Hernia DOI 10.1007/s10029-014-1275-z
ORIGINAL ARTICLE
Bacteria in hernia sac: an important risk fact for surgical site infection after incarcerated hernia repair L. Yang • H. Wang • X. Liang • T. Chen W. Chen • Y. Song • J. Wang
•
Received: 5 January 2014 / Accepted: 30 May 2014 Ó Springer-Verlag France 2014
Abstract Background Although some recent reports have proven that incarcerated and/or strangulated hernia is not contraindication to mesh repair, there is still a common concern owing to increased rate of postoperative surgical site infection (SSI). The aim of this clinical study was to evaluate factors that increase the risk of SSI after incarcerated hernia repair, and to identify the pathogens related to SSI. Methods A retrospective analysis was performed on data collected prospectively over a 4-year interval from January 2007 to December 2011. A total of 121 patients who underwent emergency surgery for incarcerated hernias were analyzed. Results 107 hernias were repaired using mesh versus 14 primary suture repairs. SSIs were observed in 9 of the 121 patients. Of 15 preoperative and intraoperative variables studied, duration of symptoms, diabetes mellitus, present of ileus, bowel resection or mesh repair performed, bacteria
present in hernia sac and cloudy fluid in hernia sac were found to be significant factors predicting SSI. On multivariate analysis only bowel resection, duration of symptoms and bacteria present in hernia sac were independent variables. The most common pathogen found in hernia sac and cultured from wound drainage or swab was Escherichia coli. The strains of bacteria cultured from wound drainage or swab were same as those cultured from fluid in hernia sac in six of nine patients. Conclusion Gut-sourced E. coli is an important common organisms associated with SSI after incarcerated hernia repair. Prosthetic mesh could be used when no bowel resection is performed, duration of symptoms less than 24 h and fluid hernia sac is clear. Keywords Infection
Incarceration Strangulation Hernia Mesh
Introduction L. Yang and H. Wang contributed equally to this work and should be considered as co-first authors. L. Yang H. Wang T. Chen W. Chen J. Wang (&) Department of Biliary-Pancreatic Surgery, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, 1630 S. Dongfang Road, Shanghai 200127, China e-mail: [email protected] H. Wang X. Liang Therapeutics Research Centre, Princess Alexandra Hospital, School of Medicine, The University of Queensland, Woolloongabba, QLD 4102, Australia Y. Song Department of Biostatistics, Institutes of Medical Sciences, School of Medicine, Shanghai Jiao Tong University, 280 S. Chongqing Road, Shanghai 200025, China
Meshes have been used for years in elective hernia repair with reduced postoperative pain and hernia recurrence rate. However, there is yet no consensus with regard to the use of prosthetic mesh in emergent repair of incarcerated hernia owing to infectious complications [1, 2]. Wound infection was reported in 0–11 % of the patients after mesh repair of the acutely incarcerated and/or strangulated hernia, which was obviously higher than those after elective hernia surgery [3]. Although recently several studies revealed effective and safe usage of mesh in patients undergoing incarcerated and strangulated hernia repair, this result has not been proven neither by preclinical studies nor by randomized controlled trials. Therefore, many surgeons are still afraid of increased rate of surgical site infection
123
Hernia
(SSI) could be associated with mesh implantation in the setting of incarcerated or strangulated bowel loop [2, 4, 5]. The US Centers for Disease Control (CDC) suggested three factors for SSI across a wide range of surgical procedures: fitness of the patient for operation, duration of surgery, and level of bacterial contamination of the wound [6]. In all three factors, the burden of pathogens inoculated into a surgical wound is relatively more important and well-recognized in mesh repair of inguinal hernia. It is reported that when foreign bodies are present, the bacterial inoculum required to cause SSI is lower [7]. Mesh bathed in nutritious body fluids, could become a fertile ground for intestinal or causative environmental bacterial colonization [8, 9]. The most common organisms reported in mesh infections are Staphylococcus aureus (S. aureus) and coagulase-negative staphylococci such as Staphylococcus epidermidis (S. epidermidis) [10–12]. Some antibiotic regimens known for their long half lives and activity against these pathogens have been used and wound infection-related readmissions were also reduced [2, 13]. However, there is no data on whether pathogens isolated from wound infection of elective hernia surgery are the same as those of incarcerated hernia repair. And there is limited data to support or refute the choice of certain prophylactic antibiotics to reduce SSI after prosthetic mesh repair of incarcerated hernia. The aim of this clinical and experimental study was to evaluate factors that increase the risk of SSI after incarcerated hernia repair, and to identify the pathogens related to SSI.
Materials and methods Patients This was a prospective analysis over a 4-year interval from January 2007 to December 2011. During the study interval, 121 consecutive patients diagnosed with incarcerated hernia admitted to the Department of General surgery, Renji Hospital. This study was undertaken after obtaining approval from the institutional committee. Incarceration was defined as irreducibility of a hernia, and a strangulated hernia was defined as an irreducible hernia with objective signs of ischemia or gangrene. Surgical procedure The skin of the patient was shaved immediately before surgery and prepared using povidone–iodine. All patients underwent general anesthesia. Perioperative IV antibiotics (2 g of ceftriaxone) was given 30 min before the operation, and continued until the fourth postoperative day. In
123
infected cases, the type of antibiotic regimen was changed according to the culture antibiogram results and hospital infection committee recommendations. Degree of contamination of operation fields was categorized according to classification from CDC [6] and American College of Surgeons. Clean wound means no inflammation was encountered and the gastrointestinal tract was not entered. Clean-contaminated wound refers to gastrointestinal tracts was entered without significant spillage. Contaminated wound has gross spillage from gastrointestinal tract without purulent inflammation. The choice of mesh repair was judged by the surgeons to have operation fields that were clean or clean-contaminated. No preference criterion was employed for the mesh repair method to be used. The mesh used in this study was monofilament polypropylene (Marlex, Bard, Ltd) and all sutures except subcuticular were 2/0 polypropylene (Prolene, Ethicon, Ltd). Skin was closed with 3–0 polyglactin (Vicryl, Ethicon, Ltd). All of the bowel resections were done without any enteric content contamination and through the primary incision. Bacterial culture studies Four-milliliter fluid from every sac of incarcerated hernia was taken for microbiologic examinations before opening the sac. If fluid in hernia sac was less than 4 mL, 4-mL sterile saline 0.9 % was injected into the hernia sac to wash the internal surface before opening. Serial tenfold dilutions of the fluid homogenate were made in 0.9 % saline and 100-lL volumes of the original suspension, then the dilutions were placed on both blood agar and differential media, and incubated at 35 °C in an atmosphere for 24 h. Bacterial growth was quantified from plates and expressed as colony-forming units per milliliter of specimen based on the volume of each specimen. Colonies on differential media were cultured 1 day more, and then inoculated and identified at the discrimination kit (bioMerieux SA, Lyon, France). Follow-up All wounds were inspected before discharge, and all incisions were carefully re-examined for early postoperative complications by the same surgeon, during suture removal at 7–9 days (first follow-up visit) and during the second follow-up visit 1 month after discharge. Patients were examined two times during the first year and yearly since the following year. The mean follow-up time was 25.6 months (11.5–52.3 months). Diagnosis of a superficial SSI or a deep SSI in followup was made according to the CDC definitions and classification [14, 15]. Superficial SSI occurs within 30 days after operation and involves only skin or
Hernia Table 1 Comparison of clinical characteristics related to SSI after prosthetic mesh repair of incarcerated hernia SSI (n = 9)
No infection (n = 112)
p
Median age (years)
69.3 ± 22.5
68.1 ± 18.2
Sex ratio (M:F)
7:2
85:17
0.165 1.000
BMI ASA grade
22.0 2
18.5 2
0.827 0.334
POSSUM physiological score
14.8
13.5
0.077
B24 h
0
89
[24 h
9
23
Direct
0
6
Indirect
5
76
Femoral
4
30
7 2
24 88
0.001
Present
8
41
0.003
Absent
1
71
Omentum
0
23
Small bowel
7
54
Colon
2
17
Duration of symptoms \0.0001
0.450
Diabetes mellitus
Ileus
Incarcerated organ
Others
a
0.287
0
2
0
16
Performed
5
10
Not performed
4
102
4 5
103 9
0.001
71.4 ± 13.5
61.7 ± 19.3
0.186
Returned Bowel resection
0.001
Mesh repair Performed Not performed Duration of operation (min) Bacteria in hernia sac Present
8
15
Absent
1
97
The Mann–Whitney U test was used to compare continuous variables and the v2 or Fisher’s exact test to compare discrete variables. Multivariate analysis was performed by means of the logistic regression method. P \ 0.050 was considered statistically significant. Statistical calculations were carried out with SPSS computer software (SPSS, Chicago, IL, USA).
Results Clinical characteristics
Hernia orifice
Present Absent
Statistical analysis
\0.0001
The median age of all patients was 68.4 (range 14.1–98.2) years. The male:female ratio was 4.8:1. The mean hospital stay was 5 days (range 2–24 days). In total, 107 hernias were repaired using mesh versus 14 primary suture repairs. All operation fields of primary suture repairs were considered ‘‘contaminated’’ by the surgeons. SSIs were observed in 9 of the 121 patients (7.4 %). Five patients had superficial SSI and four had deep SSI. None of the infected cases required mesh removal. During the follow-up period, there were no cases of mortality, recurrence or late-onset deep mesh infection. A comparison of the clinical characteristics between nine patients who had SSI and those who had no infection is shown in Table 1. Patients who had SSI after surgery were more likely to have duration of symptoms over 24 h (P \ 0.0001), diabetes mellitus (P = 0.001), with ileus (P = 0.003), bowel resection (P = 0.001) or mesh repair (P = 0.001), bacteria in hernia sac (P \ 0.0001) and with cloudy fluid in hernia sac (P \ 0.0001). Of the significant factors determined by univariate analysis (duration of symptoms, diabetes mellitus, present of ileus, bowel resection, mesh repair, bacteria present in hernia sac and cloudy fluid in hernia sac), only the bowel resection, duration of symptoms and bacteria present in hernia sac were found to be independent factors for SSI in the multivariate analysis (P \ 0.05).
Fluid in hernia sac Clear
8
13
Cloudy
1
99
\0.0001
SSI surgical site infection, BMI body mass index, POSSUM Physiological and Operative Severity Score for the enUmeration of Mortality and morbidity a
One case of bladder and one case of uterus
subcutaneous tissue of the incision. Deep SSI occurs within 1 year after surgery and involves fascial and muscle layers and also the graft.
Microbiology results Bacterial isolates were obtained in 23 of the 121 samples (19.0 %) of fluid in hernia sac. Positive rate of hernia sac fluid culture was higher in group with duration of symptoms exceeded 24 h (9/23) than group with duration of symptoms less than 24 h (0/89). Mean quantitative bacterial loads from fluid in hernia sac were 6.1 9 104/mL (6.4 9 106/mL in SSI group and 3.0 9 102/mL in group without infection). Eight species and 35 different strains of bacteria were identified and their percentages were shown
123
Hernia
Discussion
Proteus mirabilis 5.71% Citrobacter freundii 5.71% Bacillus cloacae 5.71%
Escherichia coli 37.14%
Enterococcus faecalis 8.75%
Pseudomonas aeruginosa 8.75%
Enterococcus faecium 11.43%
Klebsiella pneumoniae 17.14%
Fig. 1 Bacterial spectrum from fluid in hernia sac
Enterobacter cloacae 11.11%
Enterococcus faecalis 11.11%
Escherichia coli 33.33%
Proteus mirabilis 22.22%
Staphylococcus epidermidis 22.22%
Fig. 2 Bacterial spectrum from wound drainage or swab after SSI
in Fig. 1. The most common pathogen found in hernia sac was Escherichia coli, which was on 13 out of 35 samples (37.14 %). The second most common pathogen was Klebsiella pneumoniae, which was on 6 out of 35 samples (17.14 %). Bacterial isolates were obtained in all nine patients with SSI from wound drainage or swab culture. Five sorts and nine different strains of bacteria were identified and their percentages were shown in Fig. 2. The most common pathogen cultured from wound drainage or swab was E. coli, which was on three out of nine samples (33.33 %). The second most common pathogen was Staphylococcus epidermidis, which was on two out of nine samples (22.22 %). The strains of bacteria cultured from wound drainage or swab were same as those cultured from fluid in hernia sac in six of nine patients with SSI. In all four patients with deep SSI, the strains of bacteria cultured from wound drainage or swab were the same as those from fluid in hernia sac.
123
The majority of SSIs after hernia repair are related to pathogens found on skin flora, such as S. aureus or S. epidermidis, with S. aureus accounting for 53–75 % of all cases including mesh infection [11, 16]. Our study is the first to reveal that E. coli was another important common organisms associated with SSI after incarcerated hernia repair. To determine whether these pathogens were skinsourced or gut-sourced, collection of hernia sac fluid for bacterial culture was performed before opening the sac. We found that most strains of bacteria cultured from wound drainage or swab (6/9) were same as those cultured from fluid in hernia sac. In our series, bacteria present in hernia sac was one of the independent factors for SSI (P \ 0.05). Moreover, it was reported that the most common organism identified was also E. coli during gut bacterial translocation [17]. Thus, incision site of strangulated or incarcerated hernia, which is repaired under emergent conditions, would have more chances to be infected by virulent bacteria originating from the intestinal tract than from the skin. Previous studies have shown that wound contamination with greater than 105 microorganisms is required to cause SSI after abdominal hysterectomy [7, 18]. However, it is unlikely that intraoperative quantitative cultures would be available to surgeons, requiring clinical judgment at the time of repair. Only cloudy fluid in hernia sac would suggest the bacteria present. Eliminating gut-sourced bacterial contamination may be achieved by prophylactic antibiotherapy activity against pathogens such as E. coli, use of wound protector at the time of bowel resection, avoidance of mesh contact with the bowl or hernia sac fluid, and changing surgical gloves prior to handling the mesh [5, 19]. In our series of 121 patients underwent emergency operations, preoperative conditions such as BMI, ASA classification or POSSUM physiological score did not appear to influence the rate of SSI. Besides bacteria present in hernia sac, we found that bowel resection was also an independent factor for SSI. In all cases with bowel resection, we performed bowel resection via the same wound through which hernia repair was performed. Thus, wound might be contaminated by enteric bacteria during the bowel resection. The current study showed a tendency for SSI to occur in patients whose duration of symptoms exceeded 24 h. Previous studies have shown that the duration between the onset of symptoms and hospital admission was considered an important factor when determining the need for bowel resection [20, 21]. However, time from symptom onset to operation set as a cutoff value varied from 12 to 48 h in different reports [20–22]. We found that there were significantly more bacteria in hernia sac in patients who came to the hospital more than 24 h after symptom onset. The longer elapsed time from symptom onset to surgery
Hernia
may increase the incidence of enteric bacterial translocation of incarcerated bowel loop, and lead to SSI as a result. This could explain the association between duration of symptoms and the SSI rate in patients without bowel resection. Although some reports have proven that incarcerated and/or strangulated hernia is not contraindication to mesh repair [2, 4, 5], we suggest that prosthetic mesh could be used when no bowel resection performed, duration of symptoms less 24 h and fluid hernia sac was clear (no sign of bacteria present in hernia sac). There are some limitations to our study that deserve mention. First, the majority of patients in our study were Chinese. Differences in ethnic groups with a relatively different health status and system of care may have affected the results. Second, in this study, we were unable to study all available meshes. So our results might not be reproducible with another mesh. Third, there were different degrees of contamination in operation fields between the two repair groups. All operation fields of primary suture repairs were considered contaminated while those of mesh repairs were considered clean or clean-contaminated. Thus, only under this circumstance mesh repairs (4/103) had less SSI rate than primary suture repairs (5/9). Finally, bacterial spectrum and quantitative bacterial loads cultured from fluid in hernia sac must be viewed with caution. 4-mL fluid from sac of incarcerated hernia represents a small sample of bacterial ground evaluated. Although these results correlated nicely with our clinical and microbiologic outcomes, these might not be accurate. It is reported that mesenteric lymph nodes and serosal scrapings could be analyzed using microbiological techniques to identify gut translocation of bacteria [17]. Thus, we believe that microbiological analyzing hernia sac fluid could also quantify and evaluate gut translocation of bacteria in patients underwent operation for incarcerated hernia if no other ideal methods were developed. In conclusion, the findings of the present study revealed that gut-sourced E. coli is an important common organisms associated with SSI after incarcerated hernia repair. Prosthetic mesh could be used when no bowel resection performed, duration of symptoms less 24 h and fluid hernia sac is clear. Acknowledgments This work was supported by grants from Shanghai Bureau of the Health, China (XBR2011035, J. Wang), Shanghai Science and Technology Fund (12XD1403400, J. Wang) and Shanghai Young Teachers’ Development Program (ZZjdyx12070, H. Wang).
References 1. Atila K, Guler S, Inal A et al (2010) Prosthetic repair of acutely incarcerated groin hernias: a prospective clinical observational cohort study. Langenbecks Arch Surg 395:563–568
2. Topcu O, Kurt A, Soylu S et al (2013) Polypropylene mesh repair of incarcerated and strangulated hernias: a prospective clinical study. Surg Today 43:1140–1144 3. Bessa SS, Abdel-Razek AH (2013) Results of prosthetic mesh repair in the emergency management of the acutely incarcerated and/or strangulated ventral hernias: a seven years study. Hernia 17:59–65 4. Nieuwenhuizen J, van Ramshorst GH, ten Brinke JG et al (2011) The use of mesh in acute hernia: frequency and outcome in 99 cases. Hernia 15:297–300 5. Sawayama H, Kanemitsu K, Okuma T et al (2013) Safety of polypropylene mesh for incarcerated groin and obturator hernias: a retrospective study of 110 patients. Hernia. doi:10.1007/ s10029-013-1058-y 6. Gaynes RP, Culver DH, Horan TC, Edwards JR, Richards C, Tolson JS (2001) Surgical site infection (SSI) rate in the United States, 1992-1993: the National Nosocomial Infections Surveillance Systen basic SSI risk index. Clin Infect Dis 33:S69–S77 7. James RC, Macleod CJ (1961) Induction of staphylococcal infections in mice with small inocula introduced on sutures. Br J Exp Pathol 42:266–277 8. Geesey GG (2001) Bacterial behavior at surfaces. Curr Opin Microbiol 4:296–300 9. von Eiff C, Peters G, Heilmann C (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2:677–685 10. Taylor SG, O’Dwyer PJ (1999) Chronic groin sepsis following tension-free inguinal hernioplasty. Br J Surg 86:562–565 11. Mavros MN, Athanasiou S, Alexiou VG et al (2011) Risk factors for mesh-related infections after hernia repair surgery: a metaanalysis of cohort studies. World J Surg 35:2389–2398 12. Falagas ME, Kasiakou SK (2005) Mesh-related infections after hernia repair surgery. Clin Microbiol Infect 11:3–8 13. Yerdel MA, Akin EB, Dolalan S et al (2001) Effect of single-dose prophylactic ampicillin and sulbactam on wound infection after tension-free inguinal hernia repair with polypropylene mesh: the randomized, double-blind, prospective trial. Ann Surg 233:26–33 14. Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG (1992) CDC definitions of nosocomial surgical site infections. Infect Control Hosp Epidemiol 13:606–608 15. The Society for Hospital Epidemiology of America; The Association for Practitioners in Infection Control; The Centers for Disease Control; The Surgical Infection Society (1992) Consensus paper on the surveillance of surgical wound infections. Infect Control Hosp Epidemiol 10:599–605 16. Sadava EE, Krpata DM, Gao Y et al (2013) Does presoaking synthetic mesh in antibiotic solution reduce mesh infections? An experimental study. J Gastrointest Surg 17:562–568 17. O’Boyle CJ, MacFie J, Mitchell CJ et al (1998) Microbiology of bacterial translocation in humans. Gut 42:29–35 18. Houang ET, Ahmet Z (1991) Intraoperative wound contamination during abdominal hysterectomy. J Hosp Infect 19:181–189 19. Sanders DL, Kingsnorth AN, Lambie J et al (2013) An experimental study exploring the relationship between the size of bacterial inoculum and bacterial adherence to prosthetic mesh. Surg Endosc 27:978–985 20. Tanaka N, Uchida N, Ogihara H et al (2010) Clinical study of inguinal and femoral incarcerated hernias. Surg Today 40:1144–1147 21. Kurt N, Oncel M, Ozkan Z, Bingul S (2003) Risk and outcome of bowel resection in patients with incarcerated groin hernias: retrospective study. World J Surg 27:741–743 22. Alvarez JA, Baldonedo RF, Bear IG et al (2004) Incarcerated groin hernias in adults: presentation and outcome. Hernia 8:121–126
123
ORIGINAL ARTICLE
Bacteria in hernia sac: an important risk fact for surgical site infection after incarcerated hernia repair L. Yang • H. Wang • X. Liang • T. Chen W. Chen • Y. Song • J. Wang
•
Received: 5 January 2014 / Accepted: 30 May 2014 Ó Springer-Verlag France 2014
Abstract Background Although some recent reports have proven that incarcerated and/or strangulated hernia is not contraindication to mesh repair, there is still a common concern owing to increased rate of postoperative surgical site infection (SSI). The aim of this clinical study was to evaluate factors that increase the risk of SSI after incarcerated hernia repair, and to identify the pathogens related to SSI. Methods A retrospective analysis was performed on data collected prospectively over a 4-year interval from January 2007 to December 2011. A total of 121 patients who underwent emergency surgery for incarcerated hernias were analyzed. Results 107 hernias were repaired using mesh versus 14 primary suture repairs. SSIs were observed in 9 of the 121 patients. Of 15 preoperative and intraoperative variables studied, duration of symptoms, diabetes mellitus, present of ileus, bowel resection or mesh repair performed, bacteria
present in hernia sac and cloudy fluid in hernia sac were found to be significant factors predicting SSI. On multivariate analysis only bowel resection, duration of symptoms and bacteria present in hernia sac were independent variables. The most common pathogen found in hernia sac and cultured from wound drainage or swab was Escherichia coli. The strains of bacteria cultured from wound drainage or swab were same as those cultured from fluid in hernia sac in six of nine patients. Conclusion Gut-sourced E. coli is an important common organisms associated with SSI after incarcerated hernia repair. Prosthetic mesh could be used when no bowel resection is performed, duration of symptoms less than 24 h and fluid hernia sac is clear. Keywords Infection
Incarceration Strangulation Hernia Mesh
Introduction L. Yang and H. Wang contributed equally to this work and should be considered as co-first authors. L. Yang H. Wang T. Chen W. Chen J. Wang (&) Department of Biliary-Pancreatic Surgery, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, 1630 S. Dongfang Road, Shanghai 200127, China e-mail: [email protected] H. Wang X. Liang Therapeutics Research Centre, Princess Alexandra Hospital, School of Medicine, The University of Queensland, Woolloongabba, QLD 4102, Australia Y. Song Department of Biostatistics, Institutes of Medical Sciences, School of Medicine, Shanghai Jiao Tong University, 280 S. Chongqing Road, Shanghai 200025, China
Meshes have been used for years in elective hernia repair with reduced postoperative pain and hernia recurrence rate. However, there is yet no consensus with regard to the use of prosthetic mesh in emergent repair of incarcerated hernia owing to infectious complications [1, 2]. Wound infection was reported in 0–11 % of the patients after mesh repair of the acutely incarcerated and/or strangulated hernia, which was obviously higher than those after elective hernia surgery [3]. Although recently several studies revealed effective and safe usage of mesh in patients undergoing incarcerated and strangulated hernia repair, this result has not been proven neither by preclinical studies nor by randomized controlled trials. Therefore, many surgeons are still afraid of increased rate of surgical site infection
123
Hernia
(SSI) could be associated with mesh implantation in the setting of incarcerated or strangulated bowel loop [2, 4, 5]. The US Centers for Disease Control (CDC) suggested three factors for SSI across a wide range of surgical procedures: fitness of the patient for operation, duration of surgery, and level of bacterial contamination of the wound [6]. In all three factors, the burden of pathogens inoculated into a surgical wound is relatively more important and well-recognized in mesh repair of inguinal hernia. It is reported that when foreign bodies are present, the bacterial inoculum required to cause SSI is lower [7]. Mesh bathed in nutritious body fluids, could become a fertile ground for intestinal or causative environmental bacterial colonization [8, 9]. The most common organisms reported in mesh infections are Staphylococcus aureus (S. aureus) and coagulase-negative staphylococci such as Staphylococcus epidermidis (S. epidermidis) [10–12]. Some antibiotic regimens known for their long half lives and activity against these pathogens have been used and wound infection-related readmissions were also reduced [2, 13]. However, there is no data on whether pathogens isolated from wound infection of elective hernia surgery are the same as those of incarcerated hernia repair. And there is limited data to support or refute the choice of certain prophylactic antibiotics to reduce SSI after prosthetic mesh repair of incarcerated hernia. The aim of this clinical and experimental study was to evaluate factors that increase the risk of SSI after incarcerated hernia repair, and to identify the pathogens related to SSI.
Materials and methods Patients This was a prospective analysis over a 4-year interval from January 2007 to December 2011. During the study interval, 121 consecutive patients diagnosed with incarcerated hernia admitted to the Department of General surgery, Renji Hospital. This study was undertaken after obtaining approval from the institutional committee. Incarceration was defined as irreducibility of a hernia, and a strangulated hernia was defined as an irreducible hernia with objective signs of ischemia or gangrene. Surgical procedure The skin of the patient was shaved immediately before surgery and prepared using povidone–iodine. All patients underwent general anesthesia. Perioperative IV antibiotics (2 g of ceftriaxone) was given 30 min before the operation, and continued until the fourth postoperative day. In
123
infected cases, the type of antibiotic regimen was changed according to the culture antibiogram results and hospital infection committee recommendations. Degree of contamination of operation fields was categorized according to classification from CDC [6] and American College of Surgeons. Clean wound means no inflammation was encountered and the gastrointestinal tract was not entered. Clean-contaminated wound refers to gastrointestinal tracts was entered without significant spillage. Contaminated wound has gross spillage from gastrointestinal tract without purulent inflammation. The choice of mesh repair was judged by the surgeons to have operation fields that were clean or clean-contaminated. No preference criterion was employed for the mesh repair method to be used. The mesh used in this study was monofilament polypropylene (Marlex, Bard, Ltd) and all sutures except subcuticular were 2/0 polypropylene (Prolene, Ethicon, Ltd). Skin was closed with 3–0 polyglactin (Vicryl, Ethicon, Ltd). All of the bowel resections were done without any enteric content contamination and through the primary incision. Bacterial culture studies Four-milliliter fluid from every sac of incarcerated hernia was taken for microbiologic examinations before opening the sac. If fluid in hernia sac was less than 4 mL, 4-mL sterile saline 0.9 % was injected into the hernia sac to wash the internal surface before opening. Serial tenfold dilutions of the fluid homogenate were made in 0.9 % saline and 100-lL volumes of the original suspension, then the dilutions were placed on both blood agar and differential media, and incubated at 35 °C in an atmosphere for 24 h. Bacterial growth was quantified from plates and expressed as colony-forming units per milliliter of specimen based on the volume of each specimen. Colonies on differential media were cultured 1 day more, and then inoculated and identified at the discrimination kit (bioMerieux SA, Lyon, France). Follow-up All wounds were inspected before discharge, and all incisions were carefully re-examined for early postoperative complications by the same surgeon, during suture removal at 7–9 days (first follow-up visit) and during the second follow-up visit 1 month after discharge. Patients were examined two times during the first year and yearly since the following year. The mean follow-up time was 25.6 months (11.5–52.3 months). Diagnosis of a superficial SSI or a deep SSI in followup was made according to the CDC definitions and classification [14, 15]. Superficial SSI occurs within 30 days after operation and involves only skin or
Hernia Table 1 Comparison of clinical characteristics related to SSI after prosthetic mesh repair of incarcerated hernia SSI (n = 9)
No infection (n = 112)
p
Median age (years)
69.3 ± 22.5
68.1 ± 18.2
Sex ratio (M:F)
7:2
85:17
0.165 1.000
BMI ASA grade
22.0 2
18.5 2
0.827 0.334
POSSUM physiological score
14.8
13.5
0.077
B24 h
0
89
[24 h
9
23
Direct
0
6
Indirect
5
76
Femoral
4
30
7 2
24 88
0.001
Present
8
41
0.003
Absent
1
71
Omentum
0
23
Small bowel
7
54
Colon
2
17
Duration of symptoms \0.0001
0.450
Diabetes mellitus
Ileus
Incarcerated organ
Others
a
0.287
0
2
0
16
Performed
5
10
Not performed
4
102
4 5
103 9
0.001
71.4 ± 13.5
61.7 ± 19.3
0.186
Returned Bowel resection
0.001
Mesh repair Performed Not performed Duration of operation (min) Bacteria in hernia sac Present
8
15
Absent
1
97
The Mann–Whitney U test was used to compare continuous variables and the v2 or Fisher’s exact test to compare discrete variables. Multivariate analysis was performed by means of the logistic regression method. P \ 0.050 was considered statistically significant. Statistical calculations were carried out with SPSS computer software (SPSS, Chicago, IL, USA).
Results Clinical characteristics
Hernia orifice
Present Absent
Statistical analysis
\0.0001
The median age of all patients was 68.4 (range 14.1–98.2) years. The male:female ratio was 4.8:1. The mean hospital stay was 5 days (range 2–24 days). In total, 107 hernias were repaired using mesh versus 14 primary suture repairs. All operation fields of primary suture repairs were considered ‘‘contaminated’’ by the surgeons. SSIs were observed in 9 of the 121 patients (7.4 %). Five patients had superficial SSI and four had deep SSI. None of the infected cases required mesh removal. During the follow-up period, there were no cases of mortality, recurrence or late-onset deep mesh infection. A comparison of the clinical characteristics between nine patients who had SSI and those who had no infection is shown in Table 1. Patients who had SSI after surgery were more likely to have duration of symptoms over 24 h (P \ 0.0001), diabetes mellitus (P = 0.001), with ileus (P = 0.003), bowel resection (P = 0.001) or mesh repair (P = 0.001), bacteria in hernia sac (P \ 0.0001) and with cloudy fluid in hernia sac (P \ 0.0001). Of the significant factors determined by univariate analysis (duration of symptoms, diabetes mellitus, present of ileus, bowel resection, mesh repair, bacteria present in hernia sac and cloudy fluid in hernia sac), only the bowel resection, duration of symptoms and bacteria present in hernia sac were found to be independent factors for SSI in the multivariate analysis (P \ 0.05).
Fluid in hernia sac Clear
8
13
Cloudy
1
99
\0.0001
SSI surgical site infection, BMI body mass index, POSSUM Physiological and Operative Severity Score for the enUmeration of Mortality and morbidity a
One case of bladder and one case of uterus
subcutaneous tissue of the incision. Deep SSI occurs within 1 year after surgery and involves fascial and muscle layers and also the graft.
Microbiology results Bacterial isolates were obtained in 23 of the 121 samples (19.0 %) of fluid in hernia sac. Positive rate of hernia sac fluid culture was higher in group with duration of symptoms exceeded 24 h (9/23) than group with duration of symptoms less than 24 h (0/89). Mean quantitative bacterial loads from fluid in hernia sac were 6.1 9 104/mL (6.4 9 106/mL in SSI group and 3.0 9 102/mL in group without infection). Eight species and 35 different strains of bacteria were identified and their percentages were shown
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Discussion
Proteus mirabilis 5.71% Citrobacter freundii 5.71% Bacillus cloacae 5.71%
Escherichia coli 37.14%
Enterococcus faecalis 8.75%
Pseudomonas aeruginosa 8.75%
Enterococcus faecium 11.43%
Klebsiella pneumoniae 17.14%
Fig. 1 Bacterial spectrum from fluid in hernia sac
Enterobacter cloacae 11.11%
Enterococcus faecalis 11.11%
Escherichia coli 33.33%
Proteus mirabilis 22.22%
Staphylococcus epidermidis 22.22%
Fig. 2 Bacterial spectrum from wound drainage or swab after SSI
in Fig. 1. The most common pathogen found in hernia sac was Escherichia coli, which was on 13 out of 35 samples (37.14 %). The second most common pathogen was Klebsiella pneumoniae, which was on 6 out of 35 samples (17.14 %). Bacterial isolates were obtained in all nine patients with SSI from wound drainage or swab culture. Five sorts and nine different strains of bacteria were identified and their percentages were shown in Fig. 2. The most common pathogen cultured from wound drainage or swab was E. coli, which was on three out of nine samples (33.33 %). The second most common pathogen was Staphylococcus epidermidis, which was on two out of nine samples (22.22 %). The strains of bacteria cultured from wound drainage or swab were same as those cultured from fluid in hernia sac in six of nine patients with SSI. In all four patients with deep SSI, the strains of bacteria cultured from wound drainage or swab were the same as those from fluid in hernia sac.
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The majority of SSIs after hernia repair are related to pathogens found on skin flora, such as S. aureus or S. epidermidis, with S. aureus accounting for 53–75 % of all cases including mesh infection [11, 16]. Our study is the first to reveal that E. coli was another important common organisms associated with SSI after incarcerated hernia repair. To determine whether these pathogens were skinsourced or gut-sourced, collection of hernia sac fluid for bacterial culture was performed before opening the sac. We found that most strains of bacteria cultured from wound drainage or swab (6/9) were same as those cultured from fluid in hernia sac. In our series, bacteria present in hernia sac was one of the independent factors for SSI (P \ 0.05). Moreover, it was reported that the most common organism identified was also E. coli during gut bacterial translocation [17]. Thus, incision site of strangulated or incarcerated hernia, which is repaired under emergent conditions, would have more chances to be infected by virulent bacteria originating from the intestinal tract than from the skin. Previous studies have shown that wound contamination with greater than 105 microorganisms is required to cause SSI after abdominal hysterectomy [7, 18]. However, it is unlikely that intraoperative quantitative cultures would be available to surgeons, requiring clinical judgment at the time of repair. Only cloudy fluid in hernia sac would suggest the bacteria present. Eliminating gut-sourced bacterial contamination may be achieved by prophylactic antibiotherapy activity against pathogens such as E. coli, use of wound protector at the time of bowel resection, avoidance of mesh contact with the bowl or hernia sac fluid, and changing surgical gloves prior to handling the mesh [5, 19]. In our series of 121 patients underwent emergency operations, preoperative conditions such as BMI, ASA classification or POSSUM physiological score did not appear to influence the rate of SSI. Besides bacteria present in hernia sac, we found that bowel resection was also an independent factor for SSI. In all cases with bowel resection, we performed bowel resection via the same wound through which hernia repair was performed. Thus, wound might be contaminated by enteric bacteria during the bowel resection. The current study showed a tendency for SSI to occur in patients whose duration of symptoms exceeded 24 h. Previous studies have shown that the duration between the onset of symptoms and hospital admission was considered an important factor when determining the need for bowel resection [20, 21]. However, time from symptom onset to operation set as a cutoff value varied from 12 to 48 h in different reports [20–22]. We found that there were significantly more bacteria in hernia sac in patients who came to the hospital more than 24 h after symptom onset. The longer elapsed time from symptom onset to surgery
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may increase the incidence of enteric bacterial translocation of incarcerated bowel loop, and lead to SSI as a result. This could explain the association between duration of symptoms and the SSI rate in patients without bowel resection. Although some reports have proven that incarcerated and/or strangulated hernia is not contraindication to mesh repair [2, 4, 5], we suggest that prosthetic mesh could be used when no bowel resection performed, duration of symptoms less 24 h and fluid hernia sac was clear (no sign of bacteria present in hernia sac). There are some limitations to our study that deserve mention. First, the majority of patients in our study were Chinese. Differences in ethnic groups with a relatively different health status and system of care may have affected the results. Second, in this study, we were unable to study all available meshes. So our results might not be reproducible with another mesh. Third, there were different degrees of contamination in operation fields between the two repair groups. All operation fields of primary suture repairs were considered contaminated while those of mesh repairs were considered clean or clean-contaminated. Thus, only under this circumstance mesh repairs (4/103) had less SSI rate than primary suture repairs (5/9). Finally, bacterial spectrum and quantitative bacterial loads cultured from fluid in hernia sac must be viewed with caution. 4-mL fluid from sac of incarcerated hernia represents a small sample of bacterial ground evaluated. Although these results correlated nicely with our clinical and microbiologic outcomes, these might not be accurate. It is reported that mesenteric lymph nodes and serosal scrapings could be analyzed using microbiological techniques to identify gut translocation of bacteria [17]. Thus, we believe that microbiological analyzing hernia sac fluid could also quantify and evaluate gut translocation of bacteria in patients underwent operation for incarcerated hernia if no other ideal methods were developed. In conclusion, the findings of the present study revealed that gut-sourced E. coli is an important common organisms associated with SSI after incarcerated hernia repair. Prosthetic mesh could be used when no bowel resection performed, duration of symptoms less 24 h and fluid hernia sac is clear. Acknowledgments This work was supported by grants from Shanghai Bureau of the Health, China (XBR2011035, J. Wang), Shanghai Science and Technology Fund (12XD1403400, J. Wang) and Shanghai Young Teachers’ Development Program (ZZjdyx12070, H. Wang).
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