ORIGINAL ARTICLE

Bacteriological Profile of Patients with Intra-Abdominal Sepsis

and Superficial Surgical Site Infection Following Emergency

Abdominal Surgery—Is It Concordant?

Ridhima Aggarwal

& A R Pranavi

& Mohsina Subair

& Sathasivam SureshKumar

& G. S. Sreenath

& Sujatha Sistla

T. Mahalakshmy

& Vikram Kate

Received: 19 July 2018 /Accepted: 5 October 2019

Association of Surgeons of India 2019

Abstract

The rates of surgical site infections (SSI) continue to be reported with great variability, even for the same operation, from different

geographical areas. Hence, a hospital-based surveillance of SSI can help in designing effective preventive strategies. This study

was done to assess the risk factors, characteristics, and incidence of SSI in patients undergoing emergency gastrointestinal

surgery. The study was a case series analysis, enrolling all consecutive patients undergoing emergency gastrointestinal surgery.

The patients were examined daily for SSI using ASEPSIS score and during the post-operative period up to 30 days. For patients

with SSI, wound swab was taken for culture and sensitivity. Patient and operative characteristics were analyzed for identifying

risk factors, and the bacteriological profile and sensitivity pattern of intra-abdominal specimens were analyzed and compared

with microbiological profile of SSI. A total of 100 patients were studied. The incidence of SSI was 33%. Age (44.33 ± 18.277 vs.

39.43 ± 16.158; p 0.015) and pre-operative blood transfusion (61.1 vs. 38.9; p 0.012) were found to be significant risk factors for

SSI. On multivariate analysis, blood transfusion (p 0.027) and the duration of operation (p 0.005) were found to be independent

risk factors. In cases where the isolated organisms were Escherichia coli, Enterococcus faecalis,andKlebsiella pneumoniae,

concordance was noted between the intra-abdominal pathogens and the organisms isolated from the SSI. Risk factors for SSI in

patients undergoing emergency abdominal surgeries include increasing age, pre-operative blood transfusion, prolonged operating

time, intra-operative blood loss, and operative procedures involving bowel resection. Concordance exists between intra-

abdominal and SSI pathogens.

Keywords Surgical site infection

Antibiotic sensitivity

Dirty surgical wound

Emergency abdominal surgery

Laparotomy

wound infection

Introduction

Surgical site infection (SSI) is an important cause of post-

operative morbidity and mortality accounting for a

significant proportion of nosocomial infections. A notice-

ably larger incidence of SSI is seen in patients who have

undergone gastrointestinal surgery owing to the high

intraluminal bacterial load and chances for spillage of or-

ganic contents in the operative field, more so in case of

emergency procedures. SSI shows great variation in pre-

sentation, from small suture abscesses to deep organ space

intra-abdominal infections that can lead to fatal sepsis. A

better understanding of risk factors and the bacteriological

profile of SSI will help design effective prevention strat-

egies and antibiotic prophylaxis regimens to reduce the

current rates of SSI and the strain on finances and

resources.

ASEPSIS score [1] (additional treatment, serous discharge,

erythema, purulent exudates, separation of deep tissues, isola-

tion of bacteria, and hospital stay for > 14 days), helps to

* Vikram Kate

drvikramkate@gmail.com

Department of Surgery, Jawaharlal Institute of Postgraduate Medical

Education and Research (JIPMER), Pondicherry 605006, India

Department of Microbiology, Jawaharlal Institute of Postgraduate

Medical Education and Research (JIPMER), Pondicherry 605006,

India

Department of Preventive and Social Medicine, Jawaharlal Institute

of Postgraduate Medical Education and Research (JIPMER),

Pondicherry 605006, India

Indian Journal of Surgery

https://doi.org/10.1007/s12262-019-01997-y

differen tiate a minor disturbance in healing from a severe

wound infection.

Though many potential risk factors have been identified,

only few have been established by clinical studies. An ASA

(American Society of Anesthesiologists) score of 3 and above,

operative wounds classified as “contaminated” or “dirty,” and

prolonged duration of operation were established as indepen-

dent risk factors in the development of SSI in a report from

CDC (Centre for D isease Control) Atlanta in 1991 [2].

Similarly, patient factors such as smoking, gender, and oper-

ative factors such as blood loss, wound classification, and use

of surgical knife instead of electrocautery were all established

as risk factors in a study by Watanabe et al [3].

Currently, endogenous microorganisms implicated in SSI are

attributed to the patient’s skin and less often from gastrointestinal

(GI) tract or genitourinary (GU) tract. Exogenous microbes are

assumed to potentially come from the operator’s hands, instru-

ments, or the ambient air. Although the source of microbes is

same, the rates of SSI continue to be reported with great variabil-

ity, even for the same surgical procedure from different geo-

graphical areas [4]. This implies a hospital-based surveillance

of SSI is necessary to identify the factors which can help in

deciding effective prevention strategies for the regional setup.

Moreover, this study is also designed to investigate the pathogen

spectrum and antimicrobial sensitivity pattern of SSI in patients

undergoing emergency gastrointestinal surgery.

Patients and Methods

This study was a case series analysis wherein data was col-

lected and analyzed from patients undergoing emergency op-

erations for gastrointestinal diseases in the department of sur-

gery over a period of 4 months from a tertiary care hospital in

South India. These included procedures such as laparotomy

for gastroduodenal or bowel perforation, bowel resection for

intestinal obstruction; gangrene gut, emergency appendecto-

my, laparotomy for obstructed inguinal hernias, and intra-

abdominal abscess. Patients were operated by standard surgi-

cal techniques as per diagnosis. Any intra-operative resected

specimen (such as pus) was sent for culture. During emergen-

cy laparotomies, the peritoneal fluid (5 mL) was collected

with strict aseptic precautions and sent for culture to the mi-

crobiology lab. In cases where there was no peritoneal fluid, a

swab was taken from the peritoneal surface and sent for

culture. Two wound swabs were taken from the SSI sites with

a sterile cotton swab on the day of detection of infection and

sent to the microbiology lab.

Anatomical closure was done in layers for all cases. For

peritoneal closure, 1–0/1 polyglactin (continuous) was used.

For closure of linea, 1–polypropylene (interrupted) was used.

For closure of subcutaneous tissue, 2–0 polyglactin

(interrupted) was used. For closure of skin, 3–0 nylon

interrupted sutures were use d. None of the patients in the

study had delayed primary cl osure f or th eir laparotomie s.

Peritoneal lavage with 3 L of normal saline was given routine-

ly in all cases, which was the standard practice across units

and hence not considered an input variable.

Subject records were collected post-operatively and con-

secutively until the patient was discharged, and at the 30-day

follow-up visit or death.

The pre-operative patient variables and operative variables

were noted in the specified proforma. The patient variables

included age, gender, presence of comorbidities, hemoglobin

level, details of blood transfusion, and time of prophylactic

antibiotic dose administered before surgery (in hours). Data

about smoking habits was classified under “known smoker,”

“cessation < 1 month,”“cessation > 1 month,” and “no history

of smoking.” The ASA score calculated at the time of opera-

tion was also noted. The surgical wound was classified based

on the CDC definitions into class I (clean), class II (clean

contaminated), class III (contaminated), and class IV (dirty)

[1]. Other operative variables such as part of the GI tract in-

volved, diagnosis and type of operation done, duration of the

operation (in hours),blood loss incurred, and the placement of

a drain were noted.

After 24–48 h, culture and sensitivity reports on the intra-

operative specimen were collected and compiled with the

above data. As per standard protocol, only aerobic culture

was done on the samples. Culture media used were 5% sheep

blood agar and McConkey Agar, incubated at 37 °C for 24–48

h. Antibiotic susceptibility was performed by the Kirby Bauer

disc diffusion method and interpreted as per CLSI guidelines,

2014.

Following the operation until discharge, and at the 30-day

follow-up period, patients were examined for features sugges-

tive of SSI using the ASEPSIS score. In case of high scores

suggestive of SSI (i.e., ≥ 20), a wound swab was taken under

aseptic precautions and sent for culture and sensitivity.

Microbiology results were obtained by the same method as

for intra-operative specimens and noted alongside the above

data.

Incidence of SSI was calculated using standard formulae.

The data was entered in MS Excel and analyzed using SPSS

version 16. Categorical variables such as gender, ASA score,

blood transfusion, presence of drain, and presence of SSI were

summarized as frequency and percentages. For these vari-

ables, chi-square test of significance was used to check statis-

tical significance between the surgical site infection positive

(SSI+) group and surgical site infection negative (SSI−)

groups. Continuous variables such as operation time, amount

of blood loss, and hemoglobin were summarized as mean and

SD. For these variables, independent sample “t” test was used

to compare between the SSI+ group and SSI− group. The

variables w hich were statistically significant in univariate

analysis were factored in multivariate analysis—binary

Indian J Surg

logistic regression forward LR method. A p value of < 0.05

was considered as significant.

Results

A total of 100 patients were included in the study. The age of

the patients ranged from 15 to 80 years with a mean age of

43.3 ± 1.49 years. There were 78 men and 22 women with a

male to female ratio of 3.5:1. Among the study population,

33% developed post-operative SSI.

Incidence of SSI and Patient Characteristics

Table 1 summarizes the patient characteristics and incidence

of SSI. Age of the patient (44.33 ± 18.277 vs. 39.43 ± 16.158;

p 0.015) and pre-operative blood transfusion (p 0.012) were

significantly associated with the development of SSI follow-

ing surgery. The incidence of SSI did not show any significant

difference between genders (33.3% vs. 31.8%). Patients who

were known smokers or had ceased smoking for less than a

month before the operation had a higher incidence of SSI

(40% and 60%) in comparison with those who had ceased

smoking for more than a month or were not smokers (16.7%

and 31.1%). A relatively higher percentage of patients with an

ASA score 3 or 4 developed SSI (37.5%). Timing of pre-

operative antibiotic and hemoglobin level were not found to

be significant risk factors for SSI.

Incidence of SSI and Operative Variables

The type of operation was a significant risk factor (p 0.042) for

developing SSI. Patients who underwent bowel resection and

drainage of an intra-abdominal abscess were found to have the

highest incidence of SSI (52.9% and 50%). Occurrence of SSI

was significantly associated with intra-operative blood loss (p

0.027) and the duration of operation (p 0.005). Placement of a

drain was also found to have a higher incidence of SSI

(46.8%; p 0.011), the percentage being almost twice as com-

pared with when no drain was placed ( 20.8%). Overall,

wound class, and comparison between upper GI and lower

GI procedures, was not found to be significant risk factors

for development of SSI. However, patients belonging to “con-

taminated” or “dirty” wound classes showed a higher percent-

age of SSI (37.8% and 40%) than those with “clean contam-

inated” and “clean” wounds (17.4% and 0%).

Multivariate Analysis—Independent Risk Factors

The factors identified as significant risk factors for SSI in

univariate analysis such as age, pre-operative blood trans-

fusion, type of surgery, i ntra-operative blood loss, dura-

tion of surgery, and the placement of drainage tube were

included in multivariate analysis by binary logistic

regression—forward LR method. Among the variables an-

alyzed, blood transfusion (p 0.027) and duration of oper-

ation (p 0.005) were found to be independent risk factors

for the development of SSI.

Bacteriological profile—Intra-Operative Specimens

and SSI Wound Swabs

Out of the 90 intra-operative specimens sent for analysis, 35

specimens (38.9%) showed microbial growth, while the re-

maining 55 were sterile or had pus cells but showed no growth

even after 48 h of incubation. The most common organism

isolated was Escherichia coli (42.3% of total pathogens iso-

lated in intra-operative specimens), followed by Klebsiella

pneumoniae and Enterococcus faecalis (each contributing in-

dividually to 13.6%). In the case of SSI, 33 wound swabs were

sent for analysis and 28 showed significant microbiological

growth (84.8%). Results showed that the most common path-

ogen was again Escherichia coli, accounting for 40.9% of

total pathogens isolated in SSI followed by Candida sp. in 9

patients (20.5%) (Table 2)

Concordance in Microbiological Profile—Origin of SSI

from Intra-Abdominal Pathogens

Out of 33 surgical site infections, 18 patients had pre-

operative intra-abdominal sepsis, out of which 10 pa-

tients (55.6%) showed concordance in the bacteriological

profile, indicating that t he SSI could have in fact originat-

ed from the intra-abdominal sepsis. Seven out of the 25

patients who had Escherichia coli growth in their intra-

operative speci men also s howe d Escherichia coli growth

in their SSI wound swab (28%). Similarly, 3 out of 5

patients who had shown growth of Candida intra-

abdominally had Candida in the wound swab. T wo pa-

tients had B-hemolytic streptococci isolated both from

SSI wound swabs and intra-abdominal specimen.

Antibiotic Sensitivity Pattern of Bacterial Isolates

from Intra-Operative Specimens and SSI Wound

Swabs

Escherichia coli, Klebsiella pneumoniae, Enterococcus

faecalis, and B-hemolytic streptococci were the most common

bacteria isolated during this study. Table 3 summarizes the

antibiotic sensitivity patterns of these organisms. Separate an-

tibiotic profiles (antibiotics to which they should be originally

sensitive to) were selected for Gram-negative (E. coli and

K. pneumoniae) and Gram-positive (E. faecalis and

Streptococci) bacteria. The sensitivity pattern showed that all

strains of E. coli cultured were most sensitive to amikacin,

meropenem, and cefoperazone, with high resistance to third-

Indian J Surg

generation cephalosporins and fluoroquinolones. Furthermore,

E. coli isolated in culture of SSI wound swabs showed in-

creased resistance to all antibiotics compared with those isolat-

ed in intra-operative specimens. Similarly, Klebsiella isolated

from SSI wound swabs were more resistant to all antibiotics,

except amikacin. All strains of Gram-positive bacteria isolated

showed complete susceptibi lity to vancomycin, and both

E. faecalis and Streptococci strains isolated from SSI wound

swab showed significantly lesser resistance to the antibiotics

than those isolated intra-abdominally.

Table 1 Demographic and clinical profile of the patients and Surgical Site Infection

Characteristics No. of patients (n = 100) SSI+ (%) (n =33) SSI− (%) (n = 67) p value (univariate

analysis)

p value (multivariate

analysis)

Age 44.33 ± 18.277 39.43 ± 16.158 0.015 NS

Gender

Male 78 26 (33.3) 52 (66.7) 0.99 NS

Female 22 7 (31.8) 15 (68.2)

ASA score 0.668

1 and 2 68 21 (30.9) 47 (69.1) NS

3 and 4 32 12 (37.5) 20 (62.5)

Comorbidities

Absent 76 26 (34.2) 50 (65.8) 0.83

Present 24 7 (29.2) 17 (70.8) NS

Smoking

Known smoker 26 10 (68.9) 16 (31.1) 0.419

No history of smoking 74 23 (31.1) 51 (68.9) NS

Hemoglobin 100 11.23 ± 2.119 11.60 ± 2.004 0.391 NS

Pre-operative blood transfusion

Received 18 11 (61.1) 7 (38.9) 0.012 0.027*

Not received 82 22 (26.8) 60 (73.2)

Timing of pre-operative

antibiotics

100 3.36 ± 2.082 3.65 ± 2.095 0.517 NS

Type of operation

Closure of perforation 34 13 (38.2) 21 (61.8)

Bowel resection 17 9 (52.9) 8 (47.1) 0.042 NS

Emergency

appendectomy

35 5 (14.3) 30 (85.7)

Laparotomy for

obstructed hernia

8 3 (37.5) 5 (62.5)

Incision and drainage of

abscess

6 3 (50) 3 (50)

Wound classification

Clean 2 0 (0) 2 (100) 0.199

Clean contaminated 23 4 (17.4) 19 (82.6) 0.199 NS

Contaminated 30 12 (40) 18 (60)

Dirty 45 17 (37.8) 28 (62.2)

Blood loss 100 196.06 ± 205.1 125.9 ± 107.089 0.027 NS

Operation time 100 2.86 ± 1.516 2.02 ± 0.897 0.005 0.005*

Drainage

No drain 53 11 (20.8) 42 (79.2)

Closed non-suction

drain

47 22 (46.8) 25 (53.2) 0.011 NS

Part of GI involved

Upper GI 26 11 (42.3) 15 (57.7)

Lower GI 74 22 (29.7) 52 (70.3) 0.352 NS

* - statistically significant; SSI, surgical site infection; ASA, American Society of Anesthesiologists

Indian J Surg

Discussion

It has been recognized that SSI is associated with a sig-

nificant morbidity and mortality. It can lead to wound

dehiscence, which has a high mortality rate [5]. Reports

have shown t hat SSI surveillance itself decreases the rate

of infection [6].

The present study was carried out on patients undergoing

emergency GI surgical procedures. It has been shown in var-

ious studies that the incidence of SSI is higher following emer-

gency procedures as compared with elective procedures.

Watanabe et al. studied the SSI in 941 upper and lower gas-

trointestinal surgeries, including 207 emergency procedures

and found that the incidence of SSI following emergency

Table 2 Microbiological profile of intra-operative specimens and SSI wound swabs

Organism isolated Intra-operative specimen SSI wound swab

No. of patients % of total No. of patients % of total

B-hemolytic streptococci 6 10.2 2 4.5

Escherichia coli 25 42.3 18 40.9

Klebsiella pneumoniae 8 13.6 5 11.4

Enterococcus faecalis 8 13.6 5 11.4

Proteus vulgaris 0024.5

Staphylococcus aureus 23.400

Pseudomonas aeruginosa 35.112.3

Acinetobacter baumanii 11.724.5

Enterobacter sp. 1 1.7 0 0

Candida sp. 5 8.5 9 20.5

SSI, surgical site infection

Table 3 Bacterial antibiotic sensitivity profile in intra-operative specimen and SSI wound swab

Organism Antibiotic Isolated in Intra-operative specimen Isolated in SSI wound swab

Sensitive (%) Resistant (%) Sensitive (%) Resistant (%)

Escherichia coli Amikacin 100 0 93.3 6.7

Meropenem 78.9 21.1 80 20

Gentamicin 78.9 21.1 46.7 53.3

Ceftazidime 36.8 63.2 20 80

Ceftriaxone 31.6 68.4 13.3 86.7

Ciprofloxacin 26.3 73.7 13.3 86.7

Cefoperazone 78.9 21.1 60 40

Klebsiella pneumoniae Amikacin 66.7 33.3 80 20

Meropenem 33.3 66.7 40 60

Gentamicin 100 0 40 60

Ceftazidime 66.7 33.3 0 100

Ceftriaxone 66.7 33.3 0 100

Ciprofloxacin 66.7 33.3 40 60

Cefoperazone 66.7 33.3 40 60

Enterococcus faecalis Ampicillin 33.3 66.7 66.7 33.3

Tetracycline 66.7 33.3 66.7 33.3

Vancomycin 100 0 100 0

B-hemolytic streptococci Ampicillin 60 40 100 0

Tetracycline 80 20 100 0

Vancomycin 100 0 100 0

SSI, surgical site infection

Indian J Surg

procedures was higher [3]. An Israeli study on the determi-

nants of wound infection in gastrointestinal operations found

emergency admission to be a significant risk factor for the

development of SSI [7]. Gastrointestinal surgery raises the

surgical wound grade from clean contaminated or contaminat-

ed category due to the high intraluminal bacterial load which

increases the chance of spillage of organic content into the

peritoneal cavity, and fecal soiling of the skin and subcutane-

ous tissue, with subsequent wound infection. The risk of such

contamination is more in emergency GI surgeries where the

operative procedures are carried out in an unprepared bowel.

Watanabe et al. studied the incidence of SSI and found that

the most common risk factors for SSI were emergency proce-

dures, wound classification, blood loss, and type of operation

[3]. In the present study, pre-operative blood transfusion and

duration of operation were found to be independent risk fac-

tors for the development of SSI. However, wound class was

not associated with a higher SSI rate. This could be due to the

fact that a significant number of patients in the study popula-

tion (35%) underwent emergency appendectomy, which, un-

like bowel perforation, has a lesser chance for intra-abdominal

contamination, and hence, a lesser infection rate. Smoking

causes constriction of peripheral blood vessels, leading to hy-

povolemia and hypoxia, both of which are involved in the

initiation of SSI [8]. Affirming this fact, the present study

has shown a higher incidence of SSI in known smokers and

smokers who stopped smoking for less than 1 month.

The present study showed that the duration of operation

served as an important risk factor, wherein longer durations

resulted in higher incidence of SSI. A prospective study on

SSI noted that longer durations of operations result in longer

lengths of exposure for contamination, thus, a higher infection

rate [9]. It was found that age over 65, blood transfusion and

comorbidities—specifically diabetes and obesity—were im-

portant risk factors. Although in the present study it could

not be ascertained if comorbidity was a significant risk factor,

both age and blood transfusion were found to significantly

associate with SSI. Overall, the present study indicated that

operative factors are more likely to cause SSI than patient

factors, as reported by Poon et al. [10].

In addition to the analysis of risk factors, Di Leo et al.

reported the microbiological profiles of SSI and observed that

the pathogens isolated were predominantly Gram positive

(78%), the most common being Enterococcus faecalis follow-

ed by Staphylococcus aureus [9]. Similarly, in India, it was

reported that Staphylococcus aureus was the most frequent

organism isolated. In the present study setting, the most com-

mon organism isolated was Escherichia coli (40.9%) and the

overall profile was mostly dominated by Gram-negative bac-

teria. The variation could be due to different distribution of

surgical procedures analyzed, as these studies were not limited

to surgeries on the GI tract [9, 11]. Mirroring this result, a

study by Boueil et al. on peritoneal fluid culture in patients

with perforated appendicitis reported the commonly recovered

organism was Escherichia coli (81%) [12].

In an Indian study, Escherichia coli and Klebsiella were the

most common multidrug-resistant bacteria isolated in post-

operative infections, and the prevalence of m ultidrug-

resistant Gram-negative bacteria was seen highest in the GI

surgery department [13]. Majority of the surgeries carried out

in GI clinics belong to either clean contaminated or contami-

nated category, and at times dirty, when it is performed in

emergency. Prophylactic antibiotic usage in such cases also

a common practice. High load of bacterial strains and usage of

multidrug combinations of antibiotics increases the chances

for resurgence of resistant pathogens in GI wards. In this

study, E. coli isolated both from intra-operative specimens

and SSI wound swabs were multi drug resistant, showin g

significantly reduced susceptibility to ceftazidime, ciproflox-

acin and ceftriaxone, and moderate susceptibility to

cefoperazone + sulbactam. Similarly, Klebsiella pneumoniae,

the organism second most frequently isolated from intra-

operative specimens, was also multidrug resistant and showed

the highest resistance to meropenem. Isolates from SSI

wounds showed more resistance to common antibiotics than

those cultured from intra-operative specimen.

In the present study, the fungus Candida was the most

common organism after E.coli to be isolated from the SSI

wound swab culture. Manolakaki et al., in a study involving

trauma patients, found that the incidence of candidiasis was

significantly more in patients who underwent laparotomy pro-

cedures and received more blood transfusi ons [14]. In the

present study, out of nine patients with Candida colonization,

three had a history of pre-operative blood transfusion and

three were post-laparotomy cases. However, these numbers

are too small to draw a conclusion.

The sample size was relatively small in comparison with

other studies to investigate the influence of comorbidities on

the development on SSI, as a very small fraction of patients

presented with such histories to emergency care. Also, the

study was done by collection of data by a proforma and not

by direct observation of the surgical practice, which according

to Beldi et al. may show gaps in results even for a compre-

hensive study on incidence of SSI [15].

Conclusion

SSI was found to be a common complication with an inci-

dence of 33%. The most important risk factors were operative

variables including the type of operation, duration, blood loss,

placement of drains, and patient factors like age and pre-

operative blood transfusion. It was found that intra-

abdominal sepsis does have a significant role in the develop-

ment of SSI, while there is no influence of the part of GI

operated upon the development of SSI. The most common

Indian J Surg

organism to be isolated was Escherichia coli, and the entire

bacteriological profile of both intra-abdominal sepsis and SSI

was dominated by Gram-negative bacteria with a high

antibiotic-resistant pattern for the strains isolated from SSI.

Based on the clinical data collected, most bacteria would be

susceptible to a combination of amikacin, meropenem, and

vancomycin, making it an effective prophylaxis regime for

SSI in the present hospital setting.

Compliance with Ethical Standards

Conflict of Interest The authors declare that they have no conflict of

interest.

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