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Risk factors for surgical site infections following open versus laparoscopic colectomies: a cohort study

Abstract

Background

Surgical site infections (SSIs) are among the most common healthcare-associated infections. Evaluating risk factors for SSIs among patients undergoing laparoscopic and open colorectal resections can aid in selecting appropriate candidates for each modality.

Methods

A cohort of all consecutive patients undergoing elective colorectal resections during 2008–2017 in a single center was analyzed. SSIs were prospectively assessed by infection control personnel. Patient data were collected from electronic medical records. Risk factors for SSIs were compared between patients who underwent laparoscopic and open surgeries. A multivariate analysis was performed for significant variables.

Results

During the study period, 865 patients underwent elective colorectal resection: 596 laparoscopic and 269 open surgeries. Mean age was 68.2 ± 15.1 years, weight 72.5 ± 18.3 kg and 441 (51%) were men. The most common indication for surgery was malignancy, in 767 patients (88.7%) with inflammatory bowel diseases and diverticulitis following (4.5% and 3.9%, respectively). Patients undergoing laparoscopic surgery were younger, had fewer comorbidities, shorter pre-operative hospitalizations, lower risk index scores, and lower rates of SSI, compared with open surgery. Independent risk factors for SSI following laparoscopic surgery were chronic obstructive pulmonary disease [odds ratio (OR) 2.655 95% CI (1.267, 5.565)], risk index ≥ 2 [OR 2.079, 95% CI (1.041,4.153)] and conversion of laparoscopic to open surgery [OR 2.056 95%CI (1.212, 3.486)]. Independent risk factors for SSI following open surgery were immunosuppression [OR 3.378 95% CI (1.071, 10.655)], chronic kidney disease [OR 2.643 95% CI (1.008, 6.933)], and need for a second dose of prophylactic antibiotics [OR 2.519 95%CI (1.074, 5.905)].

Conclusions

Risk factors for SSIs differ between laparoscopic and open colorectal resections. Knowledge of specific risk factors may inform patient selection for these modalities.

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Background

Surgical site infections (SSIs) are among the most common healthcare-associated infections (HAIs), accounting for approximately 20% of HAIs in the United States [1] and Europe [2]. Colorectal surgery is associated with a particularly high risk of SSI, with SSI rates ranging from 9 to 27% [3, 4].

A Cochrane review found that antibiotic prophylaxis reduced the risk of SSI following colorectal surgery from 39 to 13% [5].

The causative organisms of SSIs after colorectal surgery originate in the intestinal lumen, and are primarily Enterobacterales and anaerobic bacteria.

The risk for an SSI following colorectal surgery relates both to patient characteristics and to procedure-related factors. Superficial SSIs, deep SSIs and organ-space infections differ in their specific risk factors for SSIs [6].

Laparoscopy is an increasingly popular surgical approach for colorectal surgery in general and for colorectal resections in particular, as it is associated with improved post-operative morbidity, lower SSI rates and reduced post-operative mortality rates [7].

Risk factors for SSIs following laparoscopic colorectal resections are not as well described as for an open surgical approach, due to limitations of previous studies, including heterogeneous patient populations and surgical indications, limited sample sizes and inconsistent results [8,9,10]. In addition, data comparing risk factors for SSIs following laparoscopic and open colorectal resections in similar patient populations are lacking.

The primary objective of this cohort study was to compare the risk factors for SSIs between patients undergoing laparoscopic vs. open colorectal resections.

Methods

Study design and patients

This study was based on a prospective cohort consisting of all consecutive patients age 18 years or older who underwent elective (non-urgent) colorectal resection surgery at Meir Medical Center in Israel from January 1, 2008 through December 31, 2017.

Data collection

During the study period, SSIs were prospectively monitored by dedicated infection control practitioners (ICP) as part of an ongoing surveillance program of post-operative colorectal patients. The surveillance included direct observation of the patient and the surgical site 72 h post-surgery, a phone call to patients at day 30 after surgery and assessment of patient electronic medical records, including outpatient clinic visits, and antibiotic prescription in the community.

Definition of SSIs and their classification (superficial wound infection, deep wound infection or organ-space infection) were based on CDC guidelines [11]. Thus anastomotic leaks were considered space-organ infections and were not included as a cause for SSIs.

Standardized data collection was prospectively performed throughout the surveillance period. Additional data were historically collected from electronic medical records. Data on the following parameters was collected: age, sex, comorbidities, previous abdominal surgeries, risk index [12], indication for surgery, colonic segment resected, duration of pre-operative hospitalization, surgery duration, prophylactic antibiotics, ileostomy/colostomy, conversion of laparoscopic to open surgery, SSI occurrence, microbial pathogens in wound/surgical/drain/blood sample cultures, antibiotic therapy, re-operation, hospitalization duration, re-admission and death within 30 days of surgery.

Statistical analysis

Descriptive data of continuous and ordinal variables are presented as mean, median and standard deviation, Categorical variables are presented as percentages.

Chi-square, independent t-test and Wilcoxon rank-sum tests were used to test for differences in characteristics between patient groups. Logistic regression models were used to test the association between SSI and each of the variables in the laparoscopic and open surgery groups. Variables deemed important or variables with P-values ≤ 0.1 were eligible for multivariate regression analysis. Odds ratio values are presented, along with 95% confidence intervals (CI). Statistical significance was defined as P < 0.05. All data were analyzed using SPSS software, version 25.0 (IBM Corp. Armonk, NY, USA).

Ethical considerations

The study was approved by the Institutional Review Board of Meir Medical Center (59-17 MMC). Due to the retrospective nature of the study the need for consent was waived.

Results

Over the 10-year study period, 865 patients underwent elective colorectal resections, 596 laparoscopic surgery and 269 open surgery. The mean age was 68.2 ± 15.1 years, the mean weight was 72.5 ± 18.3 kg and 441 (51%) were men. The most common indication for surgery was malignancy, in 767 patients (88.7%), with inflammatory bowel diseases and diverticulitis following (4.5% and 3.9%, respectively). A total of 319 patients (36.9%) had undergone abdominal surgery prior to the index operation. SSIs were diagnosed in 197 patients (22.8%), of which 109 (12.6%) were superficial and 26 (3%) were deep wound infections and 59 (6.8%) were organ/space infections. The most common bacteria identified was Escherichia coli in 75 cultures, Enterococcus spp. in 29 cultures, Pseudomonas spp. in 27 cultures and Staphylococcus aureus in 7. Re-operation was performed in 52 (6%) patients and 17 patients (2%) died within 30 days of surgery.

The characteristics of the patients undergoing laparoscopic versus open surgery differed in several aspects (Table 1). They were younger, had fewer comorbidities, had shorter hospital stays prior to surgery, had a lower risk index scores and, as expected, fewer SSIs.

Table 1 Characteristics of patients undergoing laparoscopic versus open surgery

We investigated risk factors for SSIs for each surgical modality (Table 2).

Table 2 Risk-factors for surgical site infection (SSI) with laparoscopic and open surgeries

Risk factors for SSIs following laparoscopic surgeries were chronic kidney disease (CKD), chronic obstructive pulmonary disease (COPD), and diabetes mellitus (DM), high risk index score, need for a second intra-operative prophylactic antibiotic dose, and conversion of laparoscopic surgery to open surgery. We also included age, sex and weight in the regression analysis. Independent risk factors for infection following laparoscopic surgeries found in multivariate regression analysis were: COPD, OR 2.655, 95% CI (1.267, 5.565); Risk index ≥ 2, OR 2.079, 95% CI (1.041,4.153); and conversion to open surgery, OR 2.056, 95%CI (1.212, 3.486).

Risk factors for SSI following open surgeries were CKD, rectal surgery, and the need for a second intra-operative prophylactic antibiotic dose. The regression model included age, sex, weight, immunosuppression, cardiovascular disease (CVD), COPD, and risk index. Independent risk factors for SSIs following open surgeries found in multivariate regression analysis were: immunosuppression, OR 3.378, 95% CI (1.071, 10.655); CKD, OR 2.643 95% CI (1.008, 6.933); and the need for a second intra-operative prophylactic antibiotic dose, OR 2.519, 95% CI (1.074, 5.905).

Discussion

In this study of 865 patients undergoing elective colorectal surgery, we found different risk factors for SSIs among patients undergoing laparoscopic vs. open colorectal resections. Focusing on basic patient characteristics, COPD was a risk factor for an SSI following laparoscopic surgery but not following open surgery, whereas CKD and immunosuppression were risk factors following open surgery only. Many studies focused on modifiable risk factors, such as prophylactic antibiotics, surgical techniques, and bowel preparation. Patient characteristics are not subject to change but optimal patient selection for each surgical modality may affect the risk of infection.

Laparoscopic colorectal resection has become increasingly popular in the field of colorectal surgery, increasing in incidence from 15% of all colorectal resections in 2007 [13] to 56% in a study published in 2019. This rise in popularity is in part related to lower complication rates, including lower rates of SSIs, seen in laparoscopic surgery [14].

Laparoscopic surgery has been found safe and superior to open surgery in numerous patient outcomes and in a variety of patient populations. In our study, laparoscopic surgery was selected for most patients (69%). The research question we sought to answer was whether there were specific patient populations for which open surgery would be preferable with regard to the risk of SSI. Chronic obstructive pulmonary disease was found to be an independent risk factor for SSIs following laparoscopic but not open colorectal resection. Laparoscopic surgery, although minimally invasive, requires the creation of a pneumoperitoneum, thus reducing important pulmonary function parameters, such as dynamic compliance and functional residual capacity, which increases the risk of hypoxemia [15].

Laparoscopic surgery might increase the risk for an SSI among patients with COPD. In a study by Liao et al. patient outcomes following laparoscopic cholecystectomies were worse in 3954 COPD patients compared to age-and gender-matched non-COPD patients. They found increased rates of intensive care unit admission, longer durations of mechanical ventilation and hospitalization, and higher mortality rates. SSIs were not assessed in that study [16]. Other studies identified COPD as risk factor for SSIs in a mixed patient population undergoing colorectal surgery [17, 18], but the contribution of this risk factor for infection in the different surgical modalities could not be assessed. Drosdeck et al. did not find COPD to be a risk factor for SSIs in a study of 400 patients undergoing laparoscopic colorectal surgery. Of note, inclusion criteria in this study were different, and all patients whose surgeries were converted to open surgeries were excluded [19]. A large study of 4397 COPD patients compared complications of laparoscopic versus open colorectal surgery. In that study, laparoscopic surgery improved most surgical outcomes including ventilator requirement and SSIs by almost 50%. Of note, preoperative steroid use was more frequent in the open surgery cohort, as well as partially-dependent functional status, perhaps favoring the laparoscopic surgery group in relation to the risk of SSI [20]. An important factor in reconciling our results with those of Sujatha-Bhaskar et al. [20] is that the COPD grade and severity were not assessed in either study, possibly resulting in inclusion of significantly heterogeneous COPD patient populations, making comparison more difficult. A study with a more accurate assessment of COPD severity is needed before any conclusions can be drawn.

In our study, patients who had open surgery were older, had more comorbidities and were more likely to have undergone prior abdominal surgeries. We observed a more complex clinical course in patients undergoing open surgeries, with longer hospital stays and increased re-admission, re-operation and mortality rates. Immunosuppression and CKD were independent risk factors for SSIs following open but not laparoscopic surgery. Recovery time and hospital stays are shorter after laparoscopic surgeries, an effect found in patients with malignancies as well [13]. With regard to the risk of infection, immunosuppressed patients might benefit most from shorter hospital stays, which are observed more often following laparoscopic surgery.

Advanced age per se should not be considered an indication for open surgery. In a meta-analysis comparing laparoscopic and open surgeries in an elderly population, overall morbidity, as well as cardiovascular complications were lower after laparoscopic surgery [21, 22].

Other independent risk factors for SSIs included conversion of laparoscopic surgery to open surgery and the need for a second intra-operative prophylactic antibiotic dose in open surgeries; both are markers of a more complicated surgical course. Although this information is only available post-operatively, it may still serve as an indication for increased vigilance in search of infection among post-operative patients.

This study had several limitations. It was a single center study and some of the data were collected retrospectively from patient records. Body mass index, a known risk factor for SSIs, was missing from many records, forcing us to use weight as a surrogate marker. Of note, SSI, our major outcome, was assessed prospectively in real-time by experienced ICP.

Conclusion

Patient characteristics are known, non-modifiable risk factors for SSIs. We suggest that risk factors for SSIs differ between laparoscopic and open colorectal resections, and that knowledge of specific risk factors for SSIs may inform selection of the appropriate surgical modality for every patient.

Availability of data and materials

Data will be available per request (chowersm@post.tau.ac.il).

Code availability

Not applicable.

Abbreviations

SSIs:

Surgical site infections

OR:

Odds ratio

ICP:

Infection control practitioners

CKD:

Chronic kidney disease

COPD:

Chronic obstructive pulmonary disease

DM:

Diabetes mellitus

CVD:

Cardiovascular disease

References

  1. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, Lynfield R, Maloney M, McAllister-Hollod L, Nadle J, et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014;370(13):1198–208.

    Article  CAS  Google Scholar 

  2. European Centre for Disease Prevention and Control. Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals 2011–2012. Stockholm: ECDC; 2013.

    Google Scholar 

  3. European Centre for Disease Prevention and Control. Surgical site infections. In: ECDC. Annual epidemiological report for 2016. Stockholm: ECDC; 2018. https://www.ecdc.europa.eu/en/publications-data/healthcare-associated-infections-surgical-site-infections-annual-0. accessed May 2021

  4. Bratzler DW, Dellinger EP, Olsen KM, Perl TM, Auwaerter PG, Bolon MK, Fish DN, Napolitano LM, Sawyer RG, Slain D, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm. 2013;70(3):195–283.

    Article  CAS  Google Scholar 

  5. Nelson RL, Gladman E, Barbateskovic M. Antimicrobial prophylaxis for colorectal surgery. Cochrane Database Syst Rev. 2014;5:CD001181.

    Google Scholar 

  6. Segal CG, Waller DK, Tilley B, Piller L, Bilimoria K. An evaluation of differences in risk factors for individual types of surgical site infections after colon surgery. Surgery. 2014;156(5):1253–60.

    Article  Google Scholar 

  7. Kang CY, Chaudhry OO, Halabi WJ, Nguyen V, Carmichael JC, Stamos MJ, Mills S. Outcomes of laparoscopic colorectal surgery: data from the Nationwide Inpatient Sample 2009. Am J Surg. 2012;204(6):952–7.

    Article  Google Scholar 

  8. Kurmann A, Vorburger SA, Candinas D, Beldi G. Operation time and body mass index are significant risk factors for surgical site infection in laparoscopic sigmoid resection: a multicenter study. Surg Endosc. 2011;25(11):3531–4.

    Article  Google Scholar 

  9. Kvasnovsky C, Adams K, Sideris M, Laycock J, Haji A, Haq A, Nunoo-Mensah J, Papagrigoriadis S. Elderly patients have more infectious complications following laparoscopic colorectal cancer surgery. Colorectal Dis. 2016;18(1):94–100.

    Article  CAS  Google Scholar 

  10. Yamamoto S, Fujita S, Akasu T, Ishiguro S, Kobayashi Y, Moriya Y. Wound infection after elective laparoscopic surgery for colorectal carcinoma. Surg Endosc. 2007;21(12):2248–52.

    Article  Google Scholar 

  11. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control. 1999;27(2):97–132.

    Article  CAS  Google Scholar 

  12. Pastor C, Baek J-H, Varma MG, Kim E, Indorf LA, Garcia-Aguilar J. Validation of the risk index category as a predictor of surgical site infection in elective colorectal surgery. Dis Colon Rectum. 2010;53(5):721–7.

    Article  Google Scholar 

  13. Hinojosa MW, Murrell ZA, Konyalian VR, Mills S, Nguyen NT, Stamos MJ. Comparison of laparoscopic vs open sigmoid colectomy for benign and malignant disease at academic medical centers. J Gastrointest Surg. 2007;11(11):1423–9.

    Article  Google Scholar 

  14. Wang Z, Chen J, Wang P, Jie Z, Jin W, Wang G, Li J, Ren J. Surgical site infection after gastrointestinal surgery in China: a multicenter prospective study. J Surg Res. 2019;240:206–18.

    Article  Google Scholar 

  15. Salihoglu Z, Demiroluk S, Baca B, Ayan F, Kara H. Effects of pneumoperitoneum and positioning on respiratory mechanics in chronic obstructive pulmonary disease patients during Nissen fundoplication. Surg Laparosc Endosc Percutan Tech. 2008;18(5):437–40.

    Article  Google Scholar 

  16. Liao K-M, Tseng C-J, Chen Y-C, Wang J-J, Ho C-H. Outcomes of laparoscopic cholecystectomy in patients with and without COPD. Int J Chron Obstruct Pulmon Dis. 2019;14:1159.

    Article  Google Scholar 

  17. Kamboj M, Childers T, Sugalski J, Antonelli D, Bingener-Casey J, Cannon J, Cluff K, Davis KA, Dellinger EP, Dowdy SC, et al. Risk of Surgical Site Infection (SSI) following Colorectal Resection Is Higher in Patients With Disseminated Cancer: An NCCN Member Cohort Study. Infect Control Hosp Epidemiol. 2018;39(5):555–62.

    Article  Google Scholar 

  18. Sutton E, Miyagaki H, Bellini G, Shantha Kumara HM, Yan X, Howe B, Feigel A, Whelan RL. Risk factors for superficial surgical site infection after elective rectal cancer resection: a multivariate analysis of 8880 patients from the American College of Surgeons National Surgical Quality Improvement Program database. J Surg Res. 2017;207:205–14.

    Article  Google Scholar 

  19. Drosdeck J, Harzman A, Suzo A, Arnold M, Abdel-Rasoul M, Husain S. Multivariate analysis of risk factors for surgical site infection after laparoscopic colorectal surgery. Surg Endosc. 2013;27(12):4574–80.

    Article  Google Scholar 

  20. Sujatha-Bhaskar S, Alizadeh RF, Inaba CS, Koh CY, Jafari MD, Mills SD, Carmichael JC, Stamos MJ, Pigazzi A. Respiratory complications after colonic procedures in chronic obstructive pulmonary disease: does laparoscopy offer a benefit? Surg Endosc. 2018;32(3):1280–5.

    Article  Google Scholar 

  21. Antoniou SA, Antoniou GA, Koch OO, Pointner R, Granderath FA. Laparoscopic colorectal surgery confers lower mortality in the elderly: a systematic review and meta-analysis of 66,483 patients. Surg Endosc. 2015;29(2):322–33.

    Article  Google Scholar 

  22. Fujii S, Tsukamoto M, Fukushima Y, Shimada R, Okamoto K, Tsuchiya T, Nozawa K, Matsuda K, Hashiguchi Y. Systematic review of laparoscopic vs open surgery for colorectal cancer in elderly patients. World J Gastrointest Oncol. 2016;8(7):573–82.

    Article  Google Scholar 

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Acknowledgements

We thank Faye Schreiber for editorial assistance.

Funding

No funding was received for this work.

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Authors and Affiliations

Authors

Contributions

TH: data collection, data analysis, drafted the manuscript. PS: conception and design of study MC: interpretation of data, substantial revision of manuscript. All authors have approved the submitted version. All authors have agreed both to be personally accountable for the author's own contributions and to ensure that questions related to the accuracy or integrity of any part of the work, even ones in which the author was not personally involved, are appropriately investigated, resolved, and the resolution documented in the literature.

Corresponding author

Correspondence to Michal Chowers.

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Ethics approval and consent to participate

This study was approved by the Meir Medical Center ethics committee, reference number 59-17 MMC. Due to the retrospective nature of the study consent of participant was waived by the committee.

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Not applicable.

Competing interests

No conflict of interests for any of the authors.

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Hoffman, T., Shitrit, P. & Chowers, M. Risk factors for surgical site infections following open versus laparoscopic colectomies: a cohort study. BMC Surg 21, 376 (2021). https://doi.org/10.1186/s12893-021-01379-w

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