Drug-Resistant Strains in Surgical Site Infections after Abdominal Surgery: A Prospective Study

Abstract

Background Surgical site infection (SSI) is a common complication of abdominal surgery associated with substantial discomfort, morbidity, and cost.

Objective The aim of this study was to determine the incidence, risk factors, and antimicrobial susceptibility pattern of the associated bacterial causes of SSI in patients after abdominal surgery.

Methods A prospective study over a 1-year (Jan 2019–Dec 2019) period was conducted at a tertiary care institution in North India. Postoperative patients of abdominal surgeries with SSI were included in the study. Any exudate from the surgical site was collected aseptically and was processed as per standard operating procedures.

Results Of 2,509 patients with abdominal surgeries included in the study, 75 (2.98%, majority, i.e., 50 males) developed SSI. Common risk factors found to be associated with the development of SSI include contaminated surgical sites, obesity, age, immunosuppression, and simultaneous infection at some other sites, with a predominance (89.3%) of gram-negative isolates. Escherichia coli was the most frequently isolated organism (45.3%), followed by Klebsiella spp. (20%), Acinetobacter spp.(10.6%), Pseudomonas spp., and Staphylococcus aureus (8% each). There was a very high (53%) prevalence of extended-spectrum β lactamase production among the E. coli and Klebsiella isolates. Additionally, 58.8% of the E. coli isolates were multidrug-resistant, whereas 73.3% of the Klebsiella isolates were exclusively drug resistant. All the S. aureus isolates were found to be methicillin-resistant.

Conclusion Although the SSI rates after abdominal surgery were low, multidrug-resistant gram-negative bacteria were predominant in SSI.

Keywords

abdominal surgeries - surgical site infection - risk factors - antimicrobila susceptibility - multidrug-resistant

Introduction

Surgical site infections (SSIs) or postoperative wound infections increase the hospital stay and many times complicate the recovery process. Centers for Disease Control and Prevention (CDC) has defined-“SSI is an infection occurring in an incisional site within 30 days after the procedure in which the incision was made or within 1 year if a prosthesis is implanted.”[1] SSI has been classified as superficial/incisional (limited to the skin and subcutaneous tissue), deep incisional (involving the fascia and muscle), or organ space(involving a body cavity, e.g., an abdominal cavity in case of gastrointestinal surgery).[2] [3] Deep tissue and organ space SSIs though less common but are associated with heightened morbidity/ mortality and hence can further augment cost to the patient.[4] [5] [6]

SSIs frequently complicate the postoperative recovery in 10 to 30% of the patients undergoing gastrointestinal surgeries.[2] [7] [8] [9] Patients' indigenous skin and gut flora are the primary sources responsible for SSIs in such patients.[10] Exogenous sources, such as noncompliance with aseptic precautions by the health care workers and improper sterilization of equipment, may contribute, though infrequently, to the development of SSIs.[11] SSI is associated with numerous patient-related risk factors, including advanced age, malnutrition, diabetes mellitus, smoking, morbid obesity, remote body site infection, and impaired immune system. The SSI records coming from different tertiary care hospitals are scanty. Hence, the data may not reveal the authentic extent of the problem. With this background, this study was planned to determine the incidence, concomitant risk factors, and antimicrobial susceptibility pattern of the associated bacterial agents of SSI in patients after abdominal surgery. The findings of the study will also help devise a strategy for infection control and to implement antibiotic stewardship.

Patients and Methods

Setting

This prospective study was conducted in the department of microbiology in coordination with the hospital infection control committee (HICC) and the surgery department of a tertiary care teaching hospital in Northern India after the initial approval from the institutional ethical committee. The study was performed for a period of 1 year (Jan 2019–Dec 2019) and included all the patients who underwent gastrointestinal surgery at our hospital. Patients who underwent liver transplantation surgeries were excluded from the study.

Inclusion and Data Collection

Necessary information/data was gathered from hospital records (records of the surgery department and SSI Performa filled by the infection control nurses under the supervision of HICC). The data was also collected on the associated risk factors with SSI, which included age, gender, obesity, infection/concurrent infection at a distant site, immunosuppression, immobilization, diabetes, smoking, vascular disease, prolonged preoperative hospital stay, and classification of surgical incision. Surgical incision was classified as clean, clean-contaminated, contaminated, or dirty/infected as per criteria laid down by CDC.[7]

Follow-Up

After surgery, a daily assessment of the patient was done during hospitalization. The incision site was regularly examined by the consultant surgeon. The criteria developed by the CDC and the National Nosocomial Infections Surveillance System were used to diagnose SSI. “Wound infection was diagnosed if any one of the following criteria were 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, fever more than 38°C, tenderness, induration) and wound deliberately opened up by the surgeon due to localized collection (serous/purulent).”[1] Any exudate from the surgical site was collected aseptically and was processed as per standard operating procedures. Characterization of bacterial isolates (identification, antibiotic susceptibility profile, multidrug-resistant [MDR], exclusively drug resistant [XDR], extended-spectrum β lactamase [ESBL], metallo β lactamase, AmpC β lactamase production, methicillin, and vancomycin resistance) was done per National Committee for Clinical Laboratory Standards (NCCLS) guidelines. All the patients who underwent abdominal surgeries were followed up for 1-month duration for the development of SSIs post-discharge of the patients.

Results

Patients and SSI

A total of 2,509 patients with abdominal surgeries were included in the study. [Table 1] depicts the number and type of abdominal surgeries and the number of patients who developed SSI in each category. The surgeries performed during this period included cholecystectomies (975/2,509, 39%), followed by laparotomy (508/2,509, 20.2%), fistulectomy (380/2,509, 15.1%), ileostomy/pancreatic necrosectomy (271/2,509, 10.8%), appendicectomy (192/2,509, 7.6%), hemicolectomy (84/2,509, 3.35%) splenectomy (24/2,509, 0.96%), and liver resection (12/2,509, 0.48%). The incidence of SSI was found to be highest in hemicolectomy and liver resection surgeries, 8.33% each. This was followed by appendicectomy (5.21%), laparotomy (4.33%), splenectomy (4.17%), and ileostomy/ pancreatic necrosectomy (4.06%) with an overall incidence of 2.98% (75/2509). The rate of SSIs was found to increase along the spectrum from clean (0.08%), clean-contaminated (0.5%), dirty wound types (0.5%), and contaminated (1.9%), as per the criteria laid down by CDC.

Table 1 Distribution of abdominal surgeries and surgical site infections (SSIs)

Surgical procedure	No. of patients  (n = 2509)	No. of (SSI) (n = 75)	Percentage (%) of SSI
Cholecystectomy	975	17	1.74
Appendicectomy	192	10	5.21
Laparotomy	508	22	4.33
Fistulectomy	380	4	1.05
Hepaticojejunostomy/gastrojejunostomy	63	2	3.17
Ileostomy/pancreatic necrosectomy	271	11	4.06
Hemicolectomy	84	7	8.33
Splenectomy	24	1	4.17
Liver resection	12	1	8.33

Risk Factors for SSI

Male gender was found to be associated with an increased risk of SSI as out of the 75 patients identified with SSI, the majority (50/75, 66.7%) were males. Another host demographic risk factor identified was the advanced age of the patient undergoing surgery, as many patients were greater than or equal to 50 years old (37/75, 49.3%). However, smoking was not associated with an increased risk of SSI (nonsmokers: 73/75, 97.4%). A total of 72 patients who developed SSI (96%) had a fully independent functional status, whereas 3 (4%) were immobile and required nursing care. Only three of the patients (4%) had diabetes mellitus. Other important risk factors identified were infected surgical site/concurrent infection at a distant site/sepsis (20/ 75, 26.7%) and obesity (15/75, 20%). Approximately 9.3% (7/75) had immunosuppression, and 2.6% of the patients had vascular disease.

Bacteriology of SSI

All 75 patients diagnosed with SSI revealed growth of one or the other organism from the pus discharge taken from the surgical site wound with the predominance of gram-negative organisms (89.3%). Escherichia coli was found to be the most frequent isolate (45.3%), followed by Klebsiella spp (20%), Acinetobacter spp(8%) and Pseudomonas (8%; [Fig. 1]). [Fig. 2] depicts the antibiotic resistance profile (%) of predominant gram-negative isolates in SSIs. All the isolates were found to be highly resistant to most of the antibiotics tested; however, Klebsiella and Acinetobacter were relatively more resistant. In the case of E. coli, resistance to commonly used antibiotics ranged from 11.7% (tigecycline) to 91.1% (ampicillin). However, the resistance to cephalosporins in the case of E. coli varied from 64.7% (cefuroxime) to 88.2% (cefotaxime). Additionally, 85.2% of the E. coli were resistant to fluoroquinolones. Carbapenems are relatively effective against E. coli with a resistance varying from 23.5%(imipenem) to 58.8% (ertapenem). Among Acinetobacter and Klebsiella pneumoniae isolates, resistance to third-generation cephalosporins varied from 75 to 100%. Conversely, Pseudomonas aeruginosa isolates showed relatively less resistance to commonly used antimicrobials. The prevalence of ESBL was found to be approximately 53% in the case of E. coli and Klebsiella isolates. In contrast, approximately 63% of the Acinetobacter species were found to be ESBL producers and only 16.6% of the Pseudomonas species were ESBL producers. However, a majority (83.3%) of Pseudomonas spp. were categorized as MDR, and the majority of Klebsiella isolates were XDR (73.3%; [Fig. 3]). Among the gram-positive organisms, Staphylococcus aureus remained the predominant pathogen. All S. aureus isolates were found to be resistant to ampicillin, penicillin, and methicillin (methicillin-resistant Staphylococcus aureus [MRSA]) and a few were found (12.5%) susceptible to amoxycillin–clavulanate combination. However, all the S aureus isolates from this study were found susceptible to linezolid, vancomycin, and teicoplanin.

Fig. 1 Distribution (%) of various isolates from infected surgical site (n = 75).

Fig. 2 Antibiotic-resistant profile (%) of predominant gram-negative isolates in surgical site infections.

Fig. 3 Distribution of multidrug resistant (MDR), extensively drug resistant (XDR), extended spectrum β lactamases (ESBL), AmpC β lactamases (AmpC), and metallo β lactamases (MBL) among the predominant gram-negative isolates.

Discussion

In this prospective study, the results indicate SSI incidence of 2.98% in patients with abdominal surgeries, which is far less than many previous reports from India and other developing countries with an incidence of 20 to25%.[12] [13] This may be due to the differences in surgical procedures, infection control practices, implementation of surgical prophylactic policies, antibiotic stewardship, and hospital environment. It has previously been demonstrated that stringent implementation of hospital infection control programs can drastically reduce infection by 35 to 50%.[14] [15]

The contaminated surgical site, advanced age, and male gender have been reported to be the main risk factors for SSI, as has been highlighted in various studies.[12] [13] [16] [17] [18] The patients undergoing potentially dirty surgeries had an 8 to 10-fold higher risk for developing SSI. An increase in SSI rates along the scale from clean (0.08%), clean-contaminated (0.5%), dirty wound types (0.5%), and contaminated (1.9%) has also been observed in this study as well. In this study, 49.3% of the patients had an age more than or equal to 50 years with an average of 47.3 ± 16.3 years, and there was male preponderance. It has been previously reported that there is a decreased deposition of collagen during the healing process at the surgical site in aging men may be responsible for this gender bias.[19] Further, the data obtained on the obese patient as associated risk factors in this study is corroborated by Segal et al.[5] Use of immunosuppressive/steroids has been associated with the risk of SSI; however, the underlying condition requiring these therapeutics in itself predisposes to the SSIs.[20] Therefore, additional studies to elucidate the use of immunosuppressive/steroids as the risk factors and its confounders are required. As against a previous study, diabetes mellitus was not associated with SSIs.[12] [13] [21]

The predominance of gram-negative organisms, specifically E. coli, in the development of SSIs in the patient with abdominal surgeries has already been reported in many studies,[22] [23] [24] [25] [26] although few other studies have observed K. pneumoniae as the commonest gram-negative bacteria from the SSIs.[27] All the S. aureus isolates were found to be resistant to ampicillin, penicillin, and methicillin (MRSA), and a few were found (12.5%) susceptible to amoxycillin–clavulanate combination. However, an incidence of MRSA in abdominal SSIs has been reported in the range varying from 14 to 56.5%.[28] [29] Inefficacy of penicillin in S. aureus isolates has been reported in previous studies as well.[23] However, S. aureus isolates from this study did not show any resistance toward linezolid, vancomycin, and teicoplanin. This corroborates with other studies as well.[30]

A very high level of resistance to most of the antimicrobials tested (as per the recommendations of NCCLS) among the gram-negative isolates, which is in line with previous studies (23–25, 28, 32). The level of resistance to quinolones was 85.2 to 93.3% in members of the family Enterobacteriaceae, whereas Acinetobacter species showed absolute resistance to fluoroquinolones. On the contrary, Pseudomonas species were relatively susceptible to this group of antibiotics. We observed very high levels of acquired resistance to third-generation cephalosporins, among gram-negative bacteria, with most of E. coli and K. pneumoniae being ESBL producers. These findings are supported by recent studies that show a very high proportion of ESBL-producing isolates.[24] [31] Further, carbapenems and minocycline were found to be more effective against gram-negative isolates in this study. In addition to the high rate of resistance to individual antibiotics, 100% of the gram-negative isolates were either MDR or XDR except for E. coli (90%), which is substantially higher than the previous reports.[27] [31]

Although the study included a large number (2,509) of patients with abdominal surgeries and out of these only 75 patients developed SSIs. However, the risk factors were studied only in patients with SSIs. No comparison of these risk factors was made with patients who did not develop SSIs. Hence, data could not be tested against a null hypothesis.

Conclusion

The overall SSI rate in patients undergoing abdominal surgeries in our hospital was comparatively low as compared with other Indian hospitals as well as other developing countries, indicating that a satisfactory hospital infection control program, antibiotic stewardship, and surgical prophylaxis were in place in our hospital. However, in view of the predominance of MDR gram-negative bacteria and MRSA, prophylactic strategies need to be re-evaluated to improve outcomes and minimize the emergence of antimicrobial resistance. There is a further need to improvise the implementation of antibiotic stewardship programs based on hospital infection surveillance data.

Conflict of Interest

None declared.

Acknowledgments

None.

Ethical Statement

Not applicable.

Author Contributions

All authors contributed equally to the article.

Data Availability Statement

There is no data associated with this work.

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Publication History

Received: 09 September 2022

Accepted: 07 November 2022

Article published online:
22 September 2023