Umbilical Microflora,Antiseptic Skin Preparation,and Surgical Site Infection in Abdominal Surgery

Abstract

Background:

Surgical site infections (SSI) following abdominal surgery are frequent and a major cause of postoperative morbidity and prolonged hospital stay. Besides antibiotic prophylaxis, antiseptic skin preparation is an important measure to prevent SSI.

Methods:

Here we prospectively analyzed the effectiveness of antiseptic skin preparation in a cohort of 93 patients undergoing laparotomy, with special emphasis on the umbilical region.

Results:

The microflora of the umbilicus contained a large number of resident (mostly staphylococci species and corynebacteria) and transient germs (including enterococci species). Following antiseptic skin preparation, bacteria could still be cultured from 24.7% of the patients' umbilici. In case of postoperative SSI, only one of seven SSI was caused by the microorganism that was present in the umbilicus before and after skin preparation.

Conclusion:

Antiseptic skin preparation fails to completely eradicate the microflora of the umbilical region in one quarter of the patients. However, at least in abdominal surgery, the vast majority of SSI are caused by intra-abdominal contamination rather than the skin microflora.

Post-operative surgical site infections (SSI) pose a serious health problem, accounting for as much as 15% of all nosocomial infections. Especially in abdominal surgery SSI are common with rates between 10% to more than 30% depending on the type of operation and on the level of contamination [1,2]. There is ample evidence that postoperative SSI result in increased morbidity and mortality, and lengthened hospital stay of on average about a week. The resulting direct costs sum up with the indirect costs such as loss of workforce and insurance costs and together cause significant harm to the health care system [3 –7].

Risk factors for the development of SSI include patient-related factors such as age, nutritional status, smoking, diabetes mellitus, concomitant medication, and others [8]. Whereas these factors can be influenced only to a certain extent, surgery-related factors can be significantly altered. Thus, numerous measures have been suggested to reduce the rate of SSI, some of them based on solid evidence, whilst others are not. For example, it has been clearly established that correct applied pre-operative antibiotic therapy can reduce SSI [9]. It has also been shown that factors such as shortened operation time, normal body temperature during the operation, minimal blood loss and avoidance of intra-operative contamination with intestinal contents reduce SSI rates [8]. Most recently it has been shown that a surgical site edge protecting device significantly reduced SSI in open elective abdominal surgery, especially in clean contaminated/contaminated cases [10].

Antiseptic skin preparation has been an important part in the armamentarium against SSI since the 19^th century [11]. Although there is no debate regarding the effectiveness of antiseptic skin preparation, there is some debate regarding the use of pre-operative antiseptic showering/bathing [12,13], as well as the specific antiseptic and the specific technique [14 –16].

The human skin is physiologically populated by a resident microflora consisting for example of various staphylococcus species, and a transient microflora consisting of both non-pathogenic and pathogenic germs [17,18]. The umbilicus is especially prone to microbacterial colonization [19], in part because this area is usually less well taken care of during body cleaning and it can harbor a humid microenvironment and sometimes foreign material [20]. The umbilicus is often close to the incision during laparotomy, posing a potential hazard for surgical site contamination [21]. However, only few and small studies and with a focus on laparoscopy have specifically analyzed the influence of the umbilical microflora on SSI development [22 –24].

Here we analyzed in a prospective cohort of elective abdominal surgical patients the germ spectrum in the umbilicus prior and after antiseptic skin preparation and correlated those results with postoperative SSI.

Patients and Methods

Trial design

This trial was a prospective, single center study that was approved by the Institutional Review Board. Analysis was conducted on an anonymized data set. Written informed consent was obtained from all participants.

Participants

All patients 18 years of age or older planned for open elective abdominal surgery via a 15 cm or longer median or transverse laparotomy were eligible. Operations had to be planned clean, clean-contaminated, or contaminated according to the U.S. Centers for Disease Control and Prevention (CDC) criteria [8]. Post-operative surgical site infections were classified according to the CDC guidelines for prevention of surgical site infections [8] as superficial incisional SSI, deep incisional SSI, and deep/organ space SSI.

The primary endpoint was SSI evaluated daily during the post-operative course until discharge and at 30 d follow-up. Secondary parameters were umbilical bacterial culture results before and after antiseptic skin preparation, bacterial culture results of surgical site infections, and post-operative complications that were graded according to the Dindo-Clavien classification [25]. The following parameters were additionally recorded: Age, gender, BMI, ASA score, diabetes mellitus, concomitant medication (antibiotics, anticoagulants, and cortisol), previous laparotomy, and indication for surgery.

Technique

The first culture swab was taken immediately before skin preparation in the operating room. Skin preparation was carried out using standard methods and povidon-iodine (Braunoderm; B. Braun Melsungen AG, Germany) according to the manufacturers' recommendations. Immediately before skin incision, the second culture swab was taken. All analyses were carried out at the Institute of Medical Microbiology (TU Munich). In case of SSI, another culture swab was taken and analyzed.

Statistics

Continuous variables are reported as means±SD or median (95%-CI), and were compared using a Student t-test or a Mann-Whitney-U-test, as appropriate. Categorical variables are summarized as frequency counts and percentages and were compared using Fisher exact test or Pearson chi-square test, as appropriate. A p value of <0.05 was considered as significant. All statistical analyses were performed using IBM SPSS, v21 for Windows (IBM Inc., Armonk, NY).

Results

One hundred twenty nine patients were screened for the study between 2012 and 2013. Twenty six patients had to be excluded from analysis because of protocol violation (wrong timing or place of culture swabs), nine because of re-laparotomy for other reasons than SSI, and one patient because of death within 30 d postoperatively. Ninety three patients were included in the final analysis. Ninety two out of ninety three patients received perioperative antibiotic prophylaxis/therapy: 68 sultamicillin, 13 ampicillin, five piperacillin/tazobactam, four clindamycin, one imipenem and one gentamycin.

Of the 93 analyzed patients, seven patients developed SSI (Table 1). There was no correlation between the occurrence of SSI and age, gender, BMI, ASA score, diabetes mellitus, cortisol, or anticoagulants therapy. However, there was a significant increase in the SSI rate in patients that were treated with antibiotics pre-operatively (e.g., for cholangitis).

Table 1.

Surgical Site Infection (SSI) Occurrence in Relation to Various Variables

	no SSI		SSI
	n=86		n=7		p
Gender					0.43
male	50	58.1%	3	42.9%
female	36	41.9%	4	57.1%
Age (years)					0.24
Median, min.-max.	64	32–88	73	21–90
BMI, median (min.–max.)	24.2 (18.0–37.7)		26.3 (24.0–31.2)		0.21
ASA-score					0.13
1	6	7.0%	0	0%
2	58	67.4%	5	71.4%
3	22	25.6%	1	14.3%
4	0	0%	1	14.3%
Diabetes mellitus	14	16.3%	2	28.6%	0.34
Cortisol	1	1.2%	0	0%	1
Preoperative antibiotic therapy	5	5.8%	3	42.9%	0.01
Anticoagulants	32	37.2%	3	42.9%	0.77
Previous laparotomy	54	62.8%	5	71.4%	0.31

BMI=body mass index; ASA=American Society of Anesthesiologists.

Most laparotomies were carried out for major abdominal resection (Table 2). Because of the small sample size there were no significant differences regarding the different operations (p=0.23). However, SSI occurred only in hepatopancreatobiliary and bowel operations (resections and palliative procedures; n=65), and not following stomach/esophageal resections or hernia repair (n=28) (Table 2).

Table 2.

Type of Surgery

	no SSI		SSI
n=93	n=86		n=7		p
Exploration/palliative bypass (n=7)	5	71%	2	29%	0.23
Liver resection (n=13)	13	100%	0	0%
Pancreas resection (n=26)	23	88%	3	12%
Esophageal resection (n=11)	11	100%	0	0%
Stomach resection (n=15)	15	100%	0	0%
Bowel resection (n=19)	17	89%	2	11%
Hernia repair (n=2)	2	100%	0	0%

SSI=surgical site infection.

There were no complications in 36 patients. According to the Dindo-Clavien classification, nine patients developed grade 1 complications, 32 grade 2, 10 grade 3 and six grade 4 complications. There was no significant correlation with the occurrence of SSI.

Patients that developed SSI had a longer pre-operative stay (median three versus two d; p=0.13), and a significantly prolonged postoperative hospital stay (median 21 versus 13 d; p=0.01) (Table 3).

Table 3.

Length of Hospital Stay Depending on Surgical Site Infection (SSI)

	no SSI		SSI
Hospital stay (in days)	n=86		n=7		p
Pre-operative
Mean±SD	2.6	2.7	5.4	6.0	0.13
Median, min.–max.	2.0	0–20	3.0	1–18
Post-operative
Mean±SD	13.9	5.6	29.0	17.5	0.01
Median, min.–max.	13.0	6–32	21.0	14–63

SD=standard deviation.

The analysis of the resident germ spectrum before and after antiseptic skin preparation, showed predominantly staphylococcus hominis and epidermidis. Coagulase-negative staphylococci could be identified 136 times in 93 pre-operative swabs (Table 4). Antiseptic skin preparation reduced this bacterial load by 83%. Corynebacteria were the second most common group of microorganism and antiseptic skin preparation reduced the bacterial load by 97%.

Table 4.

Resident Umbilical Microflora before and after Antiseptic Skin Preparation

Antiseptic skin preparation	Before	After
Coagulase-negative staphylococci, not specified	22	9
Staphylococcus hominis	46	3
Staphylococcus epidermidis	42	9
Staphylococcus haemolyticus	10	1
Staphylococcus capitis	5
Staphylococcus lugdunensis	4	1
Staphylococcus pasteuri	3
Staphylococcus warneri	3
Staphylococcus piscifermentans	1
Corynebacterium spp., not specified	21	1
Corynebacterium amycolatum	4
Corynebacterium minutissimum	3
Corynebacterium mucifaciens	1
Corynebacterium tuberculostearicum	1
Micrococcus luteus	3
Arthrobacter cumminsii		1
Propionibacterium spp., not specified	1
Propionibacterium avidum	2
Dermabacter hominis	3

In addition to the resident microflora, a number of microorganisms could be isolated from umbilical swabs. Enterococcus species were isolated nine times, Escherichia coli three times, streptococcus species six times (Table 5). Taken the data from the resident and transient umbilical microflora together, there were negative swabs after antiseptic skin preparation in 70 patients (75%).

Table 5.

Transient Umbilical Microflora Before and After Antiseptic Skin Preparation

Antiseptic skin preparation	before	after
Enterococci, not specified	1
Enterococcus faecalis	5	1
Enterococcus avium	3
apathogenic streptococci	5	1
Streptococcus viridans	1	1
Streptococci, not specified		2
Escherichia coli	3
Klebsiella pneumoniae	1
Klebsiella oxytoca	1
Citrobacter koseri	1
Citrobacter diversus	1
Citrobacter amalonaticus	1
Lactobacillus species	3	1
Spore-forming bacteria	1	1
Peptostreptococcus species	1
Bacteroides species	1
Not specified	1

Bacterial swabs were also taken from the seven patients that developed SSI (Table 6). Interestingly, only in one case the same microorganism was isolated before and after skin preparation and at the SSI (case 2). In the other cases the pathogen isolated in the SSI was not present on the pre-operative swabs. However, only two of seven patients that developed SSI had negative bacterial cultures after antiseptic skin preparation.

Table 6.

Microorganisms Isolated in 7 Patients That Developed SSI

Case	Before skin preparation	After skin preparation	SSI
1	S. hominis S. haemolyticus S. pasteuri C. tuberculostearicum	S. epidermidis	Klebsiella pneumoniae
2	S. piscifermentans S. epidermidis Dermabacter hominis	S. hominis S. epidermidis	S. epidermidis
3	S. hominis	S. hominis S. epidermidis	Escherichia coli Enterococcus faecalis
4	S. hominis S. epidermidis S. haemolyticus	S. epidermidis	Enterococcus faecium
5	S. epidermidis	Coagulase-negative Staphylococci	Enterococcus faecalis
6	S. hominis S. haemolyticus	sterile	Pseudomonas aeruginosa
7	S. haemolyticus S. capitis	sterile	sterile

SSI=surgical site infection; S=staphylococcus.

Discussion

SSI can develop directly from contaminated skin, from intestinal microflora via intra-operative opening of the bowel, or from outside sources such as contaminated instruments, surgeons and others. SSI can also develop indirectly via, for example, blood or lymph vessels.

The present study aimed at analyzing the microflora of the umbilicus in relation to the development of SSI following laparotomy. The umbilicus was chosen because it represents the most contaminated and most difficult part to disinfect during antiseptic skin preparation. In this context, it has been hypothesized that abdominal hair collects fibers from clothes that then accumulate together with cutaneous scales, fat, and proteins in the umbilicus where they are compacted [20].

There is not much data regarding the physiological microbiome of the umbilicus. Here, we could demonstrate a large spectrum of both resident and transient microorganism in the umbilicus of the analyzed patients. Somewhat surprising was the percentage of enterococci species and E. coli found in the umbilical region.

In the present study, we could not detect a significant correlation between the occurrence of SSI and age, gender, BMI, ASA score, diabetes mellitus, cortisol, or anticoagulants therapy. However, this was most likely because of the small sample size of the present study, because larger studies have repeatedly shown an association of these factors with the occurrence of SSI [8]. We could show that there was a significant increase in SSI in patients that were treated with antibiotics pre-operatively. Most of these cases were treated for cholangitis because of biliary stent therapy and it is well known that pre-operative stenting increase septic complications including SSI [26].

Antiseptic skin preparation resulted in a germ-free umbilicus in approximately 75% of patients; thus 25% of the patients had detectable microorganism, despite skin preparation. Similar data were reported by Bienkowski et al. [22], who demonstrated 17% positive umbilical swabs after antiseptic skin preparation. This points to the fact that this region is indeed difficult to clean, and that further improvements can be made here. This is supported by data of skin (not umbilical) swabs after antiseptic skin preparation in more than thousand patients. There, only 3.6% revealed a significant colonization of the pre-operative site [15]. Interestingly, however, in the group of patients developing SSI in our study, 5/7 (71%) had detectable bacteria after antisepsis compared with 18/86 (21%) that did not develop SSI (p<0.01), suggesting that antiseptic skin preparation was not efficient in these patients. Still, only one of seven (14%) of the surgical site infections were potentially related to incomplete antiseptic umbilical skin preparation indicated by the detection of the same bacteria. The reason why pre-operative swabs were significantly more often positive in patients developing SSI is not readily apparent. It could be speculated that positive swabs after antisepsis point to a higher bacterial load and/or a different host response. Thus, positive swabs could potentially indicate a higher susceptibility for postoperative SSI.

Irrespective, our observation that SSI are in most cases not related to incomplete antiseptic umbilical skin preparation is in line with published data showing only one of 19 (5%) of SSI related to incomplete antisepsis [22]. Hamzaoglu et al. have even shown that none of the SSI were related to the microflora of the umbilicus [23] and in the previously mentioned study of more than thousand patients, it was shown that “residual bacteria before incision were completely unrelated to the incidence of SSI” [15].

In conclusion, antiseptic skin preparation fails to completely eradicate the microflora of the umbilical region in one quarter of the patients. However, at least in abdominal surgery, the vast majority of SSI are most likely caused by intra-abdominal contamination rather than the skin/umbilical microflora.

Footnotes

Author Disclosure Statement

All authors (JK, ME, CJ, MM, FG, MH) declare that there is no actual or potential conflict of interest.

References

Culver

, Horan

, Gaynes

, et al. Surgical surgical site infection rates by surgical site class, operative procedure, and patient risk index. National Nosocomial Infections Surveillance System. Am J Med, 1991; 91:152S–157S.

Smyth

, McIlvenny

, Enstone

, et al. Four country healthcare associated infection prevalence survey 2006: Overview of the results. J Hosp Infect, 2008; 69:230–248.

Broex

, van Asselt

, Bruggeman

, van Tiel

. Surgical site infections: How high are the costs?. J Hosp Infect, 2009; 72:193–201.

de Lissovoy

, Fraeman

, Hutchins

, et al. Surgical site infection: Incidence and impact on hospital utilization and treatment costs. Am J Infect Control, 2009; 37:387–397.

Geffers

, Sohr

, Gastmeier

. Mortality attributable to hospital-acquired infections among surgical patients. Infect Control Hosp Epidemiol, 2008; 29:1167–1170.

Kirkland

, Briggs

, Trivette

, et al. The impact of surgical-site infections in the 1990s: Attributable mortality, excess length of hospitalization, and extra costs. Infect Control Hosp Epidemiol, 1999; 20:725–730.

Merle

, Germain

, Chamouni

, et al. Assessment of prolonged hospital stay attributable to surgical site infections using appropriateness evaluation protocol. Am J Infect Control, 2000; 28:109–115.

Mangram

, Horan

, Pearson

, et al. Guideline for prevention of surgical site infection, 1999. U.S. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control, 1999; 27:97–132.

Classen

, Evans

, Pestotnik

, et al. The timing of prophylactic administration of antibiotics and the risk of surgical-surgical site infection. N Engl J Med, 1992; 326:281–286.

10.

Mihaljevic

, Schirren

, Özer

, et al. Multicenter double-blinded randomized controlled trial of standard abdominal surgical site edge protection with surgical dressings vs. coverage with a sterile circular polyethylene drape for prevention of surgical site infections: A CHIR-Net trial (BaFO; NCT01181206). Ann Surg, 2014:260; 730–737.

11.

Lister

. On the antiseptic principle in the practice of surgery. Br Med J, 1867; 2:246–248.

12.

Tanner

, Gould

, Jenkins

, et al. A fresh look at preoperative body washing. J Infect Prev, 2012; 13:11–15.

13.

Webster

, Osborne

. Preoperative bathing or showering with skin antiseptics to prevent surgical site infection. Cochrane Database Syst Rev, 2012; 9:CD004985.

14.

Darouiche

, Wall

Jr. , Itani

, et al. Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. N Engl J Med, 2010; 362:18–26.

15.

Tschudin-Sutter

, Frei

, Egli-Gany

, et al. No risk of surgical site infections from residual bacteria after disinfection with povidone-iodine-alcohol in 1014 cases: A prospective observational study. Ann Surg, 2012; 255:565–569.

16.

Weed

, Bastek

, Sammel

, et al. Comparing postcesarean infectious complication rates using two different skin preparations. Obstet Gynecol, 2011; 117:1123–1129.

17.

Fredricks

. Microbial ecology of human skin in health and disease. J Investig Dermatol Symp Proc, 2001; 6:167–169.

18.

Percival

, Emanuel

, Cutting

, Williams

. Microbiology of the skin and the role of biofilms in infection. Int Wound J, 2012; 9:14–32.

19.

Hulcr

, Latimer

, Henley

, et al. A jungle in there: Bacteria in belly buttons are highly diverse, but predictable. PLoS One, 2012; 7:e47712.

20.

Steinhauser

. The nature of navel fluff. Med Hypotheses, 2009; 72:623–625.

21.

Voitk

, Tsao

. The umbilicus in laparoscopic surgery. Surg Endosc, 2001; 15:878–881.

22.

Bienkowski

, Gospodarek

, Olejarz

, Deptula

. The evaluation of skin disinfection efficacy and its influence on prevalence of surgical site infections in patients subjected to laparoscopic cholecystectomy. Med Dosw Mikrobiol, 2007; 59:183–191.

23.

Hamzaoglu

, Baca

, Boler

, et al. Is umbilical flora responsible for surgical site infection after laparoscopic surgery?. Surg Laparosc Endosc Percutan Tech, 2004; 14:263–267.

24.

Kikuchi

, Yano

. Lint in the belly button. J Plast Reconstr Aesthet Surg, 2009; 62:282–283.

25.

Dindo

, Demartines

, Clavien

. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg, 2004; 240:205–213.

26.

van der Gaag

, Rauws

, van Eijck

, et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med, 2010; 362:129–137.