higher rate of postoperative wound infection in this study could be the greater number of young adults getting operated for exploratory laparotomy for antral perforation and appendicular perforation or appendicitis. The number of females undergoing Caesarean sections and other gynecological operations in third and fifth decade is higher. This justifies the high rate of infection noted in those age groups. Statistically significant association was observed between the infection rate and wound type in this study (χ2 = 13.08; P = 0.0003). The class II wounds include the incisions made in body cavities. Hence, there is increased the risk of developing SSI. The infection rate of clean and clean-contaminated wound types observed in the present study is comparable to the rate reported by Anvikar et al. and Sangrasi et al. ,,
The increased infection rate with prolonged preoperative hospital stay may be due to lowered general resistance because of age and other diseases, which are responsible for preoperative stay and during preoperative hospital stay the patient becomes increasingly exposed to bacteria to which patient has not developed immunity, and these bacteria may be antibiotic resistant. ,,,,
Higher rate of infection was observed in the patients who had surgery under general anesthesia than in those who operated under spinal anesthesia and local anesthesia.
(χ2 =7.72; P=0.0211). 
Bacterial contamination increases with the duration of surgery, also the cells are increasingly damaged by exposure to air or to trauma due to surgical instruments or because longer procedures are more liable to be associated with blood loss and shock thereby reducing the patients general resistant. All these factors may contribute to increased rate of infection with increase in duration of surgery. ,,,
The drain itself may act as a pathway for microorganisms as it communicates the wound to the external environment. ,,,
The high rate of infection after surgeries involving the gastrointestinal system, hepatobiliary, pancreas and appendectomy is constant with the known risk associated with abdominal operations and incision of the gastrointestinal tract. These findings were comparable with the rates reported by Olson et al.  The high rate of SSI in uterus and adnexa may be due to the diabetes and sickle cell disease which was present in that study group. Most of the cases of LSCS surgeries were emergencies; this might have resulted in the high rate of SSI.
The preexisting illness increases the risk of postoperative infection due to the increase in the preoperative stay of the patient for treatment of those conditions. The prolonged preoperative stay favors the colonization with bacteria and increases the risk of infection. ,,
The high susceptibility of Enterobacteriaceae to cefotaxime and amikacin in this study proved the usefulness of cefotaxime and amikacin in Enterobacteriaceae infections. 
In this study, the susceptibility of P. aeruginosa to amikacin and ceftazidime indicates that, these drugs can be used against pseudomonal infections. Majumder et al.  have reported that 15% of S. epidermidis were oxacillin resistant, whereas 52.9% of S. aureus to be Oxacillin resistant.
| Conclusions|| |
A plethora of risk factors contributed to postoperative surgical wound infections. Although Gram-negative organisms were frequently isolated from postoperative wounds, S. aureus was the single predominant pathogen isolated.
Preoperative antibiotics, reduced hospital stay and proper control of comorbidities decrease the incidence of postoperative infections. Methicillin resistant S. aureus was not isolated in this study indicating that the resistance has not yet developed in the strains isolated from the hospital. Significant is the emergence of drug resistant strains of Acinetobacter indicating their role in hospital acquired infection. Marked resistance of isolates to commonly used antibiotics signifies the need for judicious and rational use of these drugs to prevent the emergence of antibiotic resistant strains.
The study gives us insight into the bacterial flora isolated and their resistance pattern in postoperative patients in a tertiary care hospital. This study can be further extended to other elective and emergency surgical procedures for a considerable duration. Surveillance of SSI with feedback of appropriate data to surgeons would be desirable to reduce the SSI rate.
| Acknowledgment|| |
We wish to acknowledge the staff of the Microbiology department of Indira Gandhi Government Medical College for providing help in data collection.
| References|| |
Emori TG, Gaynes RP. An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev 1993; 6:428-42.
Bradford PA. Extended-spectrum beta-lactamases in the 21st century: Characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 2001;14:933-51.
Garner JS. CDC guideline for prevention of surgical wound infections, 1985. Supersedes guideline for prevention of surgical wound infections published in 1982. (Originally published in November 1985). Revised. Infect Control 1986;7:193-200.
Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol 1999;20:250-78.
Siguan SS, Ang BS, Pala IM, Baclig RM. Aerobic surgical infection: A surveillance on microbiological etiology and antimicrobial sensitivity pattern of commonly used antibiotics. Philipp J Microbiol Infect Dis 1990;19:27-33.
Lilani SP, Jangale N, Chowdhary A, Daver GB. Surgical site infection in clean and clean-contaminated cases. Indian J Med Microbiol 2005;23:249-52.
Collee JG, Duguid JP, Fraser AG, Marmion BP, Simmons A. Laboratory strategy in the diagnosis of infective syndromes. In: Collee JG, Marmion BP, Fraser AG, Simmons A, editors. Mackie and McCartney Practical Medical Microbiology. 14 th
ed. London: Churchill Livingstone; 2006. p. 53-94.
Collee JG, Marr W. Specimen collection, culture containers and media. In: Collee JG, Marmion BP, Fraser AG, Simmons A, editors. Mackie and McCartney Practical Medical Microbiology. 14 th
ed. London: Churchill Livingstone; 2006. p. 95-111.
Clinical and Laboratory Standards Institute. "Performance Standards for Antimicrobial Susceptibility Testing," Fifteenth Informational Supplement. Approved Standard MS100-S16. Wayne, PA: CLSI; 2006
Edwards LD. The epidemiology of 2056 remote site infections and 1966 surgical wound infections occurring in 1865 patients: A four year study of 40,923 operations at Rush-Presbyterian-St. Luke's Hospital, Chicago. Ann Surg 1976;184:758-66.
Murthy R, Sengupta S, Maya N, Shivananda PG. Incidence of post operative wound infection and their antibiogram in a teaching and referral hospital. Indian J Med Sci 1998;52:553-5.
Arya M, Arya PK, Biswas D, Prasad R. Antimicrobial susceptibility pattern of bacterial isolates from post-operative wound infections. Indian J Pathol Microbiol 2005;48:266-9.
Anvikar AR, Deshmukh AB, Karyakarte RP, Damle AS, Patwardhan NS, Malik AK, et al
. A one year prospective study of 3280 surgical wounds. Indian J Med Microbiol 1999;17:129-32.
Cruse P. Wound infection surveillance. Rev Infect Dis 1981;3:734-7.
Järhult J, Sandhammar B. Postoperative infections in the small hospital. A prospective one-year study. Acta Chir Scand 1981;147:325-9.
Olson M, O'Connor M, Schwartz ML. Surgical wound infections. A 5-year prospective study of 20,193 wounds at the Minneapolis VA Medical Center. Ann Surg 1984;199:253-9.
Agarwal PK, Agarwal M, Bal A, Gahlaut YV. Incidence of post-operative wound infection at Aligarh. Indian J Surg 1984;46:326-33.
Sangrasi AK, Leghari AA, Memon A, Talpur AK, Qureshi GA, Memon JM. Surgical site infection rate and associated risk factors in elective general surgery at a public sector medical university in Pakistan. Int Wound J 2008;5:74-8.
Gupta R, Sinnett D, Carpenter R, Preece PE, Royle GT. Antibiotic prophylaxis for post-operative wound infection in clean elective breast surgery. Eur J Surg Oncol 2000;26:363-6.
Moro ML, Morsillo F, Tangenti M, Mongardi M, Pirazzini MC, Ragni P, et al.
Rates of surgical-site infection: An international comparison. Infect Control Hosp Epidemiol 2005;26:442-8.
Arenal JJ, Bengoechea-Beeby M. Mortality associated with emergency abdominal surgery in the elderly. Can J Surg 2003;46:111-6.
McNicol L, Story DA, Leslie K, Myles PS, Fink M, Shelton AC, et al.
Postoperative complications and mortality in older patients having non-cardiac surgery at three Melbourne teaching hospitals. Med J Aust 2007;186:447-52.
Moorhouse E, Fenelon L, Hone R, Smyth E, McGahon J, Dillon M. Staphylococcus aureus
sensitivity to various antibiotics - a national survey in Ireland 1993. Ir J Med Sci 1996;165:40-3.
Nagachinta T, Stephens M, Reitz B, Polk BF. Risk factors for surgical-wound infection following cardiac surgery. J Infect Dis 1987;156:967-73.
Rodgers A, Walker N, Schug S, McKee A, Kehlet H, van Zundert A, et al.
Reduction of postoperative mortality and morbidity with epidural or spinal anaesthesia: Results from overview of randomised trials. BMJ 2000;321:1493.
Haley RW, Culver DH, Morgan WM, White JW, Emori TG, Hooton TM. Identifying patients at high risk of surgical wound infection. A simple multivariate index of patient susceptibility and wound contamination. Am J Epidemiol 1985;121:206-15.
Claesson BE, Holmlund DE. Predictors of intraoperative bacterial contamination and postoperative infection in elective colorectal surgery. J Hosp Infect 1988;11:127-35.
Margenthaler JA, Longo WE, Virgo KS, Johnson FE, Oprian CA, Henderson WG, et al.
Risk factors for adverse outcomes after the surgical treatment of appendicitis in adults. Ann Surg 2003;238:59-66.
Duttaroy B, Mehta S. Extended spectrum b lactamases (ESBL) in clinical isolates of Klebsiella pneumoniae
and Escherichia coli
. Indian J Pathol Microbiol 2005;48:45-8.
Majumder D, Bordoloi JS, Phukan AC, Mahanta J. Antimicrobial susceptibility pattern among methicillin resistant Staphylococcus
isolates in Assam. Indian J Med Microbiol 2001;19:138-40.
Dr. Aniruddha S Mundhada
J11, West High Court Road, Laxmi Nagar, Nagpur, Maharashtra - 440 022
Source of Support: ICMR-Short Term Studentship (STS) 2011 grant., Conflict of Interest: None
[Table 1], [Table 2], [Table 3]
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