Randomized clinical trial of oral and intravenous versus intravenous antibiotic prophylaxis for laparoscopic colorectal resection
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1 Randomized clinical trial Randomized clinical trial of oral and intravenous versus intravenous antibiotic prophylaxis for laparoscopic colorectal resection A. Ikeda, T. Konishi, M. Ueno, Y. Fukunaga, S. Nagayama, Y. Fujimoto, T. Akiyoshi and T. Yamaguchi Department of Gastroenterological Surgery, Cancer Institute Hospital of the Japanese Foundation for Cancer Research, Ariake Koto-ku, Tokyo, , Japan Correspondence to: Dr T. Konishi ( Background: The use of oral prophylactic antibiotics for the prevention of surgical-site infection (SSI) in patients undergoing laparoscopic surgery for colorectal cancer is controversial. The aim of this RCT was to evaluate whether intravenous perioperative antibiotics are inferior to combined preoperative oral and perioperative intravenous antibiotics in this setting. Methods: Patients undergoing elective laparoscopic colorectal resection in a single cancer centre were assigned randomly to combined preoperative oral antibiotics (metronidazole and kanamycin) and perioperative intravenous antibiotics (cefmetazole) (oral/iv group) or to perioperative intravenous antibiotics (cefmetazole) alone (IV-only group). Patients were stratified for the analyses based on type of operation (colonic surgery, anterior resection or abdominoperineal resection), preoperative use of mechanical bowel preparation, preoperative chemoradiotherapy and the presence of diabetes mellitus. The primary endpoint was the overall rate of SSI. Secondary endpoints were the rates of incisional site infection, organ/space infection, anastomotic leakage, intra-abdominal abscess, adverse events and postoperative complications. Results: Of 540 patients offered participation in the trial in , 515 agreed to take part and were randomized. Some 256 patients in the IV-only group and 255 in the oral/iv group completed the treatment per protocol. The overall rate of SSI was 7 8 per cent (20 of 256) in the IV-only group and 7 8 per cent (20 of 255) in the oral/iv group, confirming that perioperative administration of intravenous antibiotics alone was not inferior to the combined regimen (P = 0 017). There were no differences in rates of incisional site infection (5 5 versus 5 9 per cent respectively), organ/space infection (2 3 versus 2 0 per cent) or other secondary endpoints between the two groups. Conclusion: Intravenous perioperative antimicrobial prophylaxis alone is not inferior to combined preoperative oral and intravenous perioperative prophylaxis with regard to SSI in patients with colorectal cancer undergoing elective laparoscopic resection. Registration number: UMIN ( Paper accepted 27 June 2016 Published online in Wiley Online Library ( DOI: /bjs Introduction Antimicrobial prophylaxis has become the standard means of preventing surgical-site infection (SSI) in patients undergoing elective colorectal cancer surgery. SSI leads to worse quality of life, longer hospital stay and increased cost. It is well established that perioperative parenteral antibiotics reduce SSI and that systemic antimicrobial prophylaxis should be a standard component of studies investigating the effects of bowel preparation. Despite some guidelines recommending administration of a combination of preoperative non-absorbable oral and perioperative intravenous antibiotics to prevent SSI in patients undergoing colorectal surgery 1, the use of oral antibiotics has declined. Previous RCTs and meta-analyses 2 6 have reported conflicting findings regarding the impact of oral and parenteral antimicrobial prophylaxis on the incidence of SSI in patients undergoing gastrointestinal surgery BJS Society Ltd BJS
2 A. Ikeda, T. Konishi, M. Ueno, Y. Fukunaga, S. Nagayama, Y. Fujimoto et al. Most studies were heterogeneous and were not focused on laparoscopic surgery, where the incidence of SSI may be reduced. The aim of this trial was to evaluate the non-inferiority of intravenous perioperative antimicrobial prophylaxis alone versus combined oral preoperative and intravenous perioperative antimicrobial prophylaxis in patients undergoing laparoscopic surgery for colorectal cancer. Methods The study was conducted with the approval of the ethics committee of the Cancer Institute Hospital of the Japanese Foundation for Cancer Research, Tokyo, Japan. Written informed consent was obtained from all participants. This trial is registered with the UMIN Clinical Trials Registry (UMIN ). Study design This prospective RCT was designed to evaluate the non-inferiority of intravenous antimicrobial prophylaxis alone versus combined oral and intravenous antimicrobial prophylaxis in patients undergoing laparoscopic colorectal surgery. The primary endpoint was the overall rate of SSI. Secondary endpoints were the rates of incisional site infection, organ/space infection, anastomotic leakage, intra-abdominal abscess, adverse events and postoperative complications. Inclusion and exclusion criteria All consecutive patients with colorectal cancer undergoing elective laparoscopic colorectal resection from June 2013 to April 2014 in the Cancer Institute Hospital of the Japanese Foundation for Cancer Research were enrolled. The following exclusion criteria were applied: age less than 20 years; patients with bowel obstruction and who could not tolerate liquid intake; pregnancy; history of allergy to the drugs in the protocol; administration of antibiotics in the 2 weeks before surgery; severe dysfunction of liver, kidney, heart or lung; and synchronous resection of other major organs such as the stomach, liver or uterus. Patients undergoing synchronous resection of the gallbladder or ovary were not excluded. Patients with incomplete bowel obstruction tolerating liquid intake were included in the study. Patient randomization Eligible patients were assigned randomly to one of the two groups. Patients in the intravenous (IV)-only group received 1 g cefmetazole intravenously at least 30 min before skin incision, then every 3 h during surgery until skin closure. After completion of surgery, two additional doses of intravenous prophylaxis were given within 24 h. Patients in the combined oral/intravenous (oral/iv) group received two oral doses of 750 mg metronidazole with 1000 mg kanamycin at and hours on the day before the surgery in addition to the same intravenous antibiotic regimen as patients in the IV-only group. The sequentially numbered, opaque, sealed envelopes system was used for patient randomization. At randomization, patients were stratified according to planned type of surgery (colonic surgery, anterior resection or abdominoperineal resection), preoperative use of mechanical bowel preparation with magnesium citrate, preoperative chemoradiotherapy, and the presence of diabetes mellitus with a haemoglobin A1c level above 7 0 mg/dl or requiring medical therapy. The sets of envelopes were prepared for each combination of the stratification categories, and patients were randomized using the corresponding sets of envelopes. Randomization was done in the trial centre. After obtaining the patient s informed consent before surgery for participation in the trial, an envelope was opened by an independent clinician. The results of the allocations were not informed to the infection control doctors or nurses who determined SSI, but neither patients nor surgeons were masked to the assignment. All antibiotics in the protocol regimen were prescribed according to standard clinical and compliance protocols. Perioperative protocols and surgical procedures All patients, except those with bowel obstruction, underwent mechanical bowel preparation with magnesium citrate at hours and sodium picosulfate at hours on the day before surgery. Patients had all hair within the proposed surgical field shaved using electrical hair-clippers after induction of anaesthesia, and the skin was prepared with povidone iodine. Mobilization of the bowel, ligation of vessels and lymph node dissection were performed intracorporeally. In patients undergoing colonic surgery an extracorporeal functional end-to-end anastomosis or intracorporeal anastomosis with a double-stapling technique was employed depending on the anastomosis location, whereas in those undergoing anterior resection an intracorporeal double-stapled or hand-sewn coloanal anastomosis was employed. Surgical wounds were covered with disposable wound protectors during the extracorporeal part of the procedure. In some patients undergoing anterior resection, closed drains were placed behind the anastomotic site. After all gloves had been changed, the fascia
3 Prophylaxis of surgical-site infection in laparoscopic colorectal resection Assessed for eligibility n = 554 Enrolment Excluded n = 39 Exclusion criteria met n = 12 Preoperative use of other antibiotics n = 8 Planned synchronous liver resection n = 1 Severe renal failure n = 1 Allergy to kanamycin n = 2 Declined participation n = 25 Other reason n = 2 Randomized n = 515 Allocation Allocated to IV-only group n = 257 Received allocated treatment n = 257 Converted to open surgery n = 1 Allocated to oral/iv group n = 258 Received allocated treatment n = 256 Did not receive allocated treatment n = 2 Oral intake not tolerated owing to obstruction n = 2 Converted to open surgery n = 1 Follow-up Lost to follow-up n = 0 Lost to follow-up n = 0 Analysis Analysed n = 256 Analysed n = 255 Fig. 1 CONSORT diagram for the study. IV, intravenous Table 1 Patient characteristics IV-only group (n = 256) Oral/IV group (n = 255) Age (years)* 62 (29 86) 65 (27 93) Sex ratio (M : F) 141 : : 114 BMI (kg/m 2 )* 22 8 ( ) 22 4 ( ) ASA fitness grade I 86 (33 6) 68 (26 7) II 165 (64 5) 180 (70 6) III 5 (2 0) 7 (2 7) Smoker 104 (40 6) 106 (41 6) Diabetes mellitus 31 (12 1) 37 (14 5) Previous history of 75 (29 3) 85 (33 3) abdominal surgery Preoperative 40 (15 6) 31 (12 2) radiotherapy Mechanical bowel preparation 216 (84 4) 223 (87 5) Values in parentheses are percentages unless indicated otherwise; *values are median (range). IV, intravenous. was closed with monofilament absorbable sutures. Incision sites were washed with saline, and subcuticular sutures were placed for skin closure. Subcutaneous drains were not used. The incisional sites were covered with sterile dressings that were removed within 48 h. Intra-abdominal drains were removed 5 7 days after the operation. All procedures were performed or supervised by six expert colorectal Table 2 Operations and pathology IV-only group (n = 256) Oral/IV group (n = 255) Surgical procedure Colonic surgery 155 (60 5) 154 (60 4) Anterior resection 89 (34 8) 88 (34 5) APR 12 (4 7) 13 (5 1) Stoma creation 57 (22 3) 63 (24 7) Duration of surgery* 232 ( ) 227 ( ) Blood loss* 15 (0 1200) 15 (0 620) Blood transfusion 0 (0) 0 (0) Abdominal drain 124 (48 4) 119 (46 7) ptnm stage 0 14 (5 5) 11 (4 3) I 71 (27 7) 77 (30 2) II 61 (23 8) 72 (28 2) III 72 (28 1) 66 (25 9) IV 29 (11 3) 19 (7 5) Other tumour 9(3 5) 10 (3 9) Values in parentheses are percentages unless indicated otherwise; *values are median (range). Three and one total abdominal colectomy operations are included in the intravenous (IV)-only group and oral/intravenous (oral/iv) group respectively. One total proctocolectomy is included in the oral/iv group. One total proctocolectomy is included in the IV-only group. Includes 12 neuroendocrine tumours, two gastrointestinal stromal tumours, four recurrent adenocarcinomas and one adenoma with severe dysplasia. APR, abdominoperineal resection.
4 A. Ikeda, T. Konishi, M. Ueno, Y. Fukunaga, S. Nagayama, Y. Fujimoto et al. Table 3 Surgical-site infections IV-only group (n = 256)* Oral/IV group (n = 255)* Absolute difference (%) Odds ratio P Overall SSI 20 (7 8) 20 (7 8) 0 03 ( 4 00, 3 94) 0 017# Incisional site infection 14 (5 5) 15 (5 9) 0 93 (0 44, 1 96) 0 840** Perineal incisional site 3of12(25) 2of13(15) 1 83 (0 25, 13 47) 0 645** Abdominal incisional site 11 (4 3) 13 (5 1) 0 84 (0 37, 1 90) 0 669** Organ/space infection 6 (2 3) 5 (2 0) 1 20 (0 36, 3 98) 1 000** Intra-abdominal abscess 0 (0) 2 (0 8) 0 249** Anastomotic leak 6 of 244 (2 5) 3 of 242 (1 2) 2 01 (0 50, 8 12) 0 504** Values in parentheses are *percentages, 90 per cent c.i. for non-inferiority and 95 per cent c.i. Analysis performed in the patients who had an abdominoperineal resection. Analysis performed in patients with an anastomosis. IV, intravenous; SSI, surgical-site infection. #One-sided P value for non-inferiority of the primary endpoint (Dunnett Gent test). **Two-sided P value for the secondary endpoint (Pearson s χ 2 or Fisher s exact test). Table 4 Surgical-site infections according to surgical procedure IV-only group (n = 256) Oral/IV group (n = 255) Odds ratio* P Overall SSIs All procedures 20 (7 8) 20 (7 8) 1 00 (0 52, 1 90) Right colectomy 6 of 70 (9) 2 of 77 (3) 3 52 (0 69, 18 03) Left colectomy 6 of 85 (7) 6 of 77 (8) 0 90 (0 28, 2 91) Anterior resection 5 of 89 (6) 8 of 88 (9) 0 60 (0 19, 1 90) APR 3of12(25) 4of13(31) 0 75 (0 13, 4 36) Incisional site infections All procedures 14 (5 5) 15 (5 9) 0 93 (0 44, 1 96) Right colectomy 6 of 70 (9) 2 of 77 (3) 3 52 (0 69, 18 03) Left colectomy 4 of 85 (5) 5 of 77 (6) 0 71 (0 18, 2 75) Anterior resection 1 of 89 (1) 5 of 88 (6) 0 19 (0 02, 1 65) APR 3of12(25) 3of13(23) 1 11 (0 18, 6 97) Organ/space infections All procedures 6 (2 3) 5 (2 0) 1 20 (0 36, 3 98) Right colectomy 0 of 70 (0) 0 of 77 (0) Left colectomy 2 of 85 (2) 1 of 77 (1) 1 83 (0 16, 20 61) Anterior resection 4 of 89 (5) 3 of 88 (3) 1 33 (0 29, 6 14) APR 0of12(0) 1of13(8) Values in parentheses are percentages unless indicated otherwise; *values in parentheses are 95 per cent c.i. IV, intravenous; SSI, surgical-site infection; APR, abdominoperineal resection. surgeons, each of whom had performed more than 500 laparoscopic colorectal operations and had a board certification in laparoscopic surgery from the Japan Society for Endoscopic Surgery. Determination of surgical-site infection SSI was defined according to the guidelines issued by the Centers for Disease Control and Prevention 1.Briefly, the criteria for incisional SSI were infections occurring at the incisional site within 30 days after the procedure and involving the skin, subcutaneous tissue, muscle and fascia but not the organ/space, together with at least one of the following: purulent drainage from the incision; an organism isolated from a culture of fluid from the incision; incisional pain, tenderness, localized swelling, redness or heat; an incision that dehisced spontaneously or was opened deliberately by a surgeon in the presence of the signs and symptoms of infection described above. Superficial and deep incisional SSIs were evaluated together under the umbrella term of incisional SSI. The criteria for organ/space SSI were infections occurring within 30 days of the procedure in any part of the anatomy that was opened or manipulated during the operation other than the incisional site, together with at least one of the following: purulent fluid from a drain placed into the organ/space; an organism isolated from a culture of fluid from the organ/space; abscess or other evidence of infection involving the organ/space found on direct examination, during reoperation, or by histopathological or radiological examination; diagnosis of an organ/space SSI by an attending physician. Patients were inspected daily for SSI until discharge by attending physicians and nurses, with follow-up for at least 30 days after surgery in the outpatient clinic. Final decisions concerning SSI were made by independent SSI surveillance doctors and infection control nurses.
5 Prophylaxis of surgical-site infection in laparoscopic colorectal resection No. of patients Odds ratio P Surgery type Mechanical BP CRT Diabetes mellitus Age (years) Sex Smoker BMI (kg/m 2 ) ptnm stage Duration of surgery (min) Blood loss (ml) Abdominal drain Ostomy creation Colon (0 61, 3 86) AR (0 19, 1 90) APR (0 13, 4 36) Yes (0 48, 1 97) No (0 22, 5 19) Yes (0 10, 1 18) No (0 65, 3 22) Yes (0 04, 3 83) No (0 55, 2 16) (0 31, 1 98) < (0 50, 3 20) M (0 41, 1 82) F (0 35, 5 17) Yes (0 24, 1 51) No (0 67, 4 55) (0 50, 6 39) < (0 38, 1 72) 0 II (0 31, 1 79) III IV (0 57, 4 55) (0 42, 2 13) < (0 35, 3 04) (0 19, 2 74) < (0 51, 2 23) Yes (0 26, 1 41) No (0 71, 6 46) Yes (0 10, 1 06) No (0 84, 4 81) Favours IV-only group Favours oral/iv group Fig. 2 Forest plot of the treatment effect of oral antimicrobial prophylaxis in the subgroups. Odds ratios are shown with 95 per cent confidence intervals, calculated by logistic regression. AR, anterior resection; APR, abdominoperineal resection; BP, bowel preparation; CRT, chemoradiotherapy; IV, intravenous Sample size The predetermined non-inferiority margin δ was an absolute 5 per cent increase in overall SSI in the IV-only group compared with the oral/iv group. Assuming a one-sided α of 0 05, a power of 80 per cent and a 5 per cent incidence of overall SSI in both groups, 235 patients per group were needed (Dunnett Gent test) 7. Assuming an 8 per cent drop-out rate, the planned required sample size was 253 patients. The non-inferiority margin of 5 per cent was set only for the primary endpoint. Non-inferiority was to be judged when the upper limit of the 90 per cent confidence interval of the absolute difference between the incidences of SSI was lower than δ=5 per cent. Statistical analysis Continuous variables were analysed using Student s t test, and categorical valuables with Pearson s χ 2 test or Fisher s exact test, as appropriate. Subgroups were analysed by logistic regression to assess the treatment effects of oral prophylaxis in various subgroups. Because of the exploratory nature of subgroup comparisons, test results were reported without multiplicity adjustments for type I error. Statistical analysis was performed using JMP software version 9 0 and SAS software version 9 4 (both from SAS Institute, Cary, North Carolina, USA). P < was considered statistically significant. Results Among a total of 554 patients with colorectal cancer undergoing elective laparoscopic colorectal resection from June 2013 to April 2014, 540 were eligible for the study and 515 agreed to participate (Fig. 1). These 515 patients were randomly assigned: 257 patients were allocated to receive only
6 A. Ikeda, T. Konishi, M. Ueno, Y. Fukunaga, S. Nagayama, Y. Fujimoto et al. Table 5 Surgical complications IV-only group (n = 256) Oral/IV group (n = 255) Odds ratio* P MI/arrhythmia 1 (0 4) 1 (0 4) 1 00 (0 06, 16 01) DVT/PE 0(0) 0(0) Small bowel obstruction 14 (5 5) 9 (3 5) 1 58 (0 67, 3 72) Anastomotic haemorrhage 3 of 244 (1 2) 3 of 242 (1 2) 0 99 (0 20, 4 96) Anastomotic leak 6 of 244 (2 5) 3 of 242 (1 2) 2 01 (0 50, 8 12) Bleeding requiring transfusion 0 (0) 0 (0) Enterocolitis 4 (1 6) 1 (0 4) 4 03 (0 45, 36 32) CD pseudomembranous colitis 1 (0 4) 0 (0) Urinary tract disorder 7 (2 7) 6 (2 4) 1 17 (0 39, 3 52) Stoma-related problem 2 (0 8) 1 (0 4) 2 00 (0 18, 22 20) Other complication 11 (4 3) 7 (2 8) 1 59 (0 61, 4 17) Readmission within 30 days 1 (0 4) 0 (0) Perioperative death 0 (0) 0 (0) Values in parentheses are percentages unless indicated otherwise; *values in parentheses are 95 per cent c.i. IV, intravenous; MI, myocardial infarction; DVT, deep vein thrombosis; PE, pulmonary embolism; CD, Clostridium difficile. intravenous antibiotics (IV-only group) and 258 to receive combined oral/intravenous antibiotics (oral/iv group). All patients except for two received the planned antimicrobial doses and were followed up for 30 days after surgery. One patient in each group had a conversion to open operation. Finally, 511 patients were analysed. Table 1 shows the patient characteristics of the two groups, which were well balanced at baseline. Forty patients in the IV-only group and 32 in the oral/iv group did not receive mechanical bowel preparation because of tumour-related bowel obstruction. Operative and pathological backgrounds were also well balanced between the two groups (Table 2). Median (range) blood loss was 15 (0 1200) ml and median (range) duration of surgery was 230 ( ) min. The rates of overall, incisional and organ/space SSI in the two groups combined were 7 8, 5 7 and2 2 per cent respectively (Table 3). The overall rate of SSI was 7 8 per cent in both the IV-only and oral/iv group. The absolute difference was 0 03 (90 per cent c.i to 3 94, 95 per cent c.i to 4 70) per cent. The upper limit of the 90 per cent c.i. for the absolute difference (3 94) was lower than the preset 5 per cent margin specified in the protocol (P = 0 017, Dunnett Gent test). The results confirmed the non-inferiority of intravenous antibiotics alone compared with combined oral/intravenous antibiotics. Anastomotic leakage was observed in 2 5 per cent of the IV-only group and in 1 2 per cent of the oral/iv group (P = 0 504) (Table 3). Additionally, there were no significant differences between the two groups in the rates of all types of SSI, including perineal and abdominal incisional site infections, and intra-abdominal abscess. The rates of SSI according to surgical procedure are summarized in Table 4. The proportions of each procedure were well balanced between the two groups. There were no significant differences between the groups in overall SSI, incisional site infections or organ/space infections for all types of procedure. When the treatment effects of oral microbial prophylaxis in various subgroups were assessed, no subgroup showed an increased incidence of overall SSI with omission of oral antimicrobial prophylaxis, including the subgroups stratified in randomization (Fig. 2). No significant differences were found between the groups in surgical complications other than SSI (Table 5). Enterocolitis occurred at a low rate: in only four patients in the IV-only group (1 6 per cent) and in one patient in the oral/iv group (0 4 per cent). One patient in the IV-only group developed Clostridium difficile pseudomembranous colitis. There were no perioperative deaths. Discussion This study found that use of intravenous antibiotics alone was not inferior to the combined administration of oral and intravenous antibiotics with regard to SSI in patients with colorectal cancer undergoing elective laparoscopic resection. The rates of overall, incisional and organ/space infection were similar in the two groups. Recent RCTs and meta-analyses have reported conflicting results concerning the benefit of oral non-absorbable antibiotics in reducing SSI in patients undergoing colorectal surgery. In an RCT in 2002, Lewis 6 found that a combination of oral and systemic antibiotics was superior to systemic antibiotics alone for the prevention of SSI in patients undergoing elective colonic surgery. However, in 2005, Espin-Basany and colleagues 3 drew the opposite conclusion: their RCT showed that adding oral to systemic antibiotics conferred no advantage over systemic
7 Prophylaxis of surgical-site infection in laparoscopic colorectal resection antibiotics alone. Kobayashi and co-workers 4,inthelargest reported RCT of the three, found that combined oral and intravenous antibiotics did not reduce the incidence of SSI compared with intravenous antibiotics alone. A meta-analysis 8 of 16 RCTs published from 1979 to 2007 reported that a combination of oral and intravenous antibiotics achieved a lower incidence of wound infection than intravenous antibiotics alone. These contradictory outcomes could be attributable to the heterogeneity of the study populations, which included cancer and benign disease, open and laparoscopic surgery, and elective and emergency operations. The present findings suggest that administration of oral antibiotics may be redundant in laparoscopic colorectal resection. Their omission would reduce healthcare costs 9, if these results were valid in other hands note that the overall SSI rate in the present study was lower than that reported from other centres 3 6, Rates of other complications were also low in this trial, indicating good surgical quality. It is unlikely that morbidity was underestimated because prospective surveillance was performed for 30 days, including outpatient clinics. Previous studies have employed a variety of regimens for oral antibiotic prophylaxis 6,9. In this study, kanamycin plus metronidazole was chosen. Kanamycin, an oral non-absorbable aminoglycoside, has a broad spectrum of activity against aerobic flora. Metronidazole is a nitroimidazole with a spectrum of activity against anaerobic bacteria. In the protocol, patients received two doses of oral antibiotics the day before operation, in contrast to most previous studies, which provided at least three doses 3,4,17. With regard to this point, Espin-Basany et al. 3 demonstrated no significant differences in the incidence of wound infection among patients receiving either three doses, one dose, or no dose of oral antibiotics. Song and Glenny 9 also demonstrated no significant differences in the incidence of wound infection among many different regimens, as long as the regimen covered both aerobic and anaerobic bacteria. Basic scientific observations of antimicrobial prophylaxis and the faecal flora have shown that production of collagenase and matrix metalloproteinase 9 by Pseudomonas aeruginosa and Enterococcus faecalis is enhanced in the inflammatory milieu of an anastomosis 18,19. These findings suggest a possible impact of these microorganisms on promoting anastomotic leakage, and thus oral microbial prophylaxis might reduce leakage by eradicating these microorganisms 9,18,19. The present study is evidently underpowered to provide any conclusions regarding the contribution of oral microbial prophylaxis in reducing anastomotic leakage. In the subset analyses, no subgroup showed an increase in SSI with omission of oral antimicrobial prophylaxis. The findings are consistent with the primary outcome of the study, although these subset analyses were exploratory in nature and not powered for differences. Other limitations include that this was a single-centre rather than a multicentre RCT, and that it was not double-blinded. The infection control doctors and nurses who determined SSIs were blinded to the assignment, thus reducing bias in assessment of the primary endpoint. Randomization was performed using the opaque envelopes system, which may have a potential risk of subversion compared with randomization by a computer program. This trial was conducted in a specialized high-volume centre with a low conversion rate, and the majority of patients were non-obese with ASA grade I or II. In these respects, characteristics of the present patients may differ from those of patients cared for in other settings, such that the results may not be generalizable. Acknowledgements The authors thank the infection control nurses (K. Ida and T. Akatsuchi) and surgeons (T. Nagasaki, J. Nagata, T. Mukai, R. Ohno, K. Tomori, A. Murata, M. Takeda, Y. Takeda, E. Kusumoto) who participated in the surveillance programme for SSI implemented at the Cancer Institute Hospital of the Japanese Foundation for Cancer Research. The authors also thank N. Ishizuka from the clinical trial department for the statistical analysis. Disclosure: The authors declare no conflict of interest. References 1 Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol 1999; 20: Nelson RL, Gladman E, Barbateskovic M. Antimicrobial prophylaxis for colorectal surgery. Cochrane Database Syst Rev 2014; (5)CD Espin-Basany E, Sanchez-Garcia JL, Lopez-Cano M, Lozoya-Trujillo R, Medarde-Ferrer M, Armadans-Gil L et al. Prospective, randomised study on antibiotic prophylaxis in colorectal surgery. Is it really necessary to use oral antibiotics? Int J Colorectal Dis 2005; 20: Kobayashi M, Mohri Y, Tonouchi H, Miki C, Nakai K, Kusunoki M et al.; Mie Surgical Infection Research Group. Randomized clinical trial comparing intravenous antimicrobial prophylaxis alone with oral and intravenous antimicrobial prophylaxis for the prevention of a surgical site infection in colorectal cancer surgery. Surg Today 2007; 37:
8 A. Ikeda, T. Konishi, M. Ueno, Y. Fukunaga, S. Nagayama, Y. Fujimoto et al. 5 Roos D, Dijksman LM, Tijssen JG, Gouma DJ, Gerhards MF, Oudemans-van Straaten HM. Systematic review of perioperative selective decontamination of the digestive tract in elective gastrointestinal surgery. Br J Surg 2013; 100: Lewis RT. Oral versus systemic antibiotic prophylaxis in elective colon surgery: a randomized study and meta-analysis send a message from the 1990s. Can J Surg 2002; 45: Dunnett CW, Gent M. An alternative to the use of two-sided tests in clinical trials. Stat Med 1996; 15: Bellows CF, Mills KT, Kelly TN, Gagliardi G. Combination of oral non-absorbable and intravenous antibiotics versus intravenous antibiotics alone in the prevention of surgical site infections after colorectal surgery: a meta-analysis of randomized controlled trials. Tech Coloproctol 2011; 15: Song F, Glenny AM. Antimicrobial prophylaxis in colorectal surgery: a systematic review of randomized controlled trials. Br J Surg 1998; 85: Tschan F, Seelandt JC, Keller S, Semmer NK, Kurmann A, Candinas D et al. Impact of case-relevant and case-irrelevant communication within the surgical team on surgical-site infection. Br J Surg 2015; 102: Bergs J, Hellings J, Cleemput I, Zurel Ö, De Troyer V, Van Hiel M et al. Systematic review and meta-analysis of the effect of the World Health Organization surgical safety checklist on postoperative complications. Br J Surg 2014; 101: Wang ZX, Jiang CP, Cao Y, Ding YT. Systematic review and meta-analysis of triclosan-coated sutures for the prevention of surgical-site infection. Br J Surg 2013; 100: Kobayashi S, Ito M, Yamamoto S, Kinugasa Y, Kotake M, Saida Y et al. Randomized clinical trial of skin closure by subcuticular suture or skin stapling after elective colorectal cancer surgery. Br J Surg 2015; 102: Roos D, Dijksman LM, Oudemans-Van Straaten HM, De Wit LT, Gouma DJ, Gerhards MF. Randomized clinical trial of perioperative selective decontamination of the digestive tract versus placebo in elective gastrointestinal surgery. Br J Surg 2011; 98: Gervaz P, Bandiera-Clerc C, Buchs NC, Eisenring M-C, Troillet N, Perneger T et al. Scoring system to predict the risk of surgical-site infection after colorectal resection. Br J Surg 2012; 99: Kelly M, Bhangu A, Singh P, Fitzgerald JE, Tekkis PP. Systematic review and meta-analysis of trainee- versus expert surgeon-performed colorectal resection. Br J Surg 2014; 101: Takesue Y, Yokoyama T, Akagi S, Ohge H, Murakami Y. A brief course of colon preparation with oral antibiotics. Surg Today 2000; 30: Olivas AD, Shogan BD, Valuckaite V, Zaborin A, Belogortseva N, Musch M et al. Intestinal tissues induce an SNP mutation in Pseudomonas aeruginosa that enhances its virulence: possible role in anastomotic leak. PLoS One 2012; 7: e Shogan BD, Belogortseva N, Luong PM, Zaborin A, Lax S, Bethel C et al. Collagen degradation and MMP9 activation by Enterococcus faecalis contribute to intestinal anastomotic leak. Sci Transl Med 2015; 7: 286.
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